THE EVOLUTIONARY

NEUROETHOLOGY OF
PAUL MACLEAN
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 THE EVOLUTIONARY
NEUROETHOLOGY OF
PAUL MACLEAN
CONVERGENCES AND FRONTIERS

Edited by Gerald A. Cory, Jr. and

Russell Gardner, Jr.

Foreword by Jaak Panksepp

Human Evolution, Behavior, and Intelligence

Seymour W. Itzkoff, Series Editor

Westport, Connecticut
London
Library of Congress Cataloging-in-Publication Data

The evolutionary neuroethology of Paul MacLean : convergences and frontiers / edited

by Gerald A. Cory, Jr. and Russell Gardner, Jr. ; foreword by Jaak Panksepp.
p. cm.—(Human evolution, behavior, and intelligence, ISSN 1063-2158)
Includes bibliographical references and index.
ISBN 0-275-97219-4 (alk. paper)
1. Brain—Evolution. 2. Animal behavior. 3. Neuropsychology. 4. MacLean, Paul D. I.
Cory, Gerald A. II. Gardner, Russell, 1938- III. Series.
QP376.E875 2002
612.8—dc21 2002021588

British Library Cataloguing in Publication Data is available.

Copyright © 2002 by Gerald A. Cory, Jr. and Russell Gardner, Jr.
All rights reserved. No portion of this book may be
reproduced, by any process or technique, without the
express written consent of the publisher.
Library of Congress Catalog Card Number: 2002021588
ISBN: 0-275-97219-4
ISSN: 1063-2158
First published in 2002
Praeger Publishers, 88 Post Road West, Westport, CT 06881
An imprint of Greenwood Publishing Group, Inc.
www.praeger.com
Printed in the United States of America

The paper used in this book complies with the

Permanent Paper Standard issued by the National
Information Standards Organization (Z39.48-1984).
10 9 8 7 6 5 4 3 2 1
 CONTENTS

Foreword: The MacLean Legacy and Some Modern Trends in Emotion

Research ix
JAAK PANKSEPP

Acknowledgments xxix
Introduction xxxi

PART I: PERSPECTIVES

1. Pribram and MacLean in Perspective

KARL H . PRIBRAM

2. Reappraising MacLean's Triune Brain Concept

G E R A L D A . C O R Y , JR.

PART II: MOLECULES, BODY PLANS, AND THE STRIATUM

3. Deep Time and the Brain: The Message of the Molecules

C . U . M . SMITH 31

4. Adaptive Functions of the Corpus Striatum: The Past and Future

of the R-Complex
NEIL GREENBERG 4 5

PART III: THE SOCIAL BRAIN: CLINICAL THEORY AND

APPLICATIONS—DEPRESSION AND MANIA

5. MacLean's Paradigm and Its Relevance for Psychiatry's Basic Science

RUSSELL GARDNER, JR. 85
vi Contents

6. The Triune Brain, Escalation De-escalation Strategies, and

Mood Disorders
J O H N S . PRICE 107

7. Involuntary Defeat Strategy as Backdrop for Depression

LEONSLOMAN 119

8. The Evolved Basis of Mood and Thought Disorders: Neuroethologic,

Game Mathematic, and Evolutionary Epidemiologic Analyses
DANIEL R. WILSON 133

PART IV: THE SOCIAL BRAIN: CLINICAL THEORY AND

APPLICATIONS—AUTISM, FORENSICS, AND ATTENTION

9. Empathy, Autism, and the Integration of the Triune Brain

JAMES C . HARRIS 155

10. Neuroethology, Exemplified by Limbic Seizures with

Motiveless Homicide in "Limbic Psychotic Trigger Reaction"
ANNELIESE A . PONTIUS 167

11. Neural and Functional Aspects of Pride and Shame

GLENN E. WEISFELD 193

12. The Triune Brain and the Functional Analysis of Attention

A L L A N F . M I R S K Y AND C O N N I E C . D U N C A N 215

PART V: INTERPRETATIONS AND CHALLENGES

13. From Physics and Evolutionary Neuroscience to Psychotherapy:

Phase Transitions and Adaptations, Diagnosis and Treatment
JAMES BRODY 231

14. Evolutionary and Philosophical Issues in Triarchic Theory

S E Y M O U R W . ITZKOFF 259

15. MacLean's Evolutionary Neuroethology: Environmental Pollution,

Brain Chemistry, and Violent Crime
ROGER D . MASTERS 275
Contents vii

PART VI: SOCIAL PSYCHOLOGY AND SOCIAL THEORY

16. Reification and Hegemony: The Human Brain as the Linkage Between
Macro and Micro Level Political Phenomena
STEVEN A . PETERSON 299

17. Upshifting and Downshifting the Triune Brain: Roles in Individual and
Social Pathology
KENT BAILEY 317

18. Algorithms of Neural Architecture, Hamilton's Rule, and the

Invisible Hand of Economics
G E R A L D A . C O R Y , JR. 345

19. Toward a Neural Network Theory of the Triune Brain

D A N I E L S. L E V I N E A N D N I L E N D U G . J A M 3 83

20. Conclusion: Convergences and Frontiers 395

G E R A L D A . C O R Y , JR. AND R U S S E L L G A R D N E R , JR.

Name Index 405

Subject Index 421
About the Contributors and Editors 431
 FOREWORD: T H E M A C L E A N L E G A C Y
A N D S O M E M O D E R N T R E N D S IN
EMOTION RESEARCH

Jaak Panksepp

I offer this foreword to validate and extend Paul MacLean's strategic conject-
ures concerning the evolved bases for emotions and related neuromental
processes. Neuroevolutionary perspectives such as those advocated by MacLean
are essential to explore the fundamental nature of the human mind. It remains a
pity that some neuroscientists currently marginalize the approach to brain/mind
organization that the MacLean legacy constitutes. I do not believe these investi-
gators provide credible theoretical alternatives. It is true that some emotion
researchers who have criticized or ignored MacLean's contributions (e.g.,
Joseph LeDoux and Edmund Rolls, respectively) have made important
contributions to relatively circumscribed areas, but MacLean sought to elucidate
the overall mind-brain puzzle as a functioning whole. Surely the path to substan-
tive progress must be paved by a synthesis of molecular and molar perspectives.
Those who pursue proximal fine-grained research ought not to pretend they
offer more robust interpretations than does MacLean (and others who hew to
more conceptually integrative points of view). Indeed, the larger evolutionary
considerations must frame molecular analyses—not vice versa.
I do not here reiterate critical points raised in the many fine chapters in this
volume (note especially the one by Jerry Cory to whose points I will add). I
certainly affirm, however, that some critics unfairly treat MacLean's legacy;
they sweep his sagacious and broad perspective away as if it were detritus of a
pre-scientific past. MacLean's "limbic system" concept (didactically sound
though it is) and his enunciation of general patterns in the evolution of brain and
emotions (sound though they are as well) have too commonly been the focus of
recent attacks by those who seem to consistently ignore MacLean's abundant
empirical contributions. Some senselessly gratuitous attacks reflect inadequate
historical or conceptual perspectives while misrepresenting MacLean's position,
perhaps with opportunistic intent.
X Foreword

The breadth of MacLean's work continues to influence individuals who are

truly interested in understanding the evolved nature of emotions in human and
animal brains. Investigators who focus on conditioning reflexive emotional
behaviors ought not pretend their work relates to the deep nature of emotionality
in the evolved brain. They would more fittingly acknowledge that they work to
clarify a modest corner of a much vaster mystery.
Work that attempts to draw broad conceptual outlines rather than to harvest
small empirical peppercorns is an ever-easy target for attack. Perhaps this is why
much of modern neuroscience is scornful of theory, calling it mere speculation.
As a result there is currently little thought—much less discussion—of how
coherent functional brain systems evolved, notably the ancient phylogenetically
derived emotional systems of the mammalo-human mind and brain. By contrast,
MacLean offers a vision of human neuromental organization that broadly
achieves such a summary perspective. Moreover, his is not mere speculation but
in fact a superb theoretical structure, with abundant predictions, built upon a
solid foundational body of data from an extensive study of the functional neural
systems of our brethren species.
Beyond the popular molecular science approaches permitted by modern
technologies, there are other more reasonable paradigmatic perspectives—for
example, distributed network models—from which to think about our emotional
nature. It's partly a matter of scale. Emotions are global state processes of the
brain that cannot yet be epistemologically incorporated into a fine-grained focus
on issues of neuronal microstructure and function, although they are
ontologically quite compatible.
Thus, this compendium should be valuable to all who would understand how
minds are created by the brain's evolved networks. I should pointedly add that
this is an especially good book for neuroscientists as many among them have
much to learn at the important evolutionary interface of mind and brain issues.
Unfortunately, many prominent emotion researchers—especially neo-behavior-
ists who now inundate neuroscience—continue to cultivate remarkably restricted
paradigms from which they claim to have achieved substantive understanding of
the nature of emotions. They fail to acknowledge or perhaps appreciate that such
systems cannot be adequately conceptualized at a level where single cells of the
brain learn about environmental contingencies. While fine-grained neurobehav-
iorism has advanced important insights into how learning can guide emotional
tendencies, such microanalyses cast only scattered dim light upon the
mammalian brain's integrative psychobehavioral systems that generate global
state/action processes comprising the basic emotions.
Investigators who pursue such microanalyses often deny that the experience
of emotion, especially in animal subjects, possesses relevance for their science.
Yet abundant reason allows us to conclude that many of the emotional states
humans experience with affective urgency are experienced similarly by other
creatures. Therefore, the continued unwillingness of behavioral neuroscientists
to address such questions openly retards understanding of how affective mental
states arise from brain dynamics. Without a more coherent elucidation of the
evolved state-processes of the brain, there is little hope neuroscience can clarify
Foreword xi

fundamental neuropsychological issues or otherwise provide a coherent

foundation for biological psychiatry.
For MacLean, one of the keys to understanding emotions hinges on how the
human brain/mind actually creates affective experiences. This bears even more
fundamentally on understanding emotions than on how other behavioral
tendencies emerge from brain activities. MacLean blazes a trail along the most
effective path in his provisional acceptance that behavioral and psychological
phenotypes arise on a continuum in nature and, consequently, that many other
species also have homologous affective experiences.
We in the neuroscience research community should willingly assume that
most species we study in behavioral neuroscience laboratories do, in fact,
experience internal feelings; that is, various positive and negative affects.
Indeed, if internalized neurobiologically based experiences do characterize
them, then without considering such neurodynamics little hope exists that we
will understand their brains, much less our own. Even in this era of PET and
fMRI mind/brain mapping, no unambiguous ways have yet been laid out for
imaging the neural details of affective states except perhaps by understanding
the brain systems for the natural emotional actions and related behavioral
choices of other animals. I suspect precisely this inferential aspect of MacLean's
work still disturbs the sensibilities of the abundant behaviorists and cognitivists
who have only lately recast themselves as neuroscientists.
Even though no one has devised a mindscope to measure emotional states,
other than through various indirect behavioral and physiological indices, we
should not marginalize neuromental constructs simply because they operate
through large-scale neurodynamics that cannot be monitored unambiguously at
the present time. To do so tacitly serves the agenda of a positivistic-behav-
ioristic tradition that has consistently denied the scientific existence of human
and animal mental processes—particularly those derived from phylogeny—
throughout the 20th century. Those who deny to other animals essential neuro-
mental abilities, such as affective experiences to guide long-term behavioral
strategies, reinforce an arrogant neo-dualistic cortical creationism that severely
constrains modern neuroscience from coming to terms with the evolved mental
apparatus of human beings. This does not deny that the cortico-cognitive
abilities of humans have brought with them an impressive rational(izing)
"higher" mind. But we must also consider that the formation of such a mind
could only have built upon a more ancient evolved apparatus of basic emotional
urges and motivational values.
Behavioristically oriented investigators rarely care to infer what our animal
brethren may feel. Hence they sustain a dismal ontological position—that mind-
less Cartesian zombies largely occupy animate life. Because they cannot directly
measure neurodynamic affective states of the animals they study, they claim that
such functions of animal brain/mind remain nothing more than statements of
faith. They appear to have conveniently chosen to forget that science thrives on
predictions, probabilities and the weight of evidence, not certainties. By exten-
sion they ignore the power of theoretically cogent empirical predictions that can
be made about human feelings from animal behavioral neurochemical studies.
xii Foreword

Mind evolution must necessarily be inferred from living brain functions, not
fossilized tissues. None can parse such issues with the precision all would
desire, but this should not prevent continuing inquiry into such important topics.
Here I note that MacLean pursued these matters with a unique devotion, one
adventurous, scientific and humanistic. Regrettably, modern molecular neuro-
science does not adequately admire his intuitive sensibility. Rather, the guiding
principle once again holds that if you can't measure it concretely and
unambiguously, it would be best to be silent. Many have forgotten or never
recognized Immanuel Kant's famous dictum from The Critique of Pure Reason:
"Concepts without factual content are empty; sense-data without concepts are
blind. The senses cannot think, the understanding cannot see. By their union
only can knowledge be produced."
The most productive avenue to understanding the evolved emotional systems
of the brain would specify how coordinated systems of neuronal activities
generate global behavioral and psychological "existential" states in sentient
organisms. Ethological study of natural behavior in animals best delineates
global functions of the brain and mind. A minute analysis of isolated elements
can lead instead to an ontological myopia that focuses on molecular analyses for
their own sake rather than conceptualizing and perceiving actual neuromental
operating systems. In other words, reductionism with no clear vision of what
needs to be reduced litters the grove of science with leaves in need of raking and
composting.
We see similar premature reductionism in biological psychiatry. A psychiatry
that only pays attention to molecules, and not to evolutionary issues of how
brain emotional systems are organized represents an extreme case of scientific
short-sightedness. It often misses the functional forests (e.g., networks) because
it details the neuronal-molecular undergrowth. Paul MacLean recognized the
necessity of viewing both the broad sweep of the canopies and the underlying
details: he charted a path by which we might study both levels. This volume
shares his broad vision, without dismissing the essential details to which all
scientists must attend.
Now all reasonable scholars, unlike the behaviorists of the 20th century,
accept that we need neuronal concepts to understand how behavior and the mind
work. But few recognize the important corollary: without certain basic
psychological concepts—ones best represented by the instinctual affective urges
of animals—we cannot understand the brain. When we understand such intrinsic
mind/brain processes, we can more ably develop an evolutionary psychiatry that
sees the ancient affective personality-creating forces of the brain/mind as novel
targets for both chemotherapy and psychotherapies. This level of analysis will
also inform us how these ancient phylogenetic progressions of brain/mind
development still affect the subjective complexities of human lives.
The specific mental contents of individual lives—thoughts and memories
that make us fully human—are brought to us abundantly by various informa-
tionally encapsulated "channel-functions" of the brain. Yet the affective founda-
tions for mental being stem from more ancient and deeply organic network
"state-functions" of the brain. These underlying organic processes generate
Foreword xiii

massive analog states of mind that we experience as primary process feelings.

They do this through the cooperation of many widely ramifying neuronal
operating circuits and systems. Although much neuronal functioning happens
unconsciously, the massively interacting neuronal networks do produce an
emergent affective consciousness. This phylogenetic emotional "intelligence",
genetically-coded to a substantial degree, permits the experiential intersubject-
ivity essential for individual social learning. There could be no emotionally
resonant infant-mother "psychic-dance"—perhaps an essential ingredient for
healthy childhood development—without the ingrained affective potentials of
the brain (Stern 1985, 1999; Panksepp 2001; Trevarthen 2001).
Such experiential capacities have causal consequences for what organisms do
in order to survive and multiply. If we envision such ancient evolved value/
action systems, interacting dynamically with the myriad individual experience-
dependent channel-control functions, we may be less tempted to pursue the
scientific reduction of individual experience and culture to molecular
neurobiology. Instead, we would seek substantive supervenient relationships
between levels of analysis. Paul MacLean's views pointed us in that direction.
A dilemma of modern neuroscience hinges on the fact that the "neuron
doctrine" that captivated neuroscientists of the 20th century does not effectively
identify the evolved global functions of the brain/mind. It simply does not do
justice to large ensembles of neurons working together in a mode that can be
transmitted via the heuristics of Darwinian evolution. For this we desperately
need a new "network doctrine."
Through impressive mental gymnastics and a profound mind-blindness,
MacLean's critics presume holistic approaches offer little; yet their approaches
typically fail to envision how different levels of organization actually exist in
nature. Ultra-positivistic approaches commonly overlook the productive philoso-
phical concept of supervenience. This accepts that there are true levels of
organization in nature, and that the higher levels of organization do not simply
reduce to lower levels. Recognition of relationships between levels of organi-
zation should encourage search for coherent linkages between levels of analysis,
rather than focus on ever more molecular levels that marginalize analyses on
more global levels or that pretend that complete reductionism between levels
can really work. An adequate recognition of this concept can allow scientists to
live more peacefully and supportively with other investigators who work at
different levels of analysis. Through supervenient approaches that aspire to sup-
plement and conceptually guide work at different levels—rather than destroy
each other—a coherent, scientifically credible appreciation of the whole may
gradually emerge. That would allow us to understand eventually how emotional
systems and affective feelings really operate.
The concept of the evolved limbic system encapsulates the most globally
integrative and productive image of emotions we presently possess. This brain
territory, as MacLean advocated, needs to be searched for the details whereby
neuronal networks construct emotional processes. Some recently have claimed
MacLean's limbic-emotional brain concept misleads and is therefore of no use
to modern neuroscience. Such a conclusion speaks more loudly about human
xiv Foreword

arrogance than thoughtful neuroscience. Were such critics to construct a compo-

site brain map of emotional processing from modern brain-imaging studies, they
would need to admit that MacLean's original concept, in fact, pointed us in the
right direction. They would also be wise to reconsider MacLean's empirical con-
tributions that brilliantly document how the ancient recesses of the brain help
elaborate specific emotional impulses.
In summarizing these general conceptual issues, let me again emphasize that
evolved emotional operating systems cannot be identified simply by studies of
single neuron activities, even though the latter can provide important correlates
between behavior and brain activities. Coherently operating brain systems must
also be identified through the neuroethological analyses of basic emotional
behavior patterns that animals exhibit spontaneously with little need for social
learning. A "network-doctrine" is essential to make sense of such global state
variables. While MacLean and various other investigators have sought to
capture those broader, system-wide emergent dynamics, most behavioristically
oriented neuroscientists focus their attentions on the fine neuronal details,
especially single unit activities related to learning experiences under stimulus
control.
Unfortunately, these neurophysiological correlates provide little insight into
the overall dynamics of emotional systems in action. Understandably, modern
scientists are always drawn to look where the light and funding is brightest,
especially as new technologies become available. However, in doing so they
commonly study more manageable proximal problems rather than the larger
concerns that must also frame insightful inquiries. With such shifts of emphasis
and amid competitive funding, they often succumb to the temptation to denigrate
the rigorous work of those still engaged with the global and holistic issues of
concern to the educated public at large.
While examining for meaningful neuromental correlates to psychological and
behavioral responses, we must accept that certain natural phenomena do exist as
complex emergent manifestations of distinct levels of organization. From this
point of view, molecular neuroscientists commonly lack tools to attack the
hardest mind-brain problems, such as the psychological consequences of many
interacting brain systems. This does not mean effective tools are unavailable, but
rather that the utilization of such tools must, by necessity, link to theoretical
inferences. Neuroscientists unfortunately are often loathe to consider these. I
think this lies at the heart of the dilemma that MacLean's theorizing poses for
many who simply detest the concept of "the limbic system" as the epicenter of
the emotional brain. They harvest data more comfortably than make predictions
from theoretical premises.
This present volume goes a long way to rectify errors of interpretation and to
reaffirm how heuristic MacLean's ideas have actually been. His lasting contri-
butions to date relate to having spurred many disciplines to think more
coherently about important issues. MacLean's thinking finally brought brain
issues to bear upon important topics where there had been no coherent
neuroscientific thought at all. MacLean always encouraged additional develop-
ment and refinement with remarkably little personal egoism. A sad day will
Foreword xv

dawn for our pedagogy and science should the superficial views of the neo-
behaviorist critics prevail indefinitely. In my estimation, intellectual travesties
ensue without a holistic view of emotions that aspires to clarify the neuronal-
network foundations upon which such large-scale mind/brain processes subsist.
The molecular analyzes of some critics have usefully worked out details of
limited problems, but shed little light on how brain matters eventually generate
coherent emotional states and affective experiences.
Thus far I have spoken generally. Now let me be more concrete and frank in
extending Jerry Cory's rebuttal of selected MacLean critics; his chapter
principally considers those who reviewed MacLean's 1990 opus. Since he
doesn't refer specifically to the views of Joseph LeDoux, I will bring these into
focus. Widely hailed as "the leading expert on the emotional brain" (Gazzaniga,
et al. 1998, Textbook of Cognitive Neuroscience, p. 516), LeDoux's empirical
work in fact represents the apotheosis of a learning-centered, neo-behaviorist
neuroscience that hasn't yet come to grips with the evolved nature of
emotionality. He has been most dismissive of MacLean's integrative views, and
he has been the most sustained opponent of the limbic system concept within
"the emotional brain" community. In articulating and pushing forward his own
agenda, LeDoux (1996, 2000) has explicitly misrepresented MacLean's perspec-
tives. To all appearances he has done so intentionally—unless he has either
misunderstood or not carefully read what MacLean actually wrote in The Triune
Brain in Evolution.
A malaise in modern brain-emotion research emerges from neuroscientists
ignoring affective states of consciousness. By applying some bitter medicine, I
hope to make some critical points that are hard to achieve using more sugar-
coated (i.e., unforthright) intellectual maneuvers. Although I may not change the
minds or hearts of those who need it most, a new generation of scholars may
learn through the mistakes and miscommunications of present and preceding
eras.
LeDoux selected what he perceives to be the weakest link in the armor of the
competition (i.e., Paul MacLean's "limbic system" concept as an anatomical
entity) for launching a subtle attack on those who accept emotional feelings as
an important topic for neuroscientific inquiry. Indeed, LeDoux has falsely
claimed that MacLean employed the "limbic system" as an explanation of a
monolithic emotion process—a simply incorrect statement. MacLean applies the
concept only to circumscribe approximate neuronal territories as appropriate
targets for inquiry. LeDoux's claim is especially arbitrary since he cites no
chapter or verse from MacLean's magnum opus (indeed, the book is not even
cited in most of his recent reviews, with preference given to MacLean's earlier
and less timely materials).
Although LeDoux's group has done excellent empirical work in the area of
fear learning, he ignores whole swaths of relevant data collected under
conceptual approaches other than his own. Along the way he has selected
subsidiary issues (e.g., the "limbic system" concept of MacLean's work, and my
own ontological position that certain other animals probably experience
emotional feelings) as reasons to disregard our empirical work and to avoid our
XVI Foreword

epistemological strategies. With marginalization of this magnitude on a topic of

mutual interest, one must suspect that factors other than scientific ones guide
strategic choices. The approach resembles a Madison Avenue type of "public
relations" campaign: namely, if one caricatures or disregards other substantive
ideas and data, the more one's own ideational progeny may thrive. In part,
competition fuels this—for difficult-to-obtain research grants. One needs to win
"Zeitgeist-compliant," molecularly-oriented, grantsmanship competitions that
often leave little room for theoretically innovative research. Parenthetically,
MacLean's work probably could not readily have been conducted anywhere else
than the safe-haven of a financially protected NIH lab.
Being one of the few behavioral neuroscientists (except for MacLean, of
course), who took evolutionarily ingrained emotional systems and animal
feelings seriously in the 1970s, I was delighted when young investigators like
LeDoux exhibited some revolutionary fervor for pursuing emotional topics of
first-rate importance, as opposed to pursuing simply the obligatory domains of
learning, memory and certain well-accepted motivational processes (e.g.,
feeding, drinking, sleeping and sexing). Practically no one in the USA obtained
extramural funding for basic brain-emotion research at the time LeDoux entered
the field—unless they complied with traditional behavioristic methodology and
atheoretical positivistic assumptions. This has continued to the present day in
behavioral neuroscience.
LeDoux learned his lesson about the power of behaviorism—then and still—
when he applied for initial funding to study the classical conditioning of fear (a
mainstay topic of behavioral analysis for the better part of the 20th century). As
he poignantly related in public (i.e., at a Society for Neuroscience Symposium in
the 90s), his first request for federal support in the 1980s provided him a
powerful, that is "emotional," lesson in modern grantsmanship. The study
section indicated that nothing in his proposal to study the brain substrates of
classical conditioning of fear required the concept of emotion. All could be done
under the concepts of learning and memory.
He chose to revise his grant as recommended. As publicly related, he merely
changed every usage of the word "emotion" to memory-related terms. Promptly
rewarded for this accommodating (duplicitous?) maneuver, he continued to
receive substantially more funding than anyone else in the animal brain-
"emotion" field ever since.
When LeDoux initiated his modern neuroscience research program, everyone
in the field had known for years that the amygdala was the optimal place for
working out the details of fear learning. His group has now made first-rate
contributions to clarifying the nature of that phenomenon, but not to the bigger
and more urgent question—the nature of the evolved brain operating systems
that mediate emotionality. He has made no major contribution to our under-
standing of animals' diverse emotional repertoires, nor has he helped us
understand the possible experiential-existential states these systems help create
in humans. Indeed, he has simply chosen to ignore the weight of evidence that
points to the importance of such issues as well as strategic ways to approach
their solution.
Foreword xvii

As the years have passed, LeDoux's investigation of amygdaloid partici-

pation in perceptual fear learning emerged as examples of how modern neuro-
science tools can effectively take up difficult problems in learning and memory.
It generally simulates Nobel Laureate Eric KandePs research in the study of
electric-shock mediated classical conditioning in Aplysia. However, the success
should not foster any illusion that the work has focused either on the
evolutionary or integrative nature of emotionality. His work resembles the
activity of the proverbial gentleman looking for his keys under the street lamp.
Curiously, in "looking well" at restricted problems, he has convinced too many
scholars that his research revealed the core processes of emotions.
By conceptualizing the amygdala as the heart of emotional processing in the
brain and by relegating subcortical meso-diencephalic core functions to simple
motor outputs, he captivated the imaginations of psychologists traditionally little
interested in brain functions. Gradually, the amygdala assumed the role of some
master integrator of many emotions. This new "insight" has been blown vastly
out of proportion in the popular press, though informed workers and clinicians
know it represents only a small part of the emotion story. This reification
represents a more simple-minded and incorrect formulation than does
MacLean's broad concept of the limbic system, and until recently, LeDoux has
done little to dissuade simplifiers from that tack. However the clinical evidence
already shows that people with bilateral amygdaloid lesions exhibit an emotional
naivete and fail to demonstrate some forms of fear conditioning, but also they
demonstrate no global disorder of emotions. Their feelings related to social
attachments remain intact, and they fully feel internally generated emotional
turmoil (Damasio 1999).
In any event, LeDoux vigorously implemented the new armamentarium of
tools created by neuroscientists in the 1970s and 1980s, even as MacLean's
career increasingly approached the "retirement phase." LeDoux's laboratory
applied these tools with impressive skill and they made a vast number of worthy
contributions. We now feel confident that the conditioning of fear to auditory
cues stems from specific amygdaloid subareas. This helps us appreciate that
amygdala, astride the diencephalic and midbrain systems that instantiate
coherent emotional responses, plays a major role in mediating ubiquitous
interactions between emotion and cognition.
Unfortunately fear conditioning tells little about how the potential for
affective experience arises from human or animal brains and minds. It contri-
butes only to our understanding of where and how neutral stimuli gain access
into a single brain emotional system. Why LeDoux has failed to emphasize the
evolutionary antecedents of fear learning (i.e., fear states) remains unanswered,
but this may hinge on the fact that deep evolutionary views don't have popular-
ity in either behavioral or cognitive neuroscience. Moreover, such attention
would entail explicit recognition of an ancient and coherently operating FEAR
system, proposed by others, that courses between the central amygdala to the
periaqueductal gray (Panksepp 1990, 1998). LeDoux, a prominent opinion-
leader in the field, does not willingly acknowledge such manifest facts. Had he
done so, contemporary neuroscience and cognitive science might already have
xviii Foreword

forthrightly contextualized fear among the manifold emotional operating

systems of the brain, and made meaningful distinctions between the system for
FEAR and others that mediate different kinds of anxiety such as social
separation distress/PANIC. Although LeDoux claims to accept an evolutionary
point of view, he ignores the varieties of brain emotional phylogenies that
MacLean recognized first amongst neuroscientists.
While LeDoux criticizes MacLean's general limbic system concept, he
commends his own approach which recognizes that "since different emotions
are involved with different survival functions—defending against danger,
finding food and mates, caring for offspring, and so on—each may well involve
different brain systems that evolved for different reasons. As a result, there may
be not one emotional system in the brain but many" (in Gazzaniga et al. 1998:
516). In response I recommend reading The Triune Brain in Evolution, because
MacLean's approach to the brain and mind distinguishes all these issues with
sophistication and completeness.
LeDoux's contributions to emotional learning have enough importance that
he need not avoid or misrepresent the contributions of others. Yet while he
claims to espouse evolutionary views, he consistently avoids detailing the work
of those who have pursued Darwinian neuroethology more systematically.
Further, while MacLean confronted a central problem of emotion research—the
nature of affective experience—LeDoux makes clear he does not consider
emotional feelings a workable puzzle for brain research, but demeans it as mere
"icing" on the "cake" (LeDoux 1996: 302). Rather, the reflexive response
patterns of unfeeling Cartesian zombies is deemed to be the central problem.
That he has convinced so much of the attentive general readership that he
actually works on understanding the full gamut of emotions, as commonly
understood, represents one of the marketing successes of modern neuroscience.
Investigators of brain and mental function know they face an enormous
challenge in linking psychobehavioral with biological concepts. Anyone courag-
eous enough to accept this challenge realizes that only successive approxi-
mations of affective phenomenological "reality" can be obtained. How unfortun-
ate that investigators who aspire to deal forthrightly with such integrative
problems find their work ignored by colleagues unwilling to sail beyond the safe
harbor of positivistic molecular and neuronal science.
Few have noticed that LeDoux characterizes feelings, the experience of
emotion, as a trivial side-show of consciousness not a main theme neuro-
scientists should try to illuminate. While those interested in consciousness incre-
asingly accept the importance of emotional feelings as a way for the brain to
assign value to world objects and behavioral strategies, LeDoux claims these
issues are epistemologically unworkable and hence ancillary to his own research
into one reflexive, and perhaps largely unconscious, emotional response.
Meanwhile, LeDoux's implicit theory of consciousness is unsophisticated,
relying as it does on a concept of "higher" working memory too little involved
with the Extended Reticulo-Thalamic Activating Systems (ERTAS). The
ERTAS essentially underpins all working memory in a manner much more
widely distributed than the dorsolateral pre-frontal cortex. Likewise, he has
Foreword xix

ignored the importance of Damasio's (1999) basic insight that body mapping
(and by implication, particularly the mapping of the needs of the body in the
environment of evolutionary adaptation) represents a foundation for integrative
neuroscience in general and consciousness studies in particular. Most theories of
attentional functions (prerequisite to working memory) assume that working
memory distills what attentional functions capture in conscious workspace. They
thereby emphasize the importance of a host of subcortical, midline thalamic and
reticular structures structurally very close to the affective core of the brain and
probably inexorably intertwined with such systems.
MacLean put these epistemic concerns at the forefront of his agenda of brain
research; for this reason, many humanists have admired his work. Rather than
conceptualize the fuller complexity of brain substrates of emotionality, LeDoux
chose to "escape from the shackles of subjectivity" (2000: 156). However, in
pursuing the "easily" doable, he employs a series of subtle "sleight of mind"
marketing-type tricks which help many believe he has actually been studying
and encouraging the study of basic emotional processes in the brain, something
rather far from the truth. In his most recent book, LeDoux (2001) lists the
various traditional memory-learning information-processing "tricks" he uses to
study "emotions." Although his traditional memory research program is solid, he
offers no credible new solution to "the emotion problem." To sustain such
Janus-faced posturing, different and more substantive ideas of others must be
ignored and/or suppressed. His studied inattention to actual neuroethological
research implicitly emphasizes such work as irrelevant to emotional processes.
Instead of dealing with substantive empirical and theoretical issues while
criticizing MacLean, LeDoux chooses shallow criticism of subsidiary or surface
issues remarkably easy to caricature. Of course, the same could easily be done
for amygdalar research (Panksepp 2000a: 139-140).
The way MacLean posits the limbic-system little resembles the way LeDoux
abuses the concept. Surely there have been many others who have employed
MacLean's ideas in oversimplified ways, but MacLean used the concept as
biologists might use taxonomic concepts such as genera, kingdoms, etc.—to
partition the complexity of nature. Most evolutionists recognize that such
concepts have no ontological reality—rather they represent "practical kinds"
that conceptualize inquiry more effectively than the positivistic harvesting of
data without guiding theories.
The main practical question about the limbic system concept concerns
whether it pointed effectively toward the main brain areas essential for
emotionality. Overwhelming evidence shows the concept is robustly affirmed,
as through meta-analysis of PET and fMRI imaging of brain arousals during
felt-emotions. Did the limbic concept give us a definitive mechanistic explana-
tion of how emotions emerge from detailed operations of enormous numbers of
neural systems that course through the limbic system? No, it did not. However,
it identified a set of neuronal correlates that must always precede causal studies.
Many investigators who take the expanded limbic neuro-geography seriously
have made enormous advances in characterizing those causes. In this context, it
is worth noting that the most comprehensive PET study of internally
XX Foreword

experienced emotions by Damasio et al. (2000) showed that the amygdala

exhibited no significant arousal except, quite surprisingly, during happiness! In
fact, those brain areas that are aroused during deep human affective experiences
are the ones strongly implicated as causal in neuroethological analyses of
spontaneous animal emotionality (MacLean 1990; Panksepp 1998).
LeDoux has not come to grips with affective experiences and the spontan-
eous emotionality of animals because he studies primarily sensory-perceptual
events that instigate one simple set of unconsciously triggered emotional
reflexes. To convince others that this work has much to do with the brain's
intrinsic evolved capacity for fear, amygdalophilic fear researchers envision
amygdala efferents as mere unconscious response systems—outputs with few
implications for experiential hermeneutics of fearfulness (not to mention other
primary emotions, uniformly ignored). This "mere output" assumption consist-
ently omits consideration of evidence that indicates how these so-called
"outputs" (which, in fact, are integrative systems) are essential for emotional
feelings.
For LeDoux, progress on the mental aspects of brain functions must await
solution of "the mind-body problem" (2000: 156). This represents a problem
(indeed, a neo-dualistic speculation) only if one does not accept emergent
psychological properties arising from complex neural network dynamics.
MacLean's position consistently affirmed the need of neuroscientists to come to
terms with the emergent subjective aspects of many brain functions. He begins
his magnum opus with a discussion of epistemics, the subjective experiences that
can arise from the evolutionary potentials of the brain. MacLean believes this
problem solvable, but most behaviorists and many information-processing
cognitivists consider it either a non-problem or unsolvable. Their nihilism stifles
needed discussion and also, because of the continued hegemony of the
neurobehaviorist counterrevolution, co-opts funding needed for the necessary
inquiries. Remarkably, certain investigators who eschew such issues in their
own work have been able simultaneously to convince the world they in fact
immerse themselves in them.
This, I believe is the crux of the matter: MacLean gives provisional solutions
to a problem most behavioral neuroscientists would rather not address, so they
have marginalized his work. In this battle over paradigmatic issues, I encourage
young investigators to side with those who argue that the role of neuromental
experience in behavioral control represents a substantial part of what the animal
brain does for adaptation to complex physical and social worlds where
unconscious reflexes do not suffice. In fact, the weight of evidence shows
emotionalities represent evolutionarily stable solutions through which values
encoded as global experiential states substantially arise from neural matrices
guiding adaptive instinctive behaviors. Perhaps the most poignant examples
show up in drug addiction.
Most investigators recognize drugs of abuse commandeer natural reward and
punishment functions of the brain organized similarly in mice and humans (Hill
& Newlin 2002). We might well ask would drug addiction exist if drugs did not
change our internal feelingsl Clearly the answer is no—and not only for
Foreword xxi

members of our own species. At this point, the neo-behaviorists (including

LeDoux 2001), commonly trot out the study of Lamb et al. (1991) to highlight
that unconscious reinforcement processes mediate addictive behaviors. Yet this
study did not involve reinforcement. In this cognitively-mediated, fixed-ratio
3000 task a substantial number of subjects felt they were getting some morphine
at the lowest doses, but certainly not enough to get high. This supposedly
unconscious reinforcement process in fact represents nothing more than a
cognitively mediated demand characteristic; because the infusions were so
dilute, Lamb's subjects probably deliberately sought something affectively
unattainable. But the experimenters did not ask simple and sensible questions
about the subjects' motivation! For a more complete analysis, see Panksepp et
al. (2002).
Animals avidly consume these same agents because they probably also
experience brain changes in many distinctly positive ways. These changes yield
to evaluation, to some extent, by state-dependent conditioning paradigms, and
also other measures such as emotional vocalizations (Knutson, Burgdorf &
Panksepp 2002; Panksepp, Knutson & Burgdorf 2002a). This does not imply
nonexistence of vast and unconscious neural properties to support the brain
functions that create feelings. Such unconscious components for emotions exist
in greater abundance than the pieces of an internal combustion engine, and just
as in an automobile, many components must operate together for effective
motility to emerge in the one case and affective urgency in the other. When
many unconscious components work together in the brain to yield system states,
a glimmer of mind begins to emerge. Many reasons point to the ideas that the
first such glimmers in the emergence of consciousness were affective feelings
(Panksepp 2000b, 2002a). Therefore, to marginalize feelings as do the neo-
behaviorists represents a disservice to science as well as to a deep and realistic
respect for animate life. MacLean always conveyed a sincere respect for those
mysteries. He was also most eager to promote research to work out the essential
details. The work of none of MacLean's critics represents that tradition, even
though some "speak" forcefully for a unified mind science (e.g., LeDoux 1999).
MacLean would surely have been more influential on my own research
program had we not been essentially tackling similar issues at the very same
time. Both of us have been intrigued by the nature of separation distress and
playfulness, (me, early in my career and he, toward the end of his laboratory
activities). However, I have always felt his a kindred spirit particularly in his
commitment to deal with the fuller complexity of the many emotional processes
of the brain that the rest of neuroscience was neglecting. Within my intellectual
home of behavioral neuroscience, practically no support existed for research of
that type, a state of affairs, that regrettably persists.
The heart of the paradigmatic battle is: are emotional feelings an important
neuroscientific topic? Those who say yes, as I do, find MacLean a sure and
guiding star. We take the position emotional feelings are thoroughly neurobiolo-
gical in a deep evolutionary sense. Those who are waiting for definitions of such
processes before they begin research, should recognize that they can't be
adequately defined before our inquiries have borne substantive fruit, and that
xxii Foreword

simply can't happen without adequate theories to get well-targeted empirical

inquiries initiated. Those who find no favor with such concerns turn away from
emotive evolution with revulsion, as if the topic were both impolite and
irrelevant (e.g., Blumberg & Sokoloff 2001, and see comments by Panksepp
2002b).
I suspect the animal-rights movement's remarkable success in quelling
research in the United States resulted partly because so many reasonable lay-
people cannot agree with investigators who assert still, as did Descartes, that
nonhuman animals are largely unconscious, unfeeling creatures. Our prolonged
agony with this problem reflects, in part, the continuing tragedy of the
behaviorist tradition that has been unwilling to conceptualize mind and
emotional feelings in neurobiological terms (have the practitioners been unable
to do that because of some alexithymia among scientists? See Panksepp 2000c).
Every neo-behaviorist needs to repeat: Affective experience is a completely
natural emergent product of neurobiological complexity within the mammalian
brain, and at the present stage of our intellectual development it must be
scientifically studied indirectly through testable neurotheoretical inferences.
Overwhelming evidence shows that animal brains elaborate many states of
affective consciousness. Some scholars feel that animal data cannot guide
predictions in humans and claim this ontological position is scientifically
unworkable. If homologous neuromechanisms exist in our brains, those scholars
must be wrong. When we, the brain/mind scientists, fail to take such emotional
perspectives seriously, we support fundamentally narrow-minded and unethical
practices and perspectives. Rather we should continue our behavioral brain
research on other animals with a more coherent and respectful vision of what we
are doing (e.g., see my Affective Neuroscience, pp. 6-7). If our recent findings
hold true, that a primordial form of joyous laughter may be emanating from the
brains of playing and tickled rats, then we may have to rethink many mind
issues (Panksepp & Burgdorf 1999).
So, do other animals experience emotional states? Of course there is no
ultimate " p r o o f in science, merely the weight of evidence. To me it remains a
mystery that certain scientists can ignore the mass of relevant evidence from: (i)
behavioral reinforcement studies, (ii) place preference-aversion studies, (iii)
manifest and ubiquitous emotional vocalizations, (iv) neuroethological studies
evoking emotional behaviors and states from the same human/animal brain
homologs and (v) the coherent translations between human and animal
psychopharmacological work. With evidence like that, the issue of animal
feelings represents more than a mere ontological ambiguity. Rather it
approaches epistemological certainty.
Perhaps I have only caricatured the position of the neo-behaviorists who
populate modern neuroscience, but my own experience tells me otherwise. The
remarkably deep rift in our shared scientific culture humiliates our self-
conception as guardians of the truth in a world where belief and persuasion
generally matter more than evidence. So what do we do with the mountain of
data, both direct and indirect, that animals have affective experiences as a birth
right of the types of brains they and we have inherited? Do we continue to
Foreword xxiii

ignore the weight of evidence, and sustain our uniquely human arrogance about
our place in nature?
LeDoux states (in Gazzaniga et al. 1998: 516): "Many emotions . . . involve
phylogenetically old brain systems that evolved to control the body behaviorally
and physiologically in response to environmental challenges. These systems take
care of things like defense against danger, sexual behavior, maternal behavior,
eating, and other things like this. These are the kinds of emotional systems we
can study in the animal brain" He skillfully avoids addressing the issue of
affect in enunciating this view. In any event, these are the types of systems
MacLean and investigators following in his tradition have long studied using all
the care of standard science. For some of us interested in human emotions, such
studies entail the reasonable corollary that a study of the neural substrates of the
objective natural emotional behaviors of animals can guide us to an
understanding of the ancestral neural sources of human feelings.
A half century ago the field of emotion research needed a preliminary
surveyor to plot the organizational framework for understanding emotions.
MacLean provided a most credible plot, as long as one is willing to absorb it all
with an open mind and appreciate that some needed "corrections" and
elaborations are inevitable (Panksepp 1998). This type of work and thinking can
interface with an understanding of psychiatric issues more readily than any other
pre-clinical strategy that is available. Emotional states probably have phenomen-
ological meaning for all mammals.
In sum, evolved functions of the brain, such as the various emotional
systems, cannot be adequately conceptualized in channel-function information-
processing terms. Additionally needed are concepts that recognize hundreds of
thousands of neurons working spontaneously together to generate organic
pressures for action and feeling within the visceral neural core of animate
existence. In 1949 and 1952 MacLean offered the "limbic system" concept as
the most suitable piece of neuroevolutionary territory wherein we could begin to
investigate emotional systems in earnest. During the ensuing forty years, he
followed his own advice well, and the weight of evidence still affirms he had
surveyed the functional terrain of the brain remarkably accurately.
Let me now re-emphasize a key distinction I have used throughout this
foreword—one all investigators need to consider if interested in the intimate
relations between brain functions and mind. Emotional feelings are not simply
informationally encapsulated "channel functions" of the brain (as Marcel
Mesulam used the term in his Behavioral Neurology). Rather, evolved emotional
systems represent global "state-functions" reliant on complex organic organi-
zation of broadly operating brain systems. Single unit electrophysiological
approaches ideally suited for studying channel functions cannot inform on the
state functions emerging from large ensembles of neurons and supportive
organic processes operating dynamically together to weave the "whole cloth" of
the basic psychobehavioral processes of the brain. To understand neuromental
"organ systems" requires experimental strategies other than single cell
recordings from one brain location; classical stimulus-control paradigms may
not optimally capture the patterned activities of such evolved brain/mind
xxiv Foreword

systems. What is needed are multiple, simultaneous recordings from many brain
sites during spontaneous emotional behaviors, and an integration of those data
with neurogenetic, neurochemical and neuroethological perspectives.
Concurrent electrophysiological and neurochemical studies may provide
great insights using many probes positioned at just the right points within
specific emotional systems (starting in higher regions of the amygdala and
working down to the periaqueductal gray). Increasingly sophisticated EEG and
MEG algorithms may usher in new and insightful neurodynamic measures that
may monitor emotional feelings more directly (e.g., as Walter Freeman's EEG
measurement of chaotic neurodynamics highlighted perceptual processes; see
How the Brain Makes Up Its Mind). The broad anatomies of emotional systems
will expand (like the "limbic system" expanded) as our knowledge ripens from
harvesting the right kinds of facts. No single center for emotions in the brain
exists, contrary to the implications of certain amygdalophiles. The "limbic
system," as originally proposed, simply recognized the major brain territory in
which our empirical confrontation with the diverse circuits for the various
emotional miseries and joys might be most successfully consummated.
MacLean's insight has proven fundamentally correct.
The information-processing metaphor holds more importance for analyzing
the many "channel functions" of the brain that control sensory processes rather
than for understanding the more organic and holistic emotional processes.
Clearly the cognitive revolution oversold "information-processing," at least for
understanding the deeper sources of our emotions and motivations, and perhaps
even the foundations of certain cognitive processes. This unfortunately draws
many young investigators to the comparatively idle pursuit of computing mind
before they gain clear understanding of the global neural underpinnings of
organic action systems that evolution built into the lower reaches of the neuro-
mental apparatus shared with so many other creatures.
Despite heavy investment in behavioristic models of fear-learning and the
associated information processing of conditioned stimuli, investigators should
open their minds to larger evolutionary issues entailed by neuro-ethological and
psycho-ethological state-systems approaches. Traditional perception-to-action
models, with response systems deemed totally unconscious, do not suffice. As
we come to understand the evolved emotional operating systems of the brain,
action-to-perception processes may end up as more important for understanding
the foundations of consciousness than the now dubious promise of cognitive
computationalism (Jerry Fodor 2000, The Mind Does Not Work That Way). In
sum, the evolved "instinctual" action systems that control emotional states of the
brain represent essential targets for study if we wish to understand how
emotional feelings arise within the brain.
MacLean sought to tackle such important issues, and we would have a much
healthier climate for research on the neural basis of emotions if all relevant
approaches could work in some type of consilience rather than the present
competitively fearsome "conformity enforcement." At least animal investigators
now agree emotional behaviors are in the objective realm of traditional science,
while many investigators of human psychology have taken the next step and also
Foreword XXV

agree that affective experiences should be included among the neuroscientific

attributes that need to be clarified. Such aspects of mind should no longer be
deemed unworkable problems, even in other animals (Panksepp et al. 2002a,b).
Indeed, the discovery of apparently homologous neurochemical codes for many
emotional and motivational processes in all mammals, allows us to go from
studies of animal emotional behaviors to a study of human affective experience
(Panksepp 1998, 1999).
Paul MacLean's great contribution was his establishment of a general
paradigm that is more realistic and experimentally more effective than any that
had gone before. As Gardner in this volume emphasizes, this lastingly contri-
buted to our continuing and realistic desire to dock mind-brain functions in
meaningful ways. We will solve the semantically created mind-body problem
gradually by confronting key issues, not by avoiding them.
No, there is no minds cope yet that we can apply to either animals or humans.
Only their behavior is testament to what is happening inside their brains.
Because of that, we have only two options: (1) to deny experiential aspects of
the mind, explicitly or implicitly, to all the other animals (as have all too many
scientists for the past 400 years since Descartes bequeathed us the endless
mischief of mind-body dualism), or (2) to study those neurobiological processes
indirectly in ways theoretically well-guided—quite as particle physicists have
probed inside the atom.
Currently, the most substantive understanding of those emotional processes
has emerged from the type of evolutionarily informed neuroethological work
epitomized in Paul MacLean's approach. He, like all great scientists, fully
understands Descartes' third law of science; that the world is a complex place,
and we cannot make progress unless we simplify, and gradually and through
successive approximations, aspire toward a more comprehensive knowledge.
MacLean also recognizes that to solve the emotion puzzle, work must
conceptually derive from the inside of the system, where core "active organism"
principles are created by evolved state-control systems of the brain/mind. The
puzzle simply will not yield to study of learned surface features (i.e., mere
information-processing). The brain does much more than that.
The chapters of this volume converge from many different perspectives to
demonstrate, with many different strengths, the intellectual force of Paul
MacLean's neuroevolutionary psychobiology. This is an important testimonial
for a neuroscientific paradigm that attempts to deal forthrightly with the full
grandeur and mystery of the neuromental assemblages that makes us the types of
spectacularly complex and difficult creatures that we are. Clearly, the fundamen-
tal nature of affect is a topic of critical importance for understanding our animal
nature.
This volume of essays amplifies the evolutionary interconnected layering of
mind so compellingly envisioned in Paul MacLean's concept of The Triune
Brain in Evolution. The various phylogenetic regressions that can transpire in
the human mental apparatus continue to inform biological psychiatry,
evolutionary psychology, and the philosophy of science. The "natural" black-
jack set of contributions in this volume summarize diverse points of view of a
xxvi Foreword

rich fabric of thought and data. Although chapters vary in depth and other
qualities, none trivializes the core processes that underpin our extremely rich
cognitive apparatus. For those interested in the archeology of mind, and the
tethers that bind us still to the evolutionary adaptations that emerged in "deep
time," this volume will be treasured. We will not understand the emergence of
new mind/brain functions, such as trends for semantically-mediated sociality,
mild-mannered deception as well as scientific Machiavellianism and the
underpinnings of cultural ritual unless we pay our full respects to the older
adaptations upon which our higher mental faculties are grounded.

NOTE
I wish to acknowledge useful comments on earlier versions of this foreword by Russell Gardner,
Anesa Miller, David Pincus, Doug Watt, and Daniel Wilson.

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 ACKNOWLEDGMENTS

The editors wish to thank Seymour Itzkoff, series editor, Dr. James Sabin,
Director of Academic and Research Development, Catherine A. Lyons,
production supervisor, Megan Peckman and Terri M. Jennings, production
editors, Greenwood Publishing Group for their support and guidance in the
production of this book. We are grateful for a grant from Pfizer Corporation in
support of the symposium on the work of Paul MacLean sponsored by the
Across Species Comparisons and Psychopathology Society (ASCAP) held in
Boston, Massachussetts, July 16-17, 1999, the essential proceedings of which
are reported in this volume. We also wish to acknowledge the valuable support
of Suzi Gardner in organizing and producing the Boston symposium. The
production of this book was further supported by a grant from the Center for
Behavioral Ecology, San Jose, California. Tony Tidwell, Alex Bayne, Nicole
Bayne, Abby Bayne and other staff members of the Center were of great support
in the research and preparation of the manuscript.

PERMISSIONS

Valerius Geist generously granted permission to use the quote contained on

page 322.

The editors wish to thank the following publishers for permissions as

indicated:

Elsevier Science for permission to use Tables 10.1 (pp. 172-173), 10.2
(175-177), and 10.3 (178-180) from Pontius, A.A. 1997. "Homicide linked
to moderate repetitive stresses kindling limbic seizures in 14 cases of Limbic
Psychotic Trigger Reaction." Aggression & Violent Behavior, 2: 125-141.

Lippincott, Williams, and Wilkins for permission to reprint Figure 12.2, page
219 (spike and wave EEG seizure discharges) from Mirsky AF, Tecce, JJ:
XXX Acknowledgments

The analysis of visual evoked potentials during spike-and wave EEG

activity. Epilepsia 1968; 9: 211-220.

Little Brown Time Warner Books for permission to reprint Figure 12.3
page 220 (diagram of centrencephalic system) from Jasper, W. and Penfield,
H.H. Epilepsy and the Functional Anatomy of the Human Brain, 1954.

The American Physiological Society for permission to reprint Figure

12.4, page 221 (the ascending reticular activating system) from Lindsley DB:
Attention, consciousness, sleep and wakefulness. In Field J, Magoun HW,
Hall VE (Eds): Handbook of Physiology, Section 1: Neurophysiology,
Volume III Washington, DC: American Physiological Society, 1960, pp.
1553-1593.

Academic Press for permission to use Figure 12.5, page 222 (effect of
electrical stimulation of the brain on visually controlled behavior in the
Macaca mulatto) from Bakay Pragay E, Mirsky AF, Fullerton BC, Oshima
HI, Arnold SW: Effect of electrical stimulation of the brain on visually
controlled (attentive) behavior in the Macaca mulatta. Experimental
Neurology 1975; 49: 203-220.

Kluwer Academic for permission to use Figure 12.6, page 223

(frequency histograms of task-related neuronal activity in single cells in the
monkey) from Mirsky AF, Duncan CC: Behavioral and electrophysiological
studies of absence epilepsy. In Avoli N, Gloor P, Kostopoulos G, Naquet R
(Eds): Generalized Epilepsy: Neurobiological Approaches. New York:
Plenum, 1990, pp. 254-269.

Kluwer Academic for permission to use Figure 12.7, page 224 (semi-
schematic representation of attention system of human brain) from Mirsky
AF, Anthony BJ, Duncan CC, Ahearn MB, Kellam SG: Analysis of the
elements of attention: A neuropsychological approach. Neuropsychology
Review 1991; 2: 109-145.
 INTRODUCTION

Paul MacLean, a trailblazer in evolutionary brain science, profoundly influenced

medical neuroscience over the last half of the twentieth century. His concepts of
the limbic system and the triune brain, deriving from an evolutionary perspec-
tive, helped biological psychiatry emerge and provided a framework and
impetus for linking brain science with social theory and moral consciousness. In
mainstream academic neuroscience, however, his work has been largely over-
looked or ignored. Amazingly, his seminal work has not even been acknow-
ledged in the newly popular primarily anthropological approach of evolutionary
psychology. Major works in mainstream evolutionary psychology contain no
references whatsoever to MacLean's work. Yet, MacLean is surely among the
most eminent and original thinkers in evolutionary neuroscience, so this
omission by researchers in evolutionary psychology is indeed glaring and
unfortunate for the health and progress of this subset of the discipline. Panksepp
and Panksepp (2000) have recently discussed in detail several of the problems
resulting from evolutionary psychology's failure to consider long-established
research findings from cross-species research in brain science.
Antonio Damasio, in his book The Feeling of What Happens (1999: 38-42)
calls attention to the root problem. Accompanying the curious scientific neglect
of emotion (in favor of cognition) in mainstream neuroscience, he cites a
parallel neglect of three other important aspects that should be central to the
study of neuroscience: (1) neglect of an evolutionary perspective, (2) neglect of
the concept of homeostasis, and (3) neglect of the concept of the organism as a
whole. Paul MacLean's work, among others, notably integrates all the lacking
elements cited by Damasio. Damasio recognizes this.
Working to correct this neglect by mainstream neuroscience and evolu-
tionary psychology, this book reports selected papers from the proceedings of a
symposium held July 16-17, 1999, in Boston, Massachussetts, to assess the
convergences and frontiers, motivated by MacLean and others' related research
and theory, across a multidisciplinary spectrum ranging from molecular
Introduction xxxii

neurobiology, clinical psychotherapy, cognitive neuroscience, through emerging

linkages in social and economic theory.
The first chapter by Karl Pribram, an early colleague of MacLean, helps to
set a historical perspective and suggests some of the controversies that have
shaped in part the discussions within neuroscience for the most recent five
decades. The two pioneers had a dialectical collaboration characterized by
alternating periods of conflict and convergence. As Pribram notes, their inter-
locking history provides a window on the scientific process, where differences
in perspective, style, and technical focus make a difference in how problems are
approached and how results are interpreted. Three essential differences seem to
stand out between the two men. (1) Reductionism versus integration. This is the
issue of the organism as a whole cited by Damasio. MacLean moves between
reductive, fine-grained research and an ambitious level of integration in
interpretation of results, whereas Pribram remains largely at a more focused,
fine-grained reductive approach. (2) Evolutionary approach versus the
structural/functional perspective (that parallels a deficit cited by Damasio).
MacLean clearly prefers an evolutionary approach; Pribram, seemingly a
functional anatomical one. (3) MacLean contemplates subjective experience and
emotion, whereas Pribram more usually inclines toward a cognitive and
objective position. The differences in perspective of the two men, in a manner,
anticipated (and perhaps contributed to) the divergences characterizing the
neuroscience community for the succeeding five decades. Some of these
legitimate differences, reflecting alternative perspectives requiring future
convergence, later became distorted by others through unreflective and
unexamined repetition.
Such distorted divergences occupy the chapter by Gerald Cory. Cory
appraises MacLean's triune brain concept in response to a rather inept and
unfortunate review of MacLean's landmark opus, The Triune Brain in
Evolution: Role in Paleocerebral Functions (1990). This review appeared in
Science (Oct 12, 1990) and inaccurately reported and somewhat caricatured
MacLean's work. This red flag review unjustifiably inhibited the use of
MacLean's important contributions by other scholars and contributed to the
further neglect of an evolutionary perspective as well as the study of emotion.
The inhibiting effect of this review article, and others that uncritically followed
it, especially impacted scholars in cognitive studies, evolutionary psychology,
and the other social sciences, who were unable to independently evaluate the
controversy. As a notable example, cognitive scientist Steven Pinker in his How
the Mind Works (1997) rejects and in the process presents an extraordinary
caricature of MacLean's position based on a single reference to the defective
review in Science. If he had consulted MacLean's work closely, Pinker may
have found it solidly underpinning his own evolving thought. Following a
detailed rebuttal of the Science review, Cory's chapter concludes that
MacLean's work is soundly grounded in evolutionary neuroscience and provides
the best foundation in neuroscience yet articulated for application to the
essential issues of cognitive science and evolutionary psychology as well as
other social sciences.
Introduction xxxiv

an important adaptive function. Daniel Wilson's paper reconciles manic-

depression with triunian neuroethology via a review and analysis of both manic-
depression and the triune brain theory with respect to (1) relevant evolutionary
epidemiology, and (2) consilience with game theoretic models.
The next three chapters take different clinical directions. James Harris
discusses the development of the essential human quality of empathy and its
failure to emerge in the disorder of autism. Harris accounts for both empathy
and autism in terms of integration of the triune brain. In autistic disorder, failure
of the development of limbic structures (amygdala, hippocampus) and cerebel-
lum may cause a failure in empathy. Anneliese Pontius' chapter focuses on a
specific neurophysiological dysfunction, which she proposes to call limbic
psychotic trigger reaction. Seizures associated with this reaction have been
triggers to apparently motiveless homicides. She discusses how MacLean's
evolutionary model of brain organization led to the insights that identified this
previously unexplained clinical phenomenon.
Glenn Weisfeld's chapter in several respects ties together the clinical picture
for an evolutionary psychiatry. He begins by acknowledging that the study of
comparative neuroanatomy makes clear that motivated behaviors evolved earlier
than complex cognitive capacities. As MacLean has repeatedly emphasized, the
brain stem, basal ganglia, and limbic system predated the neocortical expansion.
He then outlines the role of the prefrontal lobes in pride and shame as well as in
the mediating of complex social behavior.
The chapter by Allan Mirsky and Connie Duncan shifts from depression,
dysfunction, and emotion to the important complementary issue of attention.
Modern concepts have moved from the earlier notions of attention as a single
monolithic function to conceiving of it as a group of behaviors, each defined
separately with a specifically articulated function for the organism. Some
theorists have posited that each specific function depends on the integrity of a
distinct brain region, even though in the intact brain, the regions form an
integrated system. Mirsky and Duncan propose a heuristic model of attention,
derived in large part from neuropsychological data from patients with seizures
or other neurospsychiatric disorders. They hold that MacLean's triune concept
provides a remarkable armature upon which to build a concept of the organiza-
tion and development of attentional functions from the evolutionary point of
view.
The next three chapters offer differing perspectives. James Brody thought-
fully integrates Stuart Kauffman's triadic concepts in statistical physics with
MacLean's triune evolutionary model. Brody derives interesting parallels sug-
gesting that physical constraints promote binary and tertiary models. He also
links concepts from physics and evolutionary theory to clarify clinical diagnostic
theory and practice. Seymour Itzkoff argues for a perspective on vertebrate, and
especially mammalian brain evolution, led not by lower brain regions but by the
shaping effect of emerging neocortical centers. In this, he reverses the traditional
perspective that focuses on the selective prominence of the striatal and limbic
complexes. Itzkoff s analysis reminds us that the evidence can also be inter-
preted in a top-down fashion or at least in a more interactive manner. The
xxxiii Introduction

The chapter by C.U.M. Smith deals with the new findings in developmental
evolutionary biology and molecular genetics. These new fields provide insights
into the evolutionary process, which is characterized by a remarkable mix of
conservation and divergence in brain evolution as well as body plans and other
features. Smith relates these exciting new discoveries to the evolutionary
perspective of MacLean, which emphasized the conservation of ancient brain
structures as well as the variation emanating therefrom in the phylogenetic
history of change, leading toward the full evolution of the human brain. Smith
emphasizes especially the continuities in the development of the visual system.
The chapter by Neil Greenberg, who early worked with MacLean on the
striatal system in lizards, updates that earlier work with new findings that extend
our understanding of this portion of our neural architecture, already prominent in
reptiles ancestral to present-day mammals and, indeed, humans. In keeping with
MacLean's earlier insights, the striatal complex (MacLean's protoreptilian
complex) demonstrably affects and organizes not only motor behavior, but the
sequencing of complex behavior, including language and cognition. This is also
emphasized by Philip Lieberman in Human Language and Our Reptilian Brain
(2000).
Russell Gardner, Jr.'s chapter appropriately provides the foundation for a
two-part focus on clinical theory and applications. Gardner draws upon the new
findings discussed in the previous chapters to address the current lack of a
satisfactory framework for psychiatry and the related helping sciences. Gardner
sees MacLean's emphasis on social behaviors that stemmed from adaptations
originating in deep time as a impetus for a revival of MacLean's influence.
Results from data generated by the genome project, as well as other genetic and
brain research, combine with the need of psychiatry and related disciplines to
connect brain actions with normal human communicative behavior. This con-
vergence leads Gardner to the idea that psychiatry's basic science should be
designated sociophysiology. He concludes that the social brain concept allows
psychiatry and its allied clinical disciplines to utilize pathogenesis in a manner
parallel to practice in other specialties.
The next three chapters apply triune theory to the theoretical and applied
study of clinical depression. John Price applies the triune model to early
vertebrate escalation and de-escalation (fight/submission) strategies. The paleo-
mammalian, or limbic emotional centers add intense emotional tone to these
strategies including the anger, exhilaration, and rage of the escalation strategy
and the fear, depression, shame, and guilt of de-escalation. The neomammalian
or higher cortical structures bring conscious, rational decision to fight or to
submit. Depressive illness may result from conflict between the newer and older
centers.
Leon Sloman discusses the social competition model of depression to clarify
the evolutionary and communicative function of subordinate mechanisms that
contribute to psychological and biological features of depression. Within a
context inclusive of other models, such as attachment theory, discrete emotion
theory, and cognitive behavior therapy, variations in self-esteem and mood
fluctuations reflect the operation of genetically programmed mechanisms with
XXXV Introduction

chapter by Roger Masters, like that of Pontius provides a very specific, although
different focus. Applying findings of evolutionary neuroscience to social theory
and policy, he reports new information on how environmental pollution by
heavy metals affects evolved neural architecture of the human central nervous
system. Introduction of these heavy elements into the environment by modern
industrialized and technological civilization factors importantly in causing
behavioral abnormalities, including violence and learning deficits. Since these
important social effects can only be properly understood by a full appreciation
of the advances in evolutionary neuroscience, Masters concludes by calling for
an end to academic isolation between the natural and the social sciences.
Following this challenge by Masters, albeit at a different level of integration,
the next four chapters also move to a convergence between neural architecture
and social interactions. Steven Peterson's chapter opens this section with a
discussion of the connection between ancient brain structures and the socially
and politically significant phenomena of reification and hegemony. He shows
how MacLean's research provides valuable insight for understanding the
biological roots of these human social tendencies. Kent Bailey's paper
represents his most current application of phylogenetic regression-progression
theory. Building on MacLean's three levels of the brain (neocortical, paleo-
mammalian, and reptilian), Bailey's theory postulates that human experience, at
any given moment, is the product of the dynamic interplay of newer progressive
(neocortical) tendencies with older and often more urgent regressive ones. The
theory postulates that regression is inherently pleasurable, easily stimulated, and
reflects a loss or diminution of higher cortical controls linked to inhibition by
social enculturation. Bailey applies his model to explicating the recent school
tragedy at Littleton, Colorado.
Gerald Cory's chapter uses the dynamic interaction of MacLean's three-level
concept to develop reciprocal algorithms of behavior, based upon the tug and
pull of ego and empathy, neocortical representations of early vertebrate self-
preservational programming, and later evolved mammalian affectional program-
ming. Cory argues for the shaping effect of this neural architecture upon social
exchange, economics, and political institutions. The chapter by Daniel Levine
and Nilendu Jani applies contributions from the perspective of neural and
cognitive modeling to triunian theory. They construct and report preliminary
testing of a neural network model that simulates the dynamic interaction of the
ego-empathy reciprocal algorithm. Inclusively, the three chapters show potential
for convergence toward a multidimensional model of individual and social
interaction.
The concluding chapter sums up the several convergences indicated by the
previous chapters, assesses the current state of MacLean's contribution, and
focuses appropriate questions toward the frontiers of research and theory.

REFERENCES

Damasio, A. (1999) The Feeling of What Happens. NY: Harcourt, Inc.

Introduction xxxvi

Lieberman, P. (2000). Human Language and Our Reptilian Brain. Cambridge, MA:
Harvard University Press.
MacLean, P. D. (1990) The Triune Brain in Evolution: Role in Paleocerebral Functions.
NY: Plenum.
Panksepp, Jaak and Jules B. Panksepp. (2000). "The Seven Sins of Evolutionary
Psychology." Pp. 108-131 in Evolution and Cognition. Vol 6, No 2.
Science. 1990. Review of MacLean's The Triune Brain in Evolution V. 250 (Oct 12),
303-305.
 PARTI

PERSPECTIVES
 1

PRIBRAM A N D M A C L E A N
IN PERSPECTIVE

Karl H. Pribram

Shortly after accepting a position at Yale University in 1948 in John Fulton's

u
department of physiology as director of a lobotomy project" sponsored by the
Veteran's Administration, I was for the first time introduced to the politics of
academe. Politics at Yale were serious. Yale is a prestigious university and
therefore attracts ambitious individuals—that included me. But I was totally
unprepared for what I had to deal with. At one time I wrote Karl Lashley for
advice. His reply was simple: "You need to decide whether you want to do
politics or do science." I chose to do science.
The politics arose from my initial success in relating frontal lobe anatomy,
physiology, and behavior to the limbic forebrain (Fulton, Pribram, Stevenson &
Wall 1949; Kaada, Pribram & Epstein 1949; Pribram, Lennox & Dunsmore
1950; Lennox, Dunsmore, Epstein & Pribram 1950, reviewed by Pribram 1954,
1961). As a result, pressure was put on me and on John Fulton by the Veterans
Administration to add personnel to the project. As a result, among those who
joined the project was Paul MacLean, who had obtained his M.D. and was
taking a postdoctoral year at the Massachusetts General Hospital. He had asked
to come to Yale because we were doing just the kind of work he was interested
in.
My colleagues warned me that the newcomers would take over and that they
would usurp our carefully initiated research. They predicted that MacLean
would be known for the anatomical and physiological research on the limbic
forebrain, and that the psychologists would assert their territorial prerogative on
the neurobehavioral studies of the frontal and temporal lobes. I heeded Lashley's
advice and concentrated on the research, but this was not easy. I informed
Fulton when he returned from Europe of what I had been told and that I felt that
we should go ahead with the new appointments despite these dire predictions.
Trained psychologists would certainly be a great help in enlisting the advice and
cooperation of the excellent people in the psychology department and Paul
4 The Evolutionary Neuroethology of Paul MacLean

MacLean's interests and mine were so compatible that I was sure it would be a
joy to have him collaborate.
MacLean and I did a series of experiments together. He was a delightful
companion, and it was a joyous experience all around. We continued the
chemical stimulation studies begun by Warren McCulloch, Gerhardt Bonin and
Percival Bailey, concentrating on the medial and basal cortex which they had
not been able to reach (MacLean & Pribram 1953; Pribram & MacLean 1953).
We worked with monkeys, with acallosal opossums (they really smelled awful),
and found the cortical region (orbitofrontal and perirhinal) excited by electrical
stimulation of the vagus nerve. But then, when it came to writing up our results,
we encountered great difficulty. MacLean's gift for naming, though often useful
in promoting ideas, seemed to me to be applied rather rashly: The term "limbic"
used by Paul Broca (his Grande Lobe Limbique) was at that time restricted to
the cortex of the cingulate gyrus. My friend and mentor Jerzy Rose was dead set
against extending the term to the entire mediobasal rim of the hemisphere.
MacLean's persuasion won the day, and I happily supported his enterprise since
I had shown a commonality of physiological effects from electrical stimulation
of the entire region and a commonality of effects on behavior from resections of
the variety of anatomical structures that comprised the Grande Lobe (Pribram
1954; Pribram 1958a; Pribram & Bagshaw 1953; Pribram & Fulton 1954;
Pribram & Kruger 1954).
Another term that MacLean coined was the "schizophysiology" of cortical
processing. This term was based on the finding we obtained using strychnine
neuronography: Although much of the neocortex had an input to the hippo-
campus, there was apparently no direct output from the hippocampus to the
neocortex. This was an important finding, which I have used recently in trying
to model the functions in learning of the hippocampus. The term schizo-
physiology never attained the recognition it deserved, partly because chemical
stimulation of the cortex, that is, strychnine neuronography, went out of fashion.
But all did not go so smoothly with the term "visceral brain." On the basis of
the work that Livingston, Ward, Kaada, Epstein and I had done to show that
electrical excitation of the mediobasal cortex produced changes in respiratory
and heart rate, in blood pressure (and later in gastrointestinal activity), MacLean
coined the term the "visceral" brain to apply to the limbic forebrain. This reson-
ated with established views.
James Papez had pronounced his famous (limbic) circuit to be responsible
for emotions. William James had popularized the James-Lange theory that
emotions were due to feedback to the brain from the viscera when they were
engaged by a stimulating event. Walter Cannon and P. Bard had critiqued
James' theory and replaced it with a thalamic theory. Lashley had critiqued the
Cannon-Bard theory as similarly flawed. Papez and MacLean came to the
rescue: The limbic system, not the thalamus nor the viscera per se, was
responsible for our emotions—though both (hypo)thalamus and viscera are
critically involved because of their connections to the limbic brain.
Pribram and MacLean in Perspective 5

But I had reservations. These stemmed from a patient I had described who
had localized seizures of sweating (a viscero-autonomic response) induced by a
localized tumor in the classical precentral motor cortex (Bucy & Pribram 1943).
I had enlisted Patrick Wall to use the same stimulation technique I had used
to map the mediobasal (limbic) motor cortex to map viscero-autonomic
responses from the lateral cortex. We aimed to discern whether the lateral and
mediobasal responses could be distinguished as to which were more para-
sympathetic and which were more sympathetic. We were unable to make such a
distinction, but the experiments did demonstrate that the mediobasal motor
cortex is not the exclusive cortical regulator of the viscero-autonomic system
(Wall & Pribram 1950). In fact, our data supported Papez's view that emotions
were attitudes that involved the entire body, including the somatic as well as the
visceral musculature.
The lack of exclusivity of viscero-autonomic control by the mediobasal
cortex made it inappropriate to call the limbic forebrain a visceral brain. Nor
could I go along with the uncritical acceptance of the James-Lange viscerally
based theory of emotions. MacLean and I agreed to seriously disagree on this
point and did so publicly on several occasions.
Some years later, my experiments discovered the importance of the amyg-
dala to the habituation of the orienting response. My colleague Muriel Bagshaw
and I used visceral and autonomic indicators and showed that when viscero-
autonomic activity failed to be involved in generalized orienting, the response
failed to become habituated (Bagshaw, Kimble & Pribram 1965; Kimble,
Bagshaw & Pribram 1965; Pribram, Reitz, McNeil & Spevack 1979). Orienting
to novelty was, as the experiments of Eugene Sokolov had shown, due to a
mismatch between an established representation of the familiar, a neuronal
model, and the current sensory input. (Sokolov and Luria had visited my new
laboratories at Stanford University when I received an appointment there in
1959.) MacLean's intuition was not so far off after all. However, viscero-
autonomic processing had more to do with the familiarization and valuation of
episodes of experience based on familiarity, a kind of memory process, than it
has to do with emotional feeling per se.
By the end of the 1970s, I endorsed Nina Bull's attitude theory of emotions
to which Lashley had alerted me. I found out her theory was also supported by
James Papez in a chapter of her book (Bull 1951/1968). The attitude theory's
biological base included not only visceral manifestations but also endocrine and,
importantly, somatic muscular responses to social and other environmental
situations, and therefore practically the entire brain (Pribram 1970, 1980).
Another and perhaps the most widely known "name" that MacLean proposed
is that of the triune brain. The idea for a division of the brain into a core, a
limbic, and a neo- set of systems came about after World War II. Before that
time the techniques available divided the central nervous system horizontally:
spinal, brain stem, isolated forebrain and decorticated preparations were
ordinarily studied. By contrast, during the 1940s and 1950s, three groups of
investigators began to study the brain "from the inside out." Magoun and
Lindsley, first at Northwestern University in Chicago and then at the University
6 The Evolutionary Neuroethology of Paul MacLean

of California in Los Angeles, dropped electrodes into the reticular formation of

the brain stem and stimulated as well as lesioned this core system. The concept
of a reticular activating system as distinct from a "shell" of sensory-motor relays
emerged and became the focus of a number of popular explanations of mind-
brain relationships.
At the Montreal Neurological Institute, Wilder Penfield and Herbert Jasper
studied "recruiting" of rhythmic bursts of forebrain electrical activity by stimu-
lation of the midline and intralaminar nuclei of the diencephalon. The results led
them to propose a "centrencephalic locus" for management of mental function-
ing.
Finally, at Yale I developed surgical techniques to expose the medial and
basal surfaces of the forebrain so that we could (1) electrically and (2)
chemically stimulate these limbic formations to (3) record electrically from them
and to (4) resect them to study the effects of such resections on the behavior of
nonhuman primates. MacLean joined me in the chemical stimulation experi-
ments which, as noted, provided basic insights into the relationship between the
convexal and frontal cortex with limbic formations. I reviewed these studies in
1960 in the Annual Review of Psychology (Pribram 1960). MacLean added to
the conceptualizations derived from these studies by bringing to bear phylogen-
etic considerations. In this he was in tune with the earlier pre-war theorizing
with an added emphasis on the structures of the limbic forebrain.
It is with respect to the naming of the three parts of the "triune brain" that I
could not agree: Reptilian (later called the R complex), Mammalian and Primate
capture what MacLean meant it to—phylogenetic "growth spurts" in brain
development. At the same time, however, the names hide two important aspects
of brain phylogenetic development: innovative origin and current endpoint.
Major innovations occurred in amphibians as they adapted to life on land. It is
these innovations that subsequently make up the R complex. C. Judson Herrick
in his book on The Brain of the Tiger Salamander chronicles these innovations.
The origins of limbic structures, both archi- and paleo-structures, actually
antedate some of those in the R complex—e.g., elasmobranch fishes (sharks)
already possess rudimentary hippocampal tissues. As to current development,
each of the parts of the triune brain have neo-accretions. The outermost parts of
the basal ganglia—those giving rise to the cellular migrations that form adjacent
areas of cortex have been implicated in behavioral processes similar to those of
the overlying cortex; e.g., trial unique tasks for anterior frontal cortex and the
head of the caudate nucleus; visual discrimination tasks for the inferotemporal
cortex and the underlying putamen (see review in Pribram 1991, Lectures 7 &
10).
Each of the structures of the limbic forebrain also has neo-accretions with
regard to their involvement in behavior. Anatomically these paralimbic neocort-
ical accretions make up the juxallocortex. I reviewed these anatomical, physio-
logical and behavioral data in several publications during the 1950s (Pribram
1958a; Pribram 1958b; Pribram 1961; Pribram & Kruger 1954).
In summary, there is good reason to partition the brain from inside out.
However, when it comes to the relationship of core, mid, and outer parts to
Pribram and MacLean in Perspective 7

behavior, the segmentation is more appropriate to a division between extero-

ceptive, somatic and hedonic with all of the parts partaking of each division. The
further out from the core, the more refined (discriminable) the processes that are
involved.
The MacLean-Pribram collaborations, both agreements and divergences,
provide an excellent window on the scientific process. Differences in aptitude,
style, and technical facility make for differences in how problems are approach-
ed and how results are interpreted. Historically the Pasteur-Koch confrontations
and those of Freud and Jung have been well documented. What I believe has
been different in the MacLean-Pribram adventures is that Paul, through his
charm and graciousness, has made it possible for us to remain friends despite
what have often been painful differences. Over a lifetime we have been proved
pretty much even in who's "right" and who's "wrong." In closing, it appears
from MacLean's recent writings (the past decade) endorsing ideas such as
quantum neurodynamics (MacLean 1990, 1997) and mine (Pribram 1971, 1991,
1999) that we have reached the same way of thinking about what has concerned
us most—how brain processes contribute to our conscious experience.

REFERENCES

Bagshaw, M. H., Kimble, D. P. & Pribram, K. H. (1965) The GSR of monkeys during
orienting and habituation after ablation of the amygdala, hippocampus and
inferotemporal cortex. Neuropsychologia, 11, pp. 111-119.
Bucy, P. C. & Pribram, K. H. (1943) Localized sweating as part of a localized convulsive
seizure. Archives of Neurology & Psychiatry, 50, pp. 456-461.
Bull, N. (1951/1968) The Attitude Theory of Emotion. Nervous and Mental Disease
Monographs Series, No. 81. NY: Johnson Reprint Corporation.
Fulton, J. F., Pribram, K. H., Stevenson, J. A. F., & Wall, P. (1949) Interrelations
between orbital gyrus, insula, temporal tip and anterior cingulate gyrus. Transactions
of the American Neurological Association, pp. 175-179.
Kaada, B. R., Pribram, K. H. & Epstein, J. A. (1949) Respiratory and vascular responses
in monkeys from temporal pole, insula, orbital surface and consulate gyrus. Journal
of Neurophysiology, 12, pp. 347-356.
Kimble, D. P., Bagshaw, M. H. & Pribram, K. H. (1965) The GSR of monkeys during
orienting and habituation after selective partial ablations of cingulate and frontal
cortex. Neuropsychologia, 3, pp. 121-128.
Lennox, M. A., Dunsmore, R. H., Epstein, K. A., & Pribram, K. H. (1950) Electrocor-
ticographic effects of stimulation of posterior orbital, temporal, and cingulate areas of
Macaca Mulatta. Journal of Neurophysiology, 13, pp. 383-388.
MacLean, P. D. (1990) The Triune Brain in Evolution: Role in Paleocerebral Functions.
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MacLean, P. D. (1997) The brain and subjective experience: Question of multilevel role
of resonance. The Journal of Mind and Behavior, Vol. 18, Nos. 2 & 3, pp. 247 [145]
268 [166].
MacLean, P. D. & Pribram, K. H. (1953) Neuronographic analysis of medial and basal
cerebral cortex. I. Cat. Journal of Neurophysiology, 16, pp. 312-323.
Pribram, K. H. (1954) Concerning three rhinencephalic systems. Electroencephalo-
graphy & Clinical Neurophysiology, 6, pp. 708-709.
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Pribram, K. H. (1958a) Comparative neurology and the evolution of behavior. In A. Roe

& G. G. Simpson (Eds.), Behavior and Evolution. New Haven: Yale University Press,
pp. 140-164.
Pribram, K. H. (1958b) Neocortical function in behavior. In H. F. Harlow & C. N.
Woolsey (Eds.), Biological and biochemical bases of behavior. Madison: University
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Pribram, K. H. (1960) A review of theory in physiological psychology. Annual Review of
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Pribram, K. H. (1970) Feelings as monitors. In M. B. Arnold (Ed.), Feelings and
Emotions. NY: Academic Press, pp. 41-53.
Pribram, K. H. (1980) The biology of emotions and other feelings. In R. Plutchik & H.
Kellerman (Eds.), Emotion: Theory, Research & Experience, Vol. 1: Theories of
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Pribram, K. H. (1971) Languages of the Brain: Experimental Paradoxes and Principles
in Neuropsychology. Englewood Cliffs, NJ: Prentice-Hall; Monterey, CA: Brooks/
Cole, 1977; NY: Brandon House, 1982.
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Processing. Mahwah, NJ: Lawrence Erlbaum Associates.
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Pribram, K. H. & Fulton, J. F. (1954) An experimental critique of the effects of anterior
cingulate ablations in monkey. Brain, 77, pp. 34-44.
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York Academy of Science, 54, pp. 109-138.
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orbito-fronto-temporal limbic and hippocampal areas of Macaca mulatta. Journal of
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cerebral cortex. II. Monkey. Journal of Neurophysiology, 16, pp. 324-340.
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lectomy on orienting and classical conditioning. Pavlovian Journal of Biological
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Wall, P. D. & Pribram, K. H. (1950) Trigeminal neurotomy and blood pressure responses
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physiology, 13, pp. 409-412.
 2

REAPPRAISING M A C L E A N ' S TRIUNE

B R A I N CONCEPT

Gerald A. Cory, Jr.

INTRODUCTION

Paul D. MacLean is a scientific thinker well ahead of his time. Following his
deeply held interest in the larger questions of human life, he started out studying
philosophy. Being unable to find satisfactory answers to questions such as the
origin and meaning of life—why humans in spite of their unrivaled intelligence
often behaved in seemingly irrational ways threatening their individual as well
as species survival—he turned to medicine and the study of the human brain.
He anticipated the brain, as the biological substrate of these behaviors, held the
key to better understanding of these fundamental questions as well as hopefully
their answers.
MacLean was, for many years, chief of the Laboratory of Brain Evolution
and Behavior of the National Institute of Mental Health. In 1952, drawing upon
the nineteenth century French scientist Paul Broca's designation of the great
limbic node that surrounded the brain stem of mammals, he introduced the
conceptual term "limbic system" into the neuroscientific literature. In 1968 he
introduced the concept of the triune brain, which became widely popularized
after the publication of Carl Sagan's rather overly dramatic and simplified
discussion of it in The Dragons of Eden (1977). MacLean, further developing
the triune brain concept, which aroused great interest in psychiatry, education,
and the lay public, produced his detailed and highly documented volume, The
Triune Brain in Evolution: Role in Paleocerebral Functions in 1990.
10 The Evolutionary Neuroethology of Paul MacLean

THE TRIUNE BRAIN CONCEPT AND ITS CRITICS

MacLean's triune brain concept has been acknowledged the single most
influential idea in neuroscience since World War II (e.g., Durant in Harrington
1992: 268). Nevertheless, following the publication of his 1990 opus, MacLean
received highly critical reviews in two prominent science periodicals, Science
(October 12, 1990: 303-305) and American Scientist (September-October 1992:
497^498). Both reviews were written by neurobiologists who claimed that
MacLean's triune brain concept has had limited acceptance or been largely
1
ignored by professional neurobiologists.
Anton Reiner, at that time a recent graduate, wrote the Science review, the
more extensive of the two. After initially recognizing MacLean as a trailblazer
of neuroscience, whose triune brain concept has been well-received outside the
field of brain research, as the centerpiece of Sagan's popular, The Dragons of
Eden, and frequently as the only discussion of brain evolution in psychiatry and
psychology textbooks, Reiner makes several points critical of the triune brain
concept.
He notes firstly that since MacLean introduced the concept, there has been
tremendous growth in neuroscientific research that has greatly extended our
knowledge of brain function and evolution. This statement carries the general
implication, which Reiner later makes explicit, that the concept is out of date.
Second, in initiating a criticism of MacLean's concept of the limbic system,
Reiner writes: "MacLean's presentation of the role of the hippocampus in limbic
functions is not well reconciled with the current evidence that the hippocampus
plays a role in memory" (1990: 304).
Third, Reiner contends that current research indicates that MacLean's repti-
lian complex is not a reptilian invention but seems to be present in vertebrates
all the way back to jawless fishes.
Fourth, Reiner asserts that MacLean overreaches the evidence when he
claims that the basal ganglia are the neural seat for the control of species-typical
types of behaviors.
Fifth, Reiner states that the limbic system, a widely used term MacLean
authored as a pioneer neuroresearcher, is not properly represented by MacLean.
Contrary to MacLean, as Reiner would have it, the limbic system did not appear
first in early mammals. Amphibians, reptiles, and birds also have limbic features
such as the septum, amygdala, a different-looking hippocampal complex, and
maybe even a cingulate cortex.
Sixth, Reiner maintains that MacLean assigns the functions of parental
behavior, which Reiner claims that MacLean regards as uniquely mammalian, to
the mammalian cingulate cortex, ignoring the fact that some reptiles (croco-
diles), all birds, and possibly even some extinct reptiles (dinosaurs) also engaged
in parental behavior.
Seventh, Reiner makes a couple of other criticisms of MacLean concerning
(a) his preference for correspondence over the more evolutionarily appropriate
concept of homology and (b) his apparently uncritical acceptance of Haeckel's
idea that ontogeny recapitulates phylogeny.
Reappraising MacLean's Triune Brain Concept

Finally, although Reiner praises MacLean's motives and acknowledges the

appeal of the triune brain concept for dealing with "big" behaviors that we are
all interested in, such as: "How does our animal heritage affect our behavior?
Why do we do the things we do? Why can we not live together more harmoni-
ously?," he feels that there are some telling shortcomings, as recited above, in
MacLean's scholarship. He concludes that "neuroscience research can (empha-
sis mine) shed light" on these important human questions, "though perhaps
(emphasis mine) not in as global and simple a way as MacLean has
sought"(1990: 305).

CRITIQUING THE SCIENCE CRITIQUE

Book reviews because of their very nature are usually overly brief and
usually cannot deal in depth with the points they take issue with. Reviewers,
then, are often themselves guilty of the same kinds of oversimplifications and
misinterpretations that they seek to expose in their reviews. When Reiner states
"I strongly believe the triune-brain idea to be wrong," he is caught up in the
same oversimplifying tendency that he claims unjustifiably to find troublesome
in MacLean.
The triune brain concept may be wrong in some of its particulars, right in
others, but still be very useful and valid in its more general features. After all, at
this stage of our knowledge of the brain, although it is quite advanced over the
1960s and 1970s, there are not a great number of things we can say with
absolute confidence—very few generalizations that are without arguable inter-
pretations of more detailed research data. Further, Reiner takes apart but does
not offer a replacement generalization. His analysis is destructive, not construc-
tive. This type of analysis is the easy part of the job. Almost anybody can do it.
However in his apparent eagerness to discredit and take apart MacLean's
useful generalization, Reiner also fails to study his subject closely and therefore
engages in some very careless scholarship. He makes significant omissions,
outright errors, and substantial misrepresentations of MacLean's work. Let's
look at the points Reiner raises one by one.
1. Reiner blatantly misstates the facts when he claims that the triune brain
concept as well as MacLean's book are outdated and lack up-to-date document-
ation. Reiner's first point (i.e., that there has been a great growth in knowledge
about the brain since MacLean first announced his triune brain concept in the
1960s and 1970s) implies that MacLean has left the concept untouched and
undocumented since that time and has therefore not considered any of the more
recent findings. The implications of this statement are belied by the currency of
research cited by MacLean and included in his discussions. To back up his case
for the alleged outdated ideas and data in the book, Reiner baldly states "only a
handful of papers from the '80s' are cited" (Reiner 1990: 305). This categor-
ically false statement is easily contradicted by a count of bibliographic items.
The bibliography of this work contains over 180 entries (a big handful indeed!)
that date from 1980 to at least 1988 and over 220 entries that date between 1975
12 The Evolutionary Neuroethology of Paul MacLean

and 1979. This amounts to at least 400 entries of rather recent documentation—
keeping in mind that the publication date of MacLean's book and Reiner's
review was for both 1990.
2. Reiner misstates or ignores the facts when he says, "MacLean's present-
ation of the role of the hippocampus in limbic functions is not well reconciled
with the current evidence that the hippocampus plays a role in memory." The
phrasing of this statement implies that MacLean is unaware of or fails to report
on the extensive research indicating the role of the hippocampus in memory.
Such an implication is totally unwarranted. MacLean devotes fully two chapters
to reporting and discussing such research. These chapters even have "memory"
in their titles. Chapter 26 is titled Microelectric Study of Limbic Inputs Relevant
to Ontology and Memory (emphasis mine). Chapter 27 is titled Question of
Limbic Mechanisms Linking a Sense of Individuality to Memory (emphasis
mine) of Ongoing Experience. These chapters deal at length with the role of the
hippocampus in memory and propose an integrative role for the hippocampus in
tying learning to affect or emotion (For a summary of MacLean's discussion on
these matters, consult 1990: 514-516).
3. Claiming that the reptilian complex is not a reptilian invention, Reiner
misrepresents MacLean's position. On this third point, Reiner contends that
current research indicates that MacLean's reptilian complex is not a reptilian
invention but seems to be present in vertebrates all the way back to jawless
fishes. This is largely a taxonomic question. At what point do we declare
something to be a fish, an amphibian, an amniote, a reptile, or a mammal? And
do we view mammals as branching off from the amniote tree before we have
distinct reptiles in the line of descent? Or do we prefer the more likely probab-
ility that mammals descended in a line from the ancient mammal-like reptiles of
the predinosaur Permian-Triassic periods called therapsids, who represent a
branching of the ancient reptile line (cotylosaurs). Therapsids appeared approxi-
mately 230 millions years ago, and approximately 50 million years before the
emergence of the great dinosaurs of the Jurassic and Cretaceous periods.
MacLean knows these facts and clearly acknowledges them, while support-
ing a lineage for mammals that traces back to the therapsids, of the synapsida
subclass that branched off from the diapsida line that eventually produced the
great dinosaurs many years later. This is the standard position in evolutionary
theory today. One might wish to compare the phylogenetic tree in MacLean
(1990: 34) with Butler and Hodos (1996: 72), Strickberger (1996: 396), and
Hickman et al. (1984: Fig. 27.1). And it is the accepted position of standard
zoology texts (e.g., Miller & Harley 1992; Hickman et al. 1984, 1990). Mam-
mals, and ultimately us humans, then, did not evolve from dinosaurs but from a
parallel lineage that split much further back in geologic time.
If the term reptilian brain or reptilian complex causes confusion with modern
reptiles, and because the reviewers don't wish to read MacLean's work closely,
the reptilian complex could be thought of, and perhaps redesignated, as the
ancient amniote complex or even the early vertebrate complex. And, of course,
as MacLean acknowledges thoroughly, this early brain complex is not the
reptilian brain of modern reptiles but it is also not the same as that of the early
Reappraising MacLean's Triune Brain Concept 13

vertebrates, amniotes, or therapsids. At several points in his book, MacLean

makes this unequivocally clear by his reference to stem reptiles (cotylosaurs)
(MacLean 1990: 33, 82), those early reptiles from which both the diapsid and
synapsid lines branched off. To ensure the proper evolutionary context,
MacLean also uses the term "protoreptilian" in his initial definition and adds the
clarifying comment that he refers to the reptilian complex (or R-complex) only
for brevity's sake (see MacLean 1990: 15-16, 244, 519). This protoreptilian, or
stem reptile brain has been altered by modifications that include those produced
by differentiation and elaboration of earlier structures (e.g., see MacLean 1990:
243). These modifications, to include differentiations and elaborations, provide,
in addition to their previous maintenance and behavioral functions, neural
circuitry in support of the enhanced limbic structures of mammals. These
enhanced mammalian limbic structures necessarily engage and enhance prior
circuitry in the brain stem. And together these enhanced limbic and brain stem
circuits provide support for the greatly enhanced neocortex (or isocortex) which
eventually got modifications sufficient to permit language and the development
2
of complex technological societies.
4. Reiner misrepresents MacLean's position on the basal ganglia. Reiner says
he knows of no one other than MacLean who believes the basal ganglia to be the
neural seat for the control of species-typical types of behaviors (1990: 305).
This statement is a misrepresentation of MacLean's position as well as an
admission of ignorance on the part of Reiner. In the first place, MacLean never
uses the inclusive term "neural seat." Further, MacLean is not talking about all
species-typical behavior but only some. He specifically excludes from this
discussion such mammalian class/species-typical behavior as maternal nursing
and play, which are attributed primarily to other brain parts and treated in other
chapters of the book.
In Part II on the Striatal Complex with Respect to Species-Typical Behavior,
MacLean repeatedly emphasizes that the traditional view that the striatal
complex is primarily involved in motor functions represents an oversimpli-
fication. He writes that the purpose of the present investigation is to test the
hypothesis that the striatal complex plays an "essential" role in certain species
typical behaviors as well as certain basic forms of behavior common to both
reptiles and mammals (MacLean 1990: 243). At one point after reciting the
evidence, MacLean says that the results "suggest that the medial globus pallidus
(a structure of the basal ganglia) is a site of convergence of neural systems
involved in the species-typical mirror display of gothic-type squirrel monkeys"
(MacLean 1990: 189). Also, a little further on, MacLean tells us that "findings
indicate that in animals as diverse as lizards and monkeys, the R-complex is
basically involved (emphasis mine) in the organized expression of species
typical, prosematic communication of a ritualistic nature" (1990: 189).
Additional research, some predating others postdating Reiner's review and of
which Reiner is apparently ignorant, adds further support to MacLean's hypo-
thesis. For example, J. Wayne Aldridge and colleagues from the University of
Michigan in a research report titled "Neuronal Coding of Serial Order: Syntax of
Grooming in the Neostriatum,"(1993) conclude that there is "direct evidence
14 The Evolutionary Neuroethology of Paul MacLean

that the neostriatum coordinates the control (emphasis mine) of rule-governed

behavioral sequences." This study builds upon a series of earlier studies of
species-typical grooming behavior of the rat (e.g., Berridge & Fentress 1988;
Berridge & Whishaw 1992; Cromwell & Berridge 1990). These earlier and more
recent studies certainly support MacLean's hypothesis that the striatal complex
plays an essential role in some species typical behaviors of a ritualistic nature.
And, of course, there is the growing body of clinical evidence, going well
back into the 1970s and 1980s, that neurological disorders in humans (such as
Parkinson's, Huntington's, and Tourette syndromes) that involve damage to the
neostriatum produce specific deficits in the sequential order of movement,
language, and cognitive function (e.g., Holthoff-Detto et al. 1997; Cummings
1993; Benecke et al. 1987; Marsden 1982, 1984; Oberg & Divac 1979). Such
serial order patterns in behavior are phylogenetically old as well as pervasive
and often constitute the basis of identifying so-called species-typical behaviors.
Greenberg, this volume, who did early work with MacLean, provides a
comprehensive update of the research on the striatum.
5. Reiner misrepresents the facts when he claims that MacLean says the
limbic system first appeared in mammals. MacLean does not claim that the
limbic system first appeared in early mammals. He acknowledges that limbic
features appear in fishes, reptiles, and birds, but are rudimentary and poorly
developed when compared with those of mammals (MacLean 1990: 247, 287).
According to MacLean's view, then, it is not the presence or absence of limbic
features themselves in ancestral amniote or reptilian vertebrates, but rather the
significant and prominent development of limbic features in mammals that is
appropriately of interest in understanding the evolution of characteristically and
uniquely mammalian behavior. Further, care must be exercised in making
comparisons across existing modern species. We can only infer that the
structures and undeveloped and/or rudimentary homologues of such structures in
modern species were also present in ancestral lines. Brains do not fossilize, so
the point cannot be made conclusively. The currently accepted inferential posi-
tion in neuroscience is that there are homologues of limbic structures going well
back into vertebrate history, although these homologues in modern species are
often difficult to establish and sometimes downright dubious (Striedter 1997;
3
Veenman et al. 1997).
6. Reiner displays careless scholarship and misrepresents the facts of neuro-
science, evolution, and animal behavior as well as MacLean's position on
parental behavior and the cingulate cortex. He claims that MacLean assigns the
functions of parental behavior to the cingulate cortex and that MacLean regards
parental behavior as uniquely mammalian. According to Reiner, MacLean's
alleged position "ignores the fact that some reptiles, such as crocodiles, and all
birds engage in parental behavior, not to mention the possibility suggested by
paleontological data that some extinct reptiles, namely dinosaurs, also engaged
in parental behavior"(Reiner 1990: 305).
Such a blanket claim makes one wonder if Reiner felt it worth his while to
even consult the book he is reporting on. First, MacLean does not "assign"
parental behavior to the cingulate cortex. Instead he reports the recent (at that
Reappraising MacLean's Triune Brain Concept 15

time) research on maternal mechanisms in the septal or medial preoptic area

(MacLean 1990: 351-353) and indicates that this area may have provided the
initial potentiality for full scale mammalian maternal behavior (MacLean 1990:
354), that would include play and the development of empathy. The very title of
his Chapter 21 is Participation (emphasis mine) of Thalamocingulate Division
in Family-Related Behavior. Participation is participation not unilateral and
unequivocal assignment. And MacLean uses the systemic term "thalamocing-
ulate" to indicate intra-limbic nuclei and cortical connections, not simply
cingulate cortex as Reiner states. MacLean cites good evidence for thalamo-
cingulate participation in "nursing, conjoined with maternal care"(MacLean
1990: 380). After all, lesions in certain portions of the cingulate cortex interfere
with nursing and other maternal behavior (Stamm 1955, Slotnick 1967), not
with blanket parental care as Reiner asserts.
Perhaps it may be too early or simply erroneous in neuroscience to assign
anything specifically and finally to any exclusive part of the limbic area. More
likely there is some localization of minor function, but for most behaviors of any
scale there seems to be fairly wide-ranging neural circuitry that may be inter-
rupted by lesions at many different points. For example, recent research on
maternal behavior (nursing, retrieval, nestbuilding) in rats has focused on the
medial preoptic area with its connections to other limbic structures and the brain
stem (Numan 1990). Alison Fleming and her colleagues (1996), summarize
what we know about the neural control of maternal behavior. Not only the
medial preoptic area with its brain stem projections, but also other limbic sites
are involved, including the amygdala (Numan et al. 1993; Fleming et al. 1980),
hippocampus (Terlecki & Sainsbury 1978; Kimble et al. 1967), septum
(Fleischer & Slotnik 1978), and cingulate cortex (Slotnik 1967, Stamm 1955).
Most emotions, emotional behaviors, and emotional memories seem to be
distributed, involving multiple pathways. Specific behaviors and categories of
behaviors can be interrupted by lesions at varying points in these multiple
pathways. More recent research has again confirmed that the cingulate cortex is
involved in emotion and motivation (Stern & Passingham 1996). In a recent
research report John Freeman and colleagues conclude that the neural circuitry
formed by interconnected cingulate cortical, limbic thalamic, and hippocampal
neurons has fundamentally similar functions in the affective behaviors of
approach and avoidance (Freeman et al. 1996).
Like any good scientist with an open mind, MacLean, at the close of his
chapter on participation of the thalamocingulate division in family-related
behavior, calls for more neurobehavioral research to explore the extent of this
participation (MacLean 1990: 410). It is also noteworthy that MacLean is one of
the few thinkers in neuroscience who shows concern for the neural substrate of
such family-based behavior, characteristic of mammals, as play and the
underpinning but illusive quality of empathy. Although such characteristics have
been reported on behaviorally (e.g., for play, see Burghardt 1988, 1984; Fagen
1981), they have largely been ignored in the search for neural substrates, not
because they are unimportant, but because of the extreme difficulty in defining
and objectifying them. But the evidence clearly points to neocortical as well as
16 The Evolutionary Neuroethology of Paul MacLean

limbic cortical and subcortical representation (e.g., see Fuster 1997: esp. 169;
Frith 1997: 98; Frith 1989: 154-155). Recent reports by Damasio (1999),
Panksepp (1998) and Carter et al. (1997) provide hope that mainstream neuro-
science will direct more serious research toward a better understanding of these
difficult and ignored questions which are so critical to a full understanding and
appreciation of humanity.
Reiner also indiscriminately uses the blanket term "parental behavior"
coupled with attributing that same blanket usage to MacLean. In this usage,
Reiner shows a remarkable deficit of scholarship, naivete, or both. MacLean is
not discussing all parental behavior. He is discussing those nurturing behaviors
that are the most distinguishing characteristic of mammals and a fundamental
part of their taxonomic classification and differentiation from birds and reptiles.
These behaviors must be found in either new structures or modifications to
existing structures. As Butler and Hodos point out, new structures may be added
to organ systems, but modification of existing structures appears to be more
common (1996: 86). The jury is still out on the neurophysiology of these
defining mammalian behavioral features. What is more, with the emphasis on
cognition in neuroscience, until very recently surprisingly little attention has
been paid to the extensive work on the neural and hormonal basis of the
motivational and emotional aspects of maternal care. This is openly acknow-
ledged by leading scholars in the brain science field (e.g., Rosenblatt &
Snowden 1996; LeDoux 1997: 68; Kandel, Schwartz & Jessell 1995). The
previously cited works by Panksepp (1998) and Carter et al. (1997) represent a
step in the right direction.
The blanket term "parental care" as used by Reiner in his criticism of
MacLean amounts to condemnation by indiscriminate generalization. Parental
care has been defined by a leading authority as "any kind of parental behavior
that appears likely to increase the fitness of the parent's offspring" (Clutton-
Brock 1991: 8). This very broad and inclusive term includes even nest and
burrow preparation. The very production of eggs is included. This kind of
"parental care" is found in the earliest vertebrates with very primitive brains
indeed. If the all-inclusive definition of parental care can be stretched to include
the production of eggs and digging a hole to place them in, perhaps it could
conceivably be stretched to include even the sharing of cellular membranes
during asexual reproduction by single-celled organisms.
But specifically, what about parental care in modern reptiles? Contrary to
Reiner's claim, MacLean reports on parental care in crocodiles (MacLean 1990:
136-137) and also in some species of skink lizards (MacLean 1990: 136, 2 4 8 -
249). A recent review article on parental care among reptiles by Carl Gans of the
Department of Biology, University of Michigan, brings us up to date. Gans
claims that the most spectacular example of reptilian parental care takes place
among crocodiles. Both parents respond to the call of hatchlings who vocalize
underground while emerging from the eggs. The adults dig them up and
transport them to water in their large buccal pouch (Pooley 1977). The young
are then washed and stay shortly in association with the adults. After a relatively
brief period, however, the juveniles' response to the adults reverses. The
Reappraising MacLean's Triune Brain Concept 17

juveniles disperse suddenly into small, nearby channels where they may dig
themselves tunnels. Gans notes: "In view of the fact that crocodylians may be
cannibalistic (emphasis mine), there seems to be both an inhibition of cannibal-
ism in the parents and an inhibition of a possible adult avoidance reaction in the
neonates" (1996: 153).
This kind of short-lived parental care during which the cannibalism of
parents is inhibited may be impressive in reptiles, but it is a far, far cry from the
highly developed family-related behavior in mammals; behavior that is so
further developed in the human species that it extends often throughout an entire
lifetime and becomes the basis for a vastly extended social life. The equating of
parental care in reptiles with parental care in mammals is simply ludicrous. It is
this mammalian family behavior that concerns MacLean, and the neural sub-
strate is appropriately sought in the brain modifications that became prominent
with the appearance of mammals.
7. Reiner's further inaccuracies: recapitulation, homology, and correspon-
dence, and so on. Near the end of his review Reiner makes the following
isolated statement: "MacLean also errs in his apparent sweeping acceptance of
Haeckel's idea that ontogeny recapitulates phylogeny" (1990: 305). Again,
Reiner distorts and misrepresents. From a close review of the book it is by no
means clear that MacLean "sweepingly" accepts Haeckel's concept. In fact he
only refers to it once (MacLean 1990: 46), while at the same time noting the
well-known exceptions. Haeckel's concept has been largely superceded in
neuroscience today by the principles of von Baerian recapitulation. The von
Baerian version holds that while ontogeny does not recapitulate phylogeny in
the thoroughgoing Haeckelian sense, it does recapitulate the features of an
organism in terms of the organism's general to more specific classification. In
other words, the von Baerian principles state that the more general features of an
organism develop before the more specific features do (Butler & Hodos 1996:
51-52). The issue, however, is still not so clearly settled. The emergent discip-
line of evolutionary developmental biology is looking more closely into such
questions (Hall 1992; Thomson 1988). For instance, evolutionary biologist
Wallace Arthur, in summarizing the main themes of this emerging discipline,
writes: "No single comparative embryological pattern is universally found or
can be described as a 'law'. Von Baerian divergence, its antithesis (conver-
gence) and a broadly Haeckelian (quasi-recapitulatory) pattern can all be found,
depending on the comparison made"(1997: 292).
On the additional point that MacLean prefers to think in terms of correspon-
dence rather than homology probably reflects his functional-behavioral orienta-
tion. In fact it is specifically in discussing the issue of the relationship between
structure and behavior that (MacLean 1990: 37) makes this comment. Later, he
returns to a more standard use of homology (MacLean 1990: 228). There is, in
fact, presently no sure-fire way of demonstrating that homologues have the same
one-to-one functions or produce the same one-to-one behaviors across species.
In reporting that MacLean, at one point, expresses preference for the term
"correspondence" because of the confusion in the definition of homology,
Reiner shows what can only be considered a misplaced and sophomoric
18 The Evolutionary Neuroethology of Paul MacLean

"gotcha" exuberance. He writes that MacLean's comment "should leave Stephen

J. Gould, not to mention all other students of evolution, aghast," adding that
such a comment constitutes a "very critical misjudgment to make in a work on
evolution."(Reiner 1990: 305).
This is truly a naive, if not preposterous statement by Reiner. Could it be that
Reiner is not aware of the long history of the pervasive problems associated with
the definition of homology? For example, Leigh Van Valen, of the biology
department of the University of Chicago, in the first sentence of his frequently
referenced article on homology and its causes, writes: "Homology is the central
concept of anatomy, yet it is an elusive concept" (1982: 305). Further on, in
view of the persistent definitional ambiguities, Van Valen practically equates the
two terms "homologue" and "correspondence" when he writes: "In fact, homo-
logy can be defined, in a quite general way, as correspondence (emphasis mine)
caused by a continuity of information," although in a footnote Van Valen admits
that correspondence itself needs further definition beyond the scope of his paper
(305: fn. 1; cf. Roth 1994). Although there has been some sharpening of the
concept of homology, with emphasis on phyletic continuity, the ambiguities
have by no means been adequately resolved (Gehring 1998; Trevarrow 1998;
Striedter 1998; Arthur 1997: 171-177; Hall 1994, 1996). The study of molecular
biology and the genome is adding further insights into the conservation of
homologues from very early life forms indeed (e.g., see Gehring 1988; C.U.M.
Smith, this volume).
And there remains the haunting question that is still wide open for research
and investigation: Do most homologous behaviors share a homologous struc-
tural basis or can homologous behaviors be rooted in nonhomologous
structures? (see Hall 1996: 29: fin. 23). The recent report by William Blessing on
the lower brain stem emphasizes the question of multiple neural representations
of body parts and behavior, in that behavior originally represented and
controlled in the brain stem of an earlier vertebrate may maintain its brain stem
representation, but be controlled by an added representation in the frontal cortex
of a more highly developed mammal. Such multiple representations at different
levels as the brain became more complex would certainly confuse the issue of a
straightforward homologous match of structure and function (1997: 1-18; see
also, Brown 1977).
Research on very limited aspects of function is often suggestive but far from
conclusive even on such limited function. Establishing homologues of the
prefrontal cortex can be particularly vexing. A recent research article by
Gagliardo and colleagues, "Behavioural effects of ablations of the presumed
(emphasis mine) 'prefrontal cortex' or the corticoid in pigeons" (Gagliardo et al.
1996), indicates, not only in its discussion and conclusions, but in the very title
itself, the uncertainty, ambiguity, and cautions that currently characterize such
research efforts (see also Fuster 1997: 7-11).
An awful lot of assuming goes on in some quarters of neuroscience on this
issue, which simply cannot be settled at this time based on the empirical
evidence. This is one of the problems and cautions that must be acknowledged
when generalizing across species, say firom rats to humans. In maternal
Reappraising MacLean's Triune Brain Concept 19

behavior, for example, can we say factually that the medial preoptic area plays
the same part in the maternal behavior of humans that it does it the rat brain?
No, we cannot. At least not yet. But neuroscientists, after first hedging them-
selves, and following homologous logic, seem inclined to think so. Nevertheless,
it is entirely within the realm of possibility that we may find that it does so only
in part or not at all. As neuroresearcher Joseph LeDoux notes: "Some innate
(emphasis mine) behavioral patterns are known to involve hierarchically
organized response components" (1996: 120). And further on he adds: "Species
differences can involve any brain region or pathway, due to particular brain
specializations required for certain species-specific adaptations or to random
changes"(1996: 123). And neurologist Richard Restak points out that in the case
of animals, multiple limbic areas may increase, modify or inhibit aggression. He
notes further that even the same area may increase or inhibit responses under
different experimental conditions and depending on the animal selected for
experiment. As an example, he points out that the destruction of the cingulate
gyrus (a limbic component) increases aggressive behavior in cats and dogs,
whereas, on the contrary, such an operation has a calming effect in monkeys and
humans (1994: 149).
Or perhaps, as Blessing notes, there are multiple representations. Then we
might have to go to correspondence rather than homology (even homoplasy
might not apply, since homoplasy, or parallel evolution, would probably not
apply in such closely related species) to account for the behavioral circuitry. In
other words, the corresponding neural circuitry—that circuitry controlling
maternal behavior—may be found in the same, slightly differing, multiple, or
perhaps (though highly unlikely) even totally different structural homologues or
modifications.
In fact, if homology is correct and functionally, to include behaviorally,
uniform—that is, the same structures account for the same functions and
behaviors across classes, orders, and species—this finding would support the
triune brain concept as set out by MacLean, which says generally that the
protoreptilian complex common to both reptiles and mammals functions largely
the same in both classes. This finding would also support MacLean's position
that the expanded circuitry areas of the mammalian complex bear character-
istically mammalian functions and are the circuitry for characteristically mam-
malian behaviors, such as nursing; a defining taxonomic feature of mammals
(which, in part distinguishes them from reptiles and birds).
In a final series of somewhat gratuitously negative comments, Reiner writes
about some of MacLean's legitimate speculations. For example, Reiner states
"and mathematical skill (he thinks the cerebellum could be involved)"(Reiner
1990: 305).
And why not? See MacLean's discussion on the subject (MacLean 1990:
548-552). Recent research indicates that the cerebellum is not just a motor
mechanism, but is also likely involved in higher cognitive and perhaps even
language function. Especially relevant is the rather well-supported hypothesis
that indicates a cerebellar mechanism involved in all tasks that require precise
temporal computations. This could well suggest an involvement in mathe-
20 The Evolutionary Neuroethology of Paul MacLean

matical processes. True, the evidence is insufficient to permit firm conclusions

as to the cerebellar role in higher cognitive processes, but it is a research
direction that needs further refinement and is currently pursued by a number of
neurobiologists (Daum & Ackermann 1995; Dimitrov et al. 1996; Altman &
Bayer 1997: esp. 749-751).
Overall, given the outright errors, careless scholarship, misrepresentations,
and sophomoric, prejudicial tone of Reiner's review, it probably should never
have been allowed to appear in a publication of the stature and influence of
Science. Such reviewing should perhaps raise questions of standards in the
academic-scientific community.

REVIEW BY CAMPBELL IN AMERICAN SCIENTIST

The review by Campbell in American Scientist (1992) is a much shorter

review than that of Reiner. It brings up some of the same points, but is less
prejudicial in its tone. Since it is less detailed it expresses primarily the prefer-
ences and value judgements of the reviewer. Campbell repeats Reiner's erron-
eous charge about outdatedness. He writes: "that except for a very few papers,
most of the references were published prior to 1980" (1992: 498). I have already
noted that this "handful" of items amounts to more than 180 citations. One
suspects that Campbell proceeded from his preconceptions and found what he
expected to find. Campbell ends his review with the statement: "Unfortunately,
the data presented are, to some degree (emphasis mine), outdated, and the
evolutionary reasoning is unsophisticated" (1992: 498). The use of the term
"unsophisticated" by the reviewer is totally unwarranted. For anyone who has
closely read MacLean's detailed and thoughtful work, the evolutionary
reasoning is, on the contrary, quite thoughtful, well-presented, and sophisticated.
Such blanket judgments tell us more about the sociology of neuroscience and
neuroscientists that they do about the subject matter of the discipline itself.

COMMENTS OF BUTLER AND HODOS

In their recent comprehensive and overall admirable work on comparative

vertebrate anatomy, Butler and Hodos attempt to formalize the assignment of
MacLean's work to the relics of history. Their comments reflect the standard
oversimplified criticisms, misrepresentations, and errors that have become
popular to repeat ever more unreflectively. Butler and Hodos assign the triune
brain concept, inaccurately and indiscriminately, to a category they call
"theories of addition." And without any detailed discussion or analysis of the
very significant, indisputable points of accuracy in MacLean's concept, they
write that the past three decades of work in comparative neurobiology
"unequivocally" contradicts MacLean's theory (1996: 86).
How incredible that two such qualified authors should accept the same
flagrant misrepresentations, inaccuracies, and oversimplifications of MacLean's
Reappraising MacLean's Triune Brain Concept 21

work that have become commonplace in some sectors of neurobiology over the
past decade. They seemingly merely parroted the errors and misrepresentations
of Reiner and others rather than reading MacLean's 1990 work closely and
open-mindedly. There is no point in repeating the responses given earlier to
Reiner's review. The same points hold for Butler and Hodos' comments. The
rebuttal points are clearly made and easily accessible to verification by anyone
who chooses to make the effort. The categorical statement by Butler and Hodos
that the extensive body of work in comparative neurobiology over the past three
decades unequivocably contradicts MacLean's theory, which they apparently
have not read, constitutes on that point poor, if not irresponsible, scholarship.

MACLEAN'S TRIUNE BRAIN CONCEPT: UTILITY AND VALIDITY

The triune brain concept may have its limitations. But its shortcomings have
been patently misrepresented in some cases and grossly exaggerated in others.
Whatever its faults may ultimately prove to be, the triune brain concept gets at a
fundamental evolutionary pattern. The mammalian modifications, differentia-
tions, and elaborations to the early vertebrate and ancestral amniote brains had
the effect of introducing endothermy (warm-bloodedness), maternal nursing,
enhanced mechanisms of skin contact and comfort, as well as enhanced visual,
vocal, and other cues to bond parents to offspring and serve as the underpinning
for the extended and complex family life of humankind. The mammalian mod-
ifications, therefore, added greatly enhanced affectional, other-interested behav-
ior to the primarily (although not exclusively) self-preservational, self-interested
behaviors of ancestral amniotes and early vertebrates (not necessarily their
modern representatives).
The simplistic representation and attempted demolition of MacLean's triune
brain concept is not good science. Reiner's review, where it has any validity at
all, is like discovering a termite or two in the bathroom wall, and then
proceeding to pronounce a full alarm that the house is full of termites, only to
find that it is necessary to treat a few boards in the subflooring. Further, in his
deconstructive, analytic fervor, Reiner has offered no alternative higher level
generalization. The review represents a dysfunction common to a lot of scient-
ific practice, that of an analytical approach that takes apart but can't put back
together. Perhaps we should call it analytic myopia. Uninterested in the bigger
questions of humanity that we so desperately need help on, and lacking an
interest in therapy, these analytic myopics continue their fine-grained focus.
Fine-grained focus is fine, laudable, and very much needed. It becomes analyti-
cally myopic, however, when it fails to place in context what it finds and
defines, when it employs sloppy scholarship, and when it attempts prejudicially
to destroy or deconstruct that which it lacks the imagination and courage to put
together.
On the other hand, the theories of brain evolution that Butler and Hodos
review favorably and the synthesis that they present at the end of their book
focus on the immunohistological, hormonal, and morphological mechanics
22 The Evolutionary Neuroethology of Paul MacLean

(1996: 463-473). They say, in fact, almost nothing at all about behavior or the
significance for behavioral evolution of the various mechanisms of evolution
they identify. And they make no attempt whatsoever to confront the larger
behavioral questions of humanity where we need help and guidance from
neuroscience in defining the neurobiological basis of human nature in order to
establish links up the scale of generalization with the social sciences. The
theories they present are only of interest to the technical aspects of neuroscience.
They are not, however, incompatible, but tend to support MacLean's concepts
when these concepts are accurately and thoughtfully considered.
The key point in comparing these theories with that of MacLean's is that
they are comparable, at best, only in part. They ask and respond to different
questions. MacLean tries to address the larger questions of human nature and
behavior. The others show no interest in such questions but address the fine-
grained technical questions of anatomical and functional evolution. At the level
where they meet, they do not contradict each other but are largely compatible.
At the point where they diverge, they primarily address different questions. This
is, I think, the root of the tension between the two. MacLean's concept facing up
the scale of integration is useful and has been appropriately well received in the
therapeutic sciences, and is also very useful for the social sciences. On the other
hand, it has not been, but may yet become, more useful and better received in
other quarters of neuroscience, especially when subjective experience is
eventually given its due in the study of consciousness. There are, in fact, recent
signs that the importance of subjective experience, which is of great interest to
MacLean, is gaining fuller recognition in the newer studies of consciousness
(Damasio 1994, 1999; Smith 1996: 471^174; Searle 1997; Edelman & Tononi
2000, Cory 2000a,b).
The triune brain concept may need modification, then, as the body of
neuroscience grows—but certainly not outright rejection. With appropriate clari-
fications, it is still by far the best concept we have for linking neuroscience with
the larger, more highly integrated concepts of the social sciences. This is true
even if its level of integration has limited utility for some neuroscience
researchers who are doing ever more fine-grained research into neural archi-
tecture and function.
The transitions from early vertebrate to amniote to synapsid reptile to
mammal were in behavioral effect transitions from nearly exclusively self-
preserving organisms with relatively little or less complex social life to, at least
in part, a nurturing, "other-maintaining," "other-supporting," or "other-
interested" organism. And that makes all the difference in the world for human
evolution. Our other-maintaining mechanisms combined with our self-preserv-
ing ones provide the biological glue as well as the dynamic for our remarkable
behavioral evolution, our social life, and ultimately the crucial social and
political factor of our moral consciousness.
The qualitative differences between the familial and social behaviors of even
the most caring of reptiles (say, modern crocodiles), birds or social insects and
the mammal we call human are overwhelmingly evident. Humans with their
social, cognitive, and language skills, for better or for worse, dominate the
Reappraising MacLean's Triune Brain Concept 23

planet and no other species comes close. Any neurobiologist who cannot see or
appreciate the difference suffers from analytic myopia or some form of
misplaced species egalitarianism (cf. Butler & Hodos 1996: 3-4). The proper
study of humans is humans and to some extent their lineal ancestors. The triune
brain concept integrates some fundamental patterns out of much that is yet
unknown and uncertain in neuroscience. And this generalization, when properly
understood, appreciated, and applied, is the most useful bridging link, thus far
articulated, between neuroscience and the larger and pressingly critical questions
of humanity's survival, as well as the hoped for transformation of humanity into
a truly life-supporting, planet-preserving and enhancing custodial species.
When other neuroscience researchers reach the conceptual point in their
grasp of the discipline that they feel an increasing obligation to take a more
integrative view and proceed to move up the scale of generalization in order to
confront the larger questions of human life, they will likely produce concepts
closely resembling the triune brain. Homology and behavioral evolution will
almost inevitably take them in that direction. Frankly, despite its current lack of
popularity in some quarters of neurobiology, I think that the triune brain concept
will continue to be influential, and with appropriate modifications as research
progresses, provide an important underpinning for interdisciplinary communi-
cation and bridging. The chapters constituting this volume amply demonstrate
its heuristic value and it integrative utility.

NOTES

1. A highly favorable review of MacLean's 1990 book was written by Emre Kokmen,
M.D., of the Mayo Clinic, Rochester, Minnesota, in Journal of Neurosurgery. V. 75, Dec,
1991, p. 998. In this chapter I focus on the reviews in Science and American Scientist
because they have reached a wider audience and have become red flag reviews
unjustifiably inhibiting the thoughtful application of the triune brain concept in related
fields as well as in the psychological and social sciences.
2. The use of the term "additions" is deliberately avoided here because it has been the
source of some confusion (see Butler & Hodos 1996: 86). New brain structures do not
spring de novo out of nowhere but rather evolve from the differentiation of previously
existing structures. When differentiations become sufficiently established, they are often
referred to loosely as "additions." This does not deny that seemingly new additions may
possibly and occasionally arise, but the intent here is to emphasize the phylogenetic
continuity that underpins the concept of homology.
3. The accuracy and utility of the concept and term "limbic system" has itself been a
separate topic of some disagreement in recent years. Some authors state that it does not
represent a truly functional system and that the term should be discarded. Others defend
its use. Most texts continue to find the term useful and because of its longtime usage it
will probably remain in the literature. Some recent and prominent scholars illustrate the
controversy well. Pierre Gloor of the Montreal Neurological Institute, McGill University,
in his thoroughgoing work The Temporal Lobe and Limbic System, by the very use of the
term in the title indicates his position. Further on in the text, while acknowledging the
controversy he writes that this system in mammals exhibits an organization that is
24 The Evolutionary Neuroethology of Paul MacLean

sufficiently different from that characterizing other areas of the cerebral hemisphere to
merit such a designation (Gloor 1997: 106).
And well-known neurologist Richard Restak tells us that based upon a large body of
experimental work, it is appropriate to conclude that, "depending on the areas stimulated,
the limbic system serves as a generator of agreeable-pleasurable or disagreeable-aversive
affects" (1994: 143). Nevertheless, there is little agreement among neuroscientists con-
cerning the contributions of the different components, and their mutual influence on each
other (1994: 149).
On the other hand William Blessing, a neuroscientist at Flinders University, in his
study of the lower brain stem, feels that emphasis on the limbic system has detracted
from the study of brain stem mechanism, that it has been "plagued by its anatomical and
physiological vagueness and by the lack of precision with which the term is used"
(Blessing 1997: 15). Further, he thinks the term should be dropped from the literature
(Blessing 1997: 16).
A third recent author, neuroscientist Joseph LeDoux (1996: Ch. 4) argues that
because the limbic system is not solely dedicated to the single global function of emotion,
a claim that MacLean fully recognizes in his chapters on memory (1990: Chs: 26 & 27),
that the concept should be abandoned. LeDoux apparently prefers a single functional
criterion for the definition of a system, whereas MacLean seems to prefer a combination
of functional and anatomical criteria. Le Doux concludes his argument by stating: "As a
result, there may not be one emotional system in the brain but many" (1996: 103).
Compare this with the concluding line of the definitional description by Kandel et al.,
authors of the most widely used textbook on neuroscience and behavior: "The limbic
system contains neurons that form complex circuits that play an important role in
learning, memory, and emotion"(1995: 708).
The use and value of the conceptual term "limbic system," then, seems to depend on
one's research focus and how one chooses to define a system. It might be added that the
definition of what constitutes a system is controversial in all disciplines, not just in
neuroscience.

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Pooley, A . C 1977. "Nest opening response of the Nile crocodile." Journal of Zoology.
(London). 182: 17-26.
Rosenblatt, J. and Snowden, C. 1996. Parental Care: Evolution, Mechanisms, and
Adaptive Intelligence. NY: Academic Press.
Reiner, Anton. 1990. "An Explanation of Behavior" (review of MacLean's The Triune
Brain in Evolution). Science. V. 250 (Oct 12): 303-305.
Restak, Richard M. 1994. The Modular Brain. . NY: Charles Scribner's Sons.
Sagan, Carl. 1977. The Dragons of Eden. NY: Random House.
Searle, J. 1997. The Mystery of Consciousness. NY: NY Times Review of Books.
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 PART II

MOLECULES, BODY PLANS,

AND THE STRIATUM
 3
D E E P TIME A N D THE BRAIN: T H E
M E S S A G E OF THE MOLECULES

CUM. Smith

INTRODUCTION

The hallmark of Paul MacLean's neuroscience is its evolutionary perspective.

He was not, of course, the first to recognise that the human brain has a vast
evolutionary ancestry. That priority should probably be accorded Herbert
Spencer. When he was composing his pioneering Principles of Psychology
u
(1855) he wrote to his father that what he was doing was quite new and alien to
1
preceding psychologists." Much to his chagrin the first edition of the Principles
fell almost stillborn from the press; the second edition, however, published in
1870/1872, had one very influential reader: John Hughlings Jackson. Jackson
2
became a disciple. He never tired of admitting his debt to Spencer. But neither
Spencer nor Jackson left, in the one case the philosopher's study and in the other
the neurological ward, to research the behaviour of infrahuman animals in the
field. Paul MacLean did. In consequence, he may with justice be regarded as
pioneering an approach to understanding the human brain through what might
be called evolutionary neuroethology.
MacLean's extensive studies of reptilian ethology helped to provide evidence
for his well-known concept of the triune brain. His vision of the mature human
brain grows, like that of Herbert Spencer, from a conviction that it has a vast
evolutionary history. MacLean has also been touched by the molecular revolu-
tion of our times; a revolution that, we may imagine, would have also received
the enthusiastic attention of Herbert Spencer and John Hughlings Jackson.
MacLean writes of how this revolution has shown us how the cells of our remote
ancestors "must have worked" and that "in all animals there are molecular
3
commonalities . . . that carry over into complex molecular assemblies." His
clinical understanding is rooted in this evolutionary understanding. Biologists
32 The Evolutionary Neuroethology of Paul MacLean

cannot but find this approach appealing. For, as Theodosius Dobzhansky fam-
ously said, "nothing in biology makes sense without evolution."

TIME SCALES

I have titled this chapter Deep Time and the Brain because the time scales
of molecular evolution are far greater than even the 200 million years which
MacLean considers in his "palaeopsychology." Indeed, one must increase that
vast number by more than an order of magnitude. For the first biological mole-
cules appeared on the surface of the planet well over three thousand million
years ago (Figure 3.1). The earliest vestiges of living organisms can be detected
in South African and Australian rocks dating back 3.5 billion years BP. It is
humbling to realise that the world of bacteria has held tenure on the earth
throughout the vast period of time from that day to this. Homo sapiens has been
around for at most 0.001% of that duration. It took, however, an immense length
of time for the next significant development to occur: the origin of the
eukaryocytes. No doubt there were many false starts, many unsuccessful ven-
tures, but the earliest eukaryote microfossils date back little further than 1.5
4
billion years ago. Then evolution accelerates. After the elapse of only about
another 0.75 billion years we begin to find the traces of multicellular forms.
These take the form of worm tracks and the occasional simple platyhelminth-
like worm itself. Then in the Burgess shales of 525 million years ago, and the
slightly older Ediacaran outcrops in Australia, we find preserved a remarkable
array of metazoan forms. These have been brilliantly described by Stephen
Gould in his best-seller, Wonderful Life, and by Conway Morris in his equally
fascinating book, The Crucible of Creation.

MOLECULAR PALAEONTOLOGY

One of the most fascinating developments of recent years stems from the
coming together of the centuries-old subject of palaeontology and the up-to-the-
minute, laboratory-bound, highly fashionable and highly technical study of
molecular biology. For it turns out that the molecules, and not only the
molecules but also the molecular systems and cascades on which our bodies
depend have locked up in their structure messages from times past. For eyes that
can read them they speak of our ancestry and of the vicissitudes of our
ancestors. Not all biological molecules, of course. The smaller molecules and
even the sometimes quite large lipids and carbohydrates do not bear the imprint
of the past. But the molecules that have been called the "informational macro-
molecules," the proteins and nucleic acids, by that very token, do.
As mutations alter the sequence of nucleotides over geological time so the
sequence of amino acids in the proteins for which they code also alter. The
situation is not (it never is!) straightforward. Homologous genes within different
taxa evolve at different rates; different genes within the same taxa evolve at
Deep Time and the Brain 33

different rates; different sites within a given nucleotide sequence mutate at

different rates: all these (and many other subtleties) make molecular phylogeny,
at present, an inexact and controversial science. There is no space here to review
5
these different problems (see reference ). Often differential mutation rates have
clear functional significance: fibrinopeptides, for instance, evolve comparatively
rapidly, histones comparatively slowly; sequences which code for important
active sites change only slowly, if at all; sequences which code for functionally
unimportant parts of a protein, or for nothing at all, change comparatively
rapidly. Neutral mutations play an important role and have, as Kimura and
6
others have shown, to be taken into account.

DEEP TIME CHRONOLOGY

P
t
0.5xl0 9
- Burgess shale fauna 05,25x 10'
Ediacaran fauna 0.565 x 10
9

Earliest traces of metazoa

y
.OxlO --

1.5x10 Earliest eukaryocytes

PQ
9
^ 2.0 x l O -

<
3.0 x 10 « 9
t t
IEubactena
Archaebacteria
3.5 x 10 - 9
Earliest microfossils

4.0 x 10"

Figure 3.1. Deep Time Chronology of Life

34 The Evolutionary Neuroethology of Paul MacLean

In addition to evolutionary change of nucleotide sequences in the genome,

other forces for change are also at work. Again there is no space to discuss them
in detail. Suffice it to say that these include exon shuffling, the insertion and
deletion of transposons, differential posttranscriptional splicing, RNA-editing,
7
post-translational processing, and so on. A significant neurobiological example
is provided by the opioid and opioid-related proteins: alpha, beta and gamma
MSH (melanocyte stimulating hormone), ACTH (adrenocorticotropic hormone),
beta-endorphin, met- and leu-enkephalin, dynorphin, CLIP (corticotrophin-like
8
intermediate lobe protein), beta-LPH (lipotropic hormone), and so on. All these
important neuroactive peptides are derived from three large precursor proteins:
proopiomelanocortin (POMC) (265 amino acid residues), pre-proenkephalin A
(263 amino acid residues) and preproenkephalin B (256 amino acid residues) by
posttranslational processes which cut the amino-acid chain at different points.
The fact that the precursor proteins are so nearly the same size suggests that they
are derived from evolutionarily related genes by differential splicing of mRNA
chains after post-transcriptional excision of introns. It turns out that the human
pre-proenkephalin A gene is located on chromosome 12 while the POMC gene
is found on chromosome 2. It may be that this indicates an episode of transposon
shuffling in the evolutionary past. This short example gives a taste of some of
the hidden complexity of molecular evolution.
It would be wrong to finish this section without emphasising one very
important evolutionary mechanism: gene duplication and deletion. This can
occur when homologous chromosomes align themselves imprecisely at meiosis.
If a chiasmata forms between the chromatids at this point of misalignment, one
of the daughter chromosomes may contain two copies of a given gene and the
other will lack that gene altogether. If the gene codes for an important protein, it
is unlikely that the daughter cell lacking the gene will survive. The daughter cell
containing the duplicated gene will, however, be fully viable. But the selective
pressure on one of the two genes in this daughter cell will be reduced. Whilst its
twin continues programming a perhaps vital protein it can mutate comparatively
freely. Many instances of this are known in molecular biology and, as we shall
see, in molecular neurobiology. Indeed there is evidence to suggest that two
episodes of large-scale gene duplication, probably duplications of the entire
genome, occurred early in vertebrate evolution, one before the divergence of
Gnathostomata and the Agnatha, and the other before the divergence of the fish
9
and the tetrapod land fauna.

WHEN DID BRAINS BEGIN?

When did brains begin? The answer to this question depends on what is
meant by the term "brain." One is tempted to say as soon as bilaterality evolved.
The radial symmetry of the Cnidaria and Ctenophora induces little more than a
nerve net. But the so-called "urbilateralia" of 800 million years ago, like all
bilateral forms, naturally entered new environments one end pointing forwards.
Over time an antero-posterior axis would become established. At some point in
Deep Time and the Brain 35

the vast Precambrian period, the assembly of morphopoietic genes known as the
10
Hox complex developed. This complex then, as now, is responsible for
morphological differentiation along the antero-posterior axis. Each segment in
our worm-like ancestor came to have a separate identity. Well before the times
when the Ediacaran and Burgess deposits were laid down the so-called
"zootype," a heterotrophic, bilateral, anteroposteriorly differentiated, form had
evolved.
Once the antero-posterior axis had been established sensory cells—chemo-
receptors, mechanoreceptors, even photoreceptors—would tend to concentrate
on the anterior extremity where new environments were first encountered. The
11
process, which Ariens Kappers termed neurobiotaxis, would then take over.
Nerve complexes concerned with the analysis of input from the sensory surfaces
would develop in close association with these surfaces. In this process we can
see the origin of a major anteriorly placed ganglion, or "brain." Similarly neuro-
biotaxis would have ensured that ganglia and their connectives would develop in
a longitudinal strip close to the ventral surface, next to the substratum, where
tactile and other stimuli would predominate.
It is thus of considerable interest to find that several genes controlling the
early development of the neurectoderm of invertebrates {Drosophila) show
sequence homology with several of those controlling the early development of
the neurectoderm in vertebrates {Xenopus). Evidently these genetic systems
predate the evolutionary schism between the protostomata and the deutero-
stomata: an event which occurred at least 750 million years ago. But yet more
interestingly it has been shown that these homologous genes control develop-
ment of the ventral surface in invertebrates {Drosophila) and the dorsal surface
2
in vertebrates {Xenopus)} It looks as though the old idea that one of the early
events in chordate evolution was a 180° twist so that the nerve cord faces
upwards has received confirmation from modern molecular embryology. The
twist, presumably, is to be associated with the adoption of a free-swimming life-
style in the surface waters of ancient oceans by our chordate ancestors. In this
position the major sensory input, light and the shadows of predators and prey,
would come from above rather than below.
After these preliminaries let us turn to some particular instances of mole-
cular evolution in the brain. I shall start with the ubiquitous "serpentine" 7TM
proteins, then look briefly at the molecular designs of voltage—and ligand-gated
ion channels, and end with a brief account of the remarkable homogeneity of the
molecular processes at work in the early phases of neuroembryology. I hope to
leave you with an impression of the depth of the interrelationships between all
animal brains, an impression of the huge antiquity of the molecular mechanisms
at work, with, in short, the impression which the young Charles Darwin
expressed in 1837 in one of his post-Beagle notebooks: "animals our fellow
brethren in pain, disease, death and suffering . . . we may all be netted
13
together." And this, I feel sure, is also the vision that energised Paul
MacLean's thinking in developing his theory of the triune brain.
36 The Evolutionary Neuroethology of Paul MacLean

THE 7TM "SERPENTINE" MOLECULES

This is one of the most ubiquitous of all conformational motifs (see Figure
3.2).

Figure 3.2. Conformation of 7TM "Serpentine" Molecules. In the upper part, the
cylinders represent alpha-helical stretches of the molecule. The lower part represents the
"barrel of staves" conformation.

In essence the protein contains seven alpha-helical segments. These alpha-

helical segments, moreover, consist predominantly of hydrophobic amino acids.
They are consequently believed to span the membrane. The upper part shows a
Deep Time and the Brain 37

plan view. In vivo ( t h e lower part) the conformation also makes use of the third
dimension to give the so-called "barrel-of-staves" structure.
The most ancient 7TM proteins are found in the halophilic (salt-loving)
bacteria. This group of bacteria is classified with the Archaebacteria, which, in
being able to survive extreme temperatures, salt concentrations, pH, and so on,
is thought to number amongst its members representatives of the earliest life
forms on the planet's surface. The membrane of Halobacterium halobium can be
separated into three fractions: yellow, red, and purple. The purple fraction can
be formed into crystalline sheets that can be examined in the electron
microscope. In addition to lipids it contains a 26 kDa protein, bacterio-rhodop-
sin, which because of the crystalline nature of the purple membrane can be
subjected to X-ray diffraction. The seven closely packed alpha-helices extending
14
through the membrane can thus be examined in atomic detail. As with other
rhodopsins, the opsin apoprotein of bacteriorhodopsin is loosely bound to a
retinal chromophore which lies across the tunnel in the centre of the "barrel of
staves." It can, perhaps, be seen as a trapped agonist. On receipt of a photon of
appropriate wavelength the retinal transforms from an all trans to a 13-cis
configuration and transfers a proton from the cytoplasmic to the extracellular
side. In contrast to the rhodopsins of vertebrate retinae the retinal does not
detach and migrate from its opsin apoprotein to regenerate, nor does it function
as a photosensor. In the bacterial membrane it acts as a proton pump.
In the animal kingdom 7TM proteins seem to have evolved in association
with second-messenger (especially G-protein) signaling systems. G-proteins are
again, exceedingly ancient. They are well known in the prokaryocytes as well as
in the eukaryocytes. They constitute a large superfamily whose members all
15
have the ability to dephosphorylate G T P . This enables them to act as molecular
time switches. In consequence, G-proteins linked to 7TM membrane receptors
are found in many parts of the animal body, not only in many sensory systems
but also in the subsynaptic membranes of metabotropic synapses. They are at
work, for instance, in alpha and beta adrenergic synapses, muscarinic choli-
nergic synapses, dopaminergic synapses, the many subtypes of serotinergic
(5HT) synapses, in metabotropic glutamate synapses, in many peptidergic
synapses, and so on. The neurotransmitter activates a 7TM receptor, which then
activates the G-protein system and this, in turn, activates a membrane effector,
often adenylyl cyclase, to generate a second messenger, which diffuses away
into the cytosol. Some 2 to 3 % of the mammalian genome is believed to be
devoted to coding different variants of the 7TM conformation. They form a huge
16
evolutionarily related family.
7TM proteins and G-protein signaling systems also constitute the molecular
bases of many sensory systems. These include photoreceptor cells, the rods and
cones (where the G-proteins are known as transducins), olfactory cells, some,
17
but not all, gustatory cells, and, possibly, some thermoreceptors. We have
already touched on bacteriorhodopsin. Let us now look briefly at the rhodopsins
of the animal kingdom.
Although rhodopsins form the basis for photoreception throughout the
Animalia, invertebrate and vertebrate rhodopsins differ in several ways. For
38 The Evolutionary Neuroethology of Paul MacLean

instance, in the vertebrates the chromophore, retinal, on receipt of an appropriate

photon, detaches from opsin in order to regenerate the all-trans form. In the
invertebrates, in contrast, there is no such detachment. Transformation to the all-
trans form takes place in situ. There are several other differences in detail to
which it would be inappropriate to devote space in this context. Not all animal
eyes are, of course, sensitive to the same wavelengths of light. Some can see far
into the ultraviolet, others into the infrared. The wavelength to which a visual
pigment is maximally sensitive, ^ m a x ?is determined by the precise amino-acid
18,19
make-up of the opsin tunnel surrounding the retinal chromophore. The
dominant mechanism appears to be interaction of the retinal chromophore with
dipolar amino acid side chains in the surrounding helices of the barrel of
20
staves.
Sequence analysis suggests that vertebrate and insect opsins shared a
common ancestor over 750 million years ago. Colour vision based on variation
in amino acid sequence in the vicinity of retinal has evolved separately in the
two lineages. Conway Morris, in his great book on Precambrian palaeontology,
21
The Crucible of Creation, suggests that only certain "morphospaces" are
available for evolution to exploit. So far as photopigments are concerned,
rhodopsin seems to represent the colonisation of one very significant morpho-
space. Furthermore, variation in amino acid composition, independently hit upon
by opsins in the vertebrate and arthropod lines, represents the autonomous
discovery and occupation of available subdivisions of the rhodopsin morpho-
space.

VOLTAGE AND LIGAND-GATED ION CHANNELS

Let us turn from the great superfamily of 7TM, G-protein coupled channels
to the equally ubiquitous, equally important, directly operated ion channels.
There are two cases: Those that respond to voltage changes across the
membrane and those which respond to various ligands; such as Acetylcholine,
Glycine, and GABA. The former respond very rapidly (c. 0.5 msec) to changes
in voltage across the membrane in which they are situated. These are responsible
for all the electrical activity upon which the nervous system depends. The latter,
which are equally important, open (though rather more slowly) to allow the
passage of ions in response to various chemical ligands.
It has been suggested that the great assemblage of ion channels all originated
from the stretch-sensitive channels of prokaryocytes (see Figure 3.3). The latter
channels are ubiquitous. All prokaryocytes need some means of sensing and
responding to osmotic stress (caused, perhaps, by rain downpours). They also
need some means of sensing cell volume in order to trigger cell division. Two
such channels have been analysed in molecular detail in E.colr. the MscL
(mechanosensitive large) channel is unselective; the MscS (mechanosensitive
small) channel is anion selective. Stretch-sensitive channels are also well known
in the metazoa, though not (yet) at the molecular level.
Deep Time and the Brain 39

Prokaryotes

3000 Ma

Earliest prokaryotes

Figure 3 . 3 . Evolutionary Relationships of Voltage and Ligand-gated Ion Channels. Cn =

=
connexin channel; CNG = cyclic nucleotide gated channel; GABA^R gamma-amino-
butyric acid type A receptor; GlyR = glycine receptor; 5HT3R = 5-hydroxytryptamine
2 +
type 3 receptor; nAChR = nicotinic acetylcholine receptor; V G C a = voltage gated
2 + + + + 4
Ca channel; V G K = voltage gated K channel; V G N a = voltage gated Na " channel.

The voltage-gated ion channels (VGICs) of metazoan animals form a family

+
of related proteins. The earliest VGICs are the K -channels succeeded later by
2+ +
Ca -channels. Both these channels are found among the protista. The K
channel is the oldest. The best known type has a 6TM structure with, interposed
between the 5th and 6th TM segments, a "hairpin" conformation which is
+
thought to determine the ion-selectivity of the channel. The fully formed K -
channel consists of a group of four of these 6TM units arranged around a pore.
The hairpin conformation of each of the four subunits forms the lining of the
canal.
+
Because K -channels consist of four independently programmed subunits,
they show great biochemical and hence biophysical diversity. Different combi-
nations of the variant subunits ensure that more than 20 physiologically different
+
K -channels are developed. If the small nematode worm C.elegans genome is
anything to go by many more will be found when the human genome project is
40 The Evolutionary Neuroethology of Paul MacLean

+
complete. Differing populations of these variant K -channels go far to ensure
that each neuron in the brain is physiologically unique: each has its own
"personality."
2 + +
Figure 3.3 shows that voltage-gated C a and N a channels are thought to be
+
derived from the voltage-gated K -channel by two gene duplications. They
consist of a single huge protein (over 1800 amino acid residues) made up of four
+
homologous domains each of which resembles a single K -subunit. The voltage-
+
gated Na -channel has not so far been found in the protista. It appears to have
been invented by stem metazoa for long distance signaling (i.e. nerve impulses).
It is interesting to note that whilst it is found in the Cnidaria (]e\\y fish) it is
absent from the nervous system of the tiny nematode C.elegans.
Figure 3.3 summarises the evolutionary relationships amongst these ion
channels as they are presently understood. The expanding triangles of the figure
indicate the increasing diversity of each receptor over evolutionary time. This
increasing diversity over time was also, of course, a feature of the metabotrobic
receptors discussed in the previous section. At least twelve different types of G-
protein coupled 5HT receptor are known. The structural and hence biophysical
diversity of metabotropic receptors is increased yet further by the heterogeneity
of G-protein subunits and second messengers. It is also worth noting in Figure
3.3 that ligands did not gain control over ion channels until quite late in
evolutionary history and have subsequently undergone rather rapid and rather
huge diversification: 60 subtypes of nACh-R; 40 subtypes of GABA^-R, and so
on. When one speaks of "the" nACh-R, for instance, or of "the" 5HT-R, one is
not referring to a unique molecular structure such as, for instance, glucose or
phenylalanine, but of a whole family of similar molecules. The brain is
heterogeneous all the way down.

MOLECULAR EMBRYOLOGY

Molecular embryology is a vast and extremely rapidly developing subject.

The early control of the development of dorsoventrality in vertebrates and
invertebrates was mentioned in a previous section. It is impossible to do more
than merely point to one or two further relevant examples in a chapter such as
this. In this section, therefore, I shall merely outline a couple of cases that show,
at the molecular level, that animals retain hidden potentialities which can be
uncovered in appropriate circumstances. Can we see this as a molecular parallel
22
to Gardner's "psalics" or of MacLean's ideas on the uncovering of what he
calls "palaeomentation" in neuropathology? I'd like to mention two cases: the
23
work by Kollar and Fisher on hens' teeth and the recent work on Pax-6 and
24,25
eye development.
Kollar and Fisher note that embryonic induction can normally be got to work
between tissues of different origin, suggesting that the molecular mechanisms lie
latent and conserved. They point out, first, that undifferentiated chick corneal
epithelium responds to mouse dermis by producing feathers. Differentiation, in
Deep Time and the Brain 41

other words, proceeds in a way determined by the genetic repertoire of the

responding tissue. But, more interestingly, they provide evidence to show that if
mouse dental papilla are combined with chick epithelium, the latter is induced to
secrete dentine and enamel and the beginnings of teeth: Something not seen in
the avian line since the time of Archaeopteryx, more than a hundred million
years ago. It seems that the genetic information necessary for producing teeth
lies dormant in the chick, awaiting an appropriate trigger. It has not been lost
during a hundred million and more years of evolution.
In the last few years molecular genetics has begun to give us other fascinat-
ing hints of molecular commonalities. Some of the most interesting work has
concerned the ancestry of eyes. The question has often been asked, when
reviewing the vast variety of complex eyes developed in the animal kingdom:
did all these different designs arise independently, or do they share a common
ancestry? The answer may well be provided by study of the molecular biology
of early development: it is beginning to look as if a common ancestor can be
traced back to before the proterostome/deuterostome divergence some 670
million years ago. The evidence for this remarkable conclusion comes from
study of a gene known as Pax-6.
Pax-6 is one of a number of genes involved in the early development of eyes.
As its suffix number indicates it is a member of a large family of genes which
regulate the transcription of other genes. The family plays an important role
early in early embryology when its members control the transcription of
cascades of other developmental genes. The nomenclature, Pax, refers to the fact
that these genes all possess a 384 base-pair (bp) sequence which encodes a 128
amino-acid sequence that binds to DNA. This 384 bp sequence is known as the
"paired box" (hence Pax) motif since it was first found in the pair rule genes that
determine the early segmentation of Drosophila embryos. In addition to the
paired domain, all members of the Pax family share a highly conserved
homeodomain.
Pax-6 has been found in many different species of animal, from humans
through insects and molluscs to round worms (nematodes) and ribbon worms
(nemertines). In the early vertebrate embryo Pax-6 expression is at first widely
distributed in the central nervous system and it can still be detected in the adult
brain, especially in some of the nuclei of the forebrain, the substantia nigra of
the midbrain and the granule cell layer of the cerebellum. So far as the forebrain
is concerned, its expression becomes largely confined to the regions destined to
develop into olfactory (olfactory epithelium, olfactory bulb) and optic (lens,
cornea and optic vesicle) structures.
Mutations of Pax-6 have disastrous effects. In the mouse they cause a
condition known as small eye (Sey). In the heterozygous condition Sey mice
eyes have significantly smaller lenses and optic cups. Homozygous Sey is lethal.
Early mice embryos (9.5 days) show no lens placode and the neural layers of the
retina are highly abnormal. The olfactory placode, similarly, fails to develop,
and the embryo shows no sign of nasal pits nor an olfactory bulb. Clearly, Pax-6
plays a crucial role in the early development of eye and nose. Humans,
heterozygous for Sey suffer from a condition known as aniridia. In this
42 The Evolutionary Neuroethology of Paul MacLean

condition there is a complete or partial failure of the iris to develop along with
other defects including cataract, corneal opacity, glaucoma and so on. The
incidence lies between 1/64 000 and 1/96 000. In addition, mutations of Pax-6
can lead to defects in the anterior chamber of the eye, including opacity of the
central cornea, known as Peter's anomaly. In fact, differences in the degree of
inactivation of Pax-6 lead to a large number of ocular defects affecting nume-
rous parts of the eye, especially the anterior chamber.
As indicated above, Pax-6 is found throughout the animal kingdom.
Drosophila geneticists have shown that it is possible to transplant the gene into
other parts of the embryo insect's anatomy where it will induce "ectopic" eyes.
Eyes can be induced in legs, antennae, wings, and so on. The insect can be
covered with eyes! These eyes, moreover, are no mere approximations to the
real thing. They consist of a full complement of different cells and structures:
primary, secondary and tertiary pigment cells, cornea, cone and pseudocone
cells, retinula cells with fully developed rhabdomeres, and so on. The cells are
organised to form ommatidia and are electrically active. It is not yet known,
however, whether the optic nerve fibres project to the correct regions of the
insect's brain. Here, then, is a striking instance of latent morphopoietic mechan-
isms waiting to be triggered or "uncovered" in insect cells.
Further work has shown that Pax-6 extracted from embryo mice will also
induce ectopic eyes (not, of course, mouse eyes!) in Drosophila. Finally, it has
been found that Pax-6 from squid, normally essential in the early development
of cephalopod's highly evolved eye, can also induce ectopic eyes in Drosophila.
These eyes, again, are anatomically almost normal. Both squid and mouse eyes
are vesicular eyes bearing no obvious resemblance to the compound eyes of
arthropods.
All of these findings appear to point in one direction. They suggest that very
early in the evolution of the animal kingdom, perhaps at the stage represented by
the urbilateralia, a genetic system evolved to program the development of
complex eyes. This system has remained, essentially unchanged, at the basis of
all the huge variety of different complex animal eyes. Instead of a polyphyletic
origin it may be that all eyes, above the level of simple eyes (eyespots), or ocelli,
have a unitary origin. At the time of writing the jury is still out. But, taken
together with the other evidence from molecular biology discussed above, the
story of the Pax-6 gene reinforces the gathering vision of a remarkable unity in
diversity throughout the animal kingdom. We look down through more than half
a billion years and recognise ourselves.

CONCLUSION

In this chapter, I have briefly reviewed a few salient examples of the

molecular evolution of the brain. With the huge torrent of data deluging from the
laboratories of molecular biology, our understanding of the evolutionary past of
the human brain is bound to increase dramatically in the twenty-first century. It
is not only the human genome project that is nearing completion, but we shall
Deep Time and the Brain 43

soon have complete data on the mouse, Mus, the fruit fly, Drosophila, the
Zebrafish, Danio, and so on. The total genome (10, 099 genes; 97 Mbp) of the
26
nematode, Caenorhabditis elegans, was published in 1998. It appears that over
30% of the genome codes for the nervous system. Neurotransmitter receptors,
synthesis and release systems, all show remarkable molecular similarity to those
found in Homo sapiens and other mammals. The genome contains genes for
+ 2+
over 80 V G K channels, 9 V G C a channels and some 90 neurotransmitter-
27
gated channels (LGICs).
Locked up in the deluge of data from the molecular biology and molecular
neurobiology labs will be many messages detailing the evolutionary history of
the brain. Messages which will make those described in the foregoing pages pale
into insignificance. Nevertheless, even our present understanding reminds us, at
the molecular level, of MacLean's theory. The molecular mechanisms at work in
our brains, the synaptic receptors and ion channels upon which that
neurophysiology is built, reach back deep into time, to origins in the precam-
brian. Their molecular sequences speak to us of the relatedness of all living
forms. Locked up in within them are messages which hint at dramatic events in
the remote past: such as the genome duplications mentioned earlier. Molecular
embryology, furthermore, reveals that ancient systems persist, often overlaid by
more recent strata, but still waiting for, and capable of, being triggered or
uncovered by appropriate stimuli. Does this not remind us, at the molecular
level, of Paul MacLean's evolutionary neurobiology and evolutionary neuro-
psychiatry? We are thus, I believe, fully justified in concluding that the message
of the molecules is entirely consistent with his vision. The human brain is
conditioned by, and bears the mark of, the "vast backward and abysm" of
evolutionary time.

NOTES

1. Spencer, Herbert, 1855, The Principles of Psychology, London: Longman, Brown,

Green and Longmans; see also C.U.M. Smith, 1982, "Evolution and the Problem of
Mind, Part 1: Herbert Spencer," Journal of the History of Biology, 15, 55-88.
2. See Smith, C.U.M., 1982, "Evolution and the Problem of Mind, Part 2: John
Hughlings Jackson," Journal of the History of Biology, 15, 241-262.
3. MacLean, P.D., 1990, The Triune Brain in Evolution: Role in Paleocerebral
Functions. New York: Plenum, p. 13.
4. Maynard Smith, J. and E. Szathmary, 1995, The Major Transitions in Evolution,
Oxford: Freeman.
5. Lake, J. and J. Moore, 1998. "Phylogenetic analysis and comparative genomics,"
Trends in Bioinformatics, pp.22-24, Cambridge: Elsevier; see also H. Philippe and J.
Laurent, 1998, "How good are deep phylogenetic trees?" Current Opinion in Genetics
and Development, 8, 616-623.
6. Kimura, M., 1994, Population Genetics, Molecular Evolution and the Neutral
Theory, ed. N. Takahata, Chicago: University of Chicago Press.
7. See C.U.M. Smith, 2002, Elements of Molecular Neurobiology (3rd edition),
Chichester: Wiley.
44 The Evolutionary Neuroethology of Paul MacLean

8. Douglass, J., O. Clivelli and E. Herbert, 1984, "Polyprotein gene expression,"

Annual Review of Biochemistry, 53, 665-715.
9. Sidow, A., 1996, "Gen(om)e duplications in the evolution of early vertebrates,"
Current Opinion in Genetics and Development, 6, 715-722.
10. Morata, G. and E. Sanchez-Herrero, 1999, "Patterning mechanisms of the body
trunk and appendages in Drosophila," Development, 126, 2823-2828.
11. Ariens Kappers, C , 1919, "Phenomena of neurobiotaxis as demonstrated by the
position of motor nuclei of the oblongata," Journal of Nervous and Mental Disorders, 50,
1-16. A modern discussion of neurobiotaxis may be found in Nieuwenhhuys, R., H., J.
Ten Donkelar and C. Nicholson, 1998, The Central Nervous System of Vertebrates,
Berlin: Springer Verlag.
12. E. de Robertis and Y. Sasai, 1996, "A common plan for dorsoventral patterning in
bilaterali," Nature, 380, 37-40.
13. Darwin, C.R., 1837, B Transmutation Notebook: p. 232 in P. H. Barrett, 1980,
Metaphysics, Materialism and the Evolution of Mind: Early Writings of Charles Darwin,
Chicago: University of Chicago Press.
14. Henderson, R., et al., 1989, "Model for the structure of bacteriorhodopsin based
on high resolution electron cryo-microscopy," Journal of Molecular Biology, 213, 8 9 9 -
929.
15. Smith, C.U.M., 1995, "Membrane signaling systems," in Anthony Lee, ed., Bio-
membranes, vol. 1: General Principles, Greenwich, Ct: JAI Press, pp.245-270.
16. Fryxell, K. J and E. M. Meyerowitz, 1991, "The Evolution of rhodopsins and
neurotransmitter receptors," Journal of Molecular Evolution, 33, 367-378.
17. Smith, C.U.M., 2000, The Biology of Sensory Systems, Chichester: Wiley.
18. Nathans, J., D. Thomas and D. Hogness, 1986, "Molecular genetics of human
colour vision: the genes encoding blue, green and red pigments," Science, 232, 193-202.
19. Yokoyama, S., 1995, "Amino acid replacements and wavelength absorption of
visual pigments in vertebrates," Molecular Biology and Evolution, 12, 53-61.
20. Kocheudoerfer. G. G., et al., 1999, "How color visual pigments are tuned,"
Trends in Biochemical Sciences, 24, 300-305.
21. Gardner, R., 1988, "Psychiatric syndromes as infrastructure for intraspecific
communication" in M.R.A.Chance, Ed., Social Fabrics of the Mind, Hove and London:
Lawrence Erlbaum.
22. Morris, S.C., 1998, The Crucible of Creation, Oxford: Oxford University Press.
23. Kollar, E. and C. Fisher, 1980, "Tooth inductions in chick epithelium: expression
of quiescent genes for enamel synthesis," Science, 207, 993-995.
24. Callaerts, P., G. Haider and W. J. Gehring, 1997, "Pax-6 in development and
evolution," Annual Review of Neuroscience, 20, 483-532.
25. Tomarev, S. I; P. Callaerts; L. Kos; R. Zinovieva; G. Haider; W. Gehring and J.
Platigorsky, 1997, "Squid Pax-6 and eye development," Proceedings of the National
Academy of Science, 94, 2421-2426.
26. The Celegans sequencing consortium, 1998, "Genome sequence of the Nematode
Celegans: A Platform for Investigating Biology," Science, 282, 2012-2018.
27. Bargmann, C.L, 1998, "Neurobiology of the Caenorhabditis elegans Genome,"
Science, 282, 2028-2033.
 4
A D A P T I V E FUNCTIONS OF THE CORPUS
STRIATUM: T H E P A S T A N D FUTURE OF
THE R - C O M P L E X

Neil Greenberg

INTRODUCTION

As Paul MacLean indicated the basal ganglia is emerging from the shadow cast
by the most conspicuous clinical expression of its dysfunction: motor disorders.
What is revealed is the nexus of a widely distributed system which functions in
integrating action with cognition, motivation, and affect. Prominent among non-
motor functions are striatal involvement in building up of sequences of behavior
into meaningful, goal-directed patterns and repertoires and the selection of
appropriate learned or innate sequences in concert with their possible predictive
control. Further, the striatum seems involved in declarative and strategic
memory (involving intentional recollection and the management of retrieved
memories, respectively). Findings from reptile experiments indicate striatal
control over specific assemblies of innate units of behavior that involve autono-
mic modulation. Its involvement in the appropriate expression of species-typical
action patterns in reptiles and primates provides an interesting vantage point
from which to interpret its involvement in the assembly of units of behavior into
specific adaptive behavioral patterns.

THE BASAL FOREBRAIN AND STRIATAL COMPLEX

ANATOMY AND CONNECTIONS

"Basal ganglia" is the term most favored by clinicians for the striatal
complex—an array of structures collectively called the R-complex by Paul D.
MacLean ("R" for "reptilian)." It includes the corpus striatum (caudate and
putamen). The putamen is so intermeshed with an afferent projection (the globus
pallidus) that the two structures are occasionally regarded together as the
lenticular nucleus. The nucleus accumbens—once regarded as part of the septum
46 The Evolutionary Neuroethology of Paul MacLean

or olfactory system—is, along with the olfactory tubercle, sometimes called the
"olfactostriatum" in higher primates, and it is now viewed as a medial extension
of the caudate-putamen in mammals. The caudate, putamen, and globus pallidus
are sometimes referred to collectively as "neostriatum" while nucleus
accumbens, olfactory tubercle, and ventral pallidum are called "paleostriatum."
These terms suggest relative phylogenetic antiquity that Butler and Hodos
(1996) find unwarranted, and so they term these aggregates dorsal and ventral
"striato-pallidal complex," respectively, in their recent textbook of comparative
vertebrate neuroanatomy. The collection of structures includes adjacent gray
matter termed substantia innominata which encompasses nucleus basalis (the
basal nucleus of Meynert) which is well interdigitated with the overlying
lenticular nucleus.
Although often included in the basal ganglia because of topology, MacLean
did not include the amygdala and claustrum. The amygdala has multiple con-
nections with the hypothalamus and is regarded as part of the limbic system
although it may well function as the major mediator of interactions between
limbic and striatal functions. The claustrum has no known major connections
with core striatal structures. Neither did MacLean define substantia nigra as part
of the striatal complex but he discussed its outputs in concert with those of the
striatum because of the similarities of its pars reticulata to globus pallidus.
Andre Parent (1986) proposed as core structures, the dorsal striatum (caudate
nucleus, putamen), ventral striatum (nucleus accumbens and part of the olfactory
tubercle), and the pallidum. As associated structures, he identified the sub-
stantia nigra, ventral tegmental area, and subthalamic nucleus (see Table 4.1).
The core structures, striatum and pallidum, which originate in the lateral and
medial parts of the developing telencephalon along with the associated
structures, are now often regarded as a basal ganglia system. The structural plan
is very conservative and manifest from amphibians through reptiles, birds, and
mammals (Marin, Smeets & Gonzalez 1998). In the dorsal striatum, chemo-
specific stains reveal that two classes of chemically (and probably functionally)
specific cells are present. Strands of cells called "striosomes" are embedded in a
larger "matrix" and appear to possess reciprocal connections with the dopa-
minergic cells of the substantia nigra. They thus have the potential to regulate
dopaminergic activity, and indeed, stimulation in or near a striosome is more
likely to evoke self-stimulation by an animal that can control its own electrode.
The matrix consists of neurons that participate in paths between cortical areas
and lower centers.
Parent and Hazrati (for example, 1995a, 1995b) incorporate striatum, palli-
dum, and substantia nigra, along with the subthalamic nucleus as basal ganglia.
While the first three are regarded as main axis, the subthalamic nucleus, along
with the pars compacta of substantia nigra, the centromedian/ parafascicular
thalamic complex, dorsal raphe and pedunculopontine tegmental nucleus are
regarded as control structures that provide various neurochemical modulation
(Parent and Hazrati 1995b). They reviewed the anatomical details of cortico-
striatal projections, the intrinsic organization of the striatum, the striatofugal
system, and the output structures of the striatum, positing a cortico-basal
Adaptive Functions of the Corpus Striatum 47

ganglia-thalamocortical loop. The unexpected complexity of intrinsic organi-

zation and the orderliness of its highly structured repetitive units make it ideal
for selective control of psychomotor functions.

Table 4.1. Structures of the Mammalian Basal Ganglia*

CORE STRUCTURES

Striatum
caudate and putamen (sometimes "dorsal" or "non-limbic striatum"),
ventral striatum (sometimes, "limbic striatum"), n accumbens and part of
olfactory tubercle; = olfactostriatum

Pallidum (globus pallidus)

external segment
internal segment (entopeduncular n in nonprimates)
ventral pallidum (comprising part of the substantia innominata)

ASSOCIATED STRUCTURES

Substantia Nigra (reciprocal connections with caudate and putamen)

Ventral Tegmental Area (reciprocal connections with ventral striatum)
Subthalamic Nucleus (reciprocal connections with pallidum)

Note: * Adapted from Parent (1986).

To clarify the basal ganglia's potential for information processing, Parent

and Hazrati (1995a) analyzed the anatomy (as above) and considered the
evidence they provide for two views of information processing: the "parallel
processing" and the "information funneling" hypotheses. As Parent and Hazrati
characterize these, parallel processing involves processing different kinds of
cortical information through well-segregated cortico-basal-ganglia-thalamo-
cortical loops. Information funneling, on the other hand, is informed by the fact
that striatal axons from distinct functional areas are received by widely
arborizing dendrites of pallidum and substantia nigra. Parent and colleagues
(references in Parent & Hazrati 1995a) have used new and highly sensitive
anterograde tract-tracing to determine that there is extensive dendritic
arborization of pallidal and nigral neurons that could in principle lead to
convergent "funneling." But such an apparent convergence does not mean that
functional specificity is thereby lost—they acknowledge that they have yet to
ascertain if specificity is retained in the loops from cortex to basal ganglia to
thalamus to cortex.
48 The Evolutionary Neuroethology of Paul MacLean

STRIATAL CONNECTIONS WITH THE

CEREBRAL CORTEX AND THEIR POSSIBILITIES

The rich connections the striatum receives from the cortex feed forward into
other parts of the basal ganglia such as the internal and external pallidum, and
from the internal pallidum to the thalamus and thence back to the cortex. This
one-way traffic involving inhibitory as well as excitatory synapses consists of a
fairly well-separated parallel pattern. In Edelman's view, this pattern is ideally
suited to effect independent neural routines. But further, because of the way
these isolated parallel loops are connected to the thalamocortical system with its
dynamic reciprocities, these routines would remain, in Edelman and Tononi's
(2000) view, unconscious for cognitive routines much like those of motor
programs. These routines within the basal ganglia or between the basal ganglia
and cortex might then compete for representation in the cortex in a way that
maintains the seeming "unity of behavior and thought," and explains why we
tend to have or implement one conscious activity at a time (Edelman & Tononi
2000: 186).
The basal ganglia seem as important as the prefrontal cortex in the analysis
of serial order in which events or perceptions are detected and the control of
behavior based on such information. Beiser and Houk (1998) noted that frontal
lobe patients and those with Huntington's or Parkinson's disease can manifest
strikingly similar deficits. This led them to propose a model to gain insight into
the ways the prefrontal cortex and basal ganglia work to transform sequences of
input into patterns of neural activity. The model involves an encoding process
whereby the serial order of stimuli is represented as a spatial pattern of neural
activity, utilizing topographically specific circuits that loop from prefrontal
cortex through basal ganglia and thalamus and then back. Recurrent cortico-
striatal projections and collateral inhibition between striatal spiny units were
able, then, to sustain representations of contextual events in working memory.
A decoding process would then transform spatial patterns of neural activity to
sequences of actions.

The Interface: Nucleus Accumbens

The nucleus accumbens, a dominant part of the ventral striatum, is the

leading candidate for the interface between sites that integrate affective, motiva-
tional, and cognitive functions with action. As MacLean (1990) points out, as
the recipient of limbic (hippocampal and amygdalar) inputs, and by virtue of its
projections to ventral pallidum and substantia nigra, the accumbens is often
regarded as the key limbic-motor interface (for example, Mogenson et al. 1980).
"An important link between the motivational-emotional parts of the brain and
certain effector regions," as Groenewegen et al. (1996: 510), put it. Graybiel
(1997) goes further in speculating that "this limbic basal ganglia system has a
key function in translating action plans related to drive states and homeostatic
Adaptive Functions of the Corpus Striatum 49

control into action repertoires" (p. 460) or stereotyped responses (such as "fixed
action patterns") in general.
For example, the accumbens has been linked to the highly stereotyped
behavior of laughing, whether in response to a joke or contagious laughter, by
means of MRI (Shibata et al. 2000). Different causes of laughter were inter-
preted at other sites (ventromedial frontal lobe for "getting it" or anterior
supplemental motor area for contagious laughter), but all scans also showed
activity in the nucleus accumbens.
While the accumbens is also often associated with appetitive motivation (for
example, Paradiso et al. 1999) and reward (Wise & Bozarth 1984; other refer-
ences in Paradiso et al. 1999), various stressful situations evoke dopamine
release in accumbens (Salamone 1994; but not the nigrostriatal system; Herve et
al. 1982; Thierry et al. 1976, in: Bowers et al. 1987).
Accumbens is also prominently associated with negative emotional valence
in adult humans shown pictures designed to evoke affect. Subjects whose brains
were being scanned by positron emission tomography (PET) while being shown
neutral, negative, or positive affect-evoking pictures manifested different pat-
terns of activity depending on the stimulus. Negative valence would reasonably
dominate an aversive or avoidance situation while positive valence implies a
pleasant or approach situation. When compared to the effects of a neutral
stimulus, viewing unpleasant pictures stimulated increased blood flow primarily
in limbic striatum, including nucleus accumbens. Pleasant pictures, on the other
hand, evoked increased activity in the phylogenetically newer cortical limbic
areas including prefrontal cortex (Paradiso et al. 1999). The authors suggest that
detection and rapid stereotyped response to avoidance situations is reasonably
coordinated with older, conserved mechanisms, but the basal ganglia may in
Graybiel's (1995) view also be a critical part of a distributed forebrain system
that helps assemble and express learned as well as innate sequences of behavior.
Indeed, Graybiel feels evidence is accumulating that basal ganglia may parti-
cipate significantly in planning and cognition (1997).

Neurochemistry, Neuroendocrinology

The known and growing understanding of basal ganglia connections is

converging with findings about regional histochemistry. As Graybiel has pointed
out, basal ganglia contains "a remarkable diversity of neuroactive substances
organized into functional subsystems that have unique developmental histories
and vulnerabilities in neurodegenerative diseases" (1990: 254). Although the
neurotransmitter dopamine (DA) is prominently associated with the basal
ganglia because of the famous clinical manifestations of an insufficiency or
excess, the neurotransmitter of most striatal neurons is gamma aminobutyric
acid (GABA). GABA is present in striatum (as in hypothalamus) in relatively
high concentration as are the opiate-like endorphins, receptors for which were
found in high concentration in the corpus striatum. In fact, as MacLean (1990)
emphasizes, endorphin concentrations are several times higher in the external
50 The Evolutionary Neuroethology of Paul MacLean

segment of the globus pallidus than in other cerebral structures. Substance P a 5

vasodilating agent described in the 1930s, was found about 20 years later to
exist in high concentrations in the medial segment of the globus pallidus, as well
as caudate nucleus and hypothalamus.
Dopamine (DA) is the neurotransmitter most prominently associated with the
basal ganglia, and indeed, across taxa, it is one of its most conservative traits
(see Marin, Smeets & Gonzalez 1998). In mammals, different subclasses of
dopaminergic receptors, Dl and D2 are associated with the so-called direct and
indirect basal ganglia subsystems, respectively. These pathways represent the
conceptual if not anatomical basis for understanding of motor control and their
disorders. These systems are recently viewed in terms of an "opponent parallel
pathway hypothesis" in which direct and indirect systems compete with each
other to cause net inhibition or excitation of activity, respectively. This is similar
to Mink's (1996) "focused selection and inhibition hypothesis," in which a
specific motor program is activated while competing programs are broadly
inhibited. In either event, motor activity is perceived as the outcome of a balance
in activity of these pathways maintained in part by activation of Dl and D2
dopamine receptors. Thus, if the direct pathway predominated, motor activity
might be excessive (as in Huntington's disease) and if the indirect pathway was
relatively more active, Parkinsonian poverty of movement might be seen
(Graybiel 2000). Interestingly, Dl and D2 receptors can be seen in a laminar
pattern in lizards (Clark et al. 2000, see below).
In the mammalian brain, DA is found principally in the substantia nigra,
from whence it is projected to caudate/putamen (dorsal striatum), and in the
ventral tegmental area, the mesolimbic projection of which supplies forebrain
sites (including nucleus accumbens, olfactory tubercle, amygdala, septal area,
and the prefrontal cortex). There is also a dopaminergic projection from the
hypothalamus to the median eminence (where it modulates reticular formation
output), in a system around the fourth ventricle, and in local circuits intrinsic to
the retina, olfactory bulb, and the optic tectum.
The functional specificity of alternative projections was underscored by the
finding that a single gene (in the mutant mouse, weaver) could differentially
cause severe dopamine depletion in the mesolimbic and nigrostriatal systems
affecting the "nonlimbic" dorsal (caudate/putamen) but not the "limbic" ventral
(including n. accumbens) striatum (Roffler-Tarlov & Graybiel 1984). While
diseases of the basal ganglia can impair learning of sensorimotor skills, the
effects, according to Gabrieli (1998), are not uniform. Repetitive tasks appear
basal ganglia-dependent while tasks requiring new associations apparently
depend on the cerebellum. Alternatively, Gabrieli suggests that open-loop skill
learning (depends on planning and delayed feedback about errors) is cerebellar,
while closed-loop skill learning (continuous feedback about errors) is striatal.
Adaptive Functions of the Corpus Striatum 51

Striatal Functions and Dysfunctions

The R-Complex is the basal "reptilian" structure in Paul MacLean's well-

known heuristic model, the triune brain, reflecting the predominant behavioral
functions believed to have been first integrated in its constituent neural
structures in evolutionary time (MacLean 1990).
Of course, neural structures and systems continue to evolve after the initial
innovation that provided an advantage in its initializing environment of
evolutionary adaptiveness, and other structures can come to coordinate compar-
able behavioral patterns. The idea of the triune brain remains controversial, in
part because of its vulnerability to oversimplification, but the basic idea of a
nested hierarchy of structures is attractive. Point-to-point continuity, however,
cannot be expected. For example, as MacLean points out, the newest (thalamo-
cingulate) part of the limbic system has no representation in reptiles (1990: 247).
The basal ganglia are prominently associated with motor control, probably
because of the dramatic, often devastating effects of dysfunction on movement
(see below). Although an array of corollary functions such as motor learning and
automatization were long suspected, only recently are these structures coming to
be understood as indispensably involved in many functions (and dysfunctions)
beyond those traditionally ascribed to it (cf. Tables 4.1 & 4.2). Ann Graybiel's
observations that the basal ganglia have learning and memory functions driven
by cortically-derived information, identifies them as likely key components in
an assortment of behavioral disorders not commonly associated with striatal
dysfunctions (for example, 1997, 2000).
The comparative approach has brought forth some of the best insights when
unlikely constraints on behavior or an unexpected expression of an organism's
potential are manifested. A sense of the evolutionary process is evoked when
specific traits in various taxa are compared. When they are seen to be related
through a possible common ancestor, we can posit a homology between them
and explore the ways in which the function of a putative ancestral trait can be
adapted by circumstances to the needs of the organism. When comparable
functions are performed by fundamentally dissimilar structures, we suspect they
are analogous and can speculate on the capacity of organisms to cope in
different ways to similar selection pressures. There is a long history of looking
to ethology to provide possible models for understanding dysfunctional behavior
(White 1974; McGuire & Fairbanks 1974).
Another powerful way of envisioning the possibilities and constraints of
neural structures is through dysfunction, and the basal ganglia are significant
participants in several disorders that provide interesting clues. The study of basal
ganglia functions presents a wonderful exemplar of the "logic of the lamppost."
Employing this seductive mode of reasoning, traditionally treated by analogy
with looking for lost keys in a dark parking lot where we can search only under
the illumination of a solitary lamppost, we tend to forget that the keys may yet
be discovered some place in the darkness. Our illumination until recently has
been the more easily discerned evidence of motor dysfunction as a consequence
of striatal damage.
52 The Evolutionary Neuroethology of Paul MacLean

Table 4.2. Putative Functions of the Basal Ganglia*

Motor Functions
•initiates motor patterns of cognitive or motivational significance (Heimer
etal. 1982)
•motor sequence planning, coordination (Graybiel 1995)
•inhibition of competing motor programs (Mink 1996)

Sensory Functions
•somatosensory motor control (Schneider & Lidsky 1981; other refs in
Brown etal. 1997)
•somatosensory discrimination; pain (see Brown et al. 1997)
•visual discrimination (Pribram 1977) including facial expression and
•hallucinations (Middleton & Strick 1996, other refs in Brown et al. 1997)
•auditory (see Brown et al. 1997)

Cognitive Functions
•cognitive sequence planning ("acquisition, retention, and expression of
•cognitive patterns" Graybiel 1997)
•expectations, prediction (ventral striatum, Schultz et al. 1992; Schultz
1998)
•attention (Schneider 1984; Parent 1986: 247; Brown and Marsden 1998;
Hayes etal. 1998)
•categorizing (tactile stimuli, Merchant et al. 1997)
•learning (Jueptner et al. 1997); procedural memory (for habits and skills:
Jog et al. 1999); habit learning & acquisition of nonmotor dispositions
and tendencies (Knowlton et al. 1996)
•classify spatial patterns and serial ordering of sensory events (Beiser &
Houk 1998)
•executive function ("focused and sustained attention in concert with
flexibility of thought . . . planning and regulation of adaptive and goal
directed behavior . . . [utilizing] working memory" (Peigneux 2000; and
see Brown et al. 1997)
•creativity (ventral striatum becomes activated when predictions are
violated by stimuli that appear in an unexpected context: references in
Cotterill 2001).

*Note. Adapted from Brown et al. (1997), Parent (1986), and MacLean (1990) and others. These
are exemplars of research reports and reviews that demonstrate or suggest the diversity of
functions in which the basal ganglia (see Table 4.1) integrates or participates; no attempt has been
made to be exhaustive.
Adaptive Functions of the Corpus Striatum 53

Motor Functions

Deficits in motor behavior correlated with basal ganglia damage or insuffi-

ciency have dominated perceptions of its function for generations, but among
the symptoms of the "shaking palsy" described early in 1817 by James
Parkinson was also an impairment of intellectual and cognitive processes
("bradyphrenia") with an associated depression sometimes preceding the more
overt neurological symptoms. MacLean (1990) pointed out that despite a
century of prominent textbooks of neurology expressing great caution, if not
reserve, about regarding the basal ganglia as an organ of motor control, popular
textbooks continued to make the point. Autonomic dysfunctions are also present
and physical or psychological stress can alter the clinical profile in one of two
ways: "freezing," an exacerbation or precipitation of neurological deficits, or
"paradoxical kinesia," a sudden transient remission of bradykinesia when
confronted with a life-threatening emergency (Zigmond, Strieker & Berger,
1987). The extraordinary expression of motor effectiveness in otherwise dys-
kinetic Parkinson patients under conditions in which compelling stimuli are
suddenly presented (see Brown & Marsden 1998, above), suggests the neuro-
logical components of the emergency stress response may be involved (see
Greenberg 2001).
Another intriguing dimension of Parkinsonism is an apparently faulty
internal model of movement: when an unimpaired person is following the
trajectory of a moving target, he can extrapolate to fill in a brief gap in visual
feedback, while the Parkinson's patient cannot, and seems to lose track. This
seems related to the fact that while initiation and execution of motor patterns are
affected in Parkinson's, accuracy is largely unimpaired as long as there is
feedback from other senses. Indeed, other senses can seemingly ameliorate the
disorder (see Stein 1986). Mink (1996) views motor dysfunctions less as a
failure to generate the proper signals than as the result of a failure to
successfully inhibit one of several possible competing motor programs that
originated with the cerebral cortex or cerebellum.

Stereotyped Behavior: Fixed Action Patterns, Stereotypies, and

Obsessive-compulsive Behavior

Another significant class of motor-related basal ganglia functions are stereo-

typies and stereotyped "fixed action patterns," which likely share more than
mere etymology. Stereotyped behavior involves fixity of form. Social displays
are among the most prominent of these and are excellent exemplars of the
evolutionary process of ritualization—the progressive fixity in form that
develops over evolutionary time (Morris 1956; Huxley 1966). The stereotypy of
a display functions to reduce its ambiguity as a communicative signal and
enhance the precision of stimulus control. These displays are often cobbled
together from fragments of motor patterns and autonomic reflexes and can
confer clear adaptive advantages. Unlike most learned or automatized motor
54 The Evolutionary Neuroethology of Paul MacLean

patterns, they are presumed to be heavily influenced by genetics but subject to

specific shaping during early development (Hailman 1969).
Highly aroused, energized individuals may repeat stereotyped patterns
frequently; but such displays also resemble clinical stereotypies, typically
expressed at levels of repetition that are clearly inappropriate or dysfunctional.
While most dysfunctional stereotypies are manifest in abnormal contexts such as
zoos or laboratories or as a result of trauma or extreme stress (discussed below),
the stereotyped nature of adaptive expressions of behavior is observed to be
spontaneously expressed in natural habitats. The form of such ethological
stereotypies, often termed "fixed action patterns" by early ethologists (Heymer
1977; Tinbergen 1951) might involve complex motor sequences and were
presumed to be under genetic control. Once triggered by an appropriate stimulus
(a "sign stimulus" or "releaser"), the sequence was invariably completed.
Among the most interesting of fixed action patterns are those that serve
communications. Most displays have evolved from motor patterns or autonomic
reflexes with externally detectable expression; they have evolved under a
selection pressure to be unambiguous (Morris 1956) and are often used by
animals to discriminate members of their own species. Such species-typical
behavioral patterns, particularly social displays, have provided much robust data
to illuminate neural corollaries of complex behavioral functions. MacLean
(1978) demonstrated that lesions of the globus pallidus in the area where fibers
converge to form the ansa lenticularis, or of the ansa itself, impaired a species-
typical "greeting" display in the squirrel monkey, probably by interrupting the
pallidal projection to the tegmental area.
The head-bobbing display of the green anole (described below) is such a
stereotyped "greeting" display. Imposed upon the stereotyped bobbing pattern
are slight variations such as number of bobs, forelimb contribution to the
bobbing movement, erection of a slight nuchal crest, or erection of a hyoid bone
that extends a conspicuous dewlap, that can modify the message to indicate
aggressive or reproductive motivation. The expression of these and related units
of behavior is presumed to have become progressively more precise and
stereotyped because of an advantage that precision confers, such as the correct
identification of the species or gender doing the display. For example, the
anole's "signature" display, while precisely executed, is evoked by a broad
spectrum of situations but units of behavior are added or deleted to modify the
core display and send different messages (Jenssen 1978, 1979).
In a sense, stereotypies can be viewed as efforts to reduce stress or discharge
high arousal levels channeled by circumstance. Inappropriate motor patterns or
their expression in a dysfunctional context characterize dysfunctional stereo-
typies, and their possible function in reducing stress or arousal levels recalls
Freud's famous idea that a neurosis is an attempt at self-therapy. Indeed, in
addition to stereotypies, behavioral patterns such as eating, aggression, and
sexual behavior in response to mild stress have been characterized as
"chemotherapy without drugs" (Antelman & Caggiula 1980). Their expression
may be significantly affected by progressive sensitization of underlying neural
mechanisms attributable to positive feedback from the expression of the
Adaptive Functions of the Corpus Striatum 55

behavioral pattern. This possibility has informed the Jacksonian view that
stereotypies are expressed when higher nervous functions fail to control motor
patterns organized at a lower level (Dantzer 1986).
Dysfunctional stereotypies in humans are associated with schizophrenia and
early autism where they appear in apparent independence of the environment,
and in captive animals or those impaired by brain damage or dopamine-affecting
drugs, where they appear more context dependent. Repetitive patterns as rocking
movements, grooming patterns, vocalizations, and pacing, although apparently
rooted in adaptive behavioral patterns, can rapidly become dysfunctional.
Clinicians associate them with frustration such as that when a selection cannot
be made between incompatible alternatives. A stressfully barren stimulus envi-
ronment or restrictive confinement and unavoidable stress are also prominently
associated with the expression of stereotypies (see Mason 1991 for a critical
review).
Motor stereotypies were found by Canales and Graybiel (2000) to be related
to an apparent imbalance of activation between the two neurochemically distinct
elements of the striatum, striosomes and the extrastriosomal matrix, in which
they are embedded. When they induced different levels of stereotypy in rats by
applying psychomotor stimulants in concert with dopamine receptor agonists,
the degree of imbalance between activity of striosomes and the matrix predi-
cated the degree of motor stereotypy.
Motor stereotypies (and possible comparable cognitive phenomena) are often
fragments of more complex ensembles. The "chunking" of action repertoires
within the striatum was proposed by Graybiel (1998) as a counterpart of the
older idea of information chunking. As an adaptive mechanism, the assembly,
adjustment, and reassembly of a relatively small number of behavioral patterns
is much more efficient than the mastery of a huge collection of alternative
programmed sequences. For example, the striatal coding of action sequences is
apparently reorganized as the learning of new habits proceeds (Jog et al. 1999).
Tom Insel (1988) correctly cautioned that the repetitive motor performance
of obsessive-compulsive disorder may not be homologous, but their common
underlying neural circuitry in normal and inappropriate expression may yield
important clues about potential sites for therapeutic intervention. Further clues
may be expected from considering the selective modulation of circuits by
specific elements of the stress response or other neurochemically distinctive
mechanisms for maintaining balance between competing, opposing, or comple-
mentary systems. It is interesting that stereotyped motor patterns are seen in
different but related contexts. Highly adaptive forms such as species-typical
displays and clearly dysfunctional forms such as clinical stereotypies are related
not only by the fixity of expression but by stress-evoking context. Indeed,
attempts at stress reduction have been implicated in the etiology of pathological
expressions of repetitive motor patterns (Cooper & Nicol 1991).
Stereotypies beg comparison with obsessive-compulsive (OCD) behavior,
which has been associated with basal ganglia since at least the mid 1980s
(Cummings & Frankel 1985). For example, OCD was specifically associated
with lesions of the lenticular nuclei, especially the pallidum by Laplane (1994).
56 The Evolutionary Neuroethology of Paul MacLean

Ranjit C. Chachko and colleagues observed five cases in which the symptoms
presented by patients, associated with depression, could be mistaken for a delu-
sional disorder, but more likely involved an impaired cortex-basal ganglia-
thalamus-cortex circuit (Chachko et al. 2000). In Baxter's (et al. 2000) review,
activity of the caudate was significantly correlated with that of orbital cortex and
thalamus in untreated patients who subsequently responded well to treatment. In
a smaller population who did not respond well, the correlation of activity in
these brain regions was weaker.
Attention-deficit hyperactivity disorder (ADHD) is, along with Tourette's
Syndrome and OCD (with which it is often comorbid—Sheppard et al 1999),
often regarded as a dopamine-based frontostriatal neurodevelopmental disorder
(e.g., Bradshaw & Sheppard 2000). When striatal activity was determined by
tomographic assessment of regional blood flow in children with ADHD, it was
found to be low (Lou et al. 1989). This may be attributable to functional abnor-
malities of the putamen, as determined by a new type of fMRI used by Anderson
and colleagues (2000) to look at steady-state rather than dynamic brain activity.
Interestingly, students suffering from ADHD appear to have reduced sympatho-
adreno-medullary responses to cognitive challenge (Anderson et al. 2000).
Schizophrenia can also be regarded as a frontostriatal disorder. The dopa-
minergic systems have long been implicated in the etiology of psychosis and the
success of dopamine-blocking neuroleptic drugs was a major impetus to the so-
called dopamine hypothesis of schizophrenia. Projections from the ventral
tegmental area to the ventral striatum (nucleus accumbens) were especially
implicated. Haber and Fudge (1997) reviewed the dopamine system with parti-
cular attention to its amygdalar connections and hypothesized that overstimu-
lated amygdalar projections to the substantia nigra stimulates excessive mid-
brain dopaminergic activity. In a review of the few studies that examined
pathology of the basal ganglia associated with schizophrenia, Heckers (1997)
found little support for neuropathies involving regional brain volume or cell
density. Neuromodulation, on the other hand, remains an important potential
variable. Graybiel (1997) suspected that the basal ganglia's potential function as
a cognitive pattern generator that parallels its function as an organizer of motor
patterns made it a candidate for a role in schizophrenia. Shortly thereafter, Holt
(et al. 1999) hypothesized that cholinergic interneurons of the striatum might be
responsible for impaired output and tested the idea by measuring densities of
neurons marked by their immunoreactivity to choline acetyltransferase. A
patchy decrease in cell densities was identified in the ventral striatum (ventral
caudate and nucleus accumbens) of schizophrenic versus control brains. Holt's
tentative conclusion is that the reduced function of striatal interneurons
disrupted the pathways from ventral striatum that end in the prefrontal cortex.
Adaptive Functions of the Corpus Striatum 57

Stress

It is significant that the physiological stress response is so intimately

involved with the expression or exacerbation of behavioral disorders. The stress
response is one of the organism's most ancient adaptive mechanisms. While
typically defined as a response to challenges to the maintenance of homeostasis
(e.g., Moberg 1999), it also deals with many real or perceived challenges to the
capacity of the organism to meet any of a variety of needs (reviewed in
Greenberg 2002). McEwen's definition of a stressor is particularly useful
because it implicitly acknowledges that homeostasis is only the most urgent of
many possible needs: "Stress may be defined as a threat, real or implied, to the
psychological or physiological integrity of an individual" (McEwen 1999). The
literature on the effects of stress on stereotyped behavior and stereotypies
implicates the basal ganglia. For example, Scott et al. (1996) bred 5 generations
of rats that differed markedly in their susceptibility to showing decreased
struggling activity in a swim test after being exposed to an uncontrollable
stressor. Compared to susceptible rats, those that displayed no decrease in
struggling after shock manifested an array of symptoms, including more home-
cage activity, larger shock-induced depletions of norepinephrine (NE) and 3-
methoxy-4-hydroxy-phenylglycol (MHPG) in the locus coeruleus and much
higher concentrations of dopamine (DA) and dihydroxyphenylacetic acid
(DOPAC) in striatum and nucleus accumbens than susceptible rats.
Perceptions of circumstances and their potential challenges to welfare are
also important—the phrase "real or perceived" emphasizes the fact that among
the most potent stressors are expectations. Organisms apparently invoke
responses that are most likely to be adaptive, even under adverse circumstances.
A mirror image of the ecological concept of "maximizing" the effectiveness of a
strategy relative to cost, the organism's anticipatory stress response can be
viewed as "minimizing" the future adverse impact of a prospective challenge to
meeting its needs. This is directly related to an animal's perception of the
"controllability" of the stressful situation, the attribute of a stressor at the heart
of the "learned helplessness" paradigm postulated by Martin Seligman and
colleagues (e.g., Seligman 1975; Seligman et al. 1975).
Interestingly, the effects of stressful experience on the basal ganglia system's
mesoaccumbens dopaminergic system is highly dependent on an animal's
perceived controllability of the stressor (Cabib & Puglisi-Allegra 1996) and the
basal ganglia are demonstrably able to couple expectations to sensory input in
support of developing new habits (Schultz et al. 1992; Kawagoe et al. 1998).

Attention

Teuber (1976) was convinced that, along with motor difficulties, the impair-
ment of striatal structures resulted in characteristic perceptual and cognitive
deficits (see Parent 1986 on nucleus basalis). The idea that attentional
competition involves ventral striatum in a manner parallel to dorsal striatum's
58 The Evolutionary Neuroethology of Paul MacLean

apparent involvement in competition between actions was found very attractive

to Dayan et al. (2000). They speculated that stimulus reliabilities could be stored
in corticostriatal connections while stimulus predictability could be stored in the
basolateral nuclei of the amygdala.
Attention has often been associated with human striatal dysfunctions because
of the striking phenomenon of paradoxical kinesia. The phenomenon of transient
release from akinesia inspired Brown and Marsden (1998) to hypothesize that
the basal ganglia are integral to nonconscious attention (see below). They
envisioned that basal ganglia damage altered the flow of information from
sensory input to motor output. In paradoxical kinesia, if heightened attention is
demanded by a specific situation, the impairment may be overridden, often
dramatically. For example, an akinetic Parkinson's patient might successfully
avoid some sudden emergency such as an oncoming car. Brown and Marsden
hypothesized that the basal ganglia facilitate the synchronization of distributed
and perhaps competing neural responses related to action and bring them to
focus on a specific motor act or thought sequence, that is, bring them to
attention.
The basal ganglia may serve to sort and recombine information about current
circumstances and predictions about future possibilities to serve adaptive ends.
This view informs Graybiel's (2000) hypothesis that a dysfunction of excess (of
activation) might lead to repetitive actions or thoughts while one of deficit
would lead to a diminished competence of action or thought. Graybiel and
colleagues (1994) related estimates of future possibilities ("predictive control")
to relatively rare but distinctive dopamine-dependent striatal cells that are
tonically active and which are recruited and change responsiveness when
exposed to stimuli predictive of reward and then diminish during extinction. An
organism's expectations are apparently reflected in the activity of ventral
striatum (Schultz et al. 1992) as a result of error-signal detection by
dopaminergic neurons (Schultz, Dayan & Montague 1997). Schultz (1998) has
observed that the activity of dopamine neurons in the ventral striatum, once
evoked by a rewarding stimulus, come to be controlled by reward-predicting
stimuli over time. Considering the critical importance of an organism's capacity
for making predictions to create associations between stimuli and responses and
to help discriminate most favorable responses, ventral striatal neurons are
apparently involved in the information processing that underlies motivation (as
reviewed by Schultz 1998).
In Divac's (1977) attempt to reconcile conflicting views of neostriatal
function, he found that even though there was topographic evidence for indepen-
dent functional units of neostriatal areas receiving specific neocortical afferents,
the uniformity of neostriatal cytoarchitecture indicates that these units conducted
neural processing of information in comparable ways. This view, in concert with
the position of the neostriatum in the chain of neocortical control of motor
mechanisms, converged on the idea that the neostriatum intermediates between
cognition and action. Divac and Oberg (1979), impressed by the fact that
behavioral deficits subsequent to lesions of the striatum and their cortical
projection targets were comparable, suggested that striatum was directly
Adaptive Functions of the Corpus Striatum 59

involved in cognition. In this regard it is interesting that Cools and van den
Bercken (1977) regarded the neostriatum as the substrate of high-order
information processing needed to link two or more behavioral acts to form an
integrated behavioral program (Cools 1985).
The nucleus basalis varies greatly between taxa and is most distinctively
differentiated in cetaceans and primates. Functional differences between its
neurons and those of other basal ganglia (Parent 1986) and its significant
projections to limbic and widespread neocortical sites (MacLean 1990: 57)
suggest it is likely involved in cognitive functions such as learning and attention,
at least in primates (Parent 1986: 247).
Among the diversity of significant problems that attend damage to basal
ganglia, some resemble specific symptoms of schizophrenia. For example,
damage to the substantia nigra in the area where the loop involving TE is likely
to synapse (medial pars reticulata) can evoke hallucinations, probably by
altering the normal balance of inhibitory and excitatory influences in a way that
results in abnormal excitation of Area TE, known to be able to stimulate
hallucinations. Middleton and Strick (1996) pointed out that the visual anoma-
lies attributable to interfering with the TE-striatal loop are much like those
sometimes seen as a side effect of dopaminergic therapy for Parkinsonism,
"Might this mechanism also underlie the hallucinations of schizophrenia?" they
ask. There is supporting data, they note, indicative of significant changes in
activation of areas that participate in the proposed loop during hallucinations of
schizophrenics. A detailed and closely reasoned argument for the involvement
of basal ganglia in the etiology of schizophrenia was advanced by Graybiel
(1997).
The major output structures of the basal ganglia, GPi and SNr, report back to
the ventral anterior and lateral thalamic nuclei, which then project back to the
cerebral cortex. Parent and Hazrati (1995a) regard this as a source of redund-
ancy, which can make the same information available to different brain centers.
Their analysis includes other targets of the GPi and SNr, such as the centro-
median thalamic nucleus (which receives information from cortical motor and
sensory cortices as well as brain stem reticular information), the habenula (a
major limbic relay that may constitute a functional limbic interface with basal
ganglia), and the pedunculopontine tegmental nucleus (which may be a
functional interface between cerebellum and basal ganglia). Other targets are
functionally associated with memory, rewarded motor behavior, and various
ways of combining cortical information at the striatal level.
Selective neurochemistry is the key to our fullest understanding of function.
For example, there is a growing sense that the reward functions of dopamine are
less significant than—and may even be explained by—its role in underscoring
the significance of stimuli that predict reward. This in part helps explain why
nonrewarding behavior may be manifest if it is associated with a dopamine
surge, as is often the case in addiction to cigarette smoking or cocaine use (see
brief review by Wickelgren 1998 and references therein). Another unexpected
way dopamine affects behavior was shown by Hayes (et al. 1998) on
Parkinson's patients asked to shift attentional set (the conditions that regulate
60 The Evolutionary Neuroethology of Paul MacLean

responding, executive process) from (for example) the color of a stimulus to its
shape as a cue for a response. These patients were significantly slower than
control subjects and had difficulty filtering a competing but irrelevant set. When
the deficit in switching was correlated with the amelioration of motor symptoms
attributable to an 1-dopa-based medication, it became apparent that deficit is
based on dopamine insufficiency.

Memory and its Disorders

Participation of the corpus striatum in long-term memory systems, classically

known from studies of patients with brain lesions, has been more recently
complemented by functional neuroimaging techniques. This information was
reviewed recently by Gabrieli (1998), who observed that basal ganglia are
significantly involved, particularly in declarative memory (involving conscious
or intentional recollection) and strategic memory (involving the evaluation,
manipulation, and transformation of retrieved declarative memories). The
pattern of memory impairment and reasoning in diseases of the basal ganglia
such as Parkinson's or Huntington's led Gabrieli to hypothesize that strategic
memory impairment is a result of limited reasoning ability attributable to
reduced capacity for working memory. A decline in working memory, reason-
ing, and strategic memory seems to correspond to normal 5-10% per decade
reduction in dopaminergic function across the lifespan, however Gabrieli is
careful to point out that the extent to which these functions are causally related
rather than merely correlative has not yet been determined (1998).
Basal ganglia are associated with human amnesia indirectly because that
dysfunction is a core symptom of Alzheimer's disease, which also involves
(among other things) a loss of cholinergic cells in the basal ganglia.
Hemorrhage-induced basal forebrain damage can also impair memory. But the
role of the basal ganglia is generally regarded as uncertain because there is
generally related damage to medial temporal (much more often associated with
amnesia) or frontal lobes. This situation is reviewed briefly by Goldenberg (et
al. 1999), who observed a patient with amnesia who suffered damage limited
largely to the nucleus accumbens. By excluding the roles of structures that
suffered collateral damage and because the n. accumbens is positioned to
"integrate inputs from multiple cortical and subcortical areas including the
hippocampus and the amygdalae, and to exert modulatory influences on
widespread cortical function," the authors conclude the n. accumbens is an
important candidate for direct involvement in memory processes (and see an
editorial commentary by Mayes 1999).
Confabulation may be a related disorder of episodic memory generally in
concert with faulty executive functions. Although associated with forebrain
dysfunction, it has presented itself after focal basal forebrain damage in a way
suggesting that both circuits from striatum to both medial temporal and frontal
lobes must be simultaneously impaired (Fisher et al. 1995; Hashimoto et al.
Adaptive Functions of the Corpus Striatum 61

2000). When lesions were limited to the basal forebrain, a more transient
expression of confabulation may result (Fischer et al. 1995).

Cognition

The sensory and multimodal cortices of the forebrain receive information

about the world, analyze it, and share it with the prefrontal association cortex
where it may be incorporated into complex, often skilled, adaptive actions
implemented by means of the premotor and motor cortices. Many theorists
assume the function of cognition is to model reality by selective simplification
of received information. In this, shared properties of stimuli are important in the
economy of cognitive functions, and it is often assumed that the simplest
generality possible that is not contradicted by experience is utilized. But
modeling also involves potential responsive actions and, in this, the
extrapyramidal and cerebellar control systems may provide essential support.
The selection or execution of actions are then more or less energized by the
perceived relevance of the situation, necessarily involving motivational and
affective variables.
Nieuwenhuys (1996) reviewed the "greater limbic system" and its
constituent "emotional motor system," which probably executes emotional and
motivated behavioral patterns by means of fibers from the central nucleus of the
amygdala, the bed nucleus of the stria terminalis, and the lateral hypothalamic
area. The striatum is barely mentioned: Ventral striatum is identified as a
participant in a loop involved initiating locomotor activity (p: 575). The large
association area of the frontal lobe, however, manifests a pattern of linkages in
its outflow in which cascades of short association fibers connect successive
structures, suggesting their participation in the planning and sequencing of
complex motor tasks (Nieuwenhuys 1996, citing Fuster 1991).
Ann Graybiel (1995) gave important impetus to the view that the "basal
ganglia . . . are critically involved in building up sequences of behavior into
meaningful, goal-directed repertoires." Her review indicates, as she put it,

that the basal ganglia act as part of a distributed forebrain system that helps to encode
such repertoires through behavioral learning, and that is engaged in the expression of
such repertoires once they have been internalized. The basal ganglia also may be critical
to the expression of innate behavioral routines. Experimental findings on reward-based
learning suggest that neural activity in the striatum and substantia nigra, pars compacta
changes during behavioral learning. New evidence also suggests extreme specificity in
the neural connections interrelating the basal ganglia, cerebral cortex, and thalamus.
Adaptive control of behavior may centrally depend on these circuits and the evaluator-
reinforcement circuits that modulate them.

Graybiel (1997) came to call the sequences "cognitive pattern generators"

and she suggested that by analogy with the central pattern generators of the
motor system "these pattern generators operate to organize neural activity
underlying aspects of action-oriented cognition. It is further proposed that the
62 The Evolutionary Neuroethology of Paul MacLean

basal ganglia are involved in the control of cognitive as well as motor pattern
generators. Disorders of the basal ganglia may thereby contribute to neural
circuit dysfunctions that are expressed as positive and negative symptoms of
schizophrenia." Further, they are likely important in initiating volitional activity
(Graybiel 1990).
Cotterill (2001) echoes Mink's (1996) idea that basal ganglia control activity
mainly by the inhibition of competing motor programs (above) but goes further
in his belief that modulation of sensory cerebrum signals to motor areas by the
basal ganglia and cerebellum can lead to cognition and consciousness.
Assuming the primacy of output over sensation for adaptive behavior, Cotterill
considers that consciousness serves mainly to review probable outcomes of
likely motor patterns in a given situation and hold those that have potentially
adverse outcomes at a subthreshold level—thought but not actions.
Connections and loops between basal ganglia and other sites associated with
cognitive function further underscore the adaptive potential of these structures.
The cerebral frontal, parietal, and temporal cortices provide input to the basal
ganglia, while only the frontal lobe was believed to be a major target of the
striatum. The inferotemporal cerebral site known as Area TE is one of two
specific visual areas associated with visual discrimination and recognition, and
has recently been determined to also receive from, as well as project to, the basal
ganglia. Using retrograde transneuronal tracers, Middleton and Strick (1996)
observed that the pars reticulata of the substantia nigra, a major striatal output
nucleus, projects back to TE by means of the thalamus. In the authors' view, if a
portion of these connections forms a closed loop, as seems likely, striatal
structures could influence high-order visual processing, which could explain
some perceptual anomalies as well as movement disorders.
A strict segregation of striatal output pathways, however, is less certain in
light of findings by Parent and others (briefly reviewed in Parent et al. 2000) of
striatal efferents with highly collateralized axons, most of which reach two or
three target structures. "It is now apparent," Parent et al. write, "that the basal
ganglia system is a complex and widely distributed neuronal network" (2000:
S23).

Creativity

Creative behavior, despite its obvious significance in behavior is "one of

psychology's orphans" (Sternberg & Lubart 1999). Its neuropsychological
causes and consequences are rarely approached by researchers, largely due to
traditions of scholarship and academic parochialism. When carefully defined in
terms of biological adaptation however, creativity is accessible to the scrutiny of
neuroethology. The capacity to generate innovative responses represents a
behavioral trait of the highest importance, particularly when an organism
confronts unique internal or environmental challenges to its capacity to meet its
needs. Indeed, the stresses evoked by environmental change can affect organ-
isms in ways that require novel ways of coping, which can change selection
Adaptive Functions of the Corpus Striatum 63

pressures in ways that feed back to affect their subsequent evolution (see, e.g.,
Jablonski & Bottjer 1990; Hoffmann & Hercus 2000). Adaptive behavior is the
outcome of the assimilation of a continuing stream of experience into the
structure and coordination of the brain. Coping with challenges to meet adaptive
needs almost constitutes a working definition of stress, and in light of recent
ideas about the effects of coping on selective activation of specific pathways (for
example, Huether 1996; Greenberg 2001), specific neurophysiological compon-
ents of the stress response may well be central to the expression of creativity as
well as its continuing adaptive function. But deviation from the norm is a
hazardous business, and thus creativity and dysfunction are hazardously close,
linked often, at least, in popular culture.
Among the hallmarks of creative behavior is the recombination of infor-
mation from different sources in novel and potentially useful ways. The striatum
may well be capable of combining information from different cortical areas as
their respective terminal fields converge (see Parent & Hazrati 1995a). Adaptive
and dysfunctional creativity both depend upon the selective expression of neural
events that ultimately result in the creation and/or expression of novel neural
constructs, typically known by their influence on behavior. These may represent
familiar things seen in new ways, new things seen unhindered by their evocation
of stereotypes, and various combinations of clarity of discrimination or categor-
izing. Cotterill (2001) reviews the idea that stimuli detected out of expected
context likely activate the ventral striatum, as it monitors the reliability of
predictions made in the prefrontal cortex. Expectations may be cognitive as well
as motor and the fact that chemical signals of the stress response are evoked by
even mild dissonance (Hadley 1996), such as discrepancies between perceptions
and expectations (Goldstein 1987), it is reasonable that the basal ganglia, known
to be sensitive to stress (Zigmond, Strieker & Berger 1987; Salamone 1994) are
deeply involved.

NEUROETHOLOGY OF STRIATAL FUNCTIONS IN A REPRESENT-

ATIVE REPTILE: REPTILES AND REPTILE NEUROETHOLOGY

Can we penetrate appearances, misconceptions, and tangled nomenclature to

the underlying common features that could link the rich mammalian literature
with findings in reptiles? In their analysis of the paleostriatal system (PS) of
Caiman and their comparison of this reptilian PS with both avian PS and
mammalian basal ganglia, Brauth and Kitt (1980) concluded that overall design
and possibly function are comparable in these three taxa and indicate a common
function in spatial orientation and attention. (Paleostriatum is also termed ven-
tral striatum by many authors while the overlying dorsal ventricular ridge
(DVR) is also termed, dorsal striatum; the reptilian nucleus accumbens just
medial to the PS is probably homologous with that of mammals (Parent 1986)).
Unlike mammals which have comparably rich ascending and descending path-
ways from the basal ganglia, the corresponding structures in reptiles influence
motor patterns only by descending pathways (Parent 1986). The dorsal
64 The Evolutionary Neuroethology of Paul MacLean

ventricular ridge (DVR) has long been suspected to be related to the prominence
of species-typical motor patterns in the life of reptiles (Bellairs 1970: 336).
When Marin, Smeets and Gonzalez (1998) integrated their work with the
amphibian basal ganglia into a phylogenetic overview, they discerned dorsal and
ventral striatopallidal systems in all tetrapods. Inputs from the thalamus and
cortex ("pallium" in lower vertebrates) are always through the striatum and
provide access to several classes of information. The cortex of mammals has
excellent representation in the striatum, whereas the reptilian basal ganglia
receives most of its projects from the dorsal ventricular ridge. This large distinc-
tive subventricular structure is apparently derived from the pallium and often
compared to isocortex of mammals. Further, the proposition that well-organized
projections of modulatory dopaminergic neurons from a substantia nigra/ventral
tegmental complex to dorsal and ventral striatum in all tetrapods can be
defended by new findings in amphibians. They concluded that although many
functions of the basal ganglia system are unique to mammals, the conservatism
of the system is remarkable. There is, however, an interesting difference detailed
125
by Clark & Baxter (2000). They used a radio-tagged marker ( I-DOI) that
preferentially binds to specific classes of serotonergic receptors. While such
staining highlights a patchy striosomal pattern in mammals, the lizard, Anolis
carolinensis shows no such pattern.
The major connections of the basal ganglia in the lizard, Varanus are
illustrated in Figure 4.1.

Figure 4.1. Basal Ganglia Connections in a Lizard. Major connections of the basal
ganglia in the lizard, Varanus. CL = lateral cerebellar nucleus, CP = nucleus of the
posterior commissure, EA = anterior entopeduncular nucleus, EP = posterior
entopeduncular nucleus, GP = globus pallidus, IC = intercollicular nucleus, RI =
nucleus reticularis inferior, SN = substantia nigra, STR = striatum, T = optic tectum
(after Parent 1986 and Ten Donkelaar and De Boer-Van Huizen 1981).
Adaptive Functions of the Corpus Striatum 65

The successes of the ethological method are grounded in close observation of

behavioral patterns spontaneously performed in nature or in response to
naturalistic stimuli. The heuristic power of a coordinated concern for the
questions and methods of developmental biology, ecology, evolutionary
biology, and physiology has informed ethological understanding ever since
Tinbergen (1951) identified these perspectives. The ignorance of critical life
history variables and the arbitrariness of stimuli for which organisms are
unprepared had become progressively misleading to students of behavior even
as they began to appreciate in principle the comparative method. Complemen-
tary detail from neurology, the growing clarity of neurotransmitter specificity
and distribution, and even the promise of functional radiology, are converging
on a newly invigorated understanding of adaptive constraints and possibilities as
individuals as well as species endeavor to cope with a dynamic environment.

Species-typical Behavior of the Green Anole

Research on the function of the reptilian corpus striatum is based on a

detailed ethological study of social behavior of a lizard, the green anole, Anolis
carolinensis (Greenberg 1977) in conjunction with an atlas of the forebrain
(Greenberg 1982). The fine-grained resolution of such ethological studies are
important to a fuller understanding of behavior which is very likely amalgams of
several units of behavior, each with their own respective evolutionary and
developmental histories. Such ensembles of units of behavior often acquire
communicative significance and their continuing evolution to become more
precisely evoked and effective as a signal is termed "ritualization." In evolu-
tionary terms, brains are conservative: Most internal change is driven by
environmental changes and stresses they place on the organism. As the stimulus
control of units of behavior and their orchestration shifts, proximate neural
causation is affected, and to the extent the change is adaptive, becomes a new
selection pressure for evolutionary change in the brain.
When reproductively active male green anoles in a laboratory vivarium are
confronted with an intruder, they respond with a characteristic sequence of
displays. A typical first response is the "assertion" display. It is the definitive
species-typical "signature" of many lizards, Anolis carolinensis included. In
most lizards it is performed by highly alert animals, possibly patrolling their
territories. It is often seen in the absence of any apparent specific stimuli or
when an intruder of either sex becomes apparent to the focal animal. It is also
commonly seen when a lizard is apparently startled by, for example, a sudden
move by another lizard of another species or even by an insect too large to be
regarded as prey. In other words, it is an indication of elevated nonspecific
arousal rather than a response to any specific evocative stimulus.
The "signature" display of a green anole also serves as an "advertisement."
If a sexually responsive female conspecific intrudes into a displaying male's
territory and observes his display, she may provide feedback indicative of status
as a potential mating partner. Most commonly this is by responding to the
66 The Evolutionary Neuroethology of Paul MacLean

assertion display with a species-typical head-nodding behavior. This response

generally elicits a switch in the male's behavior to courtship: a series of rapid
nods performed while approaching with a unique "strutting gait." If an intruder
is a male, on the other hand, and reacts with his own sequence of headnods
coordinated with push-ups and extension of the dewlap, the resident will rapidly
escalate its display into "challenge" (see Figure 4 . 2 D ) .

Figure 4.2. Posture and Display of the Lizard, Anolis Carolinensis. A, anole at rest.
B, ethological units of behavior that are coordinated in the "bobbing" display: HN =
headnods, PU = pushups, and DW = dewlap extension. C, expression of modifier.
ET = extended throat, expressed when the animal is in the presence of a potential
adversary. D, when a conspecific adversary is identified, modifiers denoting conspec-
ific aggression appear and are often imposed upon the basic bobbing display, CC =
nuchal and dorsal crest, DW = dewlap extension, ES = darkly pigmented "eyespot"
appears, ET = extended throat, and SE = sagittal expansion, enlargement of the
profile of the body in the sagittal plane (adapted from Greenberg 1977).
Adaptive Functions of the Corpus Striatum 67

By virtue of the display, with its species-typical sequence of headbobs and

pushups, the resident apparently "recognizes" the intruder as a member of the
same species. In this context, the display is complemented by postural changes:
the animal expands the sagittal profile of his body and displays to the intruder in
a manner that maximizes its apparent size. As aggressive encounters escalate,
the male's behavior is accompanied by autonomic responses: After about 30
seconds, an erectile crest will appear along its neck and back and body color
darkens. A black "eyespot" appears just behind the eye. The intruder responds in
kind as they stalk each other with slow, deliberate, apparently tense movements.
In both lizards, the episode is often accompanied by changes between green and
brown body color as the animals appear to assess their position relative to each
other. In Anolis carolinensis, body color is dependent upon the flux and chang-
ing ratios of epinephrine and norepinephrine and relative autonomic tone may be
important: the male that first manifests the eyespot invariably wins the contest
(Summers & Greenberg 1994).

Forebrain Control of Species-typical Behavior in a Lizard

Studies in which the brain was explored by electrical stimulation failed to

reveal sites of influence on stereotyped responses in the brain of Iguana iguana
(Distel 1978). Locomotion was occasionally elicited by stimulation, but tongue-
flicking behavior was reliably elicited in the lateral striatal area, although the
stimulation of more medial sites resulted in the greatest number of such
responses of any site investigated, possibly due to the proximity to olfactory
structures. Work by Sugerman and Demski (1978) on another iguanid lizard
species, Crotaphytus collaris, did elicit stereotyped agonistic behavior in
response to electrical stimulation at several sites that roughly formed a column
from the telencephalon to the rhombencephalon, but striatal sites were not
tested. Tarr (1982) specifically stimulated striatal sites in the fence lizard,
Sceloporus occidentalis, and observed stereotyped assertion displays at or near
the tip of the lateral ventricle, nucleus accumbens. Points eliciting the more
complex challenge displays were just anterior and dorsal to the nucleus
sphericus in the posterior area of the dorsal ventricular ridge. Interpretation of
stimulation experiments is always complicated, as Distel (1978) has indicated,
by the difficulty in discriminating direct motor stimulation, sensory excitation,
motivational changes, or general arousal. Much the same problems plague
interpretation of lesion experiments. But still the techniques, in concert with
further knowledge of striatal anatomy, will help point the way to progressively
more specific hypotheses that can significantly inform future investigations of
function.
68 The Evolutionary Neuroethology of Paul MacLean

Forebrain Lesions

Many of the aforementioned attempts to identify a brain region with aggres-

siveness or stereotyped behavior were difficult to interpret because of the
diversity and nonspecificity of effects caused by the treatment. In a series of
experiments devised in the MacLean lab, we hoped these difficulties could in
part be circumvented by taking advantage of the natural split-brain preparation
that lizards provide. The absence of a corpus callosum in this taxon allows us to
experiment with unilateral lesions, which provides the advantage of each indivi-
dual being his own progressive control. Responses of animals tested when visual
input went to the lesioned hemisphere had as progressive, perfectly matched
controls, tests with visual input directed to the intact side (Greenberg et al. 1979).
Lizards were anaesthetized in crushed ice and small electrolytic lesions placed at
specific coordinates determined with the aid of a stereotaxic atlas devised for the
purpose (Greenberg 1982; animal care and research protocols in Greenberg
1992).
The behavior of lizards after surgery gave no evidence of any impairment of
behavior until they were confronted with intruding conspecifics. Only then was
it clear that lesions of the paleostriatum of male anoles profoundly alter their
social dynamics. Where vigorous territorial combat might be expected when an
individual views an intruding conspecific (Greenberg 1977), the brain-lesioned
resident, while responsive to the presence of the intruder, is unresponsive to the
species-typical releasers of territorial aggression it provides (Greenberg et al.
1979).
This inability to recognize appropriate stimulus input might be characterized
as "social agnosia." Interestingly, a striatal role in visual discrimination was
already indicated by a lesion study of the forebrain of the turtle, Chrysemys
(Reiner & Powers 1980). In other experiments, lizards with comparable lesions
courted females quite normally (Greenberg et al. 1984).
An analysis of the forebrain activity of green anoles was undertaken by
Baxter (1999; Baxter & Ackerman 1997) who used the eye-patch technique to
limit visual input to one hemisphere or the other and then used a radio-tagged
glucose (2-deoxyglucose, 2-DG) to indicate areas that were metabolically active.
After injecting 2-DG, they placed animals in habitats with a mirror that
effectively evoked displays from isolated, dominant or subordinate males. Using
this technique they determined that the hemisphere which received visual input
was significantly more active than the contralateral, "eye-patched" hemisphere.
The dorsolateral basal ganglia (DL-BG) was particularly active, and the number
of aggressive pushup displays performed correlated with the activation in the
"seeing" dorsolateral basal ganglia's activation.
Subsequent analyses were performed on individuals who had established a
dominance relationship and then isolated in a vivarium with a mirror. They each
responded to their image with their "status-typical" display, and demonstrated
that not only was activity increased in the "seeing" DL-BG of animals
performing aggressive displays, but decreased in the "seeing" ventromedial
basal ganglia (VM-BG). Further, the subjects that were submissive in the
Adaptive Functions of the Corpus Striatum 69

presence of the social dominant showed 2DG diminution in DL-BG and

increased VM-BG activity. Interestingly, activity of a lateral segment of the
overlying anterior DVR was correlated with DL-BG activation while a medial
portion of the aDVR showed 2-DG accumulation when VM-BG showed
activity.

Social Dominance

If intact animals, fresh from the field and known to be reproductively active,
are allowed to cohabit a vivarium after a territorial confrontation, the winner
typically goes about his business, alert to the cohabiting loser, but generally
unperturbed as long as the loser responds with appropriate indications of
deference when subjected to an occasional challenge display. A classic social
dominance relationship has been established. The winner monopolizes the best
sites to watch for predators, prey, or mating opportunities, while the loser, no
less active in foraging or feeding, acts with apparent indifference to the trap-
pings of power. Observed for as long a month in this condition, such subord-
inate males were found to have elevated levels of the chronic stress hormone
corticosterone (Greenberg et al. 1984) and roughly half the normal circulating
levels of the hormone testosterone (Greenberg & Crews 1990), indicating that
the change in behavior subsequent to losing a fight is more likely a consequence
of an altered hormone-mediated motivational state than a conditioned response
to a more powerful cagemate.
The significance of the famous bobbing display and its variations awaits the
clarifying resolution of ethological analysis to more fully appreciate the signifi-
cance of their control by the basal forebrain. It seems relevant, however, that the
ability to express the species-typical action pattern is unaffected, but the
capacity to recognize a conspecific and manifest the appropriate response to an
intruding male's species typical display is profoundly impaired. This is not a
mere motor impairment. If the consequences of basal ganglia lesions can be
construed as social agnosia, a defect of cognitive processing, is the process
impaired in this lizard? In mammals, one of the several cerebral cortical inputs
to basal ganglia is area TE in the inferotemporal area. This is interesting because
this area, apparently essential to visual recognition and discrimination, also
receives input from substantia nigra pars reticulata via the thalamus, creating a
circuit that allows basal ganglia to influence higher order aspects of visual
processing (Middleton & Strick 1996). Possibly related is the finding that rats
which work for stimulation of their nucleus accumbens will reduce their
responding under uncontrollable (but not controllable) stress in a way that
indicated a loss or reduction of the reinforcing value associated with the
stimulation (Bowers et al. 1987), recalling the social agnosia of paleostriatal
lesioned lizards mentioned earlier.
70 The Evolutionary Neuroethology of Paul MacLean

Neurotransmitters in the Behavior of Anoles

When territorial lizards confront each other in an experimental vivarium in

which they likely perceive each other as intruders, as observed in tests described
above, losers of territorial fights invariably became socially subordinate,
displayed darker color, selected lower perch sites, and maintained lower body
posture than the winners. The subordination was unambiguous. When midbrain
and hindbrain were analyzed for indolamines, catecholamines, and their metabo-
lites by coulochem electrode array high-pressure liquid chromatography,
Summers and I learned that central serotonin production and turnover is more
rapidly activated in losers of fights (destined to behave in a subordinate way)
than in winners (Summers & Greenberg 1995).
A closer analysis revealed that serotonergic activity in dominants and
subordinates had a distinctive time course as well as regional distribution in the
brain (Summers et al. 1998). Brain slices of dominant and subordinate males
were micropunched to isolate specific areas and analyzed by high pressure
liquid chromatography (HPLC). We found the greatest serotonergic changes in
the telencephalon of subordinate males. One hour after a fight, the hippocampal
cortex and nucleus accumbens showed increased ratios of 5-hydroxyindoleacetic
acid/serotonin. Just as in earlier studies of the brain stems of these animals
(Summers & Greenberg 1995), the ratio gradually decreased as the animal's
social status became consolidated, and within one month, ratios had returned to
normal. Measured in the brains of lizards sacrificed at an hour, day, week, and
month following a fight, changes were seen to be more rapid in dominant males.
The patterns of serotonergic activation are so similar in hippocampus, nucleus
accumbens, and brain stem that a coordinated response may be involved in
mediating short-term social stress and aggression. Similarly, medial and lateral
amygdala exhibit corresponding, but delayed patterns in subordinate males,
suggesting a coordinated response in these regions mediating longer-term stress
responses (Summers et al. 1998).
Interestingly, low serotonin levels in the brains of a primate model have been
associated with impulsiveness. Recent work by Baxter (1999) has shown in the
Anolis lizard model, that beyond a sharp increase in forebrain serotonin during
dominant displays and a decrease during subordinate displays, there was an
activation of dorsolateral basal ganglia and deactivation of the ventromedial
area. Clark and colleagues went further to analyze the subtypes of serotonin
receptors and their distribution in Anolis carolinensis, confirming important
commonalities with other taxa (Clark & Baxter 2000). In a series of analyses on
dopamine receptors, the occurrence, distribution, and pharmacological specifi-
city of dopamine Dl and D2 receptor sub-types were also seen to be similar to
those of mammals. One interesting difference, however, is that neural tissue in
the parts of basal ganglia outside the ventral striatum (see Table 4.1) character-
ized by Dl and D2 receptor subtypes is largely separated, rather than
commingled as in mammalian basal ganglia (Clark et al. 2000).
Subsequent work on free-ranging lizards, Sceloporus jarrovi, provided consi-
lient results: tissue samples from their telencephala and diencephala that were
Adaptive Functions of the Corpus Striatum 71

analyzed for monoamines, their precursors and metabolites, revealed significant

differences according to social status. There was more serotonin activity and
turnover in subordinates (satellite males without territories) compared to terri-
torial males (Matter et al. 1998). Such findings also agree with findings in fish
(Winberg et al.1992) and mammals (Yodyingyua et al. 1985, in primates), sug-
gesting a phylogenetically conserved mechanism of monoamine behavioral
modulation.
Aggression is stressful in the short run whatever one's status and whatever
the outcome, but the experience of that stressful episode apparently evokes
different long-term consequences for winners and losers. Wins or losses, real or
perceived, likely lead to significantly different endocrine tone. Serotonin eleva-
tion is associated with acute stress in all animals studied (e.g., Winberg et al.
1992 among others) but only in losers of encounters does serotonin elevation
persist.
Other data supportive of the idea of the relative resilience in dominants is
apparent in color change data. In Anolis carolinensis, the circulating epine-
phrine-dependent eyespot appears earlier during an aggressive exchange in the
future-dominant, and fades more quickly (Summers & Greenberg 1994).
The basal ganglia, the integrity of which is essential to an expression of a
green anole's aggressive display, also mediates displays that characterize social
status. Baxter and colleagues measured both activation of forebrain sites and
changes in function in lizards displaying the pushup and profile change that
characterize aggressive dominants and those that characterize subordinates. In
dominant animals but not subordinates, increased 5-HT correlated well with
dorsolateral basal ganglia activation. The complete decussation of optic tracts in
anoles was exploited by Baxter in much the same manner as Greenberg, to direct
visual stimuli to a hemisphere that can then be compared to the contralateral
14
hemisphere for an effect. The glucose mimic, 2-DG ( C-2-deoxyglucose) accu-
mulates preferentially in more active cells. When eye-patched lizards were
housed together, dominants and subordinates came to express their respective
social displays repeatedly to mirrors, and accumulations of 2-DG were seen in
the basal ganglia only of dominants and only in the hemisphere opposite the
unpatched eye (Baxter et al. 2000).

Connections

As mentioned earlier striatal structures in reptiles differ from those of

mammals in that descending pathways predominate (Parent 1986). An alter-
native attempt to clarify the connections and role of paleostriatum involved the
use of a neurotoxin that will selectively destroy dopaminergic cells. The
meperidine analog, MPTP (methylphenyltetrahydropyridine), was believed to be
toxic to dopaminergic cells by its being selectively incorporated into neurons
through their re-uptake systems. The procedure became popular because the
symptoms produced can be similar to idiopathic Parkinson's disease (Marsden
& Jenner 1987), presumably by means of toxic effects on the dopaminergic
72 The Evolutionary Neuroethology of Paul MacLean

substantia nigra pars compacta, although some studies also report effects in
locus caeruleus and the ventral tegmental area (reviewed by Langston & Irwin
1986). While the primary site of cell death is the pars compacta of the substantia
nigra (SN), the adjacent ventral tegmental area and other sites are also often
affected. The selectivity appears sensitive to both the age of the animal (less
selective in older subjects, Marsden & Jenner 1987) and the amount of MPTP
administered. In fact, at low levels, many SN cells may survive while conspi-
cuous mesostriatal axonopathies appear and tyrosine hydroxylase immuno-react-
ivity in the striatum decreases (Kitt et. al. 1987).

MPTP Experiment

To help us confirm and extend our understanding of dopaminergic pathways

and their possible influences on behavior, several Anolis carolinensis were
injected intraperitoneal^ with varying doses of MPTP. At high doses (100
mg/kg) the lizards showed postural rigidity, convulsions, stereotyped head and
neck movements, and died within 24 hrs of injection. Lower doses resulted in a
transient behavioral syndrome consisting of hypokinesia and signs of adrenal
activation. Acute behavioral changes in MPTP-treated animals included indica-
tions of a physiological stress response and, in particular, color changes, includ-
ing the formation of a post-orbital darkening (the "eye spot"), and nuchal crest
erection, both indications of adrenal activation (see Greenberg & Crews 1983).
These effects and a pronounced hypokinesia remitted in all but 8 individuals
who received in excess of 50mg/kg of the drug and subsequently died. These
individuals also developed akinesia, postural rigidity, episodic convulsions, and
occasionally manifested stereotyped head and neck movements. Most indivi-
duals, however, survived and showed no further symptoms of physiological
stress (Font, Switzer & Greenberg 1988; Font et al. 1988). This survival is
consistent with the idea of functional recovery of involved neural tissue; the
individuals that did not survive may have suffered a crisis of adaptation due to
massive and persevering adrenal activation (Barbeau et al. 1985). Most subjects
that received smaller doses, while showing clear indications of neurological
damage, displayed no significant behavioral deficits; several, however, showed
episodic rigidity and diminished spontaneous behavior. In tests of species-
typical aggressive behavior, such subjects performed appropriate stereotyped
behavior, albeit at low intensities (Greenberg et al. unpublished data).
After behavioral observations, cytopathological effects were assessed using
the cupric silver method of method of de Olmos et al. (1981). Degenerating
axons were observed ascending in the lateral forebrain bundle from the midbrain
tegmentum (substantia nigra and ventral tegmental area) to targets in the anterior
dorsal ventricular ridge, ventral striatum, nucleus accumbens, anterior and
posterior entopeduncular nuclei, dorsal nucleus of the posterior commissure, and
tectum mesencephali. Two types of argyrophilic perikarya were observed:
degenerative and reactive. Cytopathological changes were apparent at several
loci ranging from the forebrain to the cervical cord. Degenerative changes were
Adaptive Functions of the Corpus Striatum 73

also seen in striatal terminals in areas that also show catecholamine histofluore-
scence and AChE reactivity (Greenberg, Font & Switzer 1988), supporting the
putative homology of the reptilian striatal afferents and the mammalian meso-
striatal pathway.
The projections revealed by the MPTP treatment confirm and extend our
knowledge of ascending midbrain projections in lizards. Parts of this projection
system are similar to the mesostriatal dopaminergic pathway of mammals;
however, the distribution of argyrophilic perikarya found in lizards markedly
differs from reports of cell damage in MPTP treated mammals. Difficulty in
interpretation is attributable to species variability (Langston & Irwin 1986;
Kopin & Markey 1988) and the possibility that non-catecholaminergic neurons
may be affected by MPTP (Switzer & Campbell 1987 with C57 mice).
When aggressive pairs of rats set up social dominance relationships, both are
stressed, but subordination involves additional burdens. Such males manifest
behavior much like chronic depression. They appear defensive, voluntary alco-
hol consumption increases, and lifespans are shortened. Corticosterone is eleva-
ted and testosterone is reduced in rats much as in lizards (above) and most
vertebrates. Most relevant to understanding the neurochemistry of stress and
stress-related dysfunction, subordinates also manifest changes in serotonin
systems indicative of increased 5-HIAA/5-HT ratios in various brain areas and
altered 5-HT(lA) receptor binding at some sites (Blanchard et al. 1993).

ENVOI AND NEED FOR FUTURE STUDY

The diverse assortment of phenomena in which the basal ganglia participate

vividly conveys a sense of the nested priorities of organisms. The unique
qualities of the basal ganglia from its most ancient expression in vertebrates
through humankind are consistently involved with the allocation of resources
and the attempt to respond to environmental stimuli with the optimal balance of
responses. These responses include those firmly embedded in an organism's
behavioral repertoire as well as more recent and innovative behavioral patterns.
Specialists approach the problems of structure and function from their
respective perspectives. Clinicians are appropriately preoccupied with expres-
sions of pathology, most often negative symptoms such as, functional deficits or
losses, rather than positive signs such as excesses. And comparative neurologists
are acutely sensitive to the fundamental promise of the more recently evolved
structures to shape and control more "primitive" behavioral patterns organized at
lower levels. Ethology, having been guided as an emerging field more by
zoology than psychology, emphasizes the differences between organisms more
than the commonalities. It is alert to the boundary conditions that reflect the
limits of possibility. Neuroethology sought the best of both worlds: the
necessarily evolutionary conservative nervous system and the incredible
diversity of behavior manifest in diverse environments. As evolution cobbles
together fragments of the organism's rich potential into new ways of coping
with various selection pressures, only our broad experience of possibilities can
74 The Evolutionary Neuroethology of Paul MacLean

prepare us to make the most of what natural or laboratory experiments show us.
Striatal-lesioned lizards, for example, may appear unimpaired unless provided
with an appropriate venue for expression—an expression one might never look
for or find if ignorant of the details of their natural history.
In recent decades, research is becoming more collaborative. The isolation
that results from great disciplinary depth is being overcome by interdisciplinary
research teams. But even in such an environment, ideas are born in a single mind
and then shared, and often the visionary idea is the next generation's dogma. In
an echo of the evolutionary process, ideas that lead to insights that successfully
solve problems are retained and when the problems are solved they become
available for some other use or are even allowed to disappear. Insights about the
basal ganglia, which began as gross estimates based on major trauma or disease,
have become replaced by progressively more subtle understanding as more
detail becomes available and particularly as the diversity of precisely described
behavioral patterns associated with their function in a diversity of taxa and
contexts is examined.
This is the essence of the ethological method, in which an appreciation of the
expressions of comparable behavioral patterns in diverse taxa and in their
natural environments instills a sense of the awesome richness of possibilities
that nature fosters. An appreciation of this breadth of application by supreme
masters of their fields such as Paul D. MacLean will continue to enrich us by
virtue of their model of wide-ranging imagination grounded in deep disciplinary
understanding.

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 PART III

THE SOCIAL BRAIN:

CLINICAL THEORY AND
APPLICATIONS-
DEPRESSION AND MANIA
 5
M A C L E A N ' S PARADIGM A N D ITS
R E L E V A N C E FOR PSYCHIATRY'S
B A S I C SCIENCE

Russell Gardner; Jr.

The decision to move from "theory" to "reality" is one we make in

1
the absence of formal rules. (Malcolm Macmillan, 2000)

INTRODUCTION
MacLean's neuroethology flared in popularity in the third quarter of the
2
twentieth century, but then undeservedly suffered reduced reputation at the
century's end. As the new one begins, however, his emphases take on added
importance; his focus, that is, upon social behaviors that stemmed from
adaptations originating in deep time. This conclusion results from supporting
data generated by the genome project as well as other genetic and brain research,
on the one hand, and the need for psychiatry (and its allied clinical human
service disciplines) to connect brain actions with normal human communicative
behavior, on the other hand. Ability to do this helps both the assessment and
treatment of those needing care. Caretaking of any kind, a social behavior,
usually involves conspecifics (fellow members of a same species), an outcome
of the expanded human brain: These facts combined with the largely social or
communicative nature of psychiatric symptoms fostered the idea that psychi-
3 4
atry's basic science should be designated sociophysiology. ' Such a basic
science characterizes the ills of this medical specialty as variations in the social
and communicational functions of the body mediated in the brain. MacLean
underlined ancient roots of communicative behavior in a way now unfortunately
ignored by leading neuroscientists. Practical and research implications follow
from dividing psychopathology, its treatments and normal related social
communications into those evolved early versus late, roughly speaking,
components that humans share with other animals and those uniquely human.
86 The Evolutionary Neuroethology of Paul MacLean

Paul MacLean began this process; those of us doing clinical and correlated
research work need to continue it to render our efforts more rational and more
effective. MacLean's influence should foster our clinical enterprises becoming
ever more relationship-based, nonexploitative benefits of the enlarged human
brain.

PARADIGM GAINED

Among his contributions MacLean testified to the importance of communi-

cational mechanisms evolved in deep time that hold great present significance in
daily human lives. For each person other people possess great meaning. " T o be'
5
is to be related." Human relating has the ancient roots of mating and terri-
toriality seen throughout the animal kingdom with its modern expansions in
human language and storytelling. Recognition of and interaction with conspeci-
fics probably date back to the initial uses of sexual reproduction in freely
6
moving ancestral animals that countered predation on them by microparasites.
Besides mating, many other things that people do together had precursors in the
conspecifics of our remote ancestors, some behaviors seen in animals that only
remotely resemble humans, such as lizards and other reptiles. Others, group-
living animals who share space with the group-living people, seem more
7
familiar, especially dogs and cats. In many ways popular esteem continues to
regard positively MacLean's implicit focus on communication. But his work
also found disfavor among neuroscientists as the fashion of science turned away.
Yet the direction of his theory takes on substantiation from the various genome
projects that testify to origins more dramatically ancient than even the depths he
plumbed. Thus, he went no further back than reptiles, though a third century ago
such "relatives" represented a heroic distance back into deep time. The new data
take relevant history back much further still, as they show that we share many
genes with invertebrates, such as DNA elements—the homeobox—that organize
8
the body plan.
The first issues of MacLean's career entailed the temporal lobes that deal
with feelings and motivation. Clinical patterns stem from damage to the medial
temporal region; for instance, some people display partial complex seizures as
well as personality changes between seizures, including, for instance, "interper-
sonal stickiness"—an inability to disconnect from another person when in
conversation. With an unusually comprehensive perspective, MacLean imagina-
tively reconstructed the onset of the mammalian family in connection with core
structures that must have operated to allow conspecific attachments to happen.
He knew that basic plans for behavior resembled in their ancientness—yet
persistence—structural ones, such as four limbs and the vertebrate endoskeleton.
He also knew conspecifics of all kinds communicate extensively and richly,
using shared neuronal mechanisms that stemmed from genomic basic plans.
And such cellular and other structural encodings determine organism behavior.
When Mayr refined the meaning of "species," he hinged it on the behavior of
9
reproducing.
Relevance for Psychiatry's Basic Science 87

So, parallel to structure, old behaviors fulfilling their core functions persist in
various modified forms. Natural selection involved mating, territoriality and
social rank hierarchy as early and continuing devices that serve organism
function, well-being, and survival. The basic plans giving rise to proteins and
structures result in traces that remain preserved in the fossil record in contrast to
the movements that always remain inferential, never observable in the long-dead
animals that exhibited them once. Yet inferred or not, we presume from obser-
vations of present-day species that they must have occurred.
Deviations from these fundamental DNA and protein brain structures
produce present-day pathology in psychiatry and abnormal psychology. These
"disorders" appear as maladaptive communications and social functions, for
example, on direct inspection, mania represents the patient as in a state that
dictates the person take over, even when doing that gives the individual (and
10
those close to him or her) problems. The person does not represent a resource
for others as would be the case if functionally taking over leadership of, say, a
needy group. For MacLean subcortical structures that evolved as foundations to
cortex required more emphatic investigational attention than did the cortical
structures and functions themselves (he in fact worked little with cortical
mechanisms despite their great volume and structural homogeneity). Thus, he
fruitfully examined contemporary lizards, readily available reptiles whose
common ancestor with humans extended to more remotely deep time than any
mammal. In reptiles, MacLean (often with Neil Greenberg, who contributed a
chapter to the present volume) described not only courtship and territoriality
with which we are all familiar in ourselves and in fellow humans, but an added
host of behaviors that surface in an out-of-context manner after people
experience frontal lobe trauma or are impacted by damage to the subcortical
connections with the frontal lobes, especially basal ganglia.
Thus, in psychiatric clinical evaluations, I have noted the behaviors of
patients with deficient frontal lobes. Characteristic signs and symptoms of such
damage include perseveration (repetition of the same behavior), echopraxia
(imitating the examiner's behavior in an obligatory manner), and echolalia
(although reptiles do not speak, their tendency to imitate extends to this sphere
in brain-damaged humans). One easily concludes that for most of us most of the
time, cortical structures that evolved during mammalian stages of development,
suppress, modulate and/or alternatively express such tendencies. We normally
exhibit more subtle repetitions, echopraxia and echolalia in our communica-
tional repertoires; compared to someone with deficient frontal cortex, intact
brains allow a person to integrate these functions smoothly and subtly. For
instance, normal conversation features postural echoing of the participants to
each other; doing so often means each signals reassurance and good feeling. A
speaker's words earn the compliment of repetition by the listener which indi-
cates an appreciation of the speaker's point while urging continuation of the
interaction. Such smooth useful integration represents some of the benefits of
these late-developing brain parts. Old tendencies and modern talents merge in
the ebbs and flows of meaningful conversation that we take for granted.
88 The Evolutionary Neuroethology of Paul MacLean

MacLean anticipated the genomic revolution of recent times when he stated:

It is now recognized that in all animals there are molecular commonalities with respect to
genetic coding, enzymatic reactions, and so on, that carry over into complex cellular
assemblies. Nowhere is the uniformity of complex cellular assemblies more striking than
in the cerebral evolution of vertebrates . . . the human forebrain has evolved and
expanded to its great size, while retaining commonalities of three neural assemblies that
reflect an ancestral relationship to reptiles, early mammals, and late mammals.

Genetic coding for language seems to have evolved recently, concomitantly

with the expanded neocortex three times the weight in humans compared to
chimpanzees. Yet Lieberman, influenced by MacLean, notes that language
clearly features numerous subcortical components, fostered in a manner similar
to the way that echoing postures and movements take on the functions of
11
facilitating communication as I illustrated above. David Baltimore in the
12
February 15, 2001, issue of Nature that featured the genome project, asserts:

[W]e do not gain our undoubted complexity over worms and plants by using many more
genes . . .[indeed], Where do our genes come from? Mostly from the distant evolutionary
past. In fact, only 94 of 1,278 protein families in our genome appear to be specific to
vertebrates. The most elementary of cellular functions . . . evolved just once and stayed
pretty fixed since the evolution of single-celled yeast and bacteria. The biggest difference
between humans and worms or flies is the complexity of our proteins . . . The history is
one of new architectures being built from old pieces.

In his research, MacLean made ethological observations similar to those

made standard by the 1973 Nobel Prize winning European ethologists, such as
the already mentioned reptilian behaviors. Also he worked on the neurophysi-
ology of subcortical areas in monkeys using conventional techniques of the time,
deploying implanted electrodes for recording and stimulation purposes, exam-
ined neuroanatomy by using brain sections and appropriate tissue staining. But
in his speaking he, unconventionally for a neuroscientist, worked to make sense
of brain-related things for their moral and other human implications. He quoted
Cajal that everything that goes on in our perceived universe reflects the structure
13
of the brain. He urged study of "epistemics," that is, learning about the
subjective via examination of the brain. For him the value of ancient behavior
patterns and communications does not diminish because they happened to have
originated in reptiles or before. His writing especially resounds with the
importance of the mammalian family, generated in part one gathers from his
own family highly valued by him.
Part of MacLean's popularity stemmed from the wide scope of his
observations, including lizards, rats, and squirrel monkeys with information
sought on many purposive animal communicational behaviors, some territorial
and social rank hierarchical, and others sexual, for example, determining the
brain sites that when stimulated caused erections in male monkeys. He resur-
rected Broca's 19th century term, "grande lobe limbique." Broca called it that
for its rim-like (limbus) location, but eschewed speculation about function
Relevance for Psychiatry's Basic Science 89

although he knew the structure was not limited to subserving smell as previously
thought, because he found it well developed in the dolphin, an animal without
14
olfactory nerves. MacLean, however, expanded on Papez's early description of
the core circuitry for emotion and proposed that neurons in the limbic structures
possessed critical meaning for the distinctively mammalian family which he
concluded probably originated in an early mammal seemingly transitional from
reptilians. Candidate transitional animals, the therapsids, left great numbers of
fossils behind in South Africa, a fact that MacLean felt represented opportunity
for future investigations.
I recall MacLean's speaking to a completely filled auditorium at the 1982
annual meeting of the American Psychiatric Association (APA). Among many
findings, he told the audience that lizards sometimes die after losing status in a
social rank struggle. This note, significant for psychiatrists involved daily with
suicidal patients, paralleled developments from other writers, who, similar to
him and acknowledging his pioneering observations, saw affective states as
deeply inherited parts of ancient body plans that provided the neuronal
15
framework for individuals to communicate with their conspecifics. Thus, Price
10
and Gardner especially highlighted the social rank hierarchical nature of what
have been traditionally labeled "affective" disorders. Subsequently, Jaak
Panksepp, who investigates emotions in mammals, paid tribute to the pioneering
efforts of MacLean in the forward of his own impressive work entitled Affective
16
Neuroscience. Panksepp studied with John Paul Scott, a MacLean contem-
17
porary, who wrote on the evolution of culture in 1989. Panksepp demonstrated
that emotions prominently associate with conspecific social life.
MacLean's neuroethology paved the way for the sociophysiology
3, 4
framework. This holds that the physiology of social processes essentially
provides the foundation for the medical specialty as well as for its related
clinical human sciences. The postulation promises to align psychiatry with its
sister specialties in explaining its pathologies in light of normal brain operations
fashioned over evolutionary time. McKinney and Tucker in their editorial intro-
18
duction to a special issue of Seminars in Clinical Neuropsychiatry suggest that
psychiatry should redevelop as a "relationship focused enterprise grounded in
sociophysiology to encompass complex behaviors, especially communication,
ancient reaction patterns, brain functions, cellular actions and genomic mechan-
isms."
In summary, MacLean emphasized evolutionary happenings in deep time,
especially conspecific communication mediated in the brain's subcortical struc-
tures (emphasizing the cortical mantle less). He underlined the approximate
origins of family life, which he asserts the evolution of the limbic system likely
made possible. He pioneered methodology focusing on across-species compari-
sons and contrasts. These ideas and research should have importantly configured
a basic science for psychiatry utilized to frame clinical procedures and guide
research efforts for the medical specialty and its related clinical human sciences.
But as yet this does not represent common knowledge. The advent of sociophy-
siology is recent, still considered provocative rather than obvious. MacLean's
work and the paradigm that he framed out represent template-forming precursors
90 The Evolutionary Neuroethology of Paul MacLean

for our subsequent work; yet his reputation seems to have nose-dived, not even
outlasting his active career. This requires examination.

PARADIGM LOST

In Cory's discussion of the decline in MacLean's reputation (see Chapter 2

this volume), he attributed it largely to inadequate reviews that did not reflect
legitimate, data-backed contentions. A negative Science review of MacLean's
1990 book signaled, Cory concluded, that MacLean was not to be taken
seriously by the broader scientific community, who in turn cued the general
public. I agree with Cory's conclusions but also suspect that trivializing senti-
ments had spread widely well before the reviews. I suspect that these attitudes
were held though not directly or publicly articulated by senior and influential
figures in the neuroscience community. Rather, they felt this among themselves
over many years and exerted influence on their younger colleagues. The Science
review probably represented a late-appearing capstone to this sentiment, written
by a then junior figure who felt little need to check the facts assiduously (see
Cory for details) because, I presume, that he knew he was on the "right side" of
correct senior opinion. In fact, in a 1999 volume that included MacLean's and
other neuroscientists' autobiographies, the editorial inclusion on his fame
strangely referred only to his early work, mentioning the limbic system,
19
"visceral brain," and psychosomatic disease. The editor notably failed to men-
tion the triune brain or the neurobiology of family life. I sense that MacLean's
emphasis on communication and social science somehow approached a taboo
subject that during his heyday could not be countered directly, given his stature
and influence.
For indirect evidence on this conclusion, I relate a medical school exper-
ience. During a first-year neurophysiology laboratory class at the University of
Chicago in 1959, I recall the professor becoming not just angry but enraged and
plethoric when a student asked casually about the possible neurobiology of
creativity. I recall his strong feelings though not the reasons he articulated for
them. I do recall that he claimed to represent a general position. The teacher had
seemed knowledgeable and bright so his feelings communicated powerful
messages to me and my fellow students. The incident taught us that such issues
constituted off-limits questions deliberately not considered by serious scientists.
To my mind, however, the question had seemed not only unprovocative, but
highly interesting as such matters had preoccupied me since my humanities-
oriented college instruction. This made MacLean's work—when I discovered it
three years later—all the more enticing, enhanced by his own gentlemanly
demeanor. He seemed above such concerns as he ably spoke his mind. Indeed,
he seemed to feel obligated to provide the public the benefit of his thinking
given his authoritative position and grasp of truth along with his moral
convictions. I suspect that MacLean's open and articulate interest in things
beyond strict neuroanatomy and neurophysiology—stemming in part perhaps
Relevance for Psychiatry's Basic Science 91

from his being a conscientious minister's son—caused his reputation to float

away from neuroscience recognition, though hopefully not permanently.
More evidence for this includes the fact that other authorities summarized or
mentioned MacLean's work with condescending attitudes towards what I had
felt were his most important and ultimately enduring contributions. In common
they highlight arguable details of his argument, rejecting them, and then suggest
that for such reasons that the corpus of his work can be dismissed. Pierre Gloor,
for instance, contended that MacLean was wrong in alluding to age of brain
20
components using prefixes such as "archi-" and "neo-." Six-layered or
isocortex had existed from the beginning, he asserted, though to lesser extents,
that is, "mammalian neocortex has phylogenetic roots just as ancient as the
hippocampal and piriform allocortex." He summarized briefly the triune brain
but dismissed this major MacLean contribution with his contention about age of
the cortices. I take his point about isocortex being a better term than neocortex,
but of course use of time-related terms has not been limited to MacLean.
Neocortex, not isocortex, whether right or not represents a term generally used
in neuroscience literature, as seen indeed in the title and content of a Nature
21
review co-authored nine years later by Anton Reiner, the 1990 Science
reviewer who gave proximate cause for the plummeting of MacLean's reputa-
tion. Adding to the ephemeral nature of this objection, MacLean exhibited least
interest in this volumetrically elaborated part of the neuraxis.
But another trend de-emphasizing his work included a popular line of think-
ing that shifted scientific attention away from across-species comparisons to
across-species contrasts. The work of Sperry and his co-workers involved
surgical hemisphere separation in severe seizure patients, for example,
Gazzaniga gained further reputation through subsequent work on the resulting
22
hemisphere disconnection syndromes. This focused attention on the later
developed mushroomed cerebral cortices that dominate the human brain in their
appearance and in their availability for study, as with neuroimaging studies and
away from the relatively smaller deep structures that MacLean especially
examined.
Provocatively, Panksepp and Panksepp demonstrate that this may have
produced an overvaluation of the prehuman-human transition as a time of
2j
principal change in the thinking of evolutionary psychologists. They empha-
size that structures well in place before the cortical mushrooming persist in
guiding roles, dominating the programmed behavior of animals in the form of
emotions, for instance. Activation of these structures focuses the individual's
attention regardless of the more complex analyses that the neocortex might
foster. Psychiatrist Frank Koerselman suggestively notes that the cortex does
fundamentally "trivial" things; the contrasting and never trivial emotions
determine what the cortex analyzes despite the classic and misleading division
between intellect and emotions; those with a "passion for the truth" accomplish
24
worthwhile things for others. Brain structures for emotions establish values
and then matter-of-factly enlist the cortical calculations required for the
important actions. The Panksepps noted that evolutionary psychologists overly
based their thinking on the seemingly revolutionary changes in the transition
92 The Evolutionary Neuroethology of Paul MacLean

from precursor primate to human that presumably enlisted new genes to underlie
25
new behaviors. In the best sense of falsifying Popperian science. Baltimore's
above citation refutes this. Nearly all of human biology (and behavior) stems
from precursor species, not arisen de novo\
LeDoux, Gazzaniga's student, wrote a widely read and reviewed book on
26
emotions which suggested that MacLean overly emphasized how they all stem
from the limbic system as though acting singly; rather, LeDoux emphasized his
impression that each emotion had an independently acting system. Again, his
prevailing critique attacked the overall work via criticizing such details while
seeming to miss the signal contribution that connected the evolution of such
organism attributes to ancient structures stemming from deep time, on the one
hand, and the organism's need to communicate with its conspecifics on the other
hand. LeDoux's book strikingly omits reference to animals more primitive than
mammals. He may also be wrong on some items. For example, LeDoux asserted
MacLean was wrong to include the hippocampus in the emotion system, saying
this because the explicit memory function of this brain part has come clear in
recent decades. Yet in this era of understanding how brain parts interact, who
can say that it departed from the emotion system? Memory connects strongly to
emotional charge of an experience. LeDoux thus joins in the problematic
overemphasis on cortex, a tendency shared by linguists such as Pinker, who
working in the shadow of Chomsky, prefers to think of language as a localized
27
cortical function. As already mentioned, Lieberman, another linguist, more
recently argued for increased emphasis on subcortical systems. In contrast to
LeDoux, Panksepp credits MacLean for recognizing the import of ancient
evolutionarily derived systems while delineating seven emotion systems in the
16
rat subcortex.
A quarter century ago, E.O. Wilson's sociobiology sustained attacks for
28
being politically (not factually) incorrect. This may have also influenced
attitudes about MacLean's work. Segerstrale reviewed the controversies about
29
sociobiology, and concluded that Wilson's application of population biology to
the affairs of many animals, even human, was a more correct track than that of
the critics (despite her initial bias in the other direction). Why had they been so
critical? What fears dictate the preventive actions of countering such research
work? A partial factor stems from an unfortunate public infatuation with
eugenics that occurred in many countries in the early 20th century, especially
after it became conflated with the horrible and unethical research conducted by
30
the Nazi regime in World War II. Additionally, we now know that application
of eugenics to combat mental illness, mental retardation and various inherited
illnesses does not work, as inheritance mechanisms are multiplex and often
jl
weak. The full horror of the era seems to have taken some decades to sink in.
Thus, the current neglect of the work of Paul MacLean may additionally stem
from its post-World War II timing. Much of his work preceded the 1975 opus of
Wilson and bore more directly on the brain than did that of Wilson, an
entomologist. Certainly, neither Wilson's nor MacLean's thinking and research
endorsed eugenic or Nazi horrors. Rather MacLean with confidence integrated
Relevance for Psychiatry's Basic Science 93

neuroscience, family and other behaviors with evolutionary neuroscience. He

could not have been more prosocial.
Another factor may relate his interest in cultural and social factors to the
pendulum swings reflected in the Sturm und Drang over psychoanalysis. The
medical micro-culture of our times often eschewed psychoanalysis and its
offshoots as unscientific and even harmful, whereas cells, molecules, drugs and
the like seemed comfortably reliable. Research on them has long represented a
comfortable source of added information that took on more exaggerated
qualities when a revolution overtook psychiatry in the last third of the twentieth
century. A once dominant clinical paradigm in academic psychiatry, psycho-
analysis gave way in academe several decades ago to descriptive psychiatry that
stated an aim of returning to the practices of "normal" medicine. Curiously,
however, because psychoanalysis postulated many pathogenetic theories on the
psychological level alone, the new theoreticians eschewed pathogenesis. This of
course contrasts dramatically to the rest of medicine. But for psychiatry over a
quarter century, the baby of pathogenesis floated away with the bathwater of
unproven therapies and their rationale. Though MacLean's persuasive capability
helped him during his active career, such factors with the conservative attitudes
of neuroscientists seems to have pervasively reduced his impact during the last
decade of the twentieth century. Of course, knowledgable psychoanalysts, crea-
tive artists, and some in the social sciences remain interested and involved in his
findings and theories. Curiously, however, the research prompted by the critic-
isms of the psychoanalytic movement has prompted appropriately control-led
32
research that shows both efficacy and effectiveness of psychotherapy.
Kandel and Squire's extensive review of last century's neuroscience failed to
33
mention MacLean in their list of notable figures. Part of the explanation stems
from their limiting behavior-experience-mental (BME) variables to cognition
and memory only, completely omitting social and emotional factors from their
considerations. This is doubly curious because Kandel, a 2000 Nobel Prize
winner, started as a psychiatrist to become an extraordinarily accomplished
neuroscientist later by focusing attention on simple organisms such as the sea
snail, Aplysia. Despite his strategy of going after ever more finely grained
details as neurotransmitters, synaptic interactions and critical circuits, Kandel
remained interested in psychiatry and has regularly presented at the APA and
published in the American Journal of Psychiatry, effectively arguing to his
clinician audiences that measures such as psychotherapy do indeed have brain
34
effects. Indeed, only when neuroimaging showed changes in the oxygen
utilization in brain parts did this become recognized fully. The Cartesian
mind/brain split maintained itself in the minds of many people until then and
only when Kandel with his enormous prestige amplified the message did the
practicing public realize this fully. At the same time, he disavows interest in
35
changing psychiatry. "I am just a shoemaker—my specialty is the neurobiol-
ogy of learning and memory."
So in summary, why then did the sophisticated Kandel and Squire omit
MacLean? Superficially, perhaps, because Squire reigns as an expert selectively
on memory and Kandel in his experiments on Aplysia showed disinterest in the
94 The Evolutionary Neuroethology of Paul MacLean

animal's social context, instead using withdrawal of the animal's siphon when
electrically stimulated as the model for "fear" or "anxiety." Additionally, they
expressed enthusiasm towards the discoveries in the molecular-cellular-organic
(MCO) realms of analysis rather than issues in the BME realms. Thus, they
excitedly focused on discoveries involving the ancient sources of neuronal
mechanisms and propounded that this would accelerate the continued work with
BME issues. This has tremendous importance for the sociophysiological frame-
work for psychiatry and related clinical activities. But what they do not seem to
have tumbled to, or have actively avoided, are the social and communicational
facets of neuronal process. The sociophysiological perspective argues, on the
other hand, that the analyses should represent a BME-MCO docking with two-
way travel of information and discoveries.
In the meantime, mainstream psychiatry in the wake of post-psychoanalytic
thinking gained respectability for its work guided by firm operational criteria for
its disorders even though considerations no longer take center stage of mechan-
isms for how disorders come about. Effective drugs make treatments briefer and
seemingly more scientific, because their actions are anchored in brain chemistry.
Yet debate ensues about whether the overall quality of life has increased and
interminable discussions of drug side effects preoccupy many psychiatrists and
their patients during the brief "med-check" sessions, the only ones available
with present funding practices. A curious avoidance continues of discussion on
the brain's involvement with cultural, psychological, societal and humanitarian
concerns.
In my opinion, as a need for this gains power with increased public demand
for explanations, MacLean's reputation will grow again. It stems from a
confluence of factors that I sense possesses importance for clinicians and
researchers. Partly this hinges on the framework of descriptive-pharmaceutical
psychiatry combined with medical economic strictures. Influences that foster the
"twisted molecule" model of illness envision ever more precise drugs to do their
remedies by untwisting the knots (similar to the way that psychoanalysts once
aimed at untwisting developmental knots). Sensitive observers have suggested
that drug companies and managed care together work towards the "the goal of
relationshipless psychiatry." Least contact with greatest impersonality represents
an ideal powered by managed care's need to restrict costs combined with drug
companies wishing to emphasize their products. These extraordinarily powerful
economic forces frame much of a present day clinician's work with patients.
This argument does not deny drug benefits; they exist and some people benefit
greatly, but patients regret the loss of personal relationship with the
psychiatrist—of all specialties one might expect interpersonal expertise in this
realm of medicine, but this seems to be fading fast.
Dramatic evidence reveals the approach's downside. At this time, only about
500 of 15,000 U.S. medical school graduates go into psychiatry, compared to
12% of my 1962 graduating class at the University of Chicago. I conjecture that
the new trend resulted in part from the lack of a satisfying intellectual
framework for the field, as well as medical school curricula trending away from
psychiatry in order to encourage students to go into primary care specialties (if
Relevance for Psychiatry's Basic Science 95

they do not, they lose funding based on state and national strictures). In the
meantime, psychoanalytic and other psychotherapeutic clinicians provide the
time for the details of their patient's experience; they work outside managed
care. From informal contacts, I conclude that they are in demand by people
willing to pay for skill and confidentiality.
Despite these trends and facts, I believe that the time will come when not
only psychiatry, but also the humanities and other disciplines will view brain
studies as integral to their traditions in the realms of thought products and other
results of human endeavors. Daniel X. Freedman, another MacLean student and
psychiatrist leader, suggested that the term "biological psychiatry" represented a
redundancy. All psychiatry must be biological just as phenomena on the BME
level of analysis must stem from brain actions. In like vein, there can be no
6
unbiological social science. In Three Seductive Ideas, Kagan suggests"" that
clinical and social-psychological sciences must be integrated with the rest of
biology, stating specifically, "At present the fragile threads that comprise
concepts in the social sciences are far too separate." He also noted, "One must
know the history of. . . animals to predict their current behavior." Isaac Marks
in surveying anxiety disorders concluded that highly functional propensity states
underlie fear that become malfunctional in the relatively benign present human
7 38
existence/ A recent quote from biologist Deric Bownds suggests in a
MacLean-like crescendo: "Newer structures of the brain encapsulate older ones.
Their feedback to lower levels of the brain can modulate the way in which more
ancient structures regulate homeostasis, emotions, and movement."

PARADIGM EXTENDED

Thus Freedman, Kagan, Marks, and Bownds with many others testify to the
importance of a docking between BME and MCO levels of analysis. MacLean's
neuroethology explicitly pioneered this. His research program exemplified the
first clear view of the paradigm of sociophysiology. The biology of social
processes requires additional exploration. The highly similar concepts of
neuroethology and sociophysiology differ only in that the latter term more
closely coheres to the model furnished by the rest of medicine (cardiovascular,
gastrointestinal or renal physiology) and therefore more fittingly entitles a basic
science of psychiatry. Sociophysiology focuses on normal behaviors of special
relevance to psychiatry and related clinical disciplines on the one hand. Thus, all
the disturbances that bring patients or clients to caregivers entail disruptions in
social and communicational attributes; ranging from panics that are aided by
someone nearby, to certainty of harm stemming from out-group enemies
(persecutory delusions), to limitations in memory functions that then disrupt
normal social life. On the other hand, physiology refers to body-workings—
much in the brain of course—that mediate this sociality as well as its disturbing
and distressing components that bring people to the helping professional. These
can range from family quarrels and accompanying violence, to school-related
problems such as attention deficit hyperactivity disorder, to persecutory
96 The Evolutionary Neuroethology of Paul MacLean

delusions, to fear and anxiety. Of course, the over-intrusiveness of the manic

patient and the under-intrusiveness of the depressed person represent familiar
patterns to anyone. I now turn to a more intensive discussion of evolutionary
processes.
William Calvin showed that the "descent by modification" of Darwin could
39
be generalized to the products of brain action, contemporaneously with Gerald
Edelman who coined the term "neural darwinism" to describe the process by
40
which very complex brains derive from just a few thousand genes (most recent
12
estimates, about 30,000). Edelman had pioneered use of Darwin's natural
selection to body processes, namely, the immune system, for which he gained
the 1972 Nobel Prize. Calvin's Darwin machine uses six steps: (1) a pattern
exists; (2) that can be copied; (3) variations on the pattern co-occur; (4)
competition for a workspace exists; (5) the environment biases the competition
for which pattern version will win (selection); and (6) the process reiterates with
closed repeating loops for copying, variation, and selection steps.
Calvin showed that this process applies to many mental phenomena, such as
words for a story. Many word variants compete for selection according to an
environment that includes strongly the storyteller's idea of the audience for the
communication. The brain, perhaps especially the human brain, speeds up the
processes via which Darwin machine processes work. But if this mechanism
holds and is currently operative, it also does so on a stable background. Basic
plans of ancient origination and little fundamental change persist in nearly all
living creatures.
Basic plan persistence gained controversial recognition in the early nine-
teenth century. Thus, Geoffery St. Hilaire observed the lobster's anatomy find-
41
ing himself struck by how its body resembled that of vertebrates. He subse-
quently argued that the two phyla possess a body plan in common. Cuvier, the
authority of the time, however, authoritatively stated that no evidence existed for
this conception and carried the day in a famous 1830 debate. St. Hilaire's vindi-
cation came one and a half centuries later with the discovery of the homeobox.
Walter Gehring discovered these distinctive genes in 1984 and they have been
extensively studied; many mammalian—including human—genes turn out to be
8
shared by drosophila, nematodes, even yeast. Fortey suggests they existed
42
already in the long extinct trilobites. Martindale and Kourakis observe that the
body plan (or common anatomic organization) determines in what phylum a
43
metazoan resides.

[T]he body plans of almost all living animals appeared in a very short time, over half a
billion years ago, and have remained essentially unchanged ever since. The evolutionary
information from most genes . . . is lost by random mutation over this evolutionary
timescale. It would be ideal to examine evolution of the developmental regulatory genes
that are involved in generating metazoan body plans. These genes should . . . have paral-
leled the stasis of the body plans they helped to create . . . The Hox genes encode
transcription factors, and they have been found in all metazoans examined.

In summary, both the invertebrate and vertebrate body plans lay deeply
buried within their genomes. The age of common insect-vertebrate ancestor is
Relevance for Psychiatry's Basic Science 97

over 500 million years before the present. Both express central organizational
functions that have retained much in common in presently living animals. Thus,
Horn genes in drosophila homologous to Hox genes in vertebrates are both
oriented in the same direction. Knocking out anterior genes "allows" the usually
more posterior ones to actuate in the more anterior position. The mouse Hox-6
gene put in the fly produces the same developmental controls as does the fly's
8
original gene. Discovery of these "master control genes" signaled that basic
body plan extended further back in deep time than had been anticipated.
Evolution uses old architecture in its new projects.
Behavior, though it leaves no manifest traces in fossils, does dictate physical
structure. Form follows function. A highly respected neuroanatomist in the
tradition of Cajal during the first half of the twentieth century, C. Judson
Herrick, summarized this thesis in his posthumously published The Evolution of
AA
Human Nature. "In all animals that have a nervous system, it controls the
adaptation of the species to its environment. When its behavior is adequate the
species survives; the more complex the behavior, the more elaborate is the
structure of the nervous system." Conspecifics needed to recognize one another,
including their sexual identity and mating potential. Might such recognitions
stem from ancient gene constellations not yet discovered? Fly genes expressed
in developing mouse brain include orthodenticle that produces a protein almost
identical to that of drosophila. Exploring genes that clearly underlie behavior,
the drosophila gene per determines circadian cyclicity. The fly fruitless gene
less clearly determines sex, but its disruption alters the ability of fruitflies to
41
carry through the sequence of mating. Though expressed in mammals, we do
not know yet how it might represent a component of the brain base for
vertebrate mating. Yet we know already at this early stage of investigation that
this must exemplify something too important to lapse (so that natural selection
has not reinvented it). This would represent behavior as reflecting homology
rather than convergent evolution, a core tenet for the key sociophysiological
proposition that psychiatric behaviors stem from ancient origins, though poorly
timed and aimed. Curiously, Darwin's Expression of the Emotions in Man and
45
Animals made a similarly conservative argument.
15 10
Price and I suggested several decades ago that the ancient biology of
social rank hierarchy likely underpins affective illness. In fact these represent
"communicational states." Manic behavior indeed resembles out-of-context
leadership communication. With the concept of propensity states antedating
language in communication (psalic), sociophysiology proposes that communi-
46
cation and sociality represent important ancient brain states. Signaling the
47
"planful" attributes of living matter emphasized by Ernst Mayr, psalic also
refers to programmed spacings and linkages |n conspecifics, fundamental aims
of communication. Particular psalics take definition from the three legs of
existing in (1) normal humans, (2) psychiatrically disturbed humans, and (3)
animals. Two psalics alluded to here include alpha psalic (seen in mania, normal
leadership, and animal dominance) and audience psalic (state of receptivity to
conspecifics as in cult membership, normal audiences, and animal subordi-
98 The Evolutionary Neuroethology of Paul MacLean

nation). Other psalics include those labeled mating, nurturant, nurturance-

eliciting, in-group omega, and out-group omega.
Psychiatry's famous DSM-III and its successors can be viewed as a series of
ethological descriptions that recognize the "naturalness" of psychiatric disorders
that occur with high prevalences. Daniel Wilson suggests with his concept of
"evolutionary epidemiology" that such high frequency testifies to their having
adaptive features; disorders may not be adaptive for the individual but their high
prevalence shows them to possess features that served adaptations, perhaps
48
expressed in other forms. The designers of the nosology manuals labored
towards empiricism so that they did not examine the communicational meaning-
fulness of the behaviors that constitute the disorders, for example, depression
communicates low profile attitudes with no threat communicated to other
people. If they had examined such observable features, insights to psychiatric
pathogenesis might have emerged. Studying psychiatric pathogenesis should
entail examination of the purposefulness of communications and communica-
tional states along with the adaptive consequences of an individual remaining in
the same state over time (mania may resemble leadership, for instance, but the
person displaying the communications typifying the state does so at the wrong
times or to the wrong audiences, yet patients remain stubbornly in the state until
treated or the episode otherwise ends). Full analysis will require MCO levels,
aided by the pharmacology of the syndrome in question, for instance, taking into
consideration differences from the normal counterpart state, or through analysis
of animal versions of the state or via neuroimaging of people in these states.
Dissection of such provides tasks for the next decades. For instance, each
psalic needs descriptive and analytic work. Some doubtless will bear up more
adequately than others, for instance, some may meet fates similar to Kagan's
36
critiques of fear as an abstraction, one of his "three seductive ideas." He holds
that fear is not a unitary phenomenon and that the following probably involve
different brain circuits (and therefore involve different brain states): a sudden
unexpected noise, a grizzly bear lunging at your throat, seeing a light that has
been associated experimentally with electric shock, and a worry about losing job
while walking in a quiet meadow. Yet all represent fear as a unitary process. So
we think of it in a first approximation carried into our sociophysiologic and
psychiatric nomenclature to be modified with research and other new informa-
tion. I expect parallel developments with the evolution of scientific investigation
of the psalics.
Investigations of psalics may be helped by Panksepp's concept of emotion
16
systems. Following MacLean, he noted that "many of the ancient evolution-
arily derived brain systems all mammals share still serve as the foundations for
the deeply experienced affective proclivities of the human mind. Such ancient
brain functions evolved long before the emergence of the human neocortex with
its vast cognitive skills." Panksepp labeled (1) an appetitive, motivational
SEEKING system that fosters energetic search and goal-directed behaviors, (2)
a RAGE system that aroused by thwarting experiences correlates with
frustration, (3) a FEAR system that minimizes bodily destruction, (4) a PANIC
apparatus with separation distress that enhances bonding, (5) a LUST system
Relevance for Psychiatry's Basic Science 99

that fosters mating and reproduction, (6) a maternal CARE system that nurtures
infants, and (7) a roughhousing PLAY system that provides youngsters with
skill-honing opportunities.
Genome deletion syndromes represent natural experiments for future BME-
MCO interactional analyses. Examples include Fragile X Syndrome, Prader-
Willi (PWS) and Angelman Syndromes (AS). The latter two feature a deletion
in chromosome 15qll-13, and differ from each other in that PWS lacks
chromosome material from the father and AS parallel material from the mother.
This phenomenon represents parental or genomic imprinting. The two syn-
dromes differ markedly phenotypically with a hypothalamic deficiency in PWS
and in AS the cortex affected; these patients show more severe retardation; they
never learn to speak but laugh incessantly. This has permitted the speculation
that through parental imprinting mechanisms, cortex normally results from
action of the mother's genes and hypothalamic structures from the father's
counterpart genes. PWS patients show infantile flaccidity, overeating from ages
2-6 on, they remain sexually underdeveloped even with sexual hormone
treatments, but in striking contrast to AS patients show only mild to moderate
retardation. They demonstrate typical personalities. In work that I conducted at
Texas Children's Hospital, 125 patients were investigated using questionnaire
survey of parents and other significant others. All showed tempestuous demand-
ing behavior with low threshold to frustration regardless of age. They showed
tantrums and never-ending "terrible twos." On the other hand, an anecdotal case
of a patient showed overeating but not the frustration-aggression pattern had
been labeled with "acquired PWS" because he sustained hypothalamic damage
from surgery for a brain tumor in the hypothalamus; he did not in fact have PWS
at all.
Frustration-aggression needs examination. The behaviorally interactive pat-
tern also shows up in other retarded patients. In normal development any parent
is well aware of the problem. Normally this modulates over time, though as any
parent also knows, he or she—even though adult and supposedly mature—
remains also vulnerable to it as when a child becomes aggravating. Frustration-
aggression links to low levels of serotonin in the brain. How hypothalamus
connections to the orbital frontal lobe foster modulation or exacerbation of such
reactions in connections to variously intact nervous systems represents
necessary future work, part of a future MacLean-inspired research program. We
need to learn how the behavior constellation is encoded in the genome and how
it is modulated over normal development. What circuits in the brain are
activated, what circumstances with other people typically affect it, and how are
its cell assembly characteristics parallel to R-complex cell assembly? Where is it
triggered and how is it modulated?
100 The Evolutionary Neuroethology of Paul MacLean

SOCIOPHYSIOLOGY SUMMARIZED

This chapter suggests that sociophysiology fittingly represents a framework

to underpin psychiatry and other helping professions. This schema, building on
MacLean's neuroethology, labels more precisely the clinical world for which it
exhibits relevance. In connection with this, the present author began a decade
and a half ago the publication of a monthly Across-Species Comparisons and
Psychopathology (ASCAP) Newsletter that became a quarterly bulletin in 2000.
Multiple contributors wrote material then distributed internationally. This in turn
fostered The ASCAP Society in 1991 that meets annually or more often. In
1999, the group called a two-day meeting to discuss the work and implications
of Paul D. MacLean's work. Moreover, John Price, when chairman of the
Section on Psychotherapy of the World Psychiatric Association (WPA),
arranged that the Newsletter/Bulletin become the official news distributing
organ of the section—an action approved by the WPA. A number of papers in
refereed journals stemmed from discussions in the pages of the newsletter.
Notably, a paper in 1994 by Price et al. entitled, "The social competition
hypothesis of depression" was carried in the British Journal of Psychiatry and
49
subsequently anthologized by Simon Baron-Cohen in an edited book. A
volume entitled Genes on the Couch edited by Paul Gilbert and Kent Bailey has
50
also resulted.
51
Sociophysiology concerns paleopsychology and paleobiology, interper-
sonal and group relations, and psychopathology. The mission statement of the
Across-Species Comparisons and Psychopathology Society has read as follows
since its origination in 1991:

The ASCAP Society represents a group of people who view forms of

psychopathology in the context of evolutionary biology and who wish to
mobilize members and resources of various disciplines so as to enhance the
further investigation and study of the conceptual and research questions
involved. This scientific society is concerned with the basic plans of behavior
that have evolved over millions of years and that have resulted in
psychopathologically related states. We are interested in the integration of
various methods of study ranging from cellular processes to individuals in
groups.

The research committee of the Group for the Advancement of Psychiatry

52
(GAP), a specialty think-tank group agreed on the following during its Spring,
2000, meeting:

Members of the Research Committee of the Group for Advancement of

Psychiatry (GAP), a specialty think-tank, has addressed psychiatry's need for a
unifying scientific foundation. Such a foundation would consider the disorders
commonly treated by psychiatrists in terms of the physiological baseline from
which they depart, much as heart disease is understood as deviation from
Relevance for Psychiatry's Basic Science 101

normal cardiac function. The relevant physiological focus for psychiatry is the
social brain.
The social brain concept focuses on the interaction between brain physi-
ology and the individual's environment. The brain is the organ most influenced
on the cellular level by social factors across development; in turn, the
expression of brain function determines and structures an individual's personal
and social experience. The social brain framework may have greater direct
impact on the understanding of some psychiatric disorders than others.
However, it helps organize and explain all psychopathology. A single gene-
based disorder like Huntington disease is expressed to a large extent as social
dysfunction. Conversely, traumatic stress has structural impact on the brain as
does the socially interactive process of psychotherapy.
Brains, including human brains, derive from ancient adaptations to diverse
environments and are themselves repositories of phylogenetic adaptations. In
addition, individual experiences shape the brain through epigenesis, i.e., the
expression of genes is shaped by environmental influences. Thus, the social
brain is also a repository of individual development. On an ongoing basis, the
brain is further refined through social interactions; plastic changes continue
through life with both physiological and anatomical modifications.
In contrast to the conventional biopsychosocial model, the social brain
formulation emphasizes that all psychological and social factors are biological.
Conversation, feeling, and thinking can happen only from brain-actions in the
involved individuals. Non-biological and non-social psychiatry cannot exist.
Molecular and cellular sciences offer fresh and exciting contributions to such a
framework but provide limited explanations for the social facets of individual
function.
The social brain formulation is consistent with current research and clinical
data. Moreover, it ultimately must:

• unify the biological, psychological and social factors in psychiatric illness,

• dissect components of illness into meaningful functional subsets that deviate

in definable ways from normal physiology,

• improve diagnostic validity by generating testable clinical formulations

from brain-based social processes,

• guide psychiatric research and treatment,

• provide an improved language for treating patients as well as educating

trainees, patients, their families and the public, and

• account for the role of interpersonal relationships for brain function and
health.
102 The Evolutionary Neuroethology of Paul MacLean

In conclusion, the concept of the brain as an organ that manages social life
provides significant power for psychiatry's basic science. Burgeoning develop-
ments in neural and genetic areas put added demands on the conceptual
structures of psychiatry. Findings from such incoming work must be juxtaposed
and correlated with the behavioral and experiential facets of psychiatry to give
it a complete and rational basis. Psychiatry's full and unified entry into the
realm of theory-driven and data-based medical science has arrived. The social
brain concept allows psychiatry to utilize pathogenesis in a manner parallel to
practice in other specialties.

Contrasts and comparisons of humans and nonhuman animals provide ways

to approach the impact of evolutionary history on our brains and behavior
relevant to clinical work. While nearly all of the human genome has constancy
with that of the chimpanzee, the human burgeoning brain size is three times
larger than that of chimps or gorillas. Yet, we also know that it works under the
guidance of older systems heralded as important by MacLean. What does the
bigger brain accomplish? Social facilitation, communicational subtlety via both
verbal and nonverbal means, and storytelling. Jerome Kagan notes that aware-
ness that we behaved in a particular way in a particular place at a particular time
in the past is a state unique to humans, suggesting that "ability of humans to
generate ideas of events that might occur years in the future might explain why
3 6
we are the only species to have populated so much of the world." Gerald A.
Cory has been working hard to reveal neuronal algorithms that guide our
behaviors and would do so better if acknowledged directly for the power that
53 54
they possess. '
In summary, constellations of core communicative behaviors need to be
conceptually integrated with genomics (wherein individual people are identical
to one another), genetics (individuals differ), and brain systems that separately
evolve in each person yet result in remarkably similar behaviors. What patho-
genetic linkages do patients also share in common? Finally, how will Paul D.
MacLean prove to have been prophetic in his insistence on examining the most
primitive brain parts and brain states as fundamental? How will his communi-
cational paradigm be utilized in the future to benefit psychiatry, other patients of
any doctor or treating professional, and people who need more information to
guide their lives most effectively?

NOTES

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Relevance for Psychiatry's Basic Science 103

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nal Life. NY: Simon & Schuster, 1996.
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sity Press, 1975.
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30. Walker, M: German eugenics. Review of book by S.F. Weiss: Race Hygiene and
National Efficiency. Berkeley: University of California Press, 1988. Science 1988; 240:
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31. Paul, DB: A history of the eugenics movement and its multiple effects on public
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Use of Human Heredity. Alfred A. Knopf. Scientific American, January, 1986, pp 27-31.
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tific base. American Journal of Psychiatry. 2001; 158: 1-3.
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study of the brain and mind. Science. 2000; 290: 1113-1120.
34. Kandel, Eric: A new intellectual framework for psychiatry. American Journal of
Psychiatry. 1998; 155:457-469.
35. Rosack, J: Nobel-Prize winner to speak at annual meeting. Psychiatric News. May
4, 2001, pp. 16-17.
36. Kagan, Jerome: Three Seductive Ideas. Cambridge, MA: Harvard University
Press, 1998.
37. Marks, IM: Fears, Phobias, and Rituals: Panic, Anxiety, and Their Disorders.
NY: Oxford University Press, 1987.
38. Bownds, Deric: Biology of Mind: Origins and Structures of Mind, Brain, and
Consciousness. Bethesda, MD: Fitzgerald Science Press, 1999.
39. Calvin, WH: The Ascent of Mind: Ice Age Climates and the Evolution of Intelli-
gence. NY: Bantam Books, 1990.
40. Edelman, GM: Neural Darwinism: The Theory of Neuronal Group Selection. NY:
Basic Books, 1987.
41. Weiner, J: Time, Love, Memory: A Great Biologist and His Quest for the Origins
of Behavior, 1999.
42. Fortey, Richard: Trilobite: Eyewitness to Evolution. NY: Alfred A. Knopf, 2000.
43. Martindale, MQ, Kourakis, MJ: Hox clusters: size doesn't matter. Nature. 1999;
399: 730-731.
44. Bartelmez, GW: Charles Judson Herrick October 6, 1868-January 29, 1960.
National Academy of Sciences: Biographical Memoirs Volume XLIII. Washington, D.C.:
National Academy Press, 1973, pp. 77-108.
45. Darwin, C: The Expression of the Emotions in Man and Animals. London: John
Murray, 1872.
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47. Mayr, E: The Growth of Biological Thought: Diversity, Evolution, and Inher-
itance. Cambridge, MA: Harvard University Press, 1982.
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competition hypothesis of depression. British J. Psychiatry. 164: 309-315. Reprinted in
Baron-Cohen, S. (Ed.) (1997) The Maladapted Mind: Classic Readings in Evolutionary
Psychopathology. Hove, East Sussex, UK: Psychology Press.
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(November, 2000/- The Social Brain: A Unifying Foundation for Psychiatry. A

manuscript submitted for publication composed by the Research Committee of GAP.
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 6

T H E TRIUNE BRAIN, ESCALATION

DE-ESCALATION STRATEGIES, A N D
M O O D DISORDERS

John S. Price

INTRODUCTION

Paul MacLean described three "central processing assemblies" in the neomam-

malian, paleomammalian, and reptilian brains that make decisions about
responses to environmental social events relatively independently. In this chap-
ter, I apply this model to explaining the two alternative strategies of escalation
(fight) and de-escalation (escape or submission). At the neomammalian level
there is a conscious, rational decision either to fight or give in. At the paleo-
mammalian level which relates to emotions and the limbic system, there is
deployment of either the escalatory emotions of anger, exhilaration, and so on,
or of the de-escalation emotions of fear, depression, shame, etc. I suggest that at
the reptilian level of the forebrain, the escalating strategy consists of elevated
mood and the de-escalating strategy consists of depressed mood, which is
unfocused or self-focused. In some cases the responses of the levels may be
incompatible. The implications for mood disorders and their treatment are
examined.

BACKGROUND

The message I got from the work of Paul MacLean entailed the following:
the mammalian forebrain has evolved into three "central processing assemblies"
for coordination of information and decision-making about how to respond to
1
changes in the environment. These three assemblies coordinate their actions but
make somewhat independent decisions. For ease of communication I talk about
the rational brain situated roughly in the neocortex (MacLean's neomammalian
brain), an emotional brain in the limbic system (MacLean's paleomammalian
brain), and an instinctive brain situated in the corpus striatum (MacLean's
108 The Evolutionary Neuroethology of Paul MacLean

reptilian brain or R-complex). The rational brain uses all the information that we
normally consider conscious, and its decisions have the character of
voluntariness with full awareness. The emotional brain has restricted access to
the information of consciousness; its decisions have both voluntary and involun-
tary components, with only partial awareness of its decisions; the information
used in emotional brain decision-making includes elements unavailable to the
rational brain, as Pascal noted in his famous aphorism "Le coeur a ses raisons
que la raison ne connait pas" (The heart has its reasons which are not known to
Reason). The instinctive brain has different sources of information that have not
been much studied yet; its decisions are involuntary with no awareness of any
ensuing course of action until that action takes place.
This new conception of the forebrain replaced my previous idea, that of
homogeneous brain expansion since the time of the common human and
reptilian ancestor some 250 million years ago, and included the general principle
that higher centres control the lower ones, largely through inhibition.
The numerous theories of unconscious processes attest to psychiatry's
2
inevitable concern with brain or mind levels. When treating patients with
depression and anxiety, the clinician finds it obvious that higher centres do not
control the lower ones. No patient with his rational brain can command his
emotional brain to feel less depressed or anxious. From the time of Coue and
Samuel Smiles to the more recent efforts of psychological healers, people have
stood before their mirrors and repeated to themselves such phrases as, "Every
day, in every way, I am getting better and better." But these techniques do not
work. In fact, they make patients worse, because they arouse expectations of
improvement that remain unfulfilled, therefore resulting in disappointment and a
sense of failure. An outstanding feature of psychiatric practice hinges on the fact
that the rational brain of homo sapiens, the acme of the evolutionary process,
has no more control over the lower brain centres than does the rider over a
runaway horse.
Rational control over the lower brains could easily have evolved. The fact
that it has not should tell us something—namely, that painful and incapacitating
processes such as depression which emerge so much against our conscious will
are, in fact, performing one or more functions of adaptive value. It appears that
the rider does not always know best. There is survival value in having a horse
that sometimes makes the decisions.

WHAT NORMAL BEHAVIOR UNDERLIES MOOD CHANGE?

In an evolutionary analysis of psychopathology, we must determine what

kind of behaviour is being affected. A depression may or may not be adaptive,
but it likely, at least, exaggerates or distorts some piece of adaptive behaviour.
In the case of mood disorders, no general agreement exists on what this normal
adaptive behaviour might be; except, perhaps, that it involves some form of
social behaviour. The extreme incapacity of depression can only be maladaptive
for nonsocial events. Generally, we agree that when depression has a cause, it
Escalation, De-escalation, Mood Disorders 109

involves some form of loss or failure. But if, for example, in a group of our
hunter/gatherer ancestors, hunting had gone badly, it would not be adaptive for
the hunters to become so depressed that they were unable to gather effectively.
As with foraging decisions, so with predator avoidance, there is little place for
depressed mood. Only in the case of dealing with climatic adversity do we get a
suggestion that depression might perform some function analogous to hiberna-
tion during the winter, and keep us out of harm's way until spring comes along.
But, in spite of the attention devoted recently to seasonal affective disorder
(SAD), psychiatry is not a seasonal matter, and there is no suggestion that we
might close our consulting rooms during the summer and take jobs as water-ski
instructors.
Social theories of the adaptive value of depression take the form of cries for
help, changes of social niche, relinquishing of unattainable social goals, and
adjustment to loss. At the time I first became engaged with this field, it was
thought that depression served some function in relation to loss, separation or
bereavement. This reasoning never convinced me. Although it was clear that a
social or romantic bond of many years' duration could not be broken without
some grief, it never seemed likely that a depressive episode of several months'
duration could be adaptive following the loss of a good ally or partner.
Depression is incapacitating, and if you lose a partner, there is the work of the
partner to do in addition to your own, so that an increase in capacity would be
more advantageous than depression.

SOCIAL COMPETITION

More likely has been the possibility that elevation and depression of mood
serve a function in relation to social competition. The reasons for this are as
follows:

3
Depressed patients feel like failures and losers.
4
Manic patients feel successful and like winners.
The basic strategy set of social competition contains the two alternative
strategies of escalation (fight) and de-escalation (flight or submission), which
5
have similarities to elevated and depressed mood, respectively.
Competing animals can switch rapidly from escalation to de-escalation in the
way that a manic-depressive patient can switch from mania to depression.
Monkeys who have failed in social competition and thus are low ranking may
behave in a restricted and dysphoric manner similar to that of depressed
6
patients.

However, there are problems with this line of thinking:

Some high-ranking people are depressed.

Some low-ranking people are perfectly happy.
110 The Evolutionary Neuroethology of Paul MacLean

Some depressed patients are very powerful—they may be stubborn, demanding

and manipulative. Aaron Beck warned, "Beware of locking horns with a
depressed patient, or you may be pushed clean out of the consulting room!"
Depressed patients do not act in a submissive way or show deference to more
powerful people.

In our discussions of these matters, we played with ideas of there being two
different types of submission, voluntary and involuntary, and that depression
reflected only involuntary submission—so that an alternative to depression
could be those forms of voluntary submission that go under the terms of
humility, reasonableness, and willingness to compromise. But the water was
murky, and we could not see the way ahead clearly.

THE TRIUNE MIND/BRAIN

Then came triune brain theory. Although it would be too much to say that all
then was light, it did clarify our ideas greatly. One could say that we passed the
white light of escalation/de-escalation theory through the prism of triune brain
theory and saw the resolution of clearly identifiable patterns of behaviour at
each level of the triune brain (see Table 6.1 next page).
In response to social adversity, or ranking stress as we called it, each level of
the triune brain seemed to make a decision between escalation and de-escalation.
Sometimes the decisions agreed. Then there was likely to be a quick resolution
of the conflict through either defeat, acceptance of defeat, and reconciliation on
the one hand, or success, acceptance of the other's submission, and reconcil-
iation on the other. At other times the decisions did not agree, and then trouble
ensued, leading to psychopathology.
We have been concerned at the amount of criticism MacLean has received
from his fellow neuroanatomists, but we note that these criticisms have been
over details, and have not challenged the essential concept of three relatively
independent central processing assemblies; in fact, in their authoritative mono-
graph on the evolution of the vertebrate nervous system, Butler and Hodos
state: "Longitudinal transmission of information within the nervous system and
the presence of rostrocaudally localised areas of integration and control are
7, p 4 6 3
keystones of the chordate nervous system."
The most efficient way to bring about conflict resolution operates at the
rational level. One of two competitors should be able to say, "The other guy is
more powerful, so I will give in." The lower agonistic strategy sets can be left
alone and this could be called functional agonism. But, unfortunately, the human
animal often prefers to not give in. On the way to my present location, I passed a
T-shirt with the caption, "Never surrender," and this sums up a slogan which has
been reiterated over the centuries ever since the Titans were thrown out of
Heaven.
Escalation, De-escalation, Mood Disorders 111

Table 6.1. The Social Competition Strategy Set at Three Levels of the
Triune Brain/Mind

Escalation De-escalation

Rational/ Formation of goals Giving up of

Neocortical Proclamation of goals personal goals
Overcoming of opposition Adoption of
Social participation others' goals
Self-assertion Submission
Decision to fight on Acceptance
Resignation
Self-effacement

Emotional/ Joy, rapture Boredom

limbic Enthusiasm Apathy
Oceanic feeling Shame
Anger Guilt
Indignation Depressed emotion

Instinctive/ Increase ofRHP/SAHP Loss of RHP/ SAHP

Reptilian Increase of resource value Loss of resource value
Increase of "ownership" value Loss of "ownership value"
Increase of energy Loss of energy
Elevated mood (IDS) Depressed mood(ISS)

Another form of functional agonism works as follows: The rational brain

decides to fight, but the emotional and/or instinctive brains decide to de-
escalate. These de-escalations affect the thinking of the rational brain, moving it
in a more pessimistic direction. To put it technically, there is a loss of resource-
holding potential (RHP), resource value and "ownership," so that the individual
feels less confident of winning, sees the prize as less valuable, and feels less
8
entitled to the ownership of the prize. Due to this more pessimistic thinking, the
rational level switches its strategy from escalation to de-escalation, there is
graceful losing, with the way paved for reconciliation. In this process, the lower
brain controlled the upper brain. And this seems to be its function. The upper
brain seems designed for escalation, to win at all costs, and not to jeopardise its
fighting efficiency by any thought of possible damage or defeat. This moni-
toring of possible defeat has been relegated to, or retained by, the lower brain.
In some way the lower brain seems to keep a tally of punishment received, and
when this gets too great it exerts its authority telling the upper brain to de-
escalate. The upper brain, which was in any case having a fairly difficult
encounter, now has the added handicap of depressive incapacity. So, if it does
not capitulate gracefully at this stage, the individual likely gets carried out of the
arena on a stretcher.
We have identified depression with instinctive de-escalation, and the com-
monest cause of prolonged instinctive de-escalation appears to be continued
inappropriate rational escalation, or, to put it another way, blocked rational de-
112 The Evolutionary Neuroethology of Paul MacLean

escalation. There are many causes for this, and I will defer discussion of them to
a later section.
Prolonged instinctive de-escalation may also stem from inappropriate emot-
ional escalation. An example entails the parents whose child has been killed by a
drunken hit-and-run driver. The parents know there is nothing they can do at the
rational level, but there is often sustained anger that cannot be satisfied or
usefully discharged. The continued "punishment" and hurt accesses the instinc-
tive agonistic strategy set and if de-escalation is selected, chronic depression
ensues that cannot be resolved because continued emotional escalation persists.
The third clinical variety is emotional de-escalation associated with rational
escalation. This describes, characteristically, wives consulting for marriage
8
guidance. They experience emotional distress, weep, and otherwise de-escalate
emotionally. But at the rational level they have escalated in that they are
determined to change their husbands' behaviour; to make him less spendthrift,
or less unfaithful, or just to pay them more attention. Their failure to achieve this
change for the better in the husbands took them to marriage guidance. But the
husbands typically sit in the session stony-faced, turned away from their
weeping wives, apparently unmoved by their distress. They do not want to
change, but they feel confused by their wives' behaviour, escalated at one level
and de-escalated at the other.
In a fourth clinical variety the patient de-escalates at all levels, but the
submission is not being accepted by the important other person. This occurs
sometimes from ignorance, sometimes from cruelty. The fifth and final example
of dysfunctional agonism is seen when the instinctive strategy set is too easily
accessed, and de-escalation occurs inappropriately to the situation. These
patients are oversensitive, too easily moved to tears. Sloman's chapter in this
volume deals with them extensively.

TREATMENT

The treatment that arises from our model can be listed in four stages with the
injunction: Try the first stage first, and if that doesn't work, try the second stage,
and so on.
1. Find a rational solution. There is nothing wonderful about the operation of
the lower levels, and their mobilisation of emotional distress and depressed
mood suggest failsafe mechanisms because the higher-level has failed to solve
the problem.
The therapist's task involves:

(a) identifying the conflict.

(b) estimating the chances of winning, or of leaving the arena, or of

submitting the conflict to arbitration; and if any of these seem possible,
helping the patient achieve them.
Escalation, De-escalation, Mood Disorders 113

(c) if the problem is one of blocked voluntary yielding (inappropriate

rational-level escalation), devising a means for the patient to give in (or
give up) without loss of face. This best happens before the admini-
stration of antidepressant drugs, because the "giving-up" component of
the depressive cognitions may help. In fact, when this situation arises,
this giving-up depressive cognition typically has not been strong
enough to achieve the necessary yielding. It needs the depression plus
the therapist to complete the job.

(d) if a third party is causative, dealing with the problem. Such a third
party may be demanding obedience that conflicts with obedience to
another, therefore preventing the patient from making a desired submis-
sion. This occurs commonly in patients caught between the demands of
a dominant parent and a dominant spouse. They cannot submit to both
at the same time, because the demands are incompatible. Or the third
party may not accept the submission, perhaps because he or she fails to
recognise what is going on.

(e) if the patient's instinctive agonistic strategy set is too easily access-
ed, perhaps due to "kindling" by physical or emotional abuse in child-
hood, setting in motion appropriate measures. These may range from
long-term individual psychotherapy to a self-assertion class. (See
Sloman, this volume.)

(f) if the patient has had to give up some unattainable goal or much-
loved incentive, considering the need for "bereavement counselling" of
9
some sort. Rosen discusses this well.

2. Reframing the situation. If the situation that gave rise to the depression
seems insoluble, consider how it may seem differently to the patient. Here the
rational brain tries to control the informational input to the emotional brain.
Since it cannot influence the emotional brain directly, this represents the closest
approximation to influencing the decision-making function at the emotional
level. The best reframing process in the Western world is Christianity. Reframed
pain and suffering take on Christ-like qualities: the more one suffers, the more
one shares the experience of the Saviour. Gurdjieff reframed suffering to his
disciples as opportunities to work on the self and so improve the "true self"
10
which, given enough opportunity and enough work, might become immortal.
11
The classical reframing, quoted by Watzlawick, is Tom Sawyer's punishment
of having to paint a fence. This prevented him from going fishing with his
friends, so Tom reframed it as a marvellous opportunity to have fun with paint.
This reframing gained such success that his friends forgot all about fishing and
begged him to let them do the job themselves. For the parent of a child killed by
a hit-and-run driver, it may help to see the driver as someone sick rather than
bad, perhaps as someone in the throes of epilepsy or a heart attack.
114 The Evolutionary Neuroethology of Paul MacLean

3. Substitute group conflict for individual conflict. We have suggested that

the tendency to depressive illness evolved as part of the yielding component of
ritual agonistic behaviour. Essentially this stems from a dyadic interaction. The
same considerations do not apply to conflict between groups because group
conflict lacks the primitive ritual quality of dyadic encounters. In other words,
when groups lose a conflict, the members may become demoralised, but they do
not become depressed in the way that individual losers do. Therefore, if the
patient can join other people engaged in the same conflict, the whole operation
may switch from individual agonistic behaviour to an intergroup process. The
parents who lost their child to the hit-and-run driver can join other parents and
express their grief and rage in a group fashion, and hopefully thereby direct their
energies into such positive action as campaigning for more severe laws on drunk
driving.
4. Last, provide salves and ointments to the symptoms themselves. This
should represent very much a last-ditch action. One hopes that in most cases one
of the preceding three methods would have worked. If not, the symptoms may
be addressed directly. I am indebted to Leon Sloman for the vignette of the
alpine climber who has a panic attack on the side of a snow-covered mountain.
He heard a rumble and feared an avalanche. His breathing accelerated by anxiety
caused him to blow off too much carbon dioxide, his blood became alkaline, and
his muscles went into tetany. In this case, encouraging him to breathe more
slowly results in restoration of the acid-base balance of his blood to normal so
his legs move again and he can walk to safety. Of course, even here, common
sense must be used. The therapist chose the breathing. He would have had less
success if he had applied ointment to the tetanic muscles.
In this case, we accept that higher level solutions were not available. The
therapist might have done better to produce a cell phone and summon up a
helicopter to take the patient off the mountain to safety. Or reframing the
situation, he could have pointed out that they were not in fact on a real mountain
at all—they were actors taking part in an alpine movie, and the rumbling he had
heard was the movement of a mock Mont Blanc on its castors to take up a new
location. However, we accept that the deus ex machina of a helicopter is seldom
to be summoned, even with a cell phone, and that most climbers who panic at
the thought of an avalanche are on real mountains and not taking part in films.
But this direct attack on symptoms represents a last resort, unlike some
cognitive behaviour therapists who spend time trying to argue patients out of
their depressive delusions.

RESEARCH

Like other evolutionary interpretations, the foregoing represents speculation

in the last resort untestable. But definitive implications for treatment result.
These might have been deduced from another theory, but they have not.
Treatment either works or it does not; and this can be tested in a controlled trial.
The following plan would constitute such a test: (1) recruiting a center already
Escalation, De-escalation, Mood Disorders 115

conducting manualized psychotherapy of depression, e.g., interpersonal therapy

12
or IPT; (2) inserting into their research design additional or replacement
interventions based on the evolutionary theory as delineated above. We predict
that the results would show quicker and greater power.

THE TRIUNE MIND

For centuries, thinkers have expressed intimations that the mind functions in
a way dictated by the triune nature of the brain. Plato, in a chapter entitled "The
three parts of the soul" describes various functions and asks: "Are we using the
same part of ourselves in all these three experiences, or a different part in each?
Do we gain knowledge with one part, feel anger with another, and with yet a
third desire the pleasures of food, sex, and so on? Or is the whole soul at work in
l3, p 132
every impulse and in all these forms of behaviour?"
10
Eastern philosophy, brought to the West after World War I by Gurdjieff,
used the metaphor of the horse and cart to describe the mind. It talked of a
driver, a horse and a cart, and of the connections between the three elements.
The driver represents the rational mind, the horse the emotional mind, and the
cart the instinctive mind. This philosophy aimed to create a fourth element, the
"true self" representing a "master," who controlled the driver, and told him
where to go. Gurdjieff established a teaching centre near Paris; its prospectus
proclaimed:

a modern man represents three different men in a single individual—the first of whom
thinks in complete isolation from the other parts, the second merely feels, and the third
acts only automatically, according to established or accidental reflexes of his organic
functions . . . they not only never help each other, but are, on the contrary, automatically
compelled to frustrate the plans and intentions of each other; moreover, each of them, by
dominating the other in moments of intensive action, appears to be the master of the
14, p 1 3 8
situation, in this way falsely assuming the responsibility of the real "I."

CONCLUSION

In summary, the concept of the triune mind has been part of human folk
knowledge for over two millennia. Paul MacLean's description more recently
provided a neuroanatomical basis for this knowledge, offering an enormous
15
boost to the heuristic value of the triune model. In this chapter and elsewhere 1
attempted to demonstrate some applications to psychiatric practice; and in the
future I would anticipate that it will have a profound influence on the fields of
individual and social psychology.
It is, of course, just a theory, that should be compared with other theories
dealing with the same material. Birtchnell, for example, has put forward a two
16,17
level theory that may have advantages in certain circumstances; sometimes
18
it is useful to contrast the rational brain with the remainder of the brain.
However, the three-level theory has the advantage of dealing with the emotions
116 The Evolutionary Neuroethology of Paul MacLean

separately. For instance, it clarifies the relation between depressed emotion and
depressed mood (the former focused on an object rapidly responds to changes in
the object's situation, in contrast to depressed mood that remains unfocused or
self-focused, and unresponsive to circumstances present). The present theory
challenges previous theories of emotion, which, for instance, combine anger and
depressed emotion in the same category of negative emotion in contrast to the
positive emotions of joy and happiness. According to triune mind/brain theory,
anger joins with joy as an escalating emotion, in contrast to depressed emotion
seen as a component of a de-escalating strategy. Empirical research will decide
which theory most usefully conceptualizes the data.

NOTES

1. MacLean PD: The Triune Brain in Evolution. New York: Plenum Press, 1990.
2. Ellenberger HF: The Discovery of the Unconscious: The History and Evolution of
Dynamic Psychiatry. New York: Basic Books, 1970.
3. Beck AT: The development of depression. In D Freedman & H Kaplan (Eds.)
Comprehensive Textbook of Psychiatry. Philadelphia, PA: Williams and Wilkins, 1974.
Pp. 3-27.
4. Gardner R: The brain and communication are basic for clinical human sciences.
British Journal of Medical Psychology. 1998, 71: 493-508.
5. Huntingford F & Turner A: Animal Conflict. London: Chapman & Hall, 1987.
6. Price JS: The effect of social stress on the behaviour and physiology of monkeys.
In K Davison & A Keff (Eds.) Contemporary Themes in Psychiatry. London: Gaskell,
1989, pp. 459-466.
7. Butler AB & Hodos W: Comparative Vertebrate Neuroanatomy. New York: Wiley
Liss, 1996.
8. Gardner R, Jr. & Price JS: Sociophysiology and depression. In: T Joiner & JC
Coyne (Eds.) The Interactional Nature of Depression: Advances in Interpersonal
Approaches, Washington, DC: APA Books, 1999, pp. 247-268.
9. Rosen DH: Transforming Depression: Egocide, Symbolic Death, and New Life.
NewYork: Putnam, 1993.
10. Ouspensky PD: In Search of the Miraculous: Fragments of an Unknown
Teaching. London:Routledge & Kegan Paul, 1950.
11. Watzlawick P, Beavin JH, Jackson DD: The Pragmatics of Human Communi-
cation: A Study of Interactional Patterns, Pathologies and Paradoxes. New York: W.W.
Norton, 1950.
12. Weissman N M & Markowitz JC: (1994) Interpersonal psychotherapy: current
status. Archives of General Psychiatry, 1994; 51: 599-606.
13. Cornford FM: The Republic of Plato. Translated with introduction and notes.
London: Oxford University Press, 1992.
14. Bennett JG: Gurdjieff. Making a New World. London: Turnstone Books, 1976.
15. Price JS: The adaptive function of mood change. British Journal of Medical
Psychology 1998; 71: 465-477.
16. Birtchnell J: The inner brain and the outer brain. The ASCAP Newsletter, 1999,
12(01), 11-17.
Escalation, De-escalation, Mood Disorders 117

17. Birtchnell J: Relating in Psychotherapy: The Application of a New Theory.

Westport CT: Praeger, 1999.
18. Price J: A case of hedonic emotional/limbic escalation. ASCAP Newsletter 1999;
12(No.5), 10-12.
 7

INVOLUNTARY DEFEAT STRATEGY AS

B A C K D R O P FOR DEPRESSION

Leon Sloman

INTRODUCTION

The extensive history of conspecific conflict in humans makes it hard to believe

that humans can be endowed with strategies designed to prevent and terminate
fighting. However, these conflicts would have been even more severe, if it had
not been for the Involuntary Defeat Strategy (IDS), which has played a key role
in the avoidance and rapid termination of conflict. I will discuss the IDS and
show how it can, at times, have a more pathological outcome by contributing to
certain forms of depression. I plan to examine factors associated with a negative
outcome and propose that a crucial issue features whether or not the IDS
functions effectively. I will distinguish between effective and ineffective funct-
ioning of the IDS, and consider factors that render it more and less effective and
demonstrate how an ineffective functioning of the IDS contributes to depressive
disorders and other forms of psychopathology. I will also discuss the link
between dominance and mania and present the "see-saw" model of bipolar
disorder. Finally, I will describe clinical interventions designed to promote the
IDS's more effective functioning.

BACKGROUND

Price (1967) drew on Zuckermann's (1932) observations of long-tailed

macaques to note the similarity between depressed patients and animals who
lose in hierarchical encounters and are pressed into a subordinate social role. He
proposed that "states of depression, anxiety, and irritability are the emotional
concomitants of behavior patterns which are necessary for the maintenance of
dominance hierarchies in social groups" and claimed (1969:1107) that
120 The Evolutionary Neuroethology of Paul MacLean

depression, anxiety, and feelings of inferiority evolved as the "yielding

component of ritual agonistic behaviors."
According to Price (1967: 243), "factors which increase or reduce dominance
behavior will have malignant or beneficial effects on mental illness." Price et al.
(1994) renamed the "yielding subroutine" the "Involuntary Subordinate
Strategy" (ISS) and postulated that "the depressive state evolved in relation to
social competition as an unconscious ISS, enabling the individual to accept
defeat in a ritual agonistic encounter and to accommodate to what would
otherwise be unacceptably low social rank." Price and Sloman (1987) proposed
that human beings share with other vertebrates an older, more primitive
mechanism for yielding that evolved as a component of ritual agonistic in the
common ancestor of present-day birds and mammals and that the "hardware" for
this mechanism is situated in the "reptilian brain." MacLean (1985a) deleted
elements of ritual agonistic behavior by ablation studies of the "reptilian" brain.
Recently, Sloman and Gilbert (2000) introduced the term "Involuntary Defeat
Strategy" (IDS) for greater specificity.
The IDS is a genetically preprogrammed strategy triggered by an individual's
recognition that defeat in social competition is inevitable. The strategy reduces
the risk of injury or death to both combatants by convincing the loser of the
futility of further struggle and triggering either flight or submission and
promoting subjective acceptance of the new status quo. In addition, it conveys to
the winner that his opponent no longer threatens because the battle is more or
less over. This may convince him to accept his opponent's submission and end
the struggle. The IDS is "involuntary" because it is triggered automatically by
the recognition that he has lost the competitive encounter or that defeat is
inevitable. The term "defeat" refers to the fact that the IDS is triggered by defeat
and also to its role in promoting accommodation to subordinate status. The term
"strategy" reflects its genetic preprogramming to fulfill an adaptive function
(Sloman 2000).
I now explore the differences between an effective and an ineffective IDS.

THE EFFECTIVE IDS

The effective IDS reduces motivation to continue the struggle, adjusts aspira-
tions, and increases readiness to flee or submit, while engaged or considering
engaging in a confrontation. While a mild IDS may be characterized as "disap-
pointment," a more powerful IDS may be associated with feelings of depression.
Flexible responsiveness to a changed situation and a strong "sense of self"
represent hallmarks of an effective IDS. A more self-confident person finds it
easier to change his stance and admit he was wrong. The behavior of the winner
may have a substantial impact on the loser's IDS. For example, the winner may
show magnanimity and perhaps share the spoils of the fight or, in other species,
accept grooming from the defeated rival. This friendliness and positive acknow-
ledgment of the loser's prowess makes it easier to accept defeat.
Involuntary Defeat Strategy and Depression 121

The effective functioning of the IDS brings a recognition that further struggle
would be futile, which ends the conflict and leads to the acceptance of the new
status quo, which switches off of the IDS. When the conflict is over, the IDS no
longer serves any useful function, except in an attenuated form by discouraging
the individual who has lost from attacking the victor who has demonstrated
superior prowess. The effective IDS leading to acceptance of defeat thus frees
the individual to resume more productive activities, resume an affiliative
relationship with the opponent, or run away to safety. Effective functioning of
the IDS causes loss of motivation to struggle any more, which prompts the
decision that it would be useless to continue. This is followed by adjustment to
the new situation, namely, acceptance of the subordinate role which, in turn,
leads to a termination of the IDS. The outcome of such encounters may leave
people with a more realistic appraisal of their own and others' strengths and
abilities and also leave them free to move on to face new challenges. However,
in the instance of escape, the IDS may be terminated without acceptance, since
the individual may be generating resources for renewed attack.
To summarize, when the IDS functions effectively, it helps avoid unneces-
sary conflict or brings conflict to an end. Termination of the conflict leads to
escape, or submission and/or acceptance. When the submission has been
accepted and the need to submit subsides, the IDS switches off. Similarly, if one
escapes and feels free, the IDS is no longer required. However, if the IDS does
not bring them to relinquish their unattainable goals, individuals may become
depressed, abusive to others, or locked into unproductive power struggles that
lead to dysfunctional interactions in both family and other social domains
(Sloman 1981).

SOCIAL COMPETITION AND ATTACHMENT

Because attachment theory and social competition theory evolved independ-

ently, the close interrelationship between the two models (Sloman & Atkinson
2000; Sloman, Atkinson, Milligan, & Liotti, in press) is often overlooked. A
secure attachment contributes towards effective functioning of the IDS. For
example, support from someone with whom one is affiliated can give one the
confidence to challenge a competitor and, if one loses the agonistic encounter,
the presence of someone to whom one is securely attached can lower one's level
of arousal, thus enabling one to accept defeat and move on to more productive
activities. Similarly, if one has just lost an agonistic encounter with someone to
whom one is securely attached, one's trust in the other may cause one's
resentment to fade. This promotes acceptance of defeat which brings the
struggle to an end, thus turning off the IDS.
According to Hilburn-Cobb (1998), subordination mechanisms like the IDS
can be used in the services of attachment. For example, Dorothy to be described
below, would burst into tears at times of potential confrontation. These tears
were designed to head off the opponent's expected wrath. Some clients, when
faced with a challenge, turn to those closest to them for support. Therefore,
122 The Evolutionary Neuroethology of Paul MacLean

attachment mechanisms can maintain a subordinate stance (Sloman & Atkinson

2000).
Gilbert (1997) concluded that competition by attraction has largely replaced
competition by intimidation and is the main form of competition seen in
primitive tribes by anthropologists. We compete to be seen as worthy, able, and
attractive. Those with insecure preoccupied attachments require constant signals
that they are attractive, desired and wanted, and fear not being able to call on
others for support. Also, they more likely see attachment as something that must
be earned in competition. Their inner models of attachment organize around
dimensions of power, control, and competitiveness. When these individuals lose
out in competition by attraction, their IDS is triggered, which makes them feel
more inadequate and therefore more unlovable, resulting in a still more insecure
attachment. This may make them more competitive while further undermining
their chances of success.

THE INEFFECTIVE IDS

Effective functioning of the IDS reduces the likelihood of certain forms of

psychopathology, while ineffective functioning can lead to depression or other
forms of psychopathology. An effective IDS leads to submission and/or accept-
ance. However, anger associated with a need to win may force a continuation of
the struggle, even though there is no prospect of winning.
There are three possible outcomes. First, the increased effort causes the tide
to turn in one's favor, thereby switching off the IDS; second, continued failure
convinces the individual that further struggle is hopeless so that he flees, or
accepts defeat, submits, and brings the struggle to an end; third a more negative
outcome occurs in that though the IDS has been triggered, one cannot give up
the struggle because of strong feelings of resentment, or because the opponent
refuses to accept the submission. This can cause cognitions associated with the
IDS to intensify, because of the apparent futility of one's efforts. Accordingly,
one feels increasingly disempowered and becomes more and more depressed. In
these situations, the IDS continues to operate and the features that are geared to
bring the struggle to an end (i.e., to de-escalate) have failed to achieve their
purpose and, instead, caused an intensification at the intrapsychic level and
possibly at the interpsychic level. At the intrapsychic level, feelings of helpless-
ness and hopelessness, with the function of triggering submission or flight, are
no longer effective. Because these feelings are designed to terminate conflict,
the fact that the conflict continues causes them to intensify, and they then
manifest as depressive disorder. At the interpsychic level, the intensification
may manifest as power struggles (Sloman 1981), put-downs or "double-bind"
communications (Bateson et al. 1956). The presence of the persistent IDS may
prevent the individual from engaging in open conflict, but the conflict may
continue covertly.
The presence of a persistent IDS can be attributed to neuronal "kindling"
(Post & Weiss 1998; Segal, Williams, Teasdale & Gemar 1996). Kindling
Involuntary Defeat Strategy and Depression 123

accounts for how, when the IDS has been overstimulated at an earlier point in
time, a smaller amount of stimulation is subsequently required to produce the
same strength of reaction. The notion of kindling purports to explain why the
first depressive illness may be precipitated by a major loss, while subsequent
relapses are triggered by much smaller losses.
When accepting subordinate status functions better than persisting in a self-
defeating strategy, why are we not programmed to show acceptance more
readily? One answer involves fighting strategies. To win, we must maintain our
belief that victory will come our way. If we react to every minor setback, we
might betray this information to our adversary. This would give him more heart
and thus bring about our own defeat. It seems likely that one reason why the IDS
evolved was to counteract this implacable resolve to win at all costs. Social life
would not be possible with a Titan mentality (Price, personal communication).

GAME THEORY

Maynard Smith (1982), using game theory, showed how assessor strategy
allows the contestant to evaluate whether the opponent or potential opponent is
stronger or weaker and then respond appropriately. If the animal correctly
evaluates that it would lose if it came to a fight, it might be in that animal's
interest to take flight relatively uninjured. On the other hand, if the animal
correctly evaluates that it would win, its best interest may be served by fighting
and benefiting from the spoils of victory. These spoils might comprise a rise in
status with better access to food, territory, and mating partners. Thus, that the
animal makes an accurate judgment of comparative strength holds great
importance. If the assessor strategy is off the mark, the IDS might be prema-
turely triggered or may fail to be triggered at the appropriate times. Both of
these can have negative consequences for the individual.

FACTORS AFFECTING EFFECTIVENESS OF THE IDS

The individual's ability to give up the struggle to achieve an unattainable

goal may be influenced by a number of factors. One is the value the individual
attaches to the resource that is the object of the struggle. In many conflicts of
interest, the practical consequences of defeat are minor, which makes it easier to
accept that status. However, at times, submission to the opponent entails giving
up a great deal. As a result, the options of submitting or continuing the struggle
are both unacceptable so that one feels there is no way out. Richard II, as
portrayed by Shakespeare, majestically exemplifies this.
124 The Evolutionary Neuroethology of Paul MacLean

Or I'll be buried in the King's highway,

Some way of common trade, where subjects' feet
May hourly trample on their sovereign's head;
For on my heart they tread now whilst I live,
And buried once, why not upon my head?

The king's pain of having his "subjects tramping hourly on his heart" may
not appear like the IDS, because it can take the form of incapacity, such as
illness, old age, possession by the devil, or some other condition unrelated to the
contest at issue. However, for the king this helps him submit. Is it not more
reassuring to see your opponent old and sick than stepping down in full
possession of his faculties, still able to make a speech which rings our heart with
sympathy, and oratorical ability but which could have been turned alternatively
to speeches requesting allies to support him in a come-back? For the king to
become reconciled and step down gracefully may not have been a viable option
(Price, personal communication). Those of less exalted status, who experience a
major defeat may find other arenas where they can experience success so that
their setback is only temporary.
The relationship between the competitors may make it painful for the loser to
submit and for the winner to accept the submission. For example, if the
contestants feel too much bitterness, triggering of the loser's IDS may fail to
stimulate acceptance by either party. If the adversary refuses to accept
submission and continues to behave agonistically by using put-downs, for
instance, this is likely to generate more anger and resentment. There may also be
pressure from other members of the same group who want the struggle to
continue.
Support from other members of the group can also make it easier to accept
defeat. This may take the form of solicitude, or praise for the loser's efforts.

SUBMISSIVE BEHAVIOR AND VULNERABILITY

TO PSYCHOPATHOLOGY

Physical and sexual abuse as well as neglect and insecure attachment in

childhood are likely to frequently and/or powerfully trigger the IDS. This may,
in fact, help the young child adapt, but in later years foster frequent, premature,
and unneeded triggering of the IDS. Overly submissive behavior may result.
Submissiveness, or low assertiveness relates to depression and social anxiety
(Gilbert & Allan 1994). Some forms of submissive behavior, particularly those
associated with passive/withdrawal and inhibition, associate with a wide variety
of psychological problems, especially depression (Gilbert 2000; Allan & Gilbert
1997). These findings support the proposed link between the IDS and
depression.
Involuntary Defeat Strategy and Depression 125

THE BIOLOGY OF THE NORMAL IDS

During an intense competitive encounter, the human or nonhuman primate

experiences increased arousal with an adaptive rise in plasma Cortisol levels,
which mobilizes metabolic, cognitive, and behavioral resources. If the individual
clearly foresees that the encounter will be lost and that further arousal will be
counterproductive, the IDS is triggered. If effective, this serves to de-escalate
behavior and HPA (hypothalamus-pituitary-adrenal)-axis functioning. A suc-
cessful escape/submission results in acceptance of the loss and new social status,
and the IDS then terminates. At this point, the HPA-axis returns to its baseline
point and reestablishes homeostasis.
At a neuroanatomical level, the IDS can be thought of as a preprogammed
neural circuit linking the limbic system, prefrontal cortex, and striatum, which
mediate, respectively, the emotional, cognitive, and behavioral components of
the IDS. In response to an agonistic threat, the limbic system activates first with
a concomitant increase in arousal and HPA-axis functioning. Once agonistic loss
becomes inevitable, the prefrontal cortex, responsible for higher order cognitive
functions including anticipation and planning, activates and triggers cognitions
related to anticipation of defeat. Shortly thereafter, the striatum would be
activated to trigger the behavioral/motor sequence needed to produce adaptive
gesturing and, if necessary, rapid flight from the encounter. Effective function-
ing of the IDS might incorporate adaptive motor behaviors mediated by the
striatum, a new cognitive set of acceptance mediated at the prefrontal cortex,
and decreased arousal concomitant with both decreased activation of the limbic
system and HPA-axis which establishes a successful return to steady state.

RELATION BETWEEN BIOLOGICAL CHANGES IN SUBORDINATES

AND DEPRESSION

If the IDS links to depression, biological changes should be associated with

defeat and with depression. Animal studies have found a significant relationship
between the biological changes in animals experiencing defeat in hierarchical
contests and those associated with human depression (Gilbert 2000; Levitan,
Hasey & Sloman 2000; and McGuire et al. 2000).
How does one explain this apparent relationship between the biological
changes in defeat and depression? The IDS normally functions to de-escalate
conflict so that, when the IDS is ineffective, de-escalation does not occur and
the physiological activation that is normally adaptive in conflict persists. The
physiological changes in the subordinate baboon (Sapolsky, Alberts & Altmann
1997) remain because it remains primed for combat. The changes observed in
human depression may similarly be attributed to a failure of demobilization; the
clinically depressed individual remains primed for combat, though he recognizes
that he cannot win (Levitan, Hasey & Sloman 2000).
126 The Evolutionary Neuroethology of Paul MacLean

DEFEAT AND ENTRAPMENT

Schjelderup-Ebbe (1935) coined the term "pecking order" as he described the

consequences of losing dominance in barnyard fowl, where escape to a new
territory was not possible. Following defeat, the bird's "behavior becomes
entirely changed. Deeply depressed in spirit, humble with dropping wings and
head in the dust it is—at any rate directly upon being vanquished—overcome
with paralysis, though one cannot detect any physical injury. The bird's resis-
tance now seems broken, and in some cases the effects of the psychological
condition are so strong that the bird will sooner or later come to grief." These
birds' severe reaction to agonistic loss can be attributed to their inability to flee
the scene because of being in captivity.
Gilbert (2000) and Gilbert and Allan (1998) argue that having to stay in the
arena following defeat is much more problematic than being able to escape.
They suggest that, when there is a strong motive to take flight, depression and
"entrapment" may be a preferable construct to "learned helplessness" (Seligman
1975).
MacLean (1985b & 1990) also noted that reptiles who lose rank often lose
their bright colors and may die soon afterwards, and Von Hoist (1986) found
that defeated tree shrews could suffer the same fate. Defeat and entrapment can,
therefore, have severe untoward effects.

DOMINANCE, MANIA AND BIPOLAR DISORDER

Gardner (1982) found that alpha individuals on the dominance hierarchy and
manic patients responded to questionnaires in a similar fashion, and his proposal
of a relationship between dominant behavior and manic illness represents a
seminal contribution. He deduced that inborn strategies that had an adaptive
function by helping alpha individuals attain and maintain their dominant status
could also become maladaptive by contributing to manic illness. Gardner's
model of manic illness complements Price's (1969) model of depression.
According to Price, increasing intensity of the Involuntary Defeat Strategy
associated with continued agonistic loss can culminate in depressive illness.
Similarly, deduced from Gardner's formulations, an increasingly intense out-of-
control Involuntary Dominant Strategy culminates in mania.
One unanswered question is whether mania is more closely related to one
particular form of dominant behavior. For example, is it related to the immediate
reaction to winning, which is associated with feelings of elation, high self-
confidence, and ritualistic behavior like throwing one's arms up in the air or
doing a victory dance? Or, is it related to the more long-term pattern associated
with being at the top of the hierarchy? After the feelings of triumph associated
with winning have faded, a residuum often manifests as increased self-
confidence. A third pattern that can be called "pseudo-dominance,"is character-
ized by a bullying or controlling attitude towards those perceived as weaker than
oneself and hierarchically lower. This behavior could be considered to be a
Involuntary Defeat Strategy and Depression 127

defense against inner feelings of inadequacy or insecurity. Bullying additionally

involves constant put-downs of other people, unproductive power struggles and
"double-bind" (Bateson et al. 1956) interactions. Though a bullying person
works hard to avoid defeat, he cannot truly assert himself or try to win.
Paul Gilbert (2000) lists various types of submissive behavior: escape/flight
strategies, ambivalent defensive strategies and arrested flight, blocked escape
strategies, loss of control strategies, social defeat strategies, enclosed avoidance
strategies, submissive display strategies, infantile and illness strategies. He diffe-
rentiates between friendly and hostile submission. One can also subcategorize
dominant behaviors too, by distinguishing between friendly and hostile domi-
nance, for example. Greater specificity about the manic's kind of dominant
strategy would help define a postulated relationship between manic illness and
the dominant strategy.
Gilbert (1992:195) speaks of a recent shift from exerting social control via
threat/aggression towards the need to present oneself as attractive to others.
Today, in Western culture, display of strength is emphasized less than "invest in
me and I will be useful to you" (Buss 1988). Gilbert coined the term "social
attention-holding power" (SAHP), that depends on abilities to control others'
attention favorably. One can distinguish certain leaders who derive their strength
from the use of threat/aggression (e.g., Saddam Hussein) and others, who rely
more on the use of attractiveness (e.g., Bill Clinton). Oddly enough, both of
these individuals have created trouble for others by going overboard in their use
of the techniques that got them into power. If any psychopathology does
develop, the pattern of dominance might well influence the nature of psycho-
pathology. For example, Gilbert (1992: 557-558) compares the biological and
symptom differences in depression in individuals with autocratic and achieve-
ment-focused personalities who are highly up-rank motivated and those who are
more affiliative and less autocratic? He concludes "Personality studies have
found that endogenous depressives and bipolar patients are more ambitious and
competitive than neurotics."
Adversarial escalation initially triggers the flight response which, in turn,
becomes regulated by the winner and loser's reaction to the results of the
agonistic encounter. One can conceptualize the dominant (winning) and defeat
strategies as existing at opposite ends of a biological see-saw. The see-saw
model is used to illustrate the close interrelation between reactions to winning
and losing. For example, when the subordinate strategy functions normally, the
dominant strategy switches off and vice versa. The relation between the two
ends of the see-saw reminds one of a thermostat where a shift in temperature
might result in switching off the heating or air conditioning; one does not expect
the air conditioning and heating system to operate simultaneously. When a
previously successful individual falls in the hierarchy, the higher end of the
individual's see-saw falls to the ground. The close connection between winning
and defeat strategies is further emphasized by the fact that, while engaged in
agonistic encounters, we are primed, depending on the outcome, to respond
either dominantly or subordinately at very short notice. One would expect that
both responses would be primed until one or the other has been triggered. The
128 The Evolutionary Neuroethology of Paul MacLean

close interrelationship between winning and losing is also shown by the fact that
the greatest triumph may be to "pluck victory from the jaws of defeat." Gardner
(1982: 143-148) commented that both mania and depression are obviously
primitive in that they are separated from social reality. This enables one to
argue, in these conditions, the likely reptilian origins of agonistic behavior.
Early learning plays an important role in the priming of the biological see-
saw. When conditions are optimal, the child learns when to challenge and when
to submit. The abused or severely repressed child tends to be overly primed to
respond in a subordinate fashion. In later years this child's subordinate response
may be prematurely triggered by any minor or imagined slight, exhibiting an
unbalanced see-saw.
In some cases, because genetic and experiential factors interplay, forceful
and frequent moves of the see-saw lead to an oscillation between overactivation
(depression) at one end of the see-saw and overactivation (mania) at the other
end. Sharp transitions from depression to mania and vice versa may exemplify
this, as observed in bipolar disorder. This oscillation may also occur with a
lesser force in cyclothymic personality. Overactivation refers to the escal-ation
of a normally adaptive mechanism to the point that it becomes largely
maladaptive as when the IDS manifests as clinical depression, the dominant
strategy manifests as mania, or when fear, anxiety vomiting, and diarrhea, all of
which have important adaptive functions, intensify too much.

SOCIAL COMPETITION THEORY AND COGNITIVE BEHAVIORAL

THERAPY

Swallow (2000), a cognitive behavior therapist, points out that self-denigrat-

ing cognitions may be part of a submissive defensive response to terminate the
motive to keep trying in no-win situations and that the overarching goal of this
system is self-protection. It therefore makes sense, he says, for cognitive
theorists to conceptualize depressive thinking patterns in terms of their prev-
iously evolved functional significance as well as in terms of their content or
structure. Swallow argues that such a conceptualization—the IDS perspective—
might have important implications for the way cognitive therapists address
negative thinking in depression. Because the IDS perspective suggests that the
individual may be motivated to see herself as no good in order to avoid some
putative threat such as being cut down to size by another person, the person may
be quite resistant to giving up this self-denigrating belief. Therapeutically this
motivation can be clarified by asking patients to consider what protection they
obtain from the belief that they are no good. Or what concerns would emerge for
them if they did not think that way about themselves.
Involuntary Defeat Strategy and Depression 129

CLINICAL EXAMPLES

Case of Dorothy

Dorothy, a 32-year-old married woman, suffered from mild depression. Her

father exhibited violent fits of rage during her childhood. Her older and younger
sisters had been openly rebellious, but she was compliant and had always tried
to mediate when her father berated her mother. Her inability to be assertive
manifested as chronic low self-esteem and her problem in being assertive was
compounded by her tendency to use her subordinate strategy in the service of
her attachment needs. That is to say, displaying weakness and helplessness was
her way of eliciting support and reassurance. I had tried to help her avoid
triggering her subordinate strategy in situations where she had the capacity to
hold her own. She had already made good progress in terms of improved self-
assertion. Towards the end of a particular psychotherapy session she said that
whereas she normally felt better at the end of a session, that today she felt as flat
as when she first came to treatment. When I asked her how she had perceived
our relationship during the session, she said that, at one point, she had perceived
me as being judgmental of her. When I inquired whether this would have been
something she could have mentioned spontaneously, she said "no." I then sug-
gested that she must have felt angry with me and avoided expressing this by
adopting a subordinate role (the IDS). She acknowledged this had happened; and
then added she now felt less tired and more energetic. We discussed progress
she had made in eliminating the ghosts of the past—particularly the ghost of her
father—but also the work remaining to be done in this area.

Case of Leila

Leila was a 42-year-old married woman I saw in couples therapy. She had
been abused by her previous husband and we had been working on how she
could give up playing a victim role. In a dream a few days after the previous
session, Leila found herself in an anxiety-producing situation and felt that she
could react in an angry or frustrated way. She suddenly realized that she didn't
have to react in either way and felt an incredible sense of calm. She became
aware that she had been reacting as if she had a great need for power and was
reminded of the biblical injunction "The meek shall inherit the earth." She had
been trying to make sense of why she needed to take a subordinate position.
When she could give up her need for power, she became less involved in
agonistic conflicts. This, in turn, relieved her of having to take a "one-down"
position.
These cases illustrate two sides of the same coin. Dorothy illustrates the
value of freeing up people to express themselves without triggering the subordi-
nate strategy. Leila illustrates the merits of avoiding getting into agonistic
conflict with opponents who are clearly more powerful than oneself. These two
approaches are interdependent as people often compensate for feelings of
130 The Evolutionary Neuroethology of Paul MacLean

inferiority associated with their own subordinate reactions by developing an

inordinate need for power. Similarly, those with an inordinate need for power
more likely find themselves engaged in agonistic conflicts with others more
powerful than themselves, which triggers their subordinate strategies and results
in a self-defeating vicious cycle. The therapist's task involves breaking up this
vicious cycle by whatever means deemed most appropriate, including psycho-
therapy, medication, and physical education.

SUMMING UP

A variety of treatment approaches, with seemingly disparate mechanisms of

action, effectively treat depression. One explanation holds that these various
treatments intervene at different levels of the same final common pathway.
Considering first biological treatments, the two most established modalities are
antidepressant medications and electro-convulsive therapy. Serotonergic medi-
cations might work at several levels to render the IDS more effective. As
described above, increased serotonin activity decreases impulsive behavior and
hostility, while enhancing social affiliation and status in primates (Raleigh et al.
1991; Fuller et al. 1996). Recent work suggests that serotonergic drugs may also
enhance affiliative behavior in humans (Knutson et al. 1998), while improving
the symptoms of social anxiety (Stein et al. 1998). Taken as a whole, these
various lines of research suggest that serotonergic drugs may directly affect
brain mechanisms important in mediating primate affiliative behavior, so
important in promoting the normal unfolding of the IDS de-escalation strategy.
Regarding psychosocial treatments, various interventions including crisis
interventions and psychotherapeutic approaches likely have significant effects
on levels of perceived and actual stress, helping to decrease hypothalamic-
pituitary-adrenal (HPA) axis activity and arousal. Especially, this may be true in
the earlier stages of depression before the HPA-axis loses its regulatory input, or
in the partially recovered or remitted patient who might otherwise relapse in
response to stress.
How specifically might particular psychological interventions normalize the
IDS? Interpersonal therapy could enhance the effectiveness of the IDS through
several mechanisms, including augmenting affiliative relationships, acceptance
of new roles, and promotion of normal grieving. Cognitive therapy might work
by eliminating negative cognitions that inappropriately exaggerate defeat behav-
ior and/or by promoting greater acceptance in response to perceived failures.
Each of the varied approaches promotes effective functioning of the IDS by
aiding de-escalation when the conflict is clearly lost. This may explain the com-
mon therapeutic effects of otherwise distinct treatments for depression.
Involuntary Defeat Strategy and Depression 131

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 8
T H E E V O L V E D B A S I S OF M O O D A N D
THOUGHT DISORDERS-.
NEUROETHOLOGIC, G A M E
MATHEMATIC, A N D EVOLUTIONARY
EPIDEMIOLOGIC A N A L Y S E S

Daniel R. Wilson
INTRODUCTION

MacLean (1949, 1985, 1990), elaborating on the earlier ideas of Flourens

(1824), Broca (1878), and Papez (1937), has given us the classic account of
reptilian behavior. In The Triune Brain in Evolution, somber reptilian ritualized
antagonistic behavior and resource holding algorithms are noted to yet reside
amid more cozy mammalian complexes such as thermoregulation, motherhood,
parentalism, pair bonding, kin selection, play, and eusocial affiliation (MacLean
1985, 1990). Vertebrate brains have an analogue of self-esteem, with neuro-
mentalities raised or lowered by signals from conspecifics (Eibl-Eibesfeldt
1975). Such signals entail reliance on an apparatus that is phylogenetically quite
old and deeply rooted in those genomic elements that organize behavior. While
this apparatus has greatly elaborated in subsequent mammalian and primate
evolution (Bucy & Kluver 1955), changes have often come to overlay but not
wholly replace earlier features (Spencer 1855; Hughlings Jackson 1881; Brown
& Schafer 1888; Sherrington 1906; Kluver & Bucy 1937; Pribram 1958; Brady
1958; Harlow 1965).
Hence, conceptualizations of human neuromental phenomena must account
not only for reptilian origins but also ongoing retentions. Retentions were
modified in the course of integration with newer primatomammalian neuro-
mentalities (e.g., the later limbic, cortical, neo-cortical tissues, and related
neuroendocrine innovations). However, phylogenetically old adaptations can be
operationally released in certain, often pathological, circumstances, as when
functional tensions arise between R-complex and upper cortical operations—
usefully termed phylogenetic regression (Bailey 1987)—to induce pathopheno-
typies such as mania, depression, and thought disorder. It is, however, especially
134 The Evolutionary Neuroethology of Paul MacLean

revealing to explore the convergence of MacLean's concepts with another potent

model in behavioral evolution: game theoretic Darwinism. Here competition
stratifies populations in terms of reproductive fitness in each generation within
each species. Game theory models two alternatives in social competition:
escalation, Hawk, or de-escalation; Dove evolutionary stabilized strategies; or
"ESS" (Maynard Smith 1982). Variations on these strategies appear to be part of
what defines either an entire species genome or a polymorphism therein (Krebs
& Davies 1981). The Hawk-Dove ESS exemplifies deeply canalized, successive
and genetically polymorphic triune neuromentalities entirely compatible with
both the basic and clinical science germane to manic-depression (Price 1998).
This chapter attempts to reconcile mania and depression with triunian neuro-
ethological research in support of the larger project of evolutionary medicine.
This is done via a brief review of both mania and depression and the triune brain
with respect to (1) relevant historical considerations, (2) evolutionary epidemi-
ology, and (3) consilience with game theoretic models. A basic familiarity with
triune brain concepts is assumed and redundancies are avoided with material
detailed in other chapters.

HISTORICAL OVERVIEW

The triune concept of brain, though now principally associated with the work
of Paul MacLean, is actually quite a staple of medical history. The Smith Papy-
rus, ca 1750 BCE, is the earliest extant written reference to "brain" (Garrison
1929). However, despite their otherwise advanced attention to matters of body
and mind, even as the body itself was ritualistically embalmed for mummifi-
cation and all other major organs were venerated in cenoptic jars, the Egyptians
paid so little regard to the neuromental substance that it was routinely disgorged
from the brain case and discarded. The Egyptian civilization, which was advan-
ced in so many aspects, did not contribute much to neuroscience theory or
practice.
Nevertheless, the Greeks as early as Plato established sophisticated con-
cepts of brain science (although Aristotle held to the less accurate belief that the
heart was the seat of the soul). This Platonic neuroscience is noteworthy in many
respects, not the least by its close resemblance to MacLean's tripartite arrange-
ment. The "Epithimetikon" constituted the basic appetitive level over which
operated the "Thintoeides" apparatus of affect and the "Logistikon" a more
rarefied level of rationality. These clearly correspond to basal midbrain, limbic
and cerebral components identified in contemporary neurology.
Thereafter, Galen of Pergamum, among his many accomplishments, likewise
propounded a triunian concept of neuromentality. Not only was he prescient in
fixing "the seat of the soul" in the frontal lobes, he further noted this lay above
mere vegetative and animal levels of the brain. St. Augustine of Hippo, too, had
a tripartite system. This took shape in his masterful weaving of Neo-Platonism
into the fabric of Christianity. His works such as Confessiones or De civitate
Dei, and especially De Trinitate, constructed a triunian foundation upon which
Disorders: Evolutionary Epidemiologic Analyses 135

much of the apparatus of Western culture was subsequently raised. Thus, via the
extended vitality of Galenic ideas in medicine and Augustinian ideas in theo-
logy, triunian concepts secured primacy for well more than a millennium of
early neuroscience.
Hence, any triune conceptual system has considerable resonance with
essential characteristics of Western culture as well as subtle but inescapably
religious overtones. Other examples abound. More recently, Freud put forth a
highly influential triune schema with id, ego, and superego having obvious
correlates in MacLean's neuroethological discoveries (MacLean 1990).
So, old though it is, the triune model entered the 20th century with remark-
able vigor and soon came to explicitly influence contemporary neuroscience.
But other crucial discoveries accrued between the waning days of medieval
scholasticism and the extraordinary efflorescence of neuroscience in the late
20th century. These can concisely be recapped with reference to a series of
classic events that relate intimately to the theme of this chapter and this book
overall.
In 1664, Thomas Willis published the first meaningful dissection and
assessment of the functional anatomy of distinct subcortical structures including
the basal ganglia, or corpus striatum (Parent 1986). Its central position and wide
range of vivid cortical and brain stem tracts led Willis to believe it was perhaps
the "sensorium communale" of Aristotle, a structure which was at the time
thought to originate all motor efferents and receive all sensory afferents.
However, neurology soon turned its attentions toward exciting histological
studies of the cortex, and efforts to localize higher mental functions as cortical
research reigned in the 18th and 19th centuries. A few scholars sustained
research on the basal ganglia and discovered that functions long ascribed to it
were actually properties of adjacent corticospinal paths and, so, the striatum
"seemed to fall from its high estate and depreciate in physiological significance"
(Wilson 1914: 428). Yet experimental research pertaining to the striatum
advanced rapidly via lesion-induced disorders of motor functions (Wilson 1914;
Cajal 1928).
The corpus striatum re-emerged as a major element of the "extrapyramidal
motor system," which grouped it with brain stem nuclei as a complete and
independent motor unit (Carpenter 1981; Parent 1986). The term "basal ganglia"
generally refers to these major anatomical telencephalic subcortical nuclei at the
base of the forebrain, formally the corpus striatum (striatum and globus palli-
dus), with the substantia nigra and subthalamic nucleus. This work, both in
methods and findings, was of a piece with the subsequent experiments of neuro-
ethologists in general, and MacLean in particular.
Meanwhile, in 1878, Broca published his crucial hypothesis concerning "le
grande lobe linibique" which helped to begin to break loose a variety of popular
quasi- and pseudoscientific formulations (The author, who once taught medicine
and anthropology at the University of Cincinnati, is especially appreciative of
the "System of Medical Anthropology," which his predecessor, Professor
Buchanan, taught at the university in 1847 as something of a phrenology of the
body whole; as it happens, "the region of moral insanity" is depicted from the
136 The Evolutionary Neuroethology of Paul MacLean

mid-thigh to the navel of a Rubenesque lady). As for Professor Broca, his great
achievements and their connections with 20th century neuroethology are
detailed elsewhere in this and other volumes. Here it is necessary only to note
how Broca also was of a piece with the neuroethology soon to follow.
In 1921, the German-born American physiologist Otto Loewi identified the
vagusstoffi which is to say the first neurotransmitter has been known for less
than a century. From this, a plethora in structure and function of types, subtypes
and variations upon neurotransmitters continue to be identified as neuroethology
was greatly enriched by continuing research. Then in 1937, Papez extended
Broca's hypothesis toward a more complete description of the mechanisms of
emotion that MacLean subsequently elaborated in remarkable detail.
This brief sketch of the general historical context in which triunian neuro-
ethology arose is further enriched by diverse, yet keenly relevant parallel
findings, as from evolutionary neurobiology, neurotransmitter research, and
game mathematics. These findings are discussed next as prelude to a preli-
minary effort to delineate how such compatible findings from diverse fields
form a coherent picture of the Darwinian origins of mental and brain patho-
phenotypies, emphasizing manic-depression as an example. Therefore, we turn
to a brief review of neuromental evolution before examining all this in connec-
tion to disorders of mood and thought processes as typified in and by mania and
depression.

NEUROMENTAL PHYLOGENY AND ONTOGENY:

A BILLION YEARS AND BILLIONS OF BRAINS IN BRIEF

Though neurons are distinct from general somatic cells, the pattern of their
evolutionary derivation from less specialized cells is obvious. Essentially, in the
course of physiologic operations living cells inevitably induce micro-electrical
potentials across the membrane. This sets the stage in which phylogenetic
refinements of transmembrane conduction evolved from depolarization pheno-
mena. Disturbance of primitive cell membranes alters electrical potentials only
locally. Yet, rather basic refinements in the spatial and chemical aspects of cells
gave rise to processes of propagative depolarization that, coupled with synapsi-
tic complexes, provide the principal means of interneuronal communication.
From such beginnings developed dispersed neural systems, as is evident in
Medusa (jellyfish). Here there is coordinated neural action to maintain the
swimming sweep but nothing anatomically identifiable as a nervous system in a
centralized sense. The helminths are the earliest taxa with an overt central neural
apparatus. That is, worms have a brain from and to which a neural cord entrains
the rest of the soma. This arrangement is highly canalated in the HOX
(homeobox) gene cluster with imago anatomical referents in all subsequent
species (Vernier et al. 1995). Still, though a central brain of sorts is evident in
helminths, much somatic intellect is retained at this phylogenetic level; decapi-
tated worms can breed, feed, dig, locomote, and inure to mazes.
Disorders: Evolutionary Epidemiologic Analyses 137

With insects comes a more advanced neural apparatus by which a compart-

mentalized brain coordinates end-organ activity via giant fiber tracts, i.e., as in
rapid nerve conduction of motor efferents for wing muscle movement. Insect
brain has three differentiated assemblages—protocerebrum, deutocerebrum, and
tritocerebrum. Moreover, insects have a larger sensory organ domain than any
other taxonomic level including vertebrates (odors, sound, luminescence texture,
pressure, humidity, temperature and chemognosis). The concentration of these
complex sense organs in the capitum of insects is yet another layer of bio-
engineering efficiency as the depolarization circuits are all the shorter and more
alacritous. These features together account for the uncanny "intellect" all too
often on display by insect neural apparatus which is, no doubt, intimately related
to their status as the most numerous of Earthly multicellulates.
Yet vertebrates further refine the neural assemblage with a calcific armor
through which ascending and descending tracts govern more advanced activities.
With vertebrates, the central nervous system emerged as a series of three
anterior spinal cord enlargements constituting the hindbrain, midbrain and fore-
brain (analogous to the insectival anatomy and mediated via HOX genes). Late
reptiles and early mammals retained the basic vertebrate structure but further
accreted at the forebrain a paleocortical "limbic system" and then a range of
domain-specific neocortical centers as well. The efflorescence, plasticity and
self-awareness of these later structures are especially remarkable among social
mammals, notably primates.
Thus, the brain evolved in a series of three assemblages above the merely
vegetative level, quite in keeping with MacLean's synthesis (1990). At the
outset, from a most primitive dispersed neural network was centralized an
amalgamated hierarchy of brain upon neural tube, all of which was later encased
in vertebrate osseous tissue. In this growth, this brain set down neuromental
substrates for the ritualized antagonistic behavior of classic reptiles at what is
now termed the midbrain or basal ganglia. Thereafter followed greater encephal-
ization with progressively increased neuronal and synaptic density, plasticity,
and diversity in the forebrain areas. This enhancement of the range of neural
operations fostered brain and behavioral self-regulation of experience by which
novel perceptuomotor abilities, memory, and learning emerged.
An overarching theme of neuromental phylogeny is the accretion of
successively higher and more pluralistic mechanisms for executive action built
upon complex integration. Thus behavior is the business of channeling percep-
tions in relation to environmental cues. Moreover, while such cues are directed
to a wide spectrum of complex proximal biosocial ends, these are ultimately
engaged in the maximization of reproductive success. Such success is contingent
upon both acute and sustained realization—via neuromental representation and
summated behavior—of environmental referents. In the most reduced sense, and
apart from predator avoidance, such realizations must negotiate access to
nutritional and fertility needs. Even bacteria "sense" environmental realities as
with chemotaxis. However, among advanced mammals, as the biosocial
environment became more complex so too did the neuromental means by which
this complexity was represented, analyzed, and behaviorally engaged.
138 The Evolutionary Neuroethology of Paul MacLean

Such a phylogenetic perspective perhaps presumes a rather determined

neuromentalistic apparatus. However, selectionistic explanations only carry the
phenotype so far, particularly with respect to complex behavior. It is certainly
true that things are often quite tightly "wired up" (Gilbert 1989).
But it is already well established that the complexities of advanced nervous
systems exceed the semiotic encoding capacities of their associated genomes.
The human neocortex has some one thousand million million synapses while the
9
total human genome has only 3.5 billion (3.5 x 10 ) nucleotide base pairs. Thus,
the genome lacks capacity by which the details of neural connectivity could be
wholly encoded via genetic specificity.
Hence, normative neural development is contingent upon phenotypic adjust-
ments between the genomic heritage and individual experience. Quite remark-
ably, much of this phenotypic adjustment appears to be mediated by de-selection
of neurons within individual development. Ongoing, severe synaptic pruning
rapidly follows the fetal blossoming of neurons via phenotypic experience
(Charney et al. 1999). More precisely, much of this pruning is expectant reaction
to experience as is evident in autopsy sampling:

Increased synaptic density plus expansion of total cortical volume leave no doubt the
postnatal period is one of very rapid synaptogenesis in human frontal cortex. By age 2
years, synaptic density is at its maximum; at about the same time when other components
of cerebral cortex also cease growing and when total brain weight approaches that of the
adult. Synaptic density declines subsequently, reaching an adult value that is only about
6 0 % of the maximum (Huttenlocher 1990).

This accounts for much of the plasticity of behavioral phenotypes in higher

social animals. Normal neuromental development is governed by selective loss
of synaptic connectivity. Thus, it not surprising that the adult brain is subject to
increased (though not complete) constraints on learning and behavior as well as
"cortical blindness" in the wake of insufficient expectant-experiential cues from
the environment of ontogeny of which visual acuity is perhaps the best known
example. Consequently, the brains of advanced social animals are the product
not just of elaborate basic plans (as with the HOX genes). Rather, these robust
templates are modified by developmental experience. Moreover, as one moves
along the phylogenetic line, the degree to which phenotypy is simultaneously
organized by template AND environment increases.

EVOLUTIONARY EPIDEMIOLOGY OF NEUROTRANSMISSION

Neurotransmitter biology has advanced rapidly in the past generation. Yet, it

is impossible to discuss the evolution of neurotransmission in detail. After all,
this encompasses 1,000 million years of phylogeny. Moreover, in the human
brain this entails 1,000 million neurons. Each neuron may engage up to 10,000
synapses each, or in excess of 10 trillion per brain. Likewise, to catalog the
dozens of neurotransmitter systems, their molecular biology and functional
Disorders: Evolutionary Epidemiologic Analyses 139

biochemical neuroanatomy would, in itself be a Herculean effort requiring

volume upon volume. Thus, our scope at this juncture is to relate key aspects of
human neurotransmitter evolution with triune neuroethology and thereby expand
Price's (1996) game mathematic model of manic-depression.
Though the extraordinarily ancient nature of the major classes of neurotrans-
mitters has been established, neuroscience has thus far done little to consider the
implications of such ancient origins. Likewise, the degree to which the nervous
system has evolved via gene duplication or "autologous cloning" is remarkable
(Wilson 1993). But so too are woefully overlooked the implications of this
crucial mode of polymorphic diversification in the course of neurotransmitter
evolution. That is to say, for a given neurotransmitter there exist a variety of
types and subtypes of receptors originated within truly ancient multigenic
families. These families derive from terminal modifications of genes duplicated
in phylogeny. Such modifications render advantageous otherwise merely neutral
redundancies (Vernier et al. 1995). Thus a brief recap of the venerable origins
and unusual mechanisms in the phylogeny of neurotransmission is worthwhile in
itself but, further, introduces a new avenue for neurethological and evolution-ary
psychological research.
The biogenic amines are indeed old and have preserved basic functions as
intracellular signals even as they acquired later capacities for intercellular com-
munication and hormonal action. They are found in many protozoans and nearly
all metazoans. The cognate enzyme, monoamine oxidase, is found even in
prokaryotes. Moreover, the biogenic amines have a conserved secondary struc-
ture but diverged in the course of the evolution of complex neural systems.
Hence a phylogenetic hierarchy of multiple G-protein linked catecholamine
receptor subtypes accrued largely via gene duplication and subsequent modifi-
cation.
Gamma Amino Butyric Acid (GABA), identified in all flatworms, is some
1,000 million years old. One of the first events was the evocation of cate-
cholamine receptors from primordial muscarinic acetylcholine receptors. This
occurred prior to the divergence of arthropod and chordate lineages. The first to
so arise was likely a form of dopamine as it is found in all chordates. Thus, the
earliest catechols are common to vertebrates and appeared at least late in the
classic era of the cephalochordates some 700 million years ago.
Thereafter, second-messenger pathways arose homologously in both muscar-
inic and catecholamine receptor populations. This occurred after the chordate-
arthropod split but before the separation of avians and mammalians from the
common reptilian line, as norepinephrine is common to all vertebrates.
Moreover, adrenergic and dopaminergic second-messenger pathways did not
arise independently. Rather, the original receptor population was repeatedly
duplicated and modified in subsequent evolution to organize epinephrine,
norepinephrine, dopamine, and octopamine receptor systems (Fryxell 1995).
Serotonin which may have originated in chordate gut tissue is well developed
in cyclostome (lamprey) brain tissue and other primitive vertebrates. The sculpt-
ing of fetal neural development was among its first functions. Thus serotonin
arose at the chordate-vertebrate interface (Peroutka & Howell 1994).
140 The Evolutionary Neuroethology of Paul MacLean

Manifestly, these neural systems were recruited to modulate increasing

information-processing demands, psychomotor activity, attentional systems and
emotional drives. There is consensus on the early origin of prototypical neuro-
transmitter classes but only a dawning realization that the subsequent evolution-
ary diversification of these moieties—via autologous cloning and modification
of redundant gene templates—follows a hierarchical pattern. Moreover, this
hierarchy is quite compatible with MacLean's triune brain schematic in that
subcortical neurotransmission varieties are quite modal across species, whereas
far more phyletic divergence is noted in comparisons of limbic microanatomy
and remarkably more when diverse species' cortical tissues are contrasted.
Indeed, most tantalizing for neuroethology may be evidence of spectacular
evolutionary refinement of receptor subtypes in the past 100 million years of
evolution in the primate line (Peroutka & Howell, 1994). With this it is useful to
consider serotonin and dopamine in more detail.
Dopamine and serotonin long have been of special relevance to mood
disorders, but novel molecular analytic techniques have been needed to more
fully appreciate the physiological and genetic complexity of these neurotrans-
mitter systems (Owens & Risch 1995). Generally, they have reciprocal physio-
logical effects: Dopamine is an essentially stimulating neurotransmitter and
serotonin being inhibitory. This is evident in pharmacological experimentation:
Compounds active in serotonin circuits have antidepressant effects whereas
dopamine agonists serve as antipsychotic (antimanic) agents. Finally, and of
particular interest to neuroethology, serotonin and dopamine subsystems have
quite clearly coevolved in the course of mammaloprimatoid brain and social
evolution.
Dopamine was long thought to exist in only two types. More recently at least
five variant loci have been identified, some with considerable point polymor-
phism (Owens & Risch 1995). A similarly more complex picture has been
obtained with respect to serotonin (Hen 1993). There are even more detailed
racemes in each of these neurotransmitter families, both of which can be further
grouped into at least two clusters of similar function and distribution.
With respect to dopamine, five receptors have sprouted in the respective
1 2
lineages of either the original D or D typology. These aggregations reflect
similarities in anatomy, physiology, and evolution. In the present discussion, the
2 2 3 4
D cluster is of special interest. Its D , D , D subtypes appeared in later
phylogeny in clear response to requirements for more subtle facilitation of
higher level cognitive-affective expressions evolved in response to mammalian
evolutionary pressures. Notably among these pressures was the need to mediate
l
conspecific social interactions. The D cluster arose in the face of more primitive
selective pressures that shaped classical reptilian neuromental assemblages now
deeply canalized in evolution. The D cluster is therefore manifestly more primi-
tive as it subserves both extrapyramidal tract and midbrain functional demands.
Neuronal receptor networks in brain are identified by the distribution unique,
protein-typical mRNA (Chio et al. 1990). Assays of mRNA bear out differen-
2
tial distribution across the subtypes. For example, densities of the D cluster
localize to the hypothalamic, limbic, and frontocortical areas far more discrimi-
Disorders: Evolutionary Epidemiologic Analyses 141

1
nately than do those of the D cluster. Such differential distribution explains the
relative efficacy and limited toxicity of antipsychotic drugs that operate on
2
mammaloid D —opposed to more primitive reptilo-vertebrate circuits (Owens
& Risch 1995).
These very distinctive anatomical and functional dopamine receptor subtypes
indubitably derive from a phylogenetically common ancestral form. Each
subtypic modification of the template branched off as an innovative resolution
of specific selective pressures extant at different times in the environment of
phylogenetic adaptation (MacLean 1990). In mammaloprimatoid brain, such
innovations were necessary to modulate social behavior in increasingly sophisti-
cated ways.
Again, the complexity of serotonin is akin to that of dopamine (Owens &
Risch 1995). However, serotonin is even more widely distributed in the brain
(and thus may have less specific subdistribution than dopamine). Serotonin
clusters within four types with a total of more than a dozen subtypes. As it
happens, the rapid pace of discoveries in serotonergic microneuronanatomy
makes a detailed account of current knowledge not only difficult but all too
ephemeral and is, in any event, well beyond the range of present discussion.
Crucially, assays of serotonin receptor mRNA densities vary considerably
across brain regions but, taken together, these assays indicate serotonin
mediation of widely diverse cognitive and behavioral activities; notably, the
projections of the dorsal raphe-striatum. These are phylogenetically earlier
features largely fixed in the course of reptilian brain evolution in a mode similar
1
to D . The serotonin projections of medial raphe-hippocampal system originated
later in evolution and address different phylogenetic demands. Given such
robust microanatomical and functional links to limbic structures and functions,
these later serotonin innovations modulate affective-cognitive demands unique
to mammalian social evolution (MacLean 1990).
In aggregate, these rapidly accruing researches concerning neurotransmitter
subtypology call for a revised dopamine hypothesis in which normal thought
and mood are contingent upon orchestrated actions of diverse modulators—
perhaps especially dopamine and serotonin—as well as other quasi-transmitter
agents such as neurohormones and endogenous opioids. As for the classic
neurotransmitters, dopamine and serotonin appear to mediate normative moods
and thoughts whereas derangements in dopamine/serotonergic physiology
induce disease such as psychosis, abulia, mood and extrapyramidal effects.
Psychotic and mood symptoms arise when prefrontal cortex and/or meso-
limbic systems are significantly altered with respect to dopaminergic and/or
serotonergic function (Janssen et al. 1988; Davis et al. 1991; Meltzer 1992).
Serotonin depletion typically aggravates symptoms via initial escalation of
mood and activity, soon followed by irritability and thought disorder. Such
irritability is frequently accentuated by reduction of serotonergic circuits,
particularly when these are also affected by sleep deprivation (Keck, pc 1997).
Moreover, compounds with high (S i /D ) ratios of raphe-hippocampal-limbic
rh 2

circuit serotonin (S i) to dopamine of the limbic type (D ) may be especially

rh 2
142 The Evolutionary Neuroethology of Paul MacLean

efficacious in the treatment of psychotic and mood disorders, including severe

manic-depression (Meltzer 1992).
Serotonin inhibits dopamine striatal efferents while serotonin re-uptake
inhibitors rouse mood but inhibits dopaminergic limbic structures, notably the
nucleus accumbens, and can induce extrapyramidal effects. Moreover, lesions of
serotonergic dorsal raphe tracts reduce neuroleptic-induced catalepsy. Serotonin
effects on dopamine are modulated by receptors of the 1 , 2 and 3 serotonin
A

subtypes. The highly unique profile of clozapine microphysiology, both in vitro

and in vivo, is revealing in that it has increased affinity for limbic D receptors
4

and antagonizes 5-HT moieties. These moieties elicit dopamine release "down-
2

stream" in the striatum and, so, limit extrapyramidal symptoms induced by

dopamine antagonists elsewhere in the brain.
Hence, abnormalities of thought and mood (the largely mammalian capaci-
ties of positive and negative symptoms) can be ameliorated without significant
effect of lower reptilian circuits evident in involuntary motor symptoms. Thus,
novel antipsychotics such as risperidone improve both psychotic disorders of
thought and derangements of mood with few motor effects as an effect of 5-HT 2

antagonism in tandem with D (Janssen et al. 1988).

4

A significant calculus of social rank hierarchy and particulars of serotonin-

dopamine neurotransmission functions as an expression of these neuro-
modulators. Moreover, such a calculus is further embedded in algorithms of
animal behavioral escalation and de-escalation (Gawin & Ellenwood 1988;
Wyatt et al. 1988; Kosten 1993). For example, cocaine is mimetic of both manic
and depressive symptoms: Acute administration increases synaptic dopamine—
via the inhibition of pre-synaptic dopamine re-uptake—which escalates mood
and activity. Yet chronic overstimulation of D receptors eventually induces
2

down-regulated physical dependence. Likewise, abrupt cessation of cocaine

depletes dopamine and induces acute agitated depression but a chronic
syndrome of anhedonia, dysphoria, lethargy, somnolence, and apathy can extend
for up to a year.
Serotonergics reduce both pre-dependent appetites for dopaminergics and
dopamimetics as well as the post-dependent withdrawal syndromes. Dopamin-
ergics similarly affect modal activity in serotonin circuits. Thus, patterns of
dopamine physiology in humans constitute a model of manic-depressive neuro-
mentation (a discussion to be taken up anew in the context of hawk-dove
escalation/de-escalation-evolved stable strategies).

THE SOCIAL COMPETITION HYPOTHESIS

In the new field of evolutionary psychiatry there have been developments

that parallel the triumph of kinship genetics and neuroscientific progress.
Among these parallel developments is the specification of the social competi-
tion hypothesis of mood disorders in which has been marshaled a great deal of
evidence concerning the evolved basis of moral and social behavior in humans
(Price etal. 1994).
Disorders: Evolutionary Epidemiologic Analyses 143

At this juncture it is useful to summarize the essential elements of the social

competition hypothesis before relating it to kinship genetics or neuroscience.
There is general agreement that mood disorders constitute some contemporary
phenotypic expression of a phylogenetically healthy behavioral repertory (Lewis
1934; Hill 1968; Beck 1987; Glantz & Pearce 1989; Gilbert 1992; Wilson
1993). Clearly, some variant phenotypes of current mood disorders performed
adaptive functions among ancestral hominids. Thus, beyond the constraints of
clinical theory and practice, the phylogenetic precursors of what are now
diagnosed as mood disorders can be better appreciated as having performed
some function in connection to social competition (Price 1967; Sloman 1976;
Gardner 1982; Gilbert 1992; Wilson 1993).
The essential result of social competition in any taxon is that winners behave
differently than losers (Price et al. 1994). Yet phylogeny appears to have
modulated competitive drives as a key step in the emergence of sociality.
Indeed, recent trends in studies of behavioral ecology posit that most social
mammals cooperate or compete in one of two basic social modes (Chance
1988). In clinical terms these two modes, the agonic and hedonic respectively,
relate closely to syndromes of depression and mania. Clinical depression is
readily identified in evolutionary psychological terms as a strategy of de-
escalation or loss while mania is a strategy of winning via engagement and
assertion (Price et al. 1994).
A further definition of the hypothesis is that humans retain, among other
possibilities, a phylogenetically structured capacity to yield (become depressed)
or assert (become expansive) in the face of socially competitive situations. A
logical—though not explicit—extension of the hypothesis is that severe or
persistent derangements of the sociophysiological mechanisms of rank hierarchy
may induce formal disorder of thought; that is, psychosis (arising perhaps parti-
cularly as mediated by stress hormones).
The hypothesis specifies social competition algorithms at several neuro-
mental levels, which link the etiology of mood disorders to pathologies of social
competition expressed in hierarchical fashion. The hierarchy subsumes sexual
selection, social stratification, ritual antogonistic behavior, resource-holding
potential, social attention-holding potential, among other domains. These are
skillfully detailed elsewhere (Gilbert 1992; Price et al. 1994).
In the most fundamental sense, mood disorders appear to have emerged (1)
in taxonomic terms at the reptilian-mammalian interface, (2) in neurobiological
terms at the subcortical-limbic interface, and (3) in psychological terms at the
egoic/superegoic interface.
Yet such interfaces are not, in themselves, the defining aspects of mammalo-
primatoid psychology. Instead, the attainment of social dominance via social
appeal and prestige rather than hierarchical threat has come to characterize
behavior in the hominoid line (Barkow 1989; Gilbert 1992). Put differently,
influence rather than raw intimidation is more commonly successful as a means
to social dominance among primates. This has been confirmed in both
ethological and socioanthropological field studies (Paglia 1994). Moreover, an
144 The Evolutionary Neuroethology of Paul MacLean

ethological consensus accrues however much a culturogenic-socioconstructivist

view has been favored by "academes" (Paglia 1994).
Nonetheless, sociocultural factors most certainly do shape phenotypic
expression of human mood states and disorders. In humans, social competition
may induce either yielding or assertion. Such yielding or assertion may cause
emotional dysregulation, especially where there is a crescendo of interpersonal
affects. Such escalations or de-escalations may have been quite salubrious in the
environment of evolutionary adaptation. However, any further dysregulations
may, in the context of contemporary culture, constitute syndromes of clinical
depression or mania. Consequently, the neurotransmitter genetics and physio-
logy of mood disorders are relevant in that these molecules subserve crucial
variations in the phenotypic expression of behavior.
Depression and mania, as is now more widely agreed, are diseases having a
fundamentally neurobiological and genetical foundation as population poly-
morphisms (Wilson 1998). It is, therefore, useful to attempt some connection
between the social competition hypothesis and recent trends in neuroscientific
research.

MANIC ESCALATION AND DEPRESSIVE DE-ESCALATION AS

HAWK-DOVE NEUROMENTAL STATES

In most mammals, reproductive success depends on success in various social

roles. One key role is in besting others who are pursing the same resources
(Barash 1977; Gilbert 1989; Krebs & Davies 1993; Trivers 1971).
As noted earlier, primate social hierarchy is a key factor in reproductive and
social success. Those higher up have more breeding opportunities and often
make more attractive allies than those lower down. Thus, navigating hierar-
chical relationships wherein some individuals are more powerful than others has
been a selective pressure for millions of years.
Social neuromentalities evolved in the context of conspecific behaviors of
either competition or cooperation. Further, these evolved neuromentalities propi-
tiate the adoption of predictable, context-dependent roles and behaviors that
modulate both competition and cooperation (Nesse 1990). In some respects,
social neuromentalities are synonymous with the everyday term "state of mind"
to the extent that each embodies algorithms of social roles. Gradations in states
of mind are to be expected between individuals across the social hierarchy. That
is, the state of mind of a dominant differs from those of hierarchical subordi-
nates. Being neuromentalities, these differences in state of mind have proved to
be measurable psychobiological variables. The consequences can be profound.
Most remarkably, in some fishes such inhibition can cause change of sex
(significantly, the subordinate's genes can thus be maintained by mating with
dominants; Keenleyside 1979). Likewise, dominant naked mole rats and New
World monkeys have been observed to directly suppress sexual reproductive
physiology in subordinates (Abbott et al. 1989). Studies have also documented
major biological distinctions between dominant and subordinate baboons,
Disorders: Evolutionary Epidemiologic Analyses 145

notably stress hormones which have been linked to the pathophysiology of

affective and anxiety disorders (Sapolsky 1989, 1990a,b; Ray & Sapolsky
1992). Biological profiles of subordinates differ from those of more dominant
animals in other species (Henry 1982; Henry & Stephens 1977).
Pharmacological probes are also revealing. Drug effects can vary between
dominant and subordinate animals, sometimes quite markedly. For example, the
social rank of rhesus monkeys given amphetamine determines key aspects of
response. Dominants showed increased threat, chase, and attack behaviors
whereas subordinates showed increased submissive behavior, for example, fear
grimaces and turning away (Harbour et al. 1981).
Harbour and Barters (1984) reported a case in which amphetamine was given
to a female rhesus monkey that moved between two groups. In the first group,
she was highly subordinate, isolate, and fearful with quite limited affiliation.
Amphetamine accentuated all of these submissive behavioral patterns quite
dramatically. However, when moved to a new group, the alpha male conspi-
cuously favored her. Her behavior changed markedly with this increased rank.
When administered amphetamine as the dominant female in this novel social
milieu her threats increased dramatically. She did not evidence submissive
behavior as previously, but instead increased her social approach.
Several empirical studies have confirmed that social competition psycho-
biologically modulates mood states in primates. A recent review of neuro-
endocrine correlates of social rank confirms that endocrine states are highly
sensitive to social feedback (Sapolsky 1993). Hormone levels in both dominant
and subordinate animals vary as a function of group stability. However, instabil-
ity of the social rank hierarchy affects individuals differently both with respect
to directional trends in rank (going up vs. down) as well as basic temperament
(Sapolsky 1994). In this sense dominance-subordination is largely controlled by
sociophysiological feedback in the environment.
Perhaps the most significant evidence to date is the correlation of the primate
social rank spectrum with serotonin parameters that mirror human mood swings.
Physiological changes can be both the cause and the consequence of rank
changes (Raleigh et al. 1984; Hartmann 1992). Blood levels of serotonin are
significantly higher in dominant male vervet monkeys as compared to their
subordinates (Raleigh et al. 1984).
Sham deposition of the alpha male was followed by a sharp fall in his
serotonin blood level but a sharp rise in that of the subordinate male who was
raised to dominant status. Restoration some weeks later of the formerly domi-
nant male was marked by a reversal of these serotonin findings as well as his
renewed tenure as the group alpha. Significantly, this restoration led to a fall in
both social rank and serotonin level of the new dominant below that of his
original beta baseline. Social ascendance with subsequent fall in rank produced
sociophysiological changes, which rendered the subordinate in a lessened bio-
social status than had no change occurred.
Sex hormones similarly reflect such social contexts. Androgen levels in
humans, both male and female, vary at baseline depending both upon the degree
of social competition or cooperation and also vary directly with success in
146 The Evolutionary Neuroethology of Paul MacLean

competitive games (Kemper 1990). These rises can include even nonphysical
contests such as chess (Mazure et al. 1992). Thus neurotransmitter and endo-
crine parameters not only reflect general features of social status, affect, and
mood but directly link to reproductive biology itself.
Major subtypes of neurotransmitter receptors, particularly dopamine and
serotonin, have unique anatomical distributions and functional consequences.
These consequences are quite germane to, among other concerns, the resolution
of stress engendered by social competition. This resolution is most often
accomplished via innovative capacities for cognitive-affective assessment and
behavior. These capacities successively typified the brains and psychology of
reptiles, then social mammals and, most distinctively primates (Dunbar 1988;
Mithen 1996).

EXPANDING THE SOCIAL COMPETITION HYPOTHESIS:

INTEGRATING NEUROTRANSMITTER BIOLOGY AND
HAWK-DOVE GAME MATHEMATICS

Thus we come full circle. The functional anatomy of neurotransmitters as

sketched here is intended to link, in a plausible but only preliminary manner, to
the pathological sociophysiology of manic-depressive neuromentality. Such
etiopathophysiology arises as triunian brain phylogenies encounter hierarchies
of current ontogenic demands. For example, manic-depression expresses an
enduring population polymorphism of the human genome increasingly mis-
matched in the contemporary environment as the human genome reacts to novel
situations far removed from archetypic modes of tribal life.
Indeed it is timely to consider beneficial aspects that both inhere to and help
explain this manic-depressive polymorphism. Major subtypes of dopamine and
serotonin neurotransmitter receptors each has anatomical distributions and
functional consequences quite germane to, among other concerns, the behavioral
resolution of social competition via innovative cognition and affective
assessment capacities that increasingly typified the brains and psychology of
social mammals.
With this in mind, it is useful to return to the social competition hypothesis
of mood disorders to begin integrating neurotransmitter evolution and game
mathematics within this model. In tabular form it is more readily apparent how
the Platonic hierarchy closely converges on MacLean's triarchic model and,
further, how such a system gives order to a wide range of evolutionary, neuro-
biological, game theoretical, neurotransmitter genetics and psychiatric nosology
(see Table 8.1).
Disorders: Evolutionary Epidemiologic Analyses 147

Table 8.1. Triune Hierarchies

EVOLUTIONARY NEUROMENTALITIES, GAME MATHEMATICS &

NEUROTRANSMISSION

r
" HAWK " DOVE"
NEOMAMMALIAN
r
'Logistikon

CORTEX SAHP* ATTRACTIVE AVOIDANT

Sociotropic-cognitive/ SAHP Optimistic, charming Pessimistic, ashamed
Cognition > affect Manic/sociopathy Depressed/ obsessed
S2 > SI ~ D 3 , 4 > D 1 S2, D 3 , 4 & N E / / / ' g / 2 S2 Low D3,4 & NE?
*(social attention holding potential)

PALEOMAMMALIAN
y
'Thimoeides
51
LIMBIC RHP DOMINANT SUBMISSIVE
Acquisitive - emotive/ RHP Roused mood, Low mood
likely to win likely to lose
Affect > cognition Aggressive/sadistic Morbid/
Masochistic
SI > S 2 D 2 , 3 , 4 > D 1 +EPS Sl,D3,4&NE///g/z S1,D3,4&NE
*(resource holding potential) Low

REPTILIAN
'Epithimetikon"

MIDBRAIN RAB^ FIGHTING FLEEING

Territorial - instinctive/ RAB Strident, strong Cowering, weak
Instinct > affect > cognition Violent, solipsistic Fright, abulia
SI » S 2 « D 1 » D 2 , 3 , 4 Dl & NE High S? Dl & NE Low S?
N
RAB (ritualized antagonistic behavior)

SUMMARY

The neuromental advancements that characterize behavioral evolution, parti-

cularly as mediated among mammals by the limbic apparatus and neocortex,
have served to inhibit both the structures and functions of the underlying
reptilian residue. This evolution was spurred by inclusive fitness strategies
increasingly consequential to parallel growth of mammalian social capacities;
e.g., live birth, kindred bands.
Nevertheless, functional tensions can arise between the R-complex and the
operations mediated by upper neuromental strata. Typically, intellective capaci-
ties can modulate more primitive reptilian drives; however, the R-complex can
148 The Evolutionary Neuroethology of Paul MacLean

prevail either adaptively or, more often, maladaptively. The latter maladaptive
release of reptilian repertoires is usefully termed "phylogenetic regression"
(Bailey 1987).
A major inhibition on social dynamics which might otherwise tend toward
robustly Nietzschean "will to power" among individuals—kin or not—is the
mother-offspring unit itself. Many lower species, especially those of an reelect-
ed nature—depend on extravagant numbers of little cared-for offspring rather
than extravagant nurturance of few offspring; indeed, some parents, not recog-
nizing their young, cannibalize them (Pianka 1970).
However, this emphasis on quality of reproductive effort shifts toward
quality as species become more K-selected. These trends are utmost in eusocial
mammals such as the primates. As kinship becomes better recognized, inclusive
survival is promoted via more perspicacious nurturant investments such as
nursing, teaching, and so on. MacLean (1985) outlines the behavioral patterns
evolved in consequence to in the evolution of mother-offspring bonds. Caring
dependency fosters greater exploration of the environment as well as enhanced
play with peers, and so, social skills and insight are acquired.
Such skills art the cement of eusociality and are, in turn, subserved by the
magnificent efflorescence of neurotransmitter subtypologies whose evolutionary
origins and functions have been sketched here in a preliminary manner as a spur
to improved current and, especially future, understanding via novel programs of
synthetic research.

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 PART IV

THE SOCIAL BRAIN:

CLINICAL THEORY AND
APPLICATIONS-
AUTISM, FORENSICS, A N D
ATTENTION
 9

EMPATHY, AUTISM, AND THE

INTEGRATION OF THE TRIUNE BRAIN

James C. Harris

The brain provides foresight in planning for ourselves and others. There is also
evidence that it functions to help us gain insight into the feelings of others . . .
in the complex organization of the old and new structures, we have presumably
a neural ladder, a visionary ladder, for ascending from the most primitive
sexual feelings to the highest level of altruistic sentiments . . . If through
education, we could only apply what the brain already knows, the year 2000
might see the beginning of a truly golden age. (MacLean, P. D., 1968)

INTRODUCTION

Paul MacLean has long emphasized the importance of the integration of the
triune brain and spoken of our capacity to act altruistically toward others. He
brings to neuroscience and cognitive neuroscience an approach that is uniquely
an evolutionary perspective on the integration of the brain functions and beha-
vior as illustrated in this opening quotation.
I propose to focus on the evolution of sociability as the outcome of the
integration of the triune brain. In doing so I will review the contributions of
Adolph Meyer, Charles Darwin, Kropotkin and the Russian evolutionists,
Antonio Damasio, and Frans De Waal. I will discuss recent investigations in
autistic disorder to illustrate the impact of the failure of brain development on
socialization. In taking this theme I draw upon three of MacLean's key points:
(1) The integration of the brain results in empathetic responses. Vision is a
cold sense that must be linked to feeling to allow one to look with feeling; that
is, to have empathy. This linking emerges from the connections of the prefrontal
cortex with the limbic cingulate cortex (in MacLean's terms the parental cortex
and its connections). The prefrontal cortex is associated with the executive
functions of self-regulation, planning, anticipation, but also with emotion
regulation and potentially with empathetic and altruistic feelings.
156 The Evolutionary Neuroethology of Paul MacLean

(2) We should study the neurobiology of kindness. When interviewed in the

New York Times about the role of the amygdala in fearful responding and the
startle response, MacLean was quoted asking why are we not studying the
neurobiology of kindness and other prosocial emotions as well.
(3) We should demonstrate our knowledge of such integrated functioning
when dealing with others.

SELFISH GENES AND/OR EVOLUTIONARY CONTINUITY

I begin with the proposal that the evolutionary process proceeds toward
greater sociability and that brain integration is aided by mutual interpersonal
support. Still there are competing viewpoints about the value of studying the
brain to appreciate the origins of sociability. On the one hand, Richard Dawkins,
the author of The Selfish Gene (1976), writes "Be warned that if you wish, as I
do, to build a society in which individuals cooperate generously and unselfishly
toward the common good, you can expect little help from biological nature. Let
us try to teach generosity and altruism, because we are born selfish" (Dawkins
1981).
But Stephen Jay Gould counters with this statement: "Why should our nasti-
ness be the baggage of an apish past and our kindness uniquely human? Why
should we not seek continuity with other animals for our noble traits as well?"
De Waal (1996) provides evidence for the view expressed by Gould (1980,
1988). In his Good Natured: The Origins of Right and Wrong in Humans and
Other Animals, he provides the example of the Japanese macaque, Mozu, who at
age 18 had survived as a member of her troop and raised five offspring despite
having no hands and feet. From paleontology there are examples from the fossil
record of survival into adulthood of Neanderthal and other early humans
afflicted with dwarfism, paralysis of limbs, and inability to chew. The survival
of the handicapped who are a burden to the group may be the earliest example of
compassion in evolution. Although others have suggested that such evidence
may merely indicate tolerance, De Waal provides evidence from ecological
studies of macaques, chimpanzees, and bonobos where examples of animal
empathy and social intelligence have been observed. This includes observations
of responses to the distress of another, self-awareness, transmission of informa-
tion, and the manipulation of social relationships. He provides examples from
the primate literature of coalition formation where help from a friend is obtained
in a confrontation, of friendly reunions following aggressive encounters, and of
social support provided to the loser by others who were not involved.
Such interest in the evolutionary origins of culture are continuing as
discussed in the June 25, 1999 issue of Science. Two reviews, "Chimps in the
Wild Show Stirrings of Culture" (Vogel 1999) and "Are Our Primate Cousins
Conscious" provide summaries of recent research.
Consistent with the findings of De Waal, van Schaik and his colleagues
(Pennisi 1999), when comparing five chimpanzee field studies, noted that those
with the higher social tolerance (e.g., meat sharing, female-female grooming)
Empathy, Autism, and the Triune Brain 157

had the highest tool use. This suggests the importance of social tolerance in
development. The authors ask: Is there a rudimentary consciousness in chimpan-
zees, even the prerequisites for morality? We are a long way from chimpanzees
in evolutionary terms, but there were many evolutionary links to humans, with
selective forces acting from Australopithecus africanus (4.5 million years ago)
to Homo erectus (1.8 million years ago) to Cro-Magnon to Homo sapiens. The
capacity to overcome instinctive behavior is an evolutionary advance marked by
the emergence of increasing social intelligence. According to Kramer (1999)
and de Waal (1989) this may involve the ability to categorize social stimuli
(including vocal and nonvocal communication); recognize kin and non-kin;
understand dominance hierarchies; courtship and mating behavior; form
alliances; resolve conflicts; cooperate in predator vigilance and defense;
cooperate in foraging and hunting; engage in deception; and participate in social
learning.
The advances are associated with being aware of one's self and others' (and
knowing the difference), and understanding that others also have mental states, a
critical aspect of recent "theory of mind research." We have moved in our
understanding of animal behavior from David Premack's query, "Do chimps
have a theory of mind?" to Marc Hauser's "Wild Minds" and Frans de Waal's:
Good Natured: the Origins of Right and Wrong in Humans and other Animals.

HISTORICAL BACKGROUND

Charles Darwin, Kropotkin, and the Russian evolutionists offered theoretical

approaches to understanding brain evolution and behavior. Although Charles
Darwin spoke of both sociability and survival of the fittest, his followers,
notably Herbert Spencer, placed the emphasis on the survival of the fittest, a
position that became known as Social Darwinism. And Thomas Henry Huxley
in his Evolution and Ethics (1889) portrayed morality as the sword forged by
homo sapiens to slay the dragon of its animal past. He proposed combat with our
animal nature, apparently suggesting that morality is the antithesis of this nature.
This interpretation has led to evolutionary justifications for the naturalness of
aggressive behavior. Yet the complementarity of aggression and subsequent
social reunion is more commonly observed.
Dan Todes (1989), a historian in the Department of the History of Medicine
at Johns Hopkins reminds us of another school of evolutionary thought, that of
the Russian Evolutionists. In his book, Darwin without Malthus: The Struggle
for Existence in Russian Evolutionary Thought, he discusses Kropotkin and
other Russian evolutionists who emphasized mutual aid as the primary motive
force in evolution. In Kropotkin's classic book, Mutual Aid (1989), the reader is
reminded of the importance of psychosocial aspects of survival and the need for
group support.
Todes points out that Darwin described natural behavior in tropical settings
that were rich in resources, where organisms were packed tightly, wedgelike,
into every available space, where a small advantage could bring prosperity to
158 The Evolutionary Neuroethology of Paul MacLean

one form at the expense of another. Yet he reminds us that in Russia the natural
setting was a great, sparsely populated plain. "Where were Darwin's wedges in
this environment?" In Russia the populations were most obviously checked by
physical circumstances. These circumstances were often so severe that one
form's slight advantage over another could easily seem insignificant. He notes
that "a sudden blizzard or an intense drought might obliterate entire populations
of insects, birds, and cattle without regard for difference among them." Thus the
Russian evolutionists proposed "mutual aid" as the driving force in evolution
that allowed survival to continue. They pointed out that those species with the
most highly evolved brains have the greatest brain weight, show the greatest
social cooperation, and are the most sociable (Todes 1989). This view proposes
that brain evolution may be moving toward greater sociability. The work of de
Waal (1996) that was previously mentioned provides modern support for the
mutual aid hypothesis. De Waal points to the work of Trivers (1972) on the
evolution of reciprocal altruism and to the more controversial topic of group
selection for altruistic behavior (Wilson & Sober 1994).
Further support of the role of the brain in sociability and evidence for the
grounding of morality in neurobiology comes from case reports of changes in
human behavior following brain damage. The most famous case may be that of
Phineas Gage, a 25-year-old railroad foreman, whose brain damage was sus-
tained when a iron tamping rod was forced through his ventromedial frontal
cortex. Remarkably he survived with his elementary mental functions intact.
His speech was reported to be normal as was his memory, however, his person-
ality changed. Previously pleasant and reliable, he became irresponsible and lost
respect for social conventions. Damasio's Descarte's Error (1994) provides
other examples of similar antisocial personality change following brain tumors
and other damage to this brain region. Damasio continues with the theme of the
importance of the "body in the mind" in The Feeling of What Happens: Body
and Emotion in the Making of Consciousness (1999). Dolan (1999) follows up
on these findings in his "On the Neurology of Morals."

PAUL MACLEAN AND THE INTEGRATION OF THE TRIUNE BRAIN

The work of Paul MacLean has considered the brain's evolutionary under-
pinnings for social behavioral deficits and altruism. MacLean's work on the
integrated function of the triune brain is in keeping with the Russian evolution-
ists' emphasis in evolutionary theory. Such evolutionary steps toward sociabi-
lity have been investigated by MacLean in his studies of the effects of brain
lesions on behavior in lizards, rodents, and squirrel monkeys.
He discusses an increase in sociability and social responsiveness that
emerges with particular evolutionary advances in brain development as we move
up the evolutionary ladder from reptiles to primates. Most striking are those
evolutionary changes that lead to cooperation in family life. Indeed, based on
MacLean's work, it has been proposed that consciousness may have its rudimen-
tary beginnings with affective arousal directed toward the feeding of the young
Empathy, Autism, and the Triune Brain 159

(Harris 1998). Advances in sociability emerge as the mother develops the

capacity to attend to the infant's cry, nurse her infant, and provide a safe
environment for mastery play. Among primates chimpanzees display eye-to-eye
contact with the young and the capacity to grieve the loss of conspecifics. In
human evolution, not only grief, but also expressive gestures of comfort toward
the bereaved make their clearest appearance. Yet in some neurodevelopmental
disorders such as autism, there is a failure in the development of these basic
mechanism leading to sociability.
The steps in the establishment of social life linked to the separation cry,
maternal care, and play (MacLean 1985b) have received increased support in the
work of the ethologists, neuroethologists, psychologists, and psychiatrists.
Social support is being investigated through studies of attachment, hierarchies of
relationships, affective modulation, working models of relationships, and
response to novelty. The child development literature is beginning to trace the
emergence of mother-infant attunement and attachment, the physiology of the
separation response, and to address the biology of play. The role of the REM
sleep in adaptive responses that lead to psychological individuality has been
considered by Jouvet (1999).

THE CONTRIBUTIONS OF ADOLPH MEYER

An approach that emphasizes brain integration and adaptive behavior is

consistent with the proposal of Adolph Meyer that we define mental health in
terms of disciplined spontaneously responsible acts. In 1933, he wrote that "one
hears frequent inquiries about distinguishing between what one is born with and
what one acquires during life and through living, a distinction between nature
and nurture . . . the far more accessible and far more important question is what
a person does when he is pushed to act . . . what one uses out of himself and on
his own." Meyer drew attention to disciplined spontaneously effective acts, in
contrast to unreflected impulsive ones, as indicative of mental health. He asked
what occurs before the "here and now," when we are confronted, that prepares
us to act. We occupy ourselves in psychiatry with the emergent person, with the
range of the individual's spontaneity. By spontaneity, Meyer meant to know
what can we expect of a person at any moment, and in the course of time to
understand his or her own response, and the initiative leading to that response,
when challenged to perform an integrated action. For Meyer what the person
may be expected to rise to, and rise with "sua sponte," in responding to others is
to be observed. For example, is a response adaptive and responsible or dictated
by a disturbance in mood such as depression or a deviation in thought such as a
delusion. He developed a classification of the "person in action" and used the
term ergasia (from the Greek ergazomai, to be active) rather than the term
conduct or behavior to describe the person in action. In his Maudsley lecture he
said he preferred to use this term "ergasia" to refer to the performance of a
person. In his classification of ergasias, for example, he used the designation
thymergasia (from thyrnos, mood) to describe a pattern of individual
160 The Evolutionary Neuroethology of Paul MacLean

performance influenced by affective state rather than the term we use today,
depressive disorder.
Meyer spoke of integrated mental functioning and MacLean uses the meta-
phor of the integration of the triune brain. Such formulations may be helpful in
monitoring the outcome of psychotherapy as the therapist looks for examples of
spontaneous acts of prosocial behavior as evidence of integrated functioning.
An integrated performance by the individual that is responsible and that is
ethically correct is a goal to work toward in psychotherapy. One literary
example of a disciplined spontaneous gesture is in Herman Hesse's The Glass
Bead Game, when Joseph Knecht, knowing the risk to his life, dives to save a
drowning child. Although he drowns himself in the act of saving the child's life,
his act of self-sacrifice has enduring effects on the behavior of others.
What are the evolutionary origins of responsible behavior and self-sacrifice
for the benefit of others? Is it, perhaps, based in parenting behavior? Did
parental behaviors evolve only to maintain the gene pool or do they also
provide, in acts of courage or in empathetic responses, models to establish a
culture of generosity? Meyer focused on a "disciplined spontaneity" as
indicative of integrated performance of the "person in action;" responsible,
effective, and adaptive.

PSYCHOTHERAPY

One issue that becomes apparent as we study brain evolution and behavior is
that evolutionary approaches can inform psychotherapy. A goal of psycho-
therapy is to reduce self-deception in relationships with others and, in so doing,
to become empathetic and demonstrate compassion towards others. This linking
of affect and cognition is basic to psychotherapy. Psychotherapy is an
interpersonally attuned approach to the person that deals with the minute
particularities of moments of therapeutic contact between therapist and patient.
Such an interpersonal encounter provides an opportunity for empathetic
understanding and, as a result, for changes in behavior. MacLean's emphasis on
epistemics, the study of subjective understanding, is particularly important for
psychotherapy where an understanding of one's own self-deception and the
recognition of deceptive behavior towards others is most pertinent. Indeed it
may be that the goal of psychotherapy is to realize, confront, and confirm the
effects of self-deception on oneself and others and to change one's subsequent
behavior. The metaphor of the integration of the triune brain may be considered
a basis for psychotherapy as the therapist looks for spontaneous acts of prosocial
behavior as outcome variables and as evidence of integrated functioning.
Empathy, Autism, and the Triune Brain 161

FAILURE OF INTEGRATED BRAIN FUNCTIONING IN AUTISTIC

DISORDER

If there is an evolutionary trend toward the integration of the triune brain,

what we can learn about this integration from the study of neurodevelopment in
those developmental disorders where there is abnormal brain development?
Autistic disorder is a neurodevelopmental disorder where hypotheses about
the failure of integrated functioning of the triune brain can be investigated. In
this disorder social understanding is lacking, particularly in regard to the
recognition of social deception and social betrayal by others. In autistic disorder
there is a lack of social referencing, a failure in affective attunement, and a
failure in the establishment of a sense of "We-ness," the subjective sense that we
are doing something together. Severely autistic children do not demonstrate
imaginative play that is reflective of an inner language. The failure of integrated
social functioning and the lack of appropriate use of social gestures is charac-
teristic of an autistic disorder. It leads the evolutionary oriented psychiatrist
(MacLean 1985) to consider how we can profitably study those brain
mechanisms in autistic disorder that might be involved in interpersonal relation-
ships, for example; the linkage of executive function with emotion regulation,
emotional memory consolidation, and mastery play in children and adults. Such
an approach may help to clarify and to develop a model for the integration of the
triune brain.
Paul MacLean has expressed concern about relying only on neuroimaging
techniques in our study of brain and behavior. Therefore, I will begin with the
autopsy reports of brains from autistic persons by Bauman and Kemper (1985,
1994, 1995; Kemper & Bauman 1993, 1998) before discussing the proper role of
neuroimaging studies. Abnormal development of particular brain regions may
result in failure in the development of social understanding and of empathy
reported in this disorder (Gillberg 1992; Bacon et al. 1998). As Sigmund (1998)
notes, there are stable deficits in joint attention, representational play, and
responsiveness to the emotions of others in autistic persons. To follow up on
neuroanatomical findings, neuroimaging studies may be used to document
dysfunction in vivo, and hopefully, also, to monitor therapeutic change over
time.

NEUROPATHOLOGY OF AUTISM

Kemper and Bauman (1998), in summarizing their neuroanatomic studies of

autism, report failure of the appropriate development of limbic structures (e.g.,
amygdala, hippocampus) and cerebellum. These authors have carried out
systematic surveys of the whole brain and completed serial sections of the brains
of nine autistic individuals and comparable controls. They found selective
abnormalities in the forebrain limbic system and the related inferior olivary
nucleus in the brain stem and evidence for a pathological process that extends
from the period of fetal development into adulthood.
162 The Evolutionary Neuroethology of Paul MacLean

In the study of the brains of autistic individuals, brain weight was measured
in 19 cases. An age difference was noted; 8 of 11 brains from persons younger
than 12 years of age showed a significant increase in brain weight compared to
the control group. However, 6 of 8 brains of those over age 18 had weights that
were lower than expected, although not statistically significantly reduced. In the
neocortex no abnormality in external configuration of the cortex was identified.
However, on microscopic examination, 8 of the 9 brains had unusually small
and more closely packed neurons and less distinct laminar architecture in the
anterior cingulate gyrus; in one brain there was a minor malformation in the
orbitofrontal cortex in one hemisphere. The remainder of the cerebral cortex
appeared unremarkable.
In the allocortex and subcortical forebrain area no abnormalities were found
in the striatum, pallidum, thalamus, hypothalamus, basal forebrain, bed nucleus
of the stria terminalis, or in myelination. In all 9 brains the forebrain abnor-
malities were confined to the limbic system. The neurons in the hippocampal
fields, CA 1-4, subiculum, entorhinal cortex, mammillary bodies, amygdala, and
medial septal nucleus were abnormally small and more densely distributed than
in age- and sex-matched controls. When Golgi methods were used to demon-
strate neuronal processes, the neurons in hippocampal CA 1 and CA 4 regions
showed reduced complexity and in the extent of their dendritic arbors.
In the amygdala, small neuronal size and increased cell packing density were
most pronounced in the cortical, medial and central nuclei, whereas the lateral
nuclei appeared to be comparable to controls in 8 of 9 brains. The significant
exception to this pattern was in a 12-year-old boy with normal intelligence and
significant behavioral problems. In this brain the entire amygdala was diffusely
abnormal. These findings are of considerable interest because the human
amygdala is required for accurate social judgments (Bechara et al. 1995;
Adolphs & Damasio 1998). Bilateral damage to the amygdala impairs proces-
sing fearful facial expressions (Adolphs & Damasio 1998).
Abnormalities in the cerebellum and brain stem included: (1) curtailment of
normal development of neurons in the forebrain limbic system; (2) apparent
congenital decrease in the number of Purkinje cells; and (3) age related changes
in cell size and number of neurons in the nucleus of the diagonal band of Broca,
in the cerebellar nuclei, and in the inferior olive. Kemper and Bauman (1998)
conclude that, although their report is descriptive, their neuropathological find-
ings are consistent with the origins of infantile autism being in the prenatal
development of the brain with ongoing pathological processes that persist into
adult life. They note that the best correlations with clinical features of autism are
the consistent findings in the limbic forebrain. The findings in the anterior
cingulate, hippocampus, subiculum, entorhinal cortex, and mammillary body are
aspects of an interrelated forebrain circuit that is linked to the septum and
amygdala. Experimental lesions in these areas have produced deficits in
memory, emotion, and other behaviors like those described in autistic persons.
These abnormalities in the development of the cingulate and limbic brain are
consistent with MacLean's lesions revealing effects on parenting and play when
these regions are lesioned in intact animals (Murphy, MacLean & Hamilton
Empathy, Autism, and the Triune Brain 163

1981). These findings are also consistent with the work of Murray and Mishkin
(1985), who reported that bilateral ablations of the amygdala result in severe
impairment in crossmodal associative memory in monkeys. These authors pro-
pose that the amygdala may be important for the integration and generalization
of modality-specific information by multiple sensory systems in the brain, a
problem that is a characteristic feature in autism. Malkova et al. (1997) found
that socioemotional deficits that followed bilateral ablation of the amydala and
hippocampus in neonatal monkeys increased with age and persisted into
adulthood; however, comparable lesions placed in adult monkeys resulted in
relatively mild behavioral deficits. Animal models such as these are consistent
with the neurodevelopmental deficit proposed in autism because there is
evidence that representational memory in humans is normally acquired after
birth. Therefore, it is possible that a developmental abnormality in the limbic
memory circuit may become clinically evident after birth, consistent with a
deterioration in social, language, and cognitive ability that is commonly reported
in the first two years of life in autism.

NEUROIMAGING

Neuroimaging studies may be utilized to evaluate brain structure and

functioning. Such studies may be used to confirm structural changes in the
brains of autistic persons that are based on a small number of autopsied cases.
Moreover, neuroimaging studies can test functional hypotheses based on
abnormalities in brain circuits based on the same anatomical evidence. Imaging
studies may also be used to evaluate theoretical models of autism. These
include, metarepresentational models (theory of mind), affective models (lack of
eye contact, abnormal response to danger, and abnormal response in fearful
situations), and intersubjectivity (integrating cortex and limbic brain).
Fletcher et al. (1995) carried out a functional imaging study to evaluate men-
talizing or "theory of mind" in normal subjects. Story comprehension was used
to identify brain regions involved in mentalizing (theory of mind), i.e. in the
understanding of the beliefs and desires of others and having the capacity to
attribute independent mental states to others in order to explain or predict their
behavior. This imaging study in normal volunteers assessed brain activity
through story comprehension tasks necessitating the attribution of mental states.
Brain activity was compared with that measured in two control physical tasks
that did not require mental attribution. One was unlinked sentences, the other
was a physical story that did not require mental attribution. Both story
conditions, when compared to unlinked sentences, showed significant increases
in regional blood flow in the temporal poles bilaterally, the left supratemporal
gyrus, and posterior cingulate cortex. Only the theory-of-mind story when
compared with the physical story produced activation in the medial frontal gyrus
on the left suggesting its selective activation in theory-of-mind tasks. Subse-
quently, Happe et al. (1996) used the same paradigm in a PET study involving
five patients with Asperger syndrome, a variant of autism, who had normal
164 The Evolutionary Neuroethology of Paul MacLean

intellectual functioning. As predicted no task related activity was found in the

left medial prefrontal cortex but activity was found in the immediately adjacent
areas again pointing to this region as involved in understanding a brain system
involved in understanding other minds. Gallagher et al. (2000) have demon-
strated that both the story task (verbal) and a cartoon task (nonverbal) showed
overlap in activating the medial prefrontal area. In a structural MRI study in 15
high-functioning individuals with autistic disorder, Abell et al. (1999) identified
grey-matter differences in an amygdala based system when compared to 15 age
matched and IQ matched control subjects. These findings of differences in
amygdala structure are consistent with the autopsy findings in autism regarding
the amygdala. These studies also have implications for the neural basis of
autism.
Future imaging studies in autism may focus on neuroimaging of amygdala
activation in response to emotional stimuli. Such studies have been conducted in
normal volunteers. Whalen et al. (1998) report that masked presentations of
emotional facial expression modulate amygdala activation without explicit
knowledge (i.e., in the absence of knowledge that such stimuli were being
presented). Morris, Ohman, and Dolan (1999) report a subcortical pathway to
the right amygdala mediating "unseen fear."
The treatment of autistic disorder requires an understanding of the autistic
nervous system and a recognition of the failure of integration of the triune brain
in this disorder. Because this is a neurodevelopmental disorder there is the
possibility of neurodevelopmental interventions to treat the behavior abnorma-
lity. Our goal in treatment is to facilitate better integrated brain function and
establish the normalization of autistic persons in society. Thus, the model of the
integration of the triune brain may serve not only as a metaphor in our future
treatments but lead to specific early interventions.

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 10

NEUROETHOLOGY, EXEMPLIFIED BY
LIMBIC SEIZURES WITH MOTIVELESS
HOMICIDE IN "LIMBIC PSYCHOTIC
TRIGGER REACTION"

Anneliese A. Pontius

INTRODUCTION

Paul MacLean's evolutionary hierarchical model of the organization of the

human brain has paved the way toward insights into otherwise unexplainable
clinical phenomena. His model provides a basis for conceptualizing sudden,
brief atavistically regressive acts during partial nonconvulsive seizures starting
in the evolutionarily old limbic system. Secondarily, such seizures appear to
upset briefly the normal fronto-limbic balance. Thus, the reciprocally related,
evolutionarily young frontal lobe system becomes transiently dysfunctional.
Over two decades of clinical forensic studies, MacLean's model enabled me to
propose a transient "Limbic Psychotic Trigger Reaction" (LPTR) consisting of
13 specifically interrelated symptoms and signs. These implicate the neurophy-
siological mechanism of limbic seizure kindling.
The symptomatology has been delineated in the following: atavistically
regressive acts accompanied by autonomic arousal and a brief de novo
psychosis. Such apparent behavioral seizures are associated with out-of-
character motiveless, unplanned acts of sudden onset and cessation, committed
with flat affect, typically against a stranger who happened to provide an
individualized stimulus that revived a memory of past intermittent mild to
moderate stresses (a setting characteristic of limbic seizure kindling). The symp-
tomatology reflects three seizure-related phases (aura, ictus, post-ictus) with
preserved consciousness and memory of the puzzling acts of homicide (17
cases), destruction by fire (3 cases), and primitive, acquisitional bank robbery (1
case). Eleven of the 21 cases of LPTR had a known history of closed head injury
and 14 had some positive finding on a brain test in their lifetimes. LPTR
remains to be ruled out by further research on nonfelonious similarly emotion-
less sudden acts.
168 The Evolutionary Neuroethology of Paul MacLean

HISTORICAL SURVEY OF THE LIMBIC SYSTEM CONCEPT

Great concepts do not suddenly emerge like Aphrodite out of foam but have
an evolving history. Thus, in 1952 Paul MacLean, who for the first time coined
the term "limbic system" (a central part of his "three brain" or "triune brain"
concept) belongs to a lineage of great creative researchers (Mega et al. 1997).
To trace the essential steps, this lineage started with Paul Broca's (1878) "grand
lobe limbique," which focused on olfactory processing. James Papez (1937)
combined anatomical findings with clinical reports of emotional disturbances
with lesions to the cingulate and other medial structures. He proposed a
mechanism of emotions, processed within a two-way circuit, known as the
"Papez circuit," leading to internal or external expression of emotion. Next, in
1948, Paul Yakovlev distinguished three phylogenetic functional zones of brain
development, as reflected by myelogenetic stages: These zones comprised the
oldest inner zone, the visceral system or entopallium; the middle zone or the
mesopallium which includes Broca's grand limbic lobe—as well as orbitofrontal
and insular cortex; and the most recently developed neocortical outer zone.
Yakovlev's conception stemmed from physiological and cytoarchitectonic
findings.
Finally, Paul MacLean's (1952) limbic system concept links Papez' medial
circuit with Yakovlev's basal lateral structures of the "middle zone." As pointed
out in a recent survey by Mega et al. (1997: 5), MacLean's concept of the limbic
system has survived—with refinement typical in science—as "consistent
anatomic-clinical correlations have been found."
Thus, recently investigators increasingly focus on a potential role of limbic
system structures in neuropsychiatric disorders, including schizophrenia (Arnold
1997); depression (Mayberg 1997): drug abuse and the reward system (Koob &
Nestler 1997). Further research addresses the spontaneously occurring auras of
partial seizures. Such auras are frequently analogous to experiential phenomena
elicited through electrical stimulation of limbic structures (Fried 1997a).
Herein such anatomico-physiological findings are supplemented by clinical
correlation that utilizes frequently neglected contributions of clinician scientists
(Geschwind 1984). As MacLean (1998: 274) warned: "the marvelous technique
of brain imaging has led to the wrongful impression that it will replace classical
methods," including patients' case histories. Further, Reich et al. report findings
on information coding suggesting that simple averaging of neuronal firing as
used in imaging techniques significantly underestimates the information-proces-
sing that is occurring.

HALLMARK OF CREATIVE CONCEPTUALIZING

Paul MacLean, one of those rare creative conceptualizers, has dared attemp-
ting an integration of results from animal experiments with uniquely human
insights and experiences. His background in the classics and in philosophy
greatly enhanced his integrative power.
Limbic Seizures with Motiveless Homicide 169

In this chapter, I shall exemplify the stimulating influence of Paul MacLean's

work in two respects: The content of his work influenced my proposed new
subtype of a partial seizure, "Limbic Psychotic Trigger Reaction" (LPTR)
(Pontius 1981-1999). Further, MacLean's integrative work over the years
employed not only the straight-line logico-deductive reasoning of the experi-
menter, but he also dared to use formal thought processes of "retroductive
reasoning" ("abduction") for the detection of new patterns (Hanson 1965; Hayek
1964; Pontius 1995).

Retroductive (Abductive) Reasoning

The process of pattern detection, largely based on retroductive reasoning, is

"not for the faint-hearted," as Kuhn (1971) emphasizes. Retroductive pattern
detection contrasts with statistics, which, according to Hayek (a nobelist in
economics), simplifies its task by "substituting a single attribute for the
unascertainable individual attributes in the collective." (Hayek 1964). Such a
statement achieves congruence with similar ones by Hanson (1965), a theoreti-
cal physicist at Yale.
In general, with regard to research into complex human behavior, much
initial research that addresses such complex, higher-order phenomena begins
with the detection of a consistent pattern of interrelations. Initially, a process of
pattern detection does not yet fit the orthodox criteria of "prediction and control"
(Hayek 1998), a phenomenon important to note.
Both Hayek (1964) and Hanson (1965), coming from different fields of
innovative research, point out that critiques of patterns of complex phenomena
with a broad scope, such as MacLean's triune (three-in-one) brain, tend to
overlook certain important points. Thus, initially the explanatory contribution of
a pattern merely delineates a consistent pattern of complex interrelations that do
not yet offer a statistical explanation. One indication of pattern validity is not
merely accidental but persistent occurrence, although such recurrence may not
necessarily include all its details.
Only after a pattern's detection can subsequent phases of research compare
and sort it out among related phenomena heuristically useful for later study. If a
pattern persistently forms, then it can become predictable despite initially
incomplete data: and despite the impossibility of predicting individual instances
or all the detailed circumstances under which the pattern recurs. In general
patterns of complex phenomena do not allow prediction of particular individual
events, as possible with simple phenomena. Recurrence of a pattern of complex
order, however, can be defined only within general circumstances, the
recurrence of which can be falsifiable, thereby permitting empirical prediction
(Hayek 1964).
As Hayek (1964) elaborated, great practical importance hinges on knowing
the conditions in which a specific pattern will appear and to know what depends
on its preservation. This is applicable to MacLean's concepts of the limbic
system and of the triune brain, essentially containing three phylogenetically
170 The Evolutionary Neuroethology of Paul MacLean

different parts.
A less abstract clinical application of such principles, guiding the detection
of complex patterns, led to the hypothesis of a new subtype of partial seizures,
"Limbic Psychotic Trigger Reaction" (LPTR). This presents a further elabo-
ration of MacLean's conceptualizations. LPTR has been consistently found in
repeatedly clinical observations of a specific class of partial seizures, in which
essential features of the triune brain concept become manifest, observable, and
potentially measurable. Of specific relevance in LPTR is the relationship
between the evolutionarily young prefrontal lobes and the old limbic system,
noted to be reciprocally interrelated (Nauta 1971; Weinberger 1984).
A final noteworthy point, on all levels of pattern detection from the most
abstract to the clinical, holds that a theory applies to a kind of classes or
situations that give data certain general properties (i.e., that the data belong to
the class defined by the scope of the variables). One need not know anything
about individual attributes of the data so long as we are satisfied to know merely
the sort of pattern that will appear; not its particular manifestation. Nonetheless,
pattern detection extends the range of theoretical knowledge, as has been the
case with MacLean's triune brain.

Difference between Pattern Detection and Statistics

Hayek (1964) further elaborates that pattern detection provides explanations

only of the principle and describes merely the general character of complex,
higher-level generalities. Thus, the study of complex pattern addresses relation-
ships (i.e., systematic connections among elements that are organized into
structures). By contrast, statistics deal with large numbers, essentially by
eliminating complexity. Statistics deal merely with a multiplicity of relations,
disregarding the relations among the individual elements with different
attributes, as if these elements had no systematic connections. Statistics assume
that information on the frequency of the individual elements of a collective
suffices for an explanation of the phenomena and of the elements of which they
consist. In general, Hayek considers it a futile, naive belief that statistics could
discover regularities without an appropriate theory. Further, all theories describe
only a range of possibilities. A correct interpretation of a theory excludes other
conceivable courses of events outside the range of the theory, and can thus be
falsified. In conclusion, Hayek (1964) cites Popper's succinct statement that a
theory's empirical content consists of what it forbids.

Clinical Contribution: A New Subtype of Partial Seizure Implicating a

Fronto-limbic Imbalance

Emphasizing the integration of basic research findings with reports on human

experience, MacLean has focused on the long studied partial seizures of
Temporal Lobe Epilepsy (TLE), which occur, however, typically with clouding
Limbic Seizures with Motiveless Homicide 171

of consciousness and amnesia.

Inspired by his work with its evolutionary focus, I proposed a new pattern of
symptoms and signs, a subtype of partial limbic seizures, called "Limbic
Psychotic Trigger Reaction" (LPTR) (Pontius 1981-2002). LPTR's value for the
study of experience rests on LPTR patients' ability to report their bizarre
experiences because they have no quantitative impairment of consciousness and
thus remember their acts and experiences.
LPTR constitutes a working hypothesis, and as Cummings (1983: 879)
points out regarding medical syndromes in general, they all can ultimately be
verified or disconfirmed by experimentation and observation. Note, however,
that for even the major mental syndromes delineated a century ago, such as
schizophrenia and manic-depressive illness, none of their various competing
neurophysio-pathological hypotheses has been conclusively verified despite
great technical advances (Arnold 1997). Difficulties in verification are com-
pounded when the symptomatology is transient, as in seizures that probably
involve neurotransmitters, possibly a decrease in serotonin levels in syndromes
with aggression, such as in LPTR.
Additional obstacles arise in cases of felonies requiring detention in maxi-
mum security facilities, where legal considerations hamper the use of
"objective" tests with so far nonportable equipment. Moreover, even abnormal
objective test findings, however, can only reveal correlations so far, not
causation of behavior, and are therefore still generally excluded from court
testimony. Meanwhile, the diagnosis rests mostly on detailed history-taking and
careful clinical observations of repeated, consistent patterns, such as these
characteristic of partial seizure phenomena.

LIMBIC PSYCHOTIC TRIGGER REACTION (LPTR): A PROPOSED

PARTIAL SEIZURE. A CONTRIBUTION TO THE LIMBIC SYSTEM
CONCEPT IN THE FORM OF A PROPOSED FRONTO-LIMBIC
IMBALANCE

As elaborated and exemplified elsewhere (Pontius 1981-2002), the proposed

LPTR symptomatology has been consistently found and replicated in 21 bizarre
cases that fit no other known diagnosis. So far, there were 17 homicidal cases
(Pontius 1981-2002), 3 fire setters (Pontius 1999), and 1 bank robber (Pontius
2001). All cases met essentially the 16 inclusion and 13 exclusion criteria (see
Table 10.1), which may vary by degree, but not in essence.
172 The Evolutionary Neuroethology of Paul MacLean

Table 10.1. Inclusion and Exclusion Criteria for LPTR

Inclusion criteria for LPTR at the time of act.

1. Transient psychosis: hallucinations (of any modality, formed or unformed), and or

delusions (frequently of grandeur)—all with new content, in cases of pre-existing
psychosis.
2. Transient autonomic hyperactivation (e.g., epigastric sensations, nausea, bladder
incontinence, ejaculation, ice cold sensations, or profuse sweating.
3. Seizure-like course: A brief aura-like phase with ("cognitive") puzzlement or
perceptual distortions is followed by ictus with brief psychosis, homicidal acts
typically wilh.some automatization, and finally by lingering inefficient behavior post-
ictally.
4. Flat affect during the acts.
5. No quantitatively significant alteration of conscousness.
6. No amnesia for the essential features of the acts, which are remorsefully recalled.
7. Highly individualized trigger stimuli revive experiences either in concrete or sym-
bolic ways.
Revived are:
8. Mild to moderate repetitive stressful experiences (based on subjective judgement),
ruminated by social loners. Such a pattern of intermittent reexperiencing ( e.g.,
through memory revival) implicates the neurophysiological mechanism of seizure
kindling, to which the limbic system (amygdala) is particularly susceptible. Second-
ary to an implicated limbic seizure, a temporary frontal hypofunctioning is impli-
cated, because both systems are reciprocally interrelated, leading to a transient fronto-
limbic imbalance.
9. Motiveless acts.
10. No planning, no premeditation of the acts.
11. Ego-dystonic, out of character acts.
12. No blaming of others or justifying acts, but subjectively assuming full personal
responsibility for the acts, linked with serious suicidal acts in some patients.
13. No use of drugs or alcohol, at least not close to the acts at toxic levels..
14. No dementia or mental retardation.
15. In the few cases with primary psychosis, LPTR may be superimposed as a different
syndrome of brief duration.
16. Typically no family history of seizure disorders, though individuals may have had
various previous seizures.

Exclusion criteria for LPTR in the absence of required inclusion criteria

1. Long-standing psychosis, as in schizophrenia, paranoia, and mania without new
atypical symptoms.
2. Long-standing recurrence of autonomic hyperactivation, as in various panic attacks
(e.g., with sensations of suffication).
3. Explosive onset, as in intermittent cxplosive/dyscontrol disorders, or in the proposed
organic aggressive syndrome: These all lack aura-like warning and recur over time.
4. Strong emotions, as in provoked impulsive acts or in acts of passion.
5. Clouding of consciousness or disorientation during the act, as in temporal lobe
epilepsy (TLE).
6. Amnesia for the act, as in TLE.
Limbic Seizures with Motiveless Homicide 173

Table 10.1, continued

7. Typical prior history of recurrently triggered seizures by modality-specific,

nonindividualized stimuli as in reflex epilepsy (e.g., as evoked by reading text of any
content).
8. History of severe, unusual trauma (e.g., war or natural catastrophies as in post
traumatic stress disorder.
9. Motivation for the act.
10 Planning, premeditation.
11. Habitual violence, as in various personality disorders, (e.g., anti-social, impulsive,
narcissistic, borderline, and conduct disorders), all persisting over time.
12. Blaming certain traumatic events or others, or justifying behavior, as in "abuse
excuses," and/or in the above personality disorders.
13. Drug, or alchohol use or abuse, acute or chronic, or withdrawal syndromes following
such abuse.

Note. It is of note that in all 14 cases (and in 2 newly identified ones) the essential criteria were
present (Pontius, 1981, 1984, 1987, 1993b, 1994, 1996). As is the case with any syndrome in cases
where the essential pattern of LPTR is preserved, not all of the criteria would be required, except for
the following essential criteria: Transient psychosis within a pattern that implicates a partial limbic
seizure with no significant quantitative alteration of consciousness and without significant amnesia
for the unplanned, stimulus-triggered, motiveless acts.
In addition to the 14 (now 16) white homocidal men, LPTR has also been implicated in three
male juveniles charged with motiveless unplanned setting of fires (Pontius 1993b) and one man with
bizarre bank robbery (Pontius 1994).
It is important to observe that several of the clinical symptoms are objectifiable by reports from
frequently present witnesses (because the acts were unplanned) and from police reports (because of
the patients' typical confessions).

LPTR consists of the following 13 symptoms and signs, that show

indications of being neurophysiologically interrelated, not at all haphazardly
assembled as is the case with natural phenomena.
LPTR symptomatology comprises: (1) lack of drive motivation; (2) lack of
preplanning of the act and of its concealment; (3) no prior history of (severe)
aggression; (4) flat affect around the time of the act; (5) typically a known
history of (frequently overlooked) closed head injury or of other insult to the
brain, e.g. febrile infantile seizures; (6) specific, individualized trigger stimuli
implicated in the evoked out-of-character act. The stimulus constellation acutely
revives the memory of intermittently experienced past stresses, each one by
itself not severe; (7) typically, some automatized action sequence reminiscent of
"auto-piloted" action; culminated in motiveless, purposeless acts—evoked (not
emotionally provoked) by the trigger stimulus; (8) typically, an auralike puzzled
state ("cognitive mismatch"), lasting about 5 minutes, followed by ictus-like
symptomatology (about 20 minutes); (9) transient autonomic, prevailingly
parasympathetic arousal (e.g., nausea, vertigo, "ice cold" sensations or profuse
sweating, "tingling," urinary incontinence, erection, or ejaculation); (10)
transient hallucinations (of any modality, formed or unformed) and/or delusions
(frequently of grandeur); all such psychotic symptoms are new ones in those rare
cases with prior psychosis; (11) no significant quantitative alteration of
174 The Evolutionary Neuroethology of Paul MacLean

consciousness, therefore no essential memory loss, enabling virtually full recall

of the acts; (12) indications of transient prefrontal-lobe dysfunctioning around
the time of the act, secondary to implicated limbic hyperactivation, and
potentially persisting (for some hours) post-ictally; and mostly (13) self-
confession of the act, with subjective feelings of responsibility and profound
remorse (unless there is underlying schizophrenia with its habitually flat affect).
Noteworthy, is the fact that the symptoms occurred in the three phases that
characterize seizures: aura, ictus, post-ictus.

Hypothesized Neurophysiological Mechanism of Seizure Kindling

Importantly perhaps, all 21 cases of LPTR so far occurred in social loners,

with a "schizoid/avoidant personality." Loners do not share nor compare their
hurts with others but ruminate on them, not laying them to rest. This personality
type appears to contribute to the outstanding sequence of events leading to
LPTR: The LPTR symptoms appear (within c. 5 minutes) after a chance
encounter with an individualized trigger stimulus that revived the memory of
past merely mild to moderate hurts, each one in itself seemingly innocuous
(Table 10.2).
This sequence of events characterizes seizure kindling (Goddard 1967;
Goddard & Mcintyre 1986). Kindled seizures in primates are typified by the
nonconvulsive "behavioral" type (Wada 1978): The trigger stimulus, in itself
innocuous and subthreshold, resembles the preceding stresses that the trigger
revives. Thereby the specific stimulus that resembles past stresses directly or
symbolically appears to represent the last one in a series of similar hurts.
A hypothesis alternative to the kindling mechanism (albeit a hypothesis not
as fitting to the history and symptoms) might suggest that a spontaneously
occurring aura (Fried 1997a: 119-120) of an extended kind may play a primary
role in the LPTR symptomatology. Fried likens an experiential aura to a
spontaneously appearing memory. Both these phenomena cannot be eradicated
at will and cannot be eliminated by local tissue removal, implicating the
neuronal network uses parallel distributed processing (Fried 1997a).

Discussion of LPTR as a New Subtype of Partial Seizure

The goal of the presentation and discussion of LPTR entails impetus to

further inquiry into the complexity of human action. Whether LPTR should be
classified as a simple or a complex partial seizure depends on the classification
used. Meldrum (1990) and Gram (1990) used the preservation of consciousness
as a criterion for simple seizures, while Trimble (1992: 193) cited Gastaut and
Geschwind's criterion for complex partial seizures, namely impaired organized
cerebral functioning. This criterion is congruent with Dam's (1992) formulation.
Limbic Seizures with Motiveless Homicide 175

Table 10.2 Specific Interrelation Between Mild to Moderate Stresses, Specific

Trigger Stimuli Reviving The Stresses, and Homicidal Acts in LPTR

Case Mild/Moderate Stresses Stimuli Triggering Homicidal Acts

1. Several admissions to mental hospitals Fatally punching brother's heart after
by parents "for no reason." reading library card "Lizzy Borden,"
who too had been "wrongly" sent to
mental hospitals by parents.

2. Forced to perform fellatio as a child Fatally shooting brother-in-law after

and repeatedly forced to eat spagetti, he had been forced to dump "dirty
causing "gagging." pictures" and hearing of hallucinating
the term "child molester."

3. Being called "boob" (idiot) as a child Stabbing "friend" after hearing him
by adoptive mother with big breasts say "boob" while passing by a domed
("boobs"). Church with a statue of Christ, whom
"friend" seemingly "criticized" when
saying "boob."

Boot camp training with sights and Shooting blindly at eight policemen
sounds of live ammunition, often after hearing their sirens and crackling
reexperienced over years by listen- sounds in the underbrush and seeing
ing to "graduation tapes": "The Sounds their car lights flashing.
of Boot Camp" with sergeant's com-
mands: Kill! Kill!

5. Being taunted and worried about Fatal shooting of a restaurant owner

small penis since childhood. Wife, and missing several other persons after
whose faithfulness he did not doubt only seeing wife's car near restaurant.
had dropped hints about the sexual
prowess of the restaurant owner.

6. Being repeatedly refused cigarettes Fist attack on old female stranger

by mother whose gait and voice,refusing cigarette,
recalled mother's behavior.
7. Being repeatedly criticized for Knife attack on male stranger, driving
"erratic" driving "erratically" while giving patient a ride.

8. Being the only one of five male Fatal stabbing of female stranger while
family members who did not she was talking about her husband and
fulfill father's wish to become an son being officers in the Armed Forces.
officer in the Armed Services
from which he "flunked."

Seeing father's photo in family Fatal drowning of male stranger fishing

living room in posture with fly rod with a fly rod, standing sideways in
ever since father had died of a heart same position as patient's late father
attack after an argument with patient in photo.
who was four years old at the time.
176 The Evolutionary Neuroethology of Paul MacLean

Table 10.2, continued

10. Hearing mother crying when hit Fatal hitting of his crying and choking
by father. Patient had helped her infant "to save her" a day after patient's
by hitting father back. As an adult, mother died.
patient repeatedly saved his crying
and choking infant by whacking her
on the back.

11. Repeated leg injuries inflicted by Fatal stabbing of prostrate male strang-
stepfather during childhood and later er whom he first heard before he could
by stepfather-like codefendant, and see his mouth move (as in English-dub-
repeated watching of karate movies ed karate movies), while patient also
with fixed action program, culminating suffered leg pain.
in stabbing the prostrate loser.

12. Being bitten in finger by brother Stabbing friendly male stranger, mov-
as a child, later inguinal hernia operation ing his mouth while eating, which led
under local anesthesia. To patient's belief that he was about to
be "cannibalized," while hallucinating
that his testicles and entire body were
being cut.

13. Tonsilectomy as a child, later Fatal strangulation of female stranger.

recurrent painful throat infections All happened in the context of sexual
with painful external swellings, relieved foreplay, when unwittingly touching
through touching his throat. the victim's throat in a highly specific
manner. A previous potential victim
was not attacked, as she had slightly
changed her position by chance.

14. Loneliness since an anal rape Fatal hitting of female lover, who
as a child by a "friendly" man, while insisted on increased emotional close-
having stomach aches and seeing ness, unbearable to patient in context
leaves moving. Later, only seeing or of revived loneliness during severe
hearing the sound of moving leaves stomachaches with unformed visual
and/or stomachaches repeatedly revived hallucinations.
extreme feelings of loneliness, threaten-
ing annihilation.

15. Girl friend had repeatedly mentioned Girl friend mentioned again ex-wife's
his painful divorce in context of his name, and he "knew like the amen in
ex-wife's name. church" that she would continue with
painful divorce details, whereupon he
strangled her.

16. Being repeatedly jilted by women Hearing female neighbor talk decep-
with "excuses:" "it's not your fault." tively to her boy friend while a TV
sitcom was on about rejecting women
saying 7 times "its not your fault,"
whereupon he attacked one woman
Limbic Seizures with Motiveless Homicide 177

Table 10.2, continued

with a frying pan and stabbed a second

one with a kitchen knife.

17. Secretive parents repeatedly made The male survivor of a machete attack
unpleasant plans driving him to had seemed to move secretively behind
some unknown destination (e.g., a screen when another man said with-
doctors), which made him increas- out explanation: "I have to make a
ingly suspicious of unrevealed plans phone call," he killed him with a
about him. kitchen knife.

LPTR would also be consistent with Smythies' (1992: 271) definition of

consciousness as "the total of what we can introspect (i.e., our sensory fields . . .
inner images, thoughts, emotions as we experience these directly." Such defini-
tion would favor a classification of LPTR as a complex partial seizure with
special emphasis on impairment of volition and of emotional concomitants of
the action.
In general, as Trimble (1992) pointed out, of the two main kinds of seizures,
convulsive and nonconvulsive, those with the striking, readily observable
symptomatology of convulsions have historically been more readily accepted
than the "behavioral" (i.e. nonconvulsive seizures). The latter may go unnoticed,
except if "arrest" (i.e. staring is present and observable). Even dramatically out-
of-character acts are not readily attributed to seizures because of the ubiquitous
belief in "free will." It is therefore imperative to obtain patients' spontaneous
(not questionnaire-engendered) accounts of their perplexing experiences during
behavioral seizures.

DIFFERENTIAL DIAGNOSES OF LPTR AND ITS OPPOSITE

SYNDROME E

Previously, various differential diagnoses of LPTR have been ruled out in

detail (Pontius 1981-2002) so that here only a summary of various disorders
needs mention. Each other possibility typically persists over lengthy periods of
time (e.g., the major psychoses, such as schizophrenia and affective disorders
with depression and/or mania). Also distinct from LPTR are the persistent,
frequently recurrent, virtually habitual "Impulse Control Disorders," including
episodic dyscontrol. Each of these persistent disorders are also linked with
strong emotions, and occur typically without psychosis. Among the partial
seizures, temporal lobe epilepsy differs from LPTR most strikingly because of
TLE's clouded consciousness causes memory consolidation difficulties, that
then result in at least partial amnesia.
178 The Evolutionary Neuroethology of Paul MacLean

Other Criminal Acts Not Due to Seizures or Psychoses

Based on three decades as a forensic neuropsychiatrist, I must point out a

certain inaccurate generalization by MacLean (1990), that he based on anecdotal
accounts of crimes without having the benefit of specific histories and diagnoses
(MacLean 1990: 569-570). Such anecdotal accounts give the impression that
persons in general act without emotions during homicide or other criminal acts.
Absence of emotion in such instances indicates partial seizures or certain cases
of a major psychosis, such as schizophrenia.
By contrast, "compulsive social acts" (MacLean 1990), as well as impulsive
acts, typically occur with very strong emotions, when honestly reported without
trying to gain some legal advantage out of such a denial. Further, often surviving
victims of either "compulsive" or "impulsive" acts have reported emotionally
aroused verbal outbursts expressed by their attackers.
Even "cold-blooded" psychopaths, who selectively lack empathy, experience
emotions related to self-gratification during their crimes, such as triumphant
feelings of power and superiority as well as "remorse" for having been caught.

Two Opposite Homicidal Syndromes: "Syndrome E" vs. LPTR

A recently hypothesized Syndrome E (Fried 1997b) possesses special interest

because its symptomatology presents virtually a mirror image of LPTR (see
Pontius 2000 & Table 10.3 below).

Table 10.3. Comparison Between Two Hypothesized Syndromes: Syndrome E vs.

Limbic Psychotic Trigger Reaction (LPTR)

SYNDROME E LPTR
(I. Fried, Lancet 1997, 350: 1845-1848) (A. A. Pontius)

1. Long lasting c. 20 minutes duration

2. None Suggestive of seizure-like

phases (aura, ictus, post-ictus)

3. Obsessive ideation Rumination

4. Group-shared ideology Re. individual moderate stresses

5. Selected defenseless victims Unselected victims, by chance,

unwittingly providing trigger
stimulus

6. Rapid desensitization Reverse: deepening, persistent

guilt feelings with voluntary
surrender to police
Limbic Seizures with Motiveless Homicide 179

Table 10.3, continued

7. Initial "elation" later Reverse: consistently flat affect

diminished affective reactivity

8. None Brief psychosis (hallucination and/

or delusions (e.g., of grandeur)

9. Autonomic hyperarousal Same

10. General environmental dependence Specific, individualized environ-

mental or internal trigger stimuli

11. Group contagion Reverse: loners, acting alone

Risk Factors

Male sex, ages 15-50 Social isolation (possibly more

prevalent in Caucasians)
(Schzoid/avoidance type)

Early Prevention by Increased Awareness of Syndromes

"Isolation" of males "showing emerging Providing ruminating social loners

obsessive ideology, hyperarousal, with companions ("Big Brothers")
diminished affective reactivity, group to prevent seizure kindling
dependent aggression"

Differential Diagnoses

Individuals acting violently Other partial seizures and/or

psychoses (e.g., temporal lobe
epilepsy; schizophrenia, respect-
ively); episodic dyscontrol, impulsive
behaviors, and other long-persistent
syndromes

Suggested Pathopsysiology
Deficient Interaction Between Prefrontal Cortices/Amygdala

a) dorsolateral prefrontal cortex

Relatively unaffected: planning intact, Reverse: briefly affected: no

problem-solving intact planning, defective problem-
solving

b) orbitofrontal cortex

Hyperactive: obsessive ideation Not affected

180 The Evolutionary Neuroethology of Paul MacLean

Table 10.3, continued

Repetitive acts Typically single acts

c) medial prefrontal cortex

Suggested hyperactivity Reverse: no motive and

Motivation and elation Consistently flat affect

d) ventromedial prefrontal cortex

Affected: generating emotions not Possibly transiently affected

appropriate to the images conjured
by certain "acts of stimulation/stimuli"

e) interaction prefrontal cortex/amygdala

Amygdala tonically inhibited by Reverse: initially fleeting amygdala

Prefrontal activation hyperactivation, with transient
Secondary prefrontal inhibition

Syndrome E applies to ideologically motivated ethnic mass murderers, who

act in groups, plan their acts on selected helpless victims, act with "elation" (at
least initially), and show no signs of psychosis or seizure-like behavior.
Correspondingly, Syndrome E suggests the opposite neurophysiopathology
to that of LPTR. In comparison to LPTR, Syndrome E hypothesizes a reversed
sequence of dysfunctioning within the context of a shared fronto-limbic
imbalance or "fronto-limbic fracture" (Fried 1997b). Thus, an initial limbic
dysfunctioning is hypothesized in LPTR, while "Syndrome E" hypothesizes a
certain initial prefrontal dysfunctioning. (Given the reciprocity between the two
systems, this leads to a fronto-limbic imbalance in both syndromes.)
A certain difference between LPTR and Syndrome E stems from different
limbic/amygdalar subfunctions: Syndrome E emphasizes emotional dysfunction
associated with the amygdala, while LPTR focus on aggression implicating
either amygdalar and/or hypothalamic dysfunctioning, both of which are inter-
related
With regard to any localization hypotheses, Cummings (1992) warns that any
putative neuropathology will not be able to pinpoint precise locations in the
brain. Specifically, any strict localization is suspect and simplistic in partial
seizures from the limbic system and temporal lobes, because the temporal lobes'
tracts connect to all areas of the brain (Williamson et al. 1987). Thus, for
example, Dam (1992: 122) pointed out that the symptomatology of TLE and
related syndromes actually involves frontal lobe seizures in 10% of such cases.
Thus, much research is still obviously needed in LPTR; this is all the more
indicated because LPTR patients' preserved consciousness enables their quite
unique accounts of pathological experiences. Such experiential accounts may
contribute to the study of the "binding problem," of central relevance in
Limbic Seizures with Motiveless Homicide 181

neuroscience (Fried 1997a: 120). Aspects of such binding among various

behavioral components, resulting in a unified experience and a potential disrup-
tion of binding by a seizure, as possibly in LPTR, may benefit greatly from
reports by patients with retained memory, as in LPTR.

DISCUSSION: ELABORATION OF MACLEAN'S EPISTEMICS BASED

ON TEMPORAL LOBE EPILEPSY BY ADDING LIMBIC PSYCHOTIC
TRIGGER REACTION

A. The Sense of Self and Consciousness

This section focuses on the uniquely human experience in relation to the

sense of self, including originating acts through free will and being responsible
for them. To this point, evaluation of experiences during the partial seizure of
Temporal Lobe Epilepsy (TLE) has been hampered by at least partial amnesia
associated with the events. Thus, fortuitously, the LPTR new subtype of partial
seizures may help because consciousness is quantitatively preserved, as well as
the memory for the acts committed during LPTR. The preserved consciousness
is probably stems from the absence of temporal neocortical involvement in
LPTR in contrast to TLE. Otherwise, both TLE and LPTR implicate archicort-
ical and subcortical limbic structures within the temporal lobe.
Thus, the symptomatology of both TLE and LPTR share certain perplexing
features that raise philosophical questions centered about the sense of self.
During any seizure, even during the partial (i.e., nonconvulsive, "behavioral"
seizures of TLE as well as of LPTR), "free will" is seriously impaired. Thus,
without willing them, such patients may perform bizarre, out-of-character,
unintended, purposeless acts. To the onlooker such acts seem to be willed acts.
As long known in TLE, routine and subroutine behaviors occur during a seizure,
that surprisingly seem appropriately executed, as summarized by MacLean
(1990: 576). For example, TLE patients may travel around to unintended places,
buying bus tickets and performing other appropriate acts for days. But this
happens during a state of clouded consciousness because they recall nothing
afterwards. Thus, not surprisingly, during the preserved consciousness of LPTR
similar unwilled, unintended, auto-piloted but recalled acts can occur.
To rule out malingering, the skillful evaluator must consider various
behavioral concomitants (see 16 inclusion and 13 exclusion criteria, Table 10.1)
aside from LPTR patients' self-reports. Malingering by LPTR patients is ruled
out by their exaggerated sense of responsibility for all their acts. They typically
insist on being punished, mostly after having voluntarily reported their crimes.
Such not self-serving traits, uncommon in the usual criminal, strongly support
the validity of LPTR patients' self-accounts and render them valuable for
philosophical conceptualization.
Thus, LPTR patients are able to share their strange involuntary acts and
experiences quite fully and as completely, much as another kind of layperson
shows cognizance of an event both as an experiencing subject as well as an
182 The Evolutionary Neuroethology of Paul MacLean

objective observer. As laypersons, they may overlook certain subtle behavioral

changes and thus are more likely to underreport than to over report possible
additional symptoms in support of a seizure diagnosis.
All LPTR patients have shared with me their sense of the extreme
discrepancy between their unintended and motiveless acts and their strong
feeling of being responsible for them without having willed them. Such
subjective experiences emerge from the philosophical construct of the sense of
self, essentially anchored in the limbic system, as MacLean (1990) proposes,
particularly because of the limbic connections with the thalamus. The thalamus
mediates all exteroceptive input as well as the input from the viscera, mostly via
the great visceral nerve, the vagus. (See Appendix on a new hypothesis about
hippocampal irritation through recurrent vagal stimulation possibly through
recurrent otorhinopharyngeal infections).
With regard to the sense of self, it is puzzling that all LPTR patients
subjectively maintained to have been the actors of their bizarre acts, including
homicide, for which they assume full responsibility and suffer tormenting guilt
feelings. The LPTR patients could not conceive of having not been responsible
even for the most obviously auto-piloted acts, more so as they knew and
remembered having committed them. Even those men who appropriately
described their acts as having occurred like a reflex felt responsible.
By analogy, a person does not feel guilty if he kicked someone by chance
during a knee reflex test. Thus, do people draw a demarcation line with regard
to their sense of self and their responsibility by distinguishing between a simple
reflex motion compared to a rather complex series of acts occurring during a
partial seizure of TLE or LPTR? When increasing the complexity of involuntar-
ily elicited acts to the degree of electrical stimulation of brain (e.g., limbic)
structures, at what point does the sense of free will blurr? This remains a basic
question of human existence and predicament. Possibly during LPTR, despite
preserved consciousness, some splitting of the sense of self might occur which
selectively impairs the assessment of one's emotional and volitional involvement
in acts.

B. Subjective/Objective Experience

The above discussed paradoxical sense of self during partial seizures,

especially during LPTR with preserved consciousness, raises questions about
subjective/objective aspects of experience. Such patients retain a sense of
subjective responsibility for obviously purposeless, unwilled auto-piloted acts
during partial seizures, presenting signs and symptoms that implicate brain
events objectively beyond their control. What could be an essential distinction
between between subjective and objective experiences?
This age-old question occupied philosophers, who insisted on a clear
dichotomy between the subjective and the objective until Kant (1781) redefined
this superficially strict dichotomy his last, but often neglected version of the
categorical imperative, discussed elsewhere (Pontius 1971). MacLean (1990),
with a philosophical background has hinted perceptively at certain innate bases
Limbic Seizures with Motiveless Homicide 183

of human experiences that occur within specific constraints, revealing the

hallmarks of "hard-wired" determinants. Such a universally shared basis of
human experiences that extends beyond subjective ones could therefore be
characterized as constituting an objective given shared by all humans beyond
their subjective individual modifications.
Although not directly and completely communicable in detail and by
subjective elaboration, numerous indications imply that human experiences
occur within specific patterns constituting built-in constraints of subjective
experience. Such patterns merely vary or modify to some extent by subjective
life experiences within the person's sociocultural milieu. Myths and rituals share
certain basic themes worldwide, something not surprising, since all humans
share the same brain structures, though utilized to different degrees as required
for a cultural group's survival needs. Jung (1957) called such recurrent universal
patterns of experiences, archetypical patterns of behavior and considered them
to be analogous to animals' fixed action patterns known to ethologists, such as
Tinbergen and Lorenz, also referred to by MacLean (1990) in such a context.
This theme of built-in objective constraints of subjectively experiencing
constitutes yet another area for future exploration of the sense of self, to which,
so far, some contributions have been made in the forensic studies of six schizo-
phrenic men who committed bizarre acts. Two dismemberment murderers each
tried to create an ancient god-like male-female combination out of his victim
(Pontius 1975). Three firesetters attempted to unite extreme opposites by fire
(Pontius 1972). One man repeatedly threatened in writing to assassinate three
consecutive American presidents. His plans showed essential themes of ancient
king-killing rituals, distributing parts of the king's body over the land to fertilize
and rejuvenate it by propitiating a divine female creator (Pontius 1974). All
these otherwise unexplainable acts had the hallmark of reenacting world-wide
ancient myths or rituals, of which these uneducated men had been unaware.
Thus, universally shared, archetypically behavior patterns can be expressed not
only in dreams, but also in psychotics' action patterns, which would remain
incomprehensible without such an assumption.
During the fleeting psychosis associated with LPTR, no such more
cognitively determined archetypical themes have been reported so far. In
congruence with LPTR's neuroethological context, there emerged primitive
animalistic patterns of defensive or predatory killing (Pontius 1981-2002),
primitive destructiveness by fire (Pontius 1999), or simplistic acquisitional acts
in "bank robbery" (Pontius 2001).
Both the animalistic patterns of LPTR and the "archetypical" patterns in
some schizophrenics imply a hard-wired organic basis for species-specific
patterns of experience and behavior even in humans, thereby requiring a refined
determination of the subjective and the objective aspects of experience and
action.
184 The Evolutionary Neuroethology of Paul MacLean

CONCLUSION: NEUROETHOLOGICAL ASPECTS OF PARTIAL

SEIZURES IN LIMBIC PSYCHOTIC TRIGGER REACTION (LPTR)

A concluding survey will now follow, underlining the neuroethological

aspects of a clinical contribution to MacLean's creative conceptualization,
presented as the proposed partial seizures of Limbic Psychotic Trigger Reaction
(LPTR) (Pontius 1981-2002). Thereby human experience is added to the
ethological background that we share with all mammals.

A) Reciprocal Relation Between the Old Limbic and the New Frontal Lobe
Systems:
The validity of the coexistence of evolutionarily old and new parts and
functions in humans' "triune brain" becomes most directly manifest in the specific,
primarily neuroethological aspects of limbic seizures. Such factors are most apparent in
that subtype of partial seizures proposed as Limbic Psychotic Trigger Reaction (LPTR)
(Pontius 1981-2002) during which the patients do not lose consciousness, defined in
quantitative terms and operationally as responsiveness to simple commands and as the
ability to perform willful acts. In all these aspects of consciousness, LPTR patients are
not impaired, and they do lay down memories of their acts, which they recall, talking
about them with deep distress.
On a more comprehensive level of defining consciousness, however, there is an
essential qualitative difference during LPTR as compared with the LPTR patients' usual
behavior. Thus, LPTR patients cannot perform activities (except possibly during their
aura; see Pontius, in press) that are not only thoughtfully planned, but also willed and
with emotional concomitants. Instead, they act with flat affect, unthinking and without
volition like automatons, "autopiloted" or "like a reflex," as some patients put it.
Based on such symptomatology characteristic of seizures, it seems reasonable
to deduce that a limbic hyperactivation during LPTR seizures temporarily overwhelms
the evolutionarily younger prefrontal lobe system, since both systems are reciprocally
interrelated (Nauta 1971; Weinberger 1984).
The human prefrontal lobe system essentially mediates and integrates various
aspects of socialized behavior. Thus, socially destructive consequences can ensue even if
there is a transient disturbance of the normal fronto-limbic balance. Such behavioral
consequences can range from socially inappropriate, self-injurious acts (as astutely
portrayed by Proust's M. Swann, who proposed marriage to a "despised courtesan" upon
hearing a specific piece of music) (Pontius 1993b); to bizarre, unthinking, primitive
robbing of a bank by a devout monk with sudden delusions of grandeur (Pontius 2001);
to senseless firesetting by three juveniles upon encounter with fire-related stimuli
(Pontius 1999). The wide range of such strangely out-of-character acts, all of which also
occurred with fleeting autonomic activation and psychosis, also include unplanned,
motiveless, reflex-like homicidal acts in 17 social loners (Pontius 1981-2002) remini-
scent of animals' defensive or predatory patterns of killing.

B) Suggested Etiological Factors:

1. Chronic Deprivation of Limbically Mediated Basic Needs and Functions
Necessary for Mature Socialization.
a. Social Bonding: All mammals need social contact. If experimentally
isolated, primates show behavioral changes similar to those occurring
in socially isolated humans (Kling 1986), as elaborated by Gruter and
Masters (1986).
Limbic Seizures with Motiveless Homicide 185

b. Normal Forgetting, Habituation: Douglas & Pribram (1966) observed

that hippocampectomized monkeys lost habituation to repetitive stimuli, reacting to them,
as if they were new. These authors emphasized that forgetting is part of normal memory.
In human social loners, normal forgetting is hampered by their lack of sharing
and comparing their hurts with others. Instead, they perhaps ruminate on their hurts until
their minds endow everyday common stresses with exaggerated emotional validation or
meaning that may implicate amygdalar involvement. After such intermittently experi-
enced subthreshold stresses, a specific lack of habituation can occur, called reverse
habituation. Intermittent exposures (such as by memory rumination) prevents habituation
for which continued stimulation is required and thus sets the stage for seizure kindling
(Goddard 1967). Of all brain systems, the limbic system is most susceptible to kindling
particularly its amygdala and hippocampus (Goddard & Mclntyre 1986). In primates,
kindling typically elicits behavioral seizures (Wada 1978) in contrast to the convulsive
ones kindled in lower mammals. Additionally, some human cases of inadvertent kindling
have been reported (Heath et al., 1957; Sramka et al. 1984).
c. Normal Remembering has Context-Relevance vs. Memory Priming by a
Cue. In LPTR an individualized trigger stimulus (suddenly reviving such patients'
memories of past hurts but without context-relevance) resembles priming by a cue in
animals (Eiserer & Hoffman 1983).

2. Disturbance of Normal Balance between Reciprocally Related Brain Systems

a. An imbalance between prefrontal and limbic systems may be indicated
by the symptomatology of LPTR, as implied by seizure-related limbic hyperactivation
associated with relatively secondarily too weak prefrontal controls.
b. Amygdalar-hippocampal imbalance. Both these limbic structures,
hippocampus and amygdala, reciprocally interrelate, as experimentally shown with cats
(Adamec 1987: 448-450). Thus, an initial overactivation of either one may elicit a
temporary imbalance between them, thereby contributing to a functional fragility of
certain limbic functions (possibly facilitating kindling?).
aa) Amygdalar stimulation elicits aggression especially in dominant
animals, but has a reverse effect on submissive ones. A human case of electrically elicited
amygdala aggression has also been reported (Mark & Ervin 1970). In many respects,
LPTR aggression resembles "sham rage" (Kaada 1967) which can be elicited by
hypothalamus stimulation. Decorticate cats with sham rage demonstrate posture and
certain behavior indistinguishable from emotionally elicited rage, as elaborated elsewhere
(Pontius 2001a).
bb) "Experiential Phenomena"—reportable by humans only. A striking
analogy exists between amygdalar hyperactivation from memory revival of hurts during
the aural phase of LPTR and similar effects elicited by direct electrical amygdalar
stimulation of electrode implants in presurgery patients (Gloor et al. 1982). Further,
electrical stimulation of amygdalar implants in presurgery patients elicited "experiential
phenomena" (Gloor et al. 1982) strikingly similar to those of LPTR (Pontius 1997, Table
14, p. 162). Gloor et al.'s reports are congruent with those by Wieser (1983), Fried
(1997b), and Palmini & Gloor (1992), all of which elicited "experiential phenomena"
through direct electrical stimulation in various brain areas that was similar to auras
spontaneously experienced during partial seizures of the temporal lobes. These three
reports thereby supported the ability to frequently localize (though not to lateralize) the
source of seizures based on the kind of patients' auras.
cc) A possible hippocampal overstimulation might occur through
recurrent vagal stimulation in recurrent nasopharyngeal infections (see Appendix).
186 The Evolutionary Neuroethology of Paul MacLean

APPENDIX

Hypothesis about potential limbic irritation by recurrent vagal stimulation in

recurrent infections of the oro-nasopharynx (including sinuses).
4 cases of partial seizures (3 with homicide in Limbic Psychotic Trigger Reaction
(LPTR) and 1 case with episodic exhibitionism in Temporal Lobe Epilepsy (TLE)
An understanding of potential etiological factors in partial seizures can further benefit
from increased specification. In general, space-occupying and/or irritating lesions of
limbic structures, particularly in the hippocampus are implicated. Herein a new kind of
potential irritative impact on certain limbic structures through vagal stimulation is
hypothesized. The proposed testable working hypothesis links vagal limbic (especially
hippocampal) stimulation with certain cases of partial seizures based on MRI findings of
infections of sinuses (2 cases of LPTR and 1 case of TLE), or of nasal mucosa (1 case of
LPTR). In addition, 1 case of LPTR, who did not get a MRI scan, had a history of
recurrent severe aphtous stomatitis).
This hypothesis was inspired by Paul MacLean's triune brain (1990: 514) experi-
mentally demonstrating that "only vagal stimuli were effective in eliciting complete
excitation of hippocampal units." Furthermore, in testing the thalamus (closely
interconnected with limbic structures), he found that 27% of the units tested in the medial
dorsal nucleus of the thalamus were responsive to vagal volleys. Other limbic structures,
too, respond to vagal stimulustion: In animal experimentation with the awake encephale
isole preparation (reported by Dell & Olson, 1951 as cited by MacLean, 1990: 468)
showed that vagal shock evoked a slow-wave response in the amygdala and within the
buried cortex within the anterior rhinal sulcus.
It is of note, that the hippocampus indirectly influences the amygdala, as both
structures are interconnected and these two limbic structures are also the most susceptible
to seizure kindling of all brain structures tested by Goddard & Mclntyre (1986).
Thus, it appears reasonable to speculate that spontaneous recurrent mild vagal
stimulation can occur in association with recurrent infections in areas with vagal
afferents, such as those of the naso-pharynx areas that happened to appear on brain MRI
scans, and that such vagal stimulation may have asserted a certain irritative impact on
limbic structures, particularly on the hippocampus (Pontius & LeMay, in press).
Thus, MacLean's experimental findings (1990: 497, 514, 531, 562; 1992 & 25 fig.
24; reinforced by personal communication 7/8/1999) have focused attention on the
important role of the hippocampus and its relevance in partial seizures: As he
emphasized, due to its position, the hippocampus enables the integration of information
from two systems, the exteroceptive one (from all sensory modalities) as well as
interoceptive system (especially from the vagus, "the great visceral nerve", afferents of
which also subserve the naso-pharynx).
Thus, by way of such integration of the extero- and intero-ceptive systems, the hippo-
campus plays a central role specifically with respect to those functions known to be
impaired in partial seizures: The hippocampus influences neurovegetative, somato-
visceral, and emotional functions "in, regard to mechanisms underlying a feeling of
individuality, that, in turn, is requisite for certain aspects of memorization," as MacLean
(1990: 497-498) put it.
MacLean's conclusion appears to be congruent with the even more comprehensive
one offered by Trimble, Mendez & Cummings (1997, p. 127 in The Neuropsychiatry of
Limbic and Subcortical Disorders, S. Salloway, P. Malloy, J. Cummings, Eds.). They
stated that "the hippocampus may be a nodal area for delusions given its role in memory,
in receiving emotional valencing from the amygdala, and in facilitating, perceptual
associations."
Limbic Seizures with Motiveless Homicide 187

In the context of delusional experiences, it may also be of note that recent imaging
studies of the brain in presurgery patients by Fried (1997: 118; ibid.book) showed that
auras and various psychotic symptoms and experiential phenomena known to occur in
partial seizures could also be elicited by direct electrical brain stimulation within the
temporal lobe. A comprehensive study by Palmini & Gloor (1992) assigned localizing,
though not lateralizing, significance to most types of auras when elicited by careful
history taking. With respect to an implicated role of extero- and/or intero-ceptive
experiences in partial seizures, their influences can be represented in the phenomenology
of aural delusions in TLE (MacLean 1990: 496).
Further, specifically in LPTR, any one of both kinds of extero- or interoceptive
experiences (and their typical input into the hippocampus) might also be represented by
the phenomenology of the various individualized stimuli. Such stimuli are viewed as
triggering seizure kindling, since those stimuli appear to represent and constitute the final
stimuli in a preceeding series of a similar kind, and thereby ultimately kindling the limbic
seizure of LPTR.
Alternatively, it could be hypothesized that the auras and experiential phenomena in
LPTR may already represent ictal events, or at least merge imperceptibly into ictal events
whereby a proposed kindling mechanism would not be necessary. Rather, recurrent
sinusitis or other nasopharyngeal infections could just constitute a sufficiently irritating
hippocampal stimulation to elicit a seizure.
With respect to a more comprehensive role of the ventromedial temporal lobe (which
includes hippocampus and amygdala), recent research by Arnold (1997) and van Hoesen
(1997: 19-20, 27-28) has implicated this area in a variety of psychiatric disorders
(including schizophrenia) and in neurological disorders, particularly those following
mechanical injuries to the particularly vulnerable area around the tentorium cerebelli.
(Here it may also be of note that the MRI of LPTR case 17 showed that "the
subarachnoid spaces in the posterior fossa and supratentorial compartments are dilated").

MRI findings of sinus or nasal infections in 3 cases of LPTR:

It is of note that only for the following six most recent unselected felony cases
examined by me on court orders had MRI scans become potentially available. Thus, the
following findings appear to be remarkable.
Case #13, homicides during LPTR, age 32, whose family declined to pay for an MRI,
had, however, recurrent severe, very painful aphtous stomatitis, requiring bed rest for 4
days at a time with temperature up to F 104.
Case #14, homicides during LPTR, age 43: On MRI the nasal cavity shows mucosal
thickening left more than right.
Case #15, age 40, homicide during LPTR. MRI showed mild dilation of the
ventricles and prominence of the sulci, more than would be expected for his age.
Impression "Mild cortical atrophy and a large retention cyst in both maxillary sinuses."
No focal right temporal lobe pathology.
Case #16. age 36, homicide during LPTR: MRI within normal limits.
Case #17, age 28, homicide during LPTR c. 10 minutes after an externally interrupted
homicide attempt at another person was aborted by a witness. His MRI showed "atrophy
involving the posterior fossa and supratentorial portions of the brain. Note is made of
extensive inflammatory changes involving both maxillary and the right ethmoid sinuses."
One differential case of partial seizures turned out not to be LPTR but TLE (of which
only this one case of mine had an MRI). This 34-year-old man had episodic
exhibitionism without physical contact. His MRI showed "Chiari malformation
(extension of the cerebellar tonsils below foramen magnum to the level of bilateral
frontal ethmoid of C 1 and left maxillary sinusitis, mucosal thickening and inflam-
188 The Evolutionary Neuroethology of Paul MacLean

mation."
In summary, three out of the four LPTR cases who had MRI scans showed signs of
inflammation in the nasal-pharyngeal area (inch sinus), as did the one TLE patient. In
addition, one LPTR case who had no MRI had recurrent severe aphtous stomatitis,
leaving only one out of six partial seizure patients without problems in the naso-
pharyngeal area. These findings may alert the clinician to a potential link between partial
seizures and vagal overstimulation. Such may also occur in other areas of the body. It just
happens that MRI scans of the brain also depict the areas here presented.
In addition, the findings on MRI or on other scans need to be supplemented by
extensive detailed history taking, as emphasized by Fenwick (1993: 569), who stated that
MRI or other "objective tests" being reported as "within normal limits" may be highly
significant when combined with clinical and neuropsychometric findings which implicate
temperolimbic damage. Thus "normal" findings on "objective tests" do not exclude the
possibility of fleeting partial seizures.

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 11

NEURAL AND FUNCTIONAL ASPECTS

OF PRIDE AND SHAME

Glenn E. Weisfeld

INTRODUCTION

In this chapter an ethological perspective will be applied to the role of the frontal
lobes in the emotion of pride and shame. First the neural mediation of emotion
in general will be described using fear as an example. Then the mediation of
dominance motivation will be traced; many ethologists believe that dominance
behavior underlies pride and shame in humans. Next the mediation of complex
social behavior by the prefrontal cortex will be addressed. Last, a modification
of the emotion-reason dichotomy will be proposed in light of the foregoing
discussion.

THE PRIMACY OF EMOTION

The study of comparative neuroanatomy makes clear that motivated behav-

iors evolved earlier than complex cognitive capacities. The brain stem, basal
ganglia, and limbic system antedated expansion of the neocortex, as MacLean
(1990) has tirelessly emphasized.
This phylogenetic view is compatible with a functional, ethological
perspective. Natural selection acts most directly on behavioral acts. Animals
must behave in adaptive ways first and foremost. The earliest protozoan must
have exhibited endogenous behavior, a basic property of animals. Action must
have evolved first, and only later been guided by sensory stimuli, perception,
learning, and cognition. Consistent with the biogenetic law, sensation and
especially cognition develop somewhat behind motoric capacities. And basic
emotions, such as pride and shame, develop before higher cognitive abilities and
therefore do not depend on them (Weisfeld 1997a).
194 The Evolutionary Neuroethology of Paul MacLean

NEURAL MEDIATION OF EMOTION

In the last few years the phylogenetic approach to the study of behavior has
been advanced dramatically by Joseph LeDoux and by Jaak Panksepp. These
investigators have adopted an ethological approach to the study of the brain.
Ethologists investigate the basic behaviors that have evolved in a given species.
An ethological approach to neuroanatomy starts with one of these basic, species-
wide behaviors and seeks to analyze its neural mediation. This is opposite to the
experimental and clinical approach of starting with a particular brain structure
and trying to determine its behavioral effects.
One advantage of complementing the experimental and clinical approaches
with the ethological approach is that the latter emphasizes a complete, balanced
view of the animal's entire set of evolved behaviors, its ethogram. Ethology,
with its focus on behavior as it occurs in natural or semi-natural habitats rather
than in laboratory or clinical settings, draws attention to the essential adaptive
behaviors of the organism. By contrast, the clinical and experimental views of
the organism's behavior are liable to be fragmented and artificial, comprising
isolated neural mechanisms such as the function of the cranial nerves and the
perception of visual stimuli. Ethology focuses on emotions, or motives, because
these generally correspond with the behavioral elements of an animal's
ethogram—feeding, mating, defensive aggression, flight, and so on.
Taking this functional, ethological approach, LeDoux (1996) traced the
neural pathway for the rat's response to fear stimuli.

Ear

Thalamus
\
Amygdala

Hypothalamus Midbrain

Figure I L L Limbic Fear Pathway

Aspects of Pride and Shame 195

In the simplest, most archaic form, a mammal typically responds to species-

specific signs of danger, such as a snake, by a defensive act, such as freezing.
Neural impulses travel from sensory receptors to the thalamus to the central
nucleus of the amygdala and midbrain (Figure 11.1). This same general route
mediates a conditioned fear response, say, to a tone that has been repeatedly
paired with electric shock.

Ear
— i —
Thalamus
i
Neocortex
— i —
Amygdala
Midbrain
hypothalamus
Figure 11.2. Neocortical Fear Pathway

This conditioned fear response occurs even in the absence of the neocortex.
The neocortex merely refines responsiveness to stimuli, so that in its absence the
rat also freezes in reaction to tones that differ from the warning one (Figure
11.2). In other words, with inadequate specification of the stimulus, the organ-
ism errs on the side of caution and freezes. The neocortex merely refines the
emotional response, but is not essential for it. Thus these neural mechanisms are
consistent with a phylogenetic analysis of the evolution and importance of the
limbic system compared with the neocortex. Analogously, the primary soma-
tosensory cortex refines localization of pain stimuli, which are less precisely
localized by subcortical structures.
Additional components of the emotion of fear are evoked through the amyg-
dala also. The hypothalamus directs the sympathetic division to orchestrate
appropriate adjustments of the viscera, and directs the pituitary to do the same
for the endocrine system. The freezing response itself, and associated emotional
expressions (or displays), are coordinated by the midbrain, which is a primitive,
196 The Evolutionary Neuroethology of Paul MacLean

brain stem structure that mediates various fixed action patterns (Panksepp 1998).
The affect of fear seems to register in the amygdala, and possibly also the
hypothalamus and limbic midbrain; the pleasure and pain centers of the brain are
confined to limbic structures. Contextual cues associated with fear (i.e., the
subject's surroundings when traumatized), are remembered by the hippocampus.
Thus the characteristic facets of an emotion—eliciting stimuli, affect, overt
behavior, emotional expressions, and visceral and hormonal adjustments—are
all accounted for by LeDoux's model.
This system seems to be representative of other mammalian emotional
pathways too, involving various senses in addition to audition. Emotions in
general are elicited by sensory input passing through the thalamus to the
amygdala, hippocampus, and other limbic structures and on to the hypothalamus
1
and midbrain. Responsiveness likewise is modified via a neocortical detour
between the thalamus and the limbic system. Thus, the limbic system and
especially the amygdala seem to have evolved to modify brain stem mechanisms
of motivated behaviors. The origins of this system are indicated by the fact that
the oldest part of the amygdala, the medial nucleus, receives inputs from the
vomeronasal organ, which responds to pheromones bearing social information.
The amygdala appears to be especially devoted to social and alimentary
emotions. Patients with amygdaloid seizures report anger, guilt, sadness, loneli-
ness, disgust, and (in women only) erotic sensations (Gloor 1997).

ROLE OF THE AMYGDALA IN DOMINANCE BEHAVIOR

It has been proposed by human ethologists such as Freedman (1967), Barkow

(1975), Mazur (1983), Savin-Williams (1977), and of course by Darwin (1872)
that the emotion of pride and shame in humans evolved from dominance and
subordination behavior in other species. This hypothesis is supported by
evidence of behavioral, expressional, and hormonal parallels between domi-
nance/submission in simians and pride/shame in humans (reviewed by Weisfeld
1980, 1994, 1997a). Do neuroscience data also support this interpretation?
What is known of the neural mediation of dominance/submission behavior in
simians and of pride/shame in humans?
Panksepp (1998) reviewed the neural pathways of various mammalian
emotions. The route for inter-male, or dominance, aggression passes from
sensory receptors to the thalamus to the medial amygdala to the preoptic-
anterior hypothalamic area to the periaqueductal grey of the midbrain (Figure
11.3). The neurons in this amygdala-to-limbic midbrain pathway are rich in
testosterone receptors, consistent with the strong sex difference in dominance
aggression (Ellis 1986). This is the same general route taken by fear, but it
constitutes a separate pathway. Likewise, the route for angry aggression (or
rage) is parallel to, but distinct from, these other two.
The amygdala seems to direct dominance and submission behavior.
Amygdalar stimulation typically enhances aggressive behavior in dominant
animals and submissive behavior in subordinates (Huntingford & Turner 1987).
Aspects of Pride and Shame 197

Bilateral amygdalar lesions in lizards, hamsters, dogs, and monkeys often result
in a decline in dominance aggression and/or a fall in rank (Kling & Mass 1974;
Kling & Brothers 1992). In one representative study, two macaques with amyg-
dalar lesions failed to form a dominance relationship (Kling 1972).

Sensory
Receptor

Tin. a.1 a m u s

Amyg dala

j
Hypothalamus

X
]Vticil>raLixT

Figure 11.3. Dominance Pathway

The amygdala is also involved in other functions essential for participation in

dominance hierarchies. These include individual recognition; some amygdalar
neurons fire in response to photographs of particular individuals in cats (Kling &
Brothers 1992). Maintenance of a dominance hierarchy necessitates keeping
track of individuals' ranks.
Another such function is sending emotional expressions (e.g., threat and
submission displays). Electrical stimulation of the amygdala in monkeys and
humans can elicit various vocal and facial expressions, including those of threat
(Kling & Brothers 1992). In psychomotor epilepsy, patients sometimes exhibit
threat displays such as hissing, spitting, stamping, teeth gritting, and fist
clenching (MacLean 1990). Amygdalar lesions can reduce dominance and
submission displays in lizards (Kling & Brothers 1992) and simians (Kling &
Mass 1974), thus showing the role of this structure as well as of the basal
ganglia in these displays (MacLean 1990). Facial displays in primates seem to
arise in the amygdala and other limbic structures and to be organized in the
midbrain and executed by brain stem nuclei via the cranial nerves (Panksepp
1998).
In addition, the amygdala seems to participate in receiving facial and vocal
expressions. Lesions can reduce monkeys' (Kling & Mass 1974) perception of
198 The Evolutionary Neuroethology of Paul MacLean

threat signals and people's perception of the emotional meaning of tone of

voice. Humans whose amygdalas were stimulated would sometimes report
experiencing mnemonic fragments of threat displays, accompanied by negative
affect (Kling & Brothers 1992).
Lastly, a wide range of affects seem to be mediated by the amygdala,
especially fear, which is exhibited by subordinate animals particularly (Gloor
1992). Psychomotor epilepsy, which involves the amygdala and other temporal
lobe structures, can result in self-reports of various other affects, as mentioned
above, including guilt, shame, and "troubled conscience" (MacLean 1990; Gloor
1992). Thus the amygdala, implicated in dominance behavior, appears to be
involved in the emotion of pride/shame. This emotion, and feelings of domi-
nance and subordination in other primates, seem to be related to brain serotonin
levels; serotonin receptors abound in the amygdala. High serotonin levels
characterize competitively successful monkeys and men, and selective serotonin
re-uptake inhibitors (e.g., fluoxetine) counteract clinical depression. Serotonin
levels rise in male vervet monkeys in response not only to a rise in rank but also
to receiving a submission display or to copulation (Masters & McGuire 1994).
On the other hand, serotonin levels fall when the male observes another male
copulating, as though the subject has been humbled. Similarly, plasma
testosterone level, which also acts on amygdalar receptors and is associated with
self-reported euphoria, rises in response to a monkey's or man's triumph (Mazur
& Booth 1998).
Thus, the amygdala appears to participate in various behavioral and affective
functions of direct relevance to dominance behavior.

ROLE OF THE ORBITOFRONTAL CORTEX IN DOMINANCE:

BEHAVIOR IN PRIMATES

But the structure that is most specifically associated with dominance

behavior is the orbitofrontal cortex (OFC), especially its posterior portion.
Consistent with its role in emotion, this is a limbic structure. Its cytoarchitecture,
connections, and early ontogenetic development (much earlier than the rest of
the prefrontal cortex) confirm its limbic origin (Fuster 1997; Kandel, Schwartz
& Jessell 1995). Further, it is affectively sensitive, as revealed by stimulation
and self-stimulation studies (Passingham 1983; Rolls 1975; Fuster 1997).
Various neurons respond to primary and secondary reinforcers; thus, frontal
lobotomy can reduce the agony of painful stimulation (Rolls 1999). Stimulation
of the OFC can elicit the emotional expression of smiling as well as pleasure in
humans (MacLean 1990). It is the only cortical area that projects directly to the
hypothalamus, where the various affects converge and perhaps are compared so
that behavior can be prioritized.
If pride and shame evolved from dominance aggression, then we would
expect the functions of the amygdala to be similar to those of the OFC and the
two structures to be closely connected. Indeed, research has revealed many
similarities between them. Like amygdalar lesions, OFC lesions in monkeys
often result in reduced aggressiveness and lower rank (Fuster 1997). Both
Aspects of Pride and Shame 199

structures receive multimodal sensory input from the thalamus and also direct
information from the olfactory bulb. Both respond to a range of primary and
secondary reinforcers (Rolls 1999). The OFC sends signals to the amygdala and
also directly to the hypothalamus and midbrain (Figure 11.4), thus both
projecting to and bypassing the amygdalar pathway for dominance. These
frontal lobe projections may contribute to emotional expression (Crosby,
Humphrey & Lauer 1962), as do downstream amygdalar outputs. Furthermore,
the OFC and amygdala are involved in the recognition of faces and facial
expressions (Rolls 1999). Electrical stimulation of the OFC, like the amygdala,
can result in autonomic changes (Butter, Snyder & McDonald 1970). And, like
the amygdala, the OFC is rich in serotonin receptors (Masters & McGuire 1994).
Serotonin receptors are more abundant in dominant vervet monkeys than in
subordinates (Damasio 1994).

Orbitofrontal
Cortex

Amygdala

Hypothalamus
I

Midbrain
Figure 11.4. Dominance Pathway with Orbitofrontal Cortical Imput

What, then, do these two structures do differently, so that both are necessary?
Morgan's canon reminds us that lower neural structures ought to be invoked to
explain a given behavior wherever possible; in phylogenetic terms, we might say
that even primitive organisms needed to fulfill all the functions necessary for
survival and reproduction, so that any capacities that evolved later had to be
elaborations of these earlier mechanisms. In general, primitive brain structures
are not superseded by later ones, but are modified by them. Nature is basically
conservative, and evolution tends to proceed by accretion, not by radical
replacement. In the case of the OFC, this structure, which is cephalad to the
200 The Evolutionary Neuroethology of Paul MacLean

amygdala and evolved later, appears to modulate the actions of the amygdala
(see Panksepp 1998). The OFC does not seem to have eclipsed the amygdala.
Indeed, the amygdala expanded in the primate line leading to hominids (Kling &
Brothers 1992), perhaps mainly to process inputs from the OFC. Chance (1961)
suggested that this burgeoning of the amygdala and associated parts of the
prefrontal cortex in hominid evolution relates to the increased complexity of
dominance competition in our species, to be discussed below.
One clue to the relation between the OFC and the amygdala may be found in
the processing of olfactory stimuli, olfaction being a primitive vertebrate sense
that partially bypasses the thalamic sensory relay station (Stuss & Benson 1986).
The amygdala receives information directly from the olfactory bulb and
vomeronasal organ (Halgren 1992; Gloor 1997). This information might include
the odor of a threatening adult male. Thus, the amygdala may respond to direct,
unprocessed olfactory releasers (i.e., it may contain more innate releasing
mechanisms). By contrast, the OFC is considered the highest-order processor of
olfactory information. The anterolateral (neocortical) part of the OFC, especially
on the right side, may interpret olfactory and gustatory information and then
pass it on to the amygdala for a more refined behavioral response (Gloor 1997).
The OFC receives input from all sensory modalities and is the only cortical
structure to do so. In sum, these neocortical regions of the OFC may act as other
areas of the neocortex do in the conditioning of emotional responses: They may
refine emotional responsiveness to stimuli from various sensory modalities.
They may provide a less direct but more precise pathways for learned emotional
reactions.
The OFC does seem to refine dominance behavior as mediated by the
amygdala. As noted above, monkeys with bilateral OFC lesions usually with-
draw from dominance encounters and therefore fall in rank (Fuster 1997). In
addition, lesions often result in behavior that is inappropriate for the animal's
rank. A dominant animal may defer to a subordinate; a subordinate may attack a
superior and seem surprised at being attacked in return (Fulton 1951). A low-
ranking operate may steal food from under the nose of a dominant one (Brody &
Rosvold 1952). Thus, bilateral OFC lesions in a group of monkeys usually de-
stabilize the dominance hierarchy.
Brody and Rosvold (1952) attributed this hierarchical disorganization to the
"disappearance or marked diminution of learned avoidance responses in the low-
status animals" (p. 415). Lesioned high-status animals might likewise fail to
retain attack responses learned previously. Snyder (1970) explained the effects
of OFC lesions as resulting from decreased aggression, inappropriate or dimi-
nished submission signaling, and inability to perceive threat signals. However,
these deficits could be accounted for by ignorance of cagemates' ranks, as
proposed by Brody and Rosvold. Recent evidence indicates that the OFC can
learn and unlearn associations faster than the amygdala (Rolls 1999), which it
generally inhibits (Davidson 2001). Thus, the OFC may mediate learning about
other animals' ranks, much as the auditory neocortex helps to identify tones
associated with pain. An OFC-lesioned animal generally avoids dominance
encounters, but perhaps from an inability to choose appropriate opponents rather
Aspects of Pride and Shame 201

than from a disinclination to compete. Sometimes a lesioned animal exhibits

heightened aggression, but still falls in rank because of a deficit in appropriate
hierarchical behavior (Mass 1972).
Another observation supports the notion of a loss of sensitivity to social
ranks with bilateral OFC lesions. A chacma baboon in which both prefrontal
areas were removed no longer exhibited jealousy when another monkey was
petted (Bianchi 1922). This sort of tripartite social comparison resembles the
effect of witnessing another vervet male copulate with a female: a lowering of
serotonin levels and hence of self-perceived rank (see preceding section).

ROLE OF THE ORBITOFRONTAL CORTEX IN PRIDE AND SHAME

IN HUMANS

The limbic orbitofrontal cortex, then, seems to be involved in dominance

behavior in simians. It also plays a major role in pride and shame in humans.
Clinical evidence in humans, including studies of various lobotomy surgical
procedures, suggests that decreased motivation for social success is a direct
effect of OFC lesions. People with bilateral OFC lesions seem unconcerned with
their social standing and reputation. They tend to be boorish, impolite, and
unrestrained, and may lie, cheat, boast, neglect their appearance, and swear
profusely (Fuster 1997). Prefrontal leucotomy patients have reported a decline in
feeling or emotion (Partridge 1950). The famous Phineas Gage was described as
lacking deference for others (i.e., submissive behavior). Such patients seem not
to be affected by the societal values that otherwise guide and constrain human
behavior. It is as though they lack dominance motivation, that is, the urge and
ability to protect, communicate, and advance one's standing by the multiplicity
of values that guide human behavior. Likewise, these patients characteristically
neglect their occupations, the highly specialized and culturally variable paths to
2
social standing.
There have been few studies of OFC lesions in children, but one such case
suggests that damage early in life appears to be permanent. A 3-year-old boy
who sustained a 3-inch incisive wound of the left eye orbit near the midline
subsequently exhibited severe and intractable behavioral problems. If repri-
manded, he understood that he had broken a rule but showed no signs of shame
in demeanor; instead, he often immediately asked for a favor. Asked how he felt
when his mother yelled at him, he replied that he did not like it "because her
voice goes up real high and I don't like the way it sounds." He used profanity
freely, and in a word association test came up with "tit" and "nigger" for words
beginning with "t" and "n." Due to his size, aggressiveness, and quick temper,
he terrorized his classmates. He had no friends; he antagonized other children by
swearing at them, throwing things at them, or knocking them out of his way.
Despite his exemplary home background and a well-ordered, superior private
school, he did schoolwork only when required to do so before being allowed to
go home for the day (from patient's medical record and observations by Carol C.
3
Weisfeld, his teacher).
202 The Evolutionary Neuroethology of Paul MacLean

As these clinical cases indicate, OFC lesions interfere with a multitude of

social acts, not just physically aggressive behaviors as in other species. That is,
the human OFC mediates the panoply of acts that affect social standing in our
species. Unlike other primates, we complete for dominance in multiple,
culturally variable ways. Physical traits count, but so do various accomplish-
ments, attributes, altruistic deeds, allies, and acts of propriety (or impropriety).
Almost any act has status value (i.e., influences one's social standing). We do
not just lunge for a piece of bread; we ask politely. We engage in elaborate
4
strategies to advance our social standing and to avoid losing face.
Where does the social salience of these various deeds and attributes register
in the brain? The learned, culture-specific values by which our acts are assessed
by others may be represented in the OFC. As discussed earlier, learned domi-
nance cues may register in the OFC of monkeys and humans. Like the
amygdala, the OFC may assign emotional valence to previously neutral stimuli,
including ranks to other individuals and prestige value to various actions and
"status symbols."
The effects of temporary derangement of this system for constraining
behavior within socially approved bounds are illustrated by some cases of
epileptic automatism. These episodes arise from ictal interference with function-
ing of the temporal lobe, and may invade adjacent structures, usually bilaterally.
The automatism may be restricted to rhythmic chewing or swallowing, or may
extend to complex, purposive movements (Gloor 1997):

[The] patient does not respond normally to social signals . . . and may therefore not
interact in any socially insightful or appropriate way with persons around him and may in
addition engage in socially unacceptable behavior such as undressing in a public place.
This probably indicates a combination of defects that are partially perceptual—not at an
elementary level, but rather on the level of relating environmental signals to the fund of
personal memories and acquired social attitudes that guide our behavior in everyday
living. This probably indicates a lack of proper interplay of temporal and frontal associ-
ation cortex with the hippocampal system and the amygdala (p. 707).

In summary, the OFC seems to modulate dominance behavior by processing

multimodal sensory stimuli and acting on the amygdala and other downstream
limbic structures. The OFC appears to mediate learned dominance/subordi-
nation cues as well as affective processes involved in success and failure.
Clinical lesions to the OFC also usually involve the adjacent, dorsolateral area
of the prefrontal cortex, and the two areas are interconnected. Therefore the
dorsolateral prefrontal cortex will be considered next.

FUNCTIONS OF THE DORSOLATERAL PREFRONTAL CORTEX

The dorsolateral prefrontal cortex is distinct, in its connections and functions,

from the limbic OFC (Fuster 1997). In laboratory studies on monkeys, dorso-
lateral ablations do not seem to affect social rank as do orbital lesions (Kling &
Mass 1974). The dorsolateral cortex has been implicated in the ability to carry
Aspects of Pride and Shame 203

out a series of actions aimed at a later objective. The dorsolateral cortex (DL) is
considered the highest level of organization of the voluntary motor system of the
frontal lobe, as will now be reviewed very briefly.
The simplest, most primitive level is the primary motor cortex in the
precentral gyrus. Neurons from this area, laid out somatotopically, send output
to the motor neurons of the spinal cord via the pyramidal and extrapyramidal
tracts. This constitutes the basic wiring diagram for voluntary action; all the
motor units are innervated.
The premotor cortex constitutes the next higher level of organization. Here
more organized, functionally meaningful movement patterns are represented.
The premotor cortex is more directly related to adaptive behaviors than is the
primary motor area, through which it operates. The premotor area mediates the
execution of functional, rather than robotic, skilled movement patterns, such as
driving a car (Crosby, Humphrey & Lauer 1962). These motor skills are
presumably built up through practice; we develop skills appropriate for our
particular environment and circumstances. The supplementary motor area,
dorsal to the premotor cortex, seems to be active when we mentally rehearse a
contemplated action, as well as while we carry out the act (Kolb & Whishaw
1990).
The DL seems to supervise and coordinate even more complex functional
actions, those protracted over some period of time. It operates through the
premotor and primary motor areas. A DL lesion might result in difficulty in
carrying out a purposeful series of actions, such as those involved in taking a
cigarette and a match from their packages and lighting the cigarette (Crosby et
al. 1962), or making a sandwich. A patient with a DL lesion might perform
actions out of sequence or perseverate at one step in the process. The DL is also
necessary for performing delayed-response tasks, in which the rhesus or human
infant must pause for some interval before making the correct response (Levin et
al. 1991). Likewise, the DL has been shown to be essential for the Piagetian
capacity of object permanence in rhesus and human infants, the ability to
remember the existence of objects that have passed from view (Diamond 1985).
The DL is one of the last parts of the cortex to develop and evolve, and is far
larger in humans than in the chimpanzee (Girgis 1971). It therefore can be
expected to mediate some of our most distinctively human aptitudes, of which
the formulation and execution of long-term plans is certainly one. The late
ontogeny of the DL is reflected by children's impulsiveness and their difficulty
in sustaining attention to a task. The prefrontal cortex grows rapidly between
ages 2 and 5 (Petrie 1952); by about age 5, children are generally low enough in
impulsiveness to enter school and sustain attention to the teacher or task. Not
until adolescence is the area fully myelinated, thus allowing for the full maturity
of sustained attention, planning, and logical chains of reasoning by about age 12
(Fuster 1997). Presumably, behavioral maturation in adulthood is largely a
matter of developing adaptive plans for practical and social tasks, and continu-
ing to refine these plans in the light of experience. Consistent with the late
evolution of this structure, it can be lesioned quite extensively without causing
204 The Evolutionary Neuroethology of Paul MacLean

very profound or even noticeable behavioral deficits, let alone death. For
example, IQ may remain unchanged (Teuber 1972).
The DL is connected with the lateral thalamus, dorsal caudate, and hippo-
campus, and with other high-order areas of the neocortex. This would allow it to
assemble perceptual information and memories of past events in order to build
up a plan of action. A person needs to remember the elements of the plan while
constructing and executing it, an aptitude sometimes referred to as working
memory and doubtless demanded in delayed response tasks. DL lesions can also
disrupt the directing of eye and head movements, which appear to be involved in
attention (Fuster 1997). Being able to sustain attention on sources of task-
relevant visual input would seem to be essential for planning. Children with
attention deficit disorder sometimes show decrements on prefrontal lobe
function tests.
What of the role of the adjacent OFC in these planned movement sequences?
The OFC seems to aid this capacity by buffering the DL from distraction (Fuster
1997). It insulates the DL from interference by extraneous sensory input, and
thus lessens impulsiveness. The observed failure of OFC patients to pursue their
occupation, or exhibit "drive" and "motivation," may result partly from inter-
ference in the planning function of the DL (Stuss & Benson 1986). By contrast,
some patients with obsessive-compulsive disorder show heightened activity of
the OFC, as though they are overly fixated on a goal (Malloy 1987; Panksepp
5
1998). Malloy (1987) suggested that their behavior is opposite to that of
sociopaths, who are impulsive and often exhibit diminished OFC activity (Fuster
1997; Pontius 1972; Schore 1994). However, attention deficit disorder may be a
more directly opposite condition to obsessive-compulsive disorder, since socio-
pathy adds the symptom of reduced sensitivity to pride and shame. The
impulsivity of sociopaths may stem from reduced sensitivity to social evalu-
ation. The sociopath is freed from the constraints imposed by social evaluation,
and therefore can formulate intentions simply and quickly.

EMOTIONAL NATURE OF PREFRONTAL LESION DEFICITS

It seems incomplete to reduce the antisocial behavior of prefrontal lobe

patients to impulsiveness and planning deficits alone, however. Again, this is not
simply a cognitive deficit, but also an emotional one, at least insofar as the OFC
is involved. OFC patients may not have forgotten the rules of politeness, but
they are unmoved by them. Sociopaths can engage in long-term planning, often
with diabolical consequences, and may feign remorse and empathy, but are
largely impervious to pride, shame, and empathy.
Emotional terms such as shame are invoked in most contemporary
explanations of OFC pathology (e.g., Fuster 1997; MacLean 1990), whereas
previously these effects were often explained as deficits in foreseeing the
consequences of one's actions or in the capacity for fear. One of the earliest
allusions to an emotional deficit associated with OFC lesions was offered by
MacLean (1949), who explicitly mentioned a decrease in guilt. It is only certain
Aspects of Pride and Shame 205

consequences that the patient fails to foresee or to care about. I once observed a
man who had suffered a stroke around the anterior portion of the circle of Willis.
He could very well anticipate the pain of an injection; in fact, he protested
vociferously and shamelessly about receiving it. Thus, he foresaw, and feared,
pain but he did not anticipate or experience shame. He was boorish and profane,
and appeared unconcerned with pursing his career as a professor—with
maintaining his social status. In another case, a middle-aged man with a frontal
lobe tumor delighted in playing practical jokes such as turning a garden hose on
his neighbors (Critchley, O'Leary & Jennett 1972). Obviously, he too foresaw
the consequences of his actions, but did not fear the outrage of his victims.
The distinctively emotional nature of OFC function may have been obscured
in the earlier literature by (1) the interconnections between and proximity of the
OFC and DL, which is involved in planning; (2) a failure to appreciate the
limbic nature of the OFC; and (3) the prevalence of behaviorism over ethology
in American psychology.
The emotional nature of prefrontal lobe function is suggested by an addi-
tional line of argument. Planning any action probably requires anticipating
various types of affective consequences, not just pride and shame. Biological
goals are emotional; we seek to execute behaviors that make us feel better. We
mentally rehearse our possible courses of action by imagining their affective
consequences, and then choose the most promising one. We also ruminate over
past successes and failures, repeatedly experiencing the affects associated with
the events, presumably so that we learn from these reenactments (Nesse 1990).
Temporal lobe seizures, probably involving the hippocampus and amygdala,
sometimes result in vivid recollections of past experiences, complete with the
original affective tone (LeDoux 1996). Then too, when we experience an
emotion vicariously, by imagining its occurrence, we tend to undergo some of
the visceral changes associated with that emotion, indicating that the
6
anticipatory experience is actually emotional and not just cognitive. If we
merely contemplated various possible action sequences, we would have no way
of evaluating them. All evaluation is affective (see Pugh 1977).
This evaluation of the affective payoffs of various extended plans seems to
involve the prefrontal cortex in humans (Damasio 1994), although other species
that lack this structure can foresee future events and formulate simple plans or
intentions. Well before Damasio, Nauta (1973) proposed that this interaction
between the frontal cortex and the limbico-subcortical axis could be, among
other things, an important prerequisite for the normal human ability to compare
alternatives of thought and action plans. This suggestion attributes to the
limbico-subcortical axis the function of a "sounding board" or "internal test-
ground" enabling man to preview the affective consequences in any particular
action he might consider (p. 312).
Consistent with this interpretation, the OFC contains neurons that fire only in
response to stimuli that have been paired with rewards. Such neurons would be
necessary for anticipating the payoff of a given course of action (Panksepp
7
1998). MacLean (1993) added some insights to this matter of behavioral
planning. First, he recognized the emotional nature of planning and the involve-
206 The Evolutionary Neuroethology of Paul MacLean

u
ment of the frontal lobe. He noted that the frontal cortex affords an endless
number of prospects that at the emotional level can induce concern and anxiety
or joyful anticipation" (p. 81). He observed that this ability to anticipate
emotional consequences is diminished by prefrontal lobotomy. He invoked the
term "envision" for this capacity and related it to the fact that the visual part of
the pulvinar nucleus is connected with the prefrontal cortex. We envision the
consequences of our actions.
Damasio (1994) suggested that the DL specializes in evaluating impersonal,
abstract plans. Social planning seems to include the OFC as well. OFC lesions
do not seem to impair the ability to solve hypothetical social problems affecting
imaginary people, but only the subject's ability to formulate his own social plans
(Bechara, Damasio, Damasio & Anderson 1994). Such a patient may deliberate
endlessly, unable to take a simple decision. Much earlier, Teuber (1964)
characterized this effect of an OFC lesion as follows: "the patient is not
altogether devoid of capacity to anticipate the course of events, but cannot
picture himself in relation to those events as a potential agent. Abnormal fixity,
or abnormal oscillation of action, other-directedness, and impulsiveness, all
could follow from such a change" (p. 440). These two abilities seem to be
developmentally distinct as well. Moore (1999) concluded that patients who
sustain prefrontal cortical damage in infancy never develop the ability to analyze
moral situations involving others, but patients with damage in adulthood may.
In summary, the OFC, acting on the amygdala, seems to motivate us to
maintain and enhance our prestige, or social rank, or self-esteem. It contains
neurons that respond to stimuli that have been paired with rewards, perhaps
including representations of socially valued deeds. The DL seems to participate
in evaluation of the anticipated emotional consequences of planned courses of
action. Anticipation of the affective consequences, for pride and shame specifi-
cally, of our planned actions appears to involve the OFC as well as the DL.

NEURAL MEDIATION OF COMPLEX SOCIAL BEHAVIOR

MacLean (1993) drew attention to another complexity of human social

behavior: our allegiance to our families. He implicated the connections between
the prefrontal cortex and the adjacent thalamocingulate division in parental
behavior. He went on to propose that parental tendencies came to be extended to
nonkin as well: "it might be supposed that a sense of parental responsibility
generalizes to other members of the species, becoming what we variously
qualify as conscience, empathic concern, and altruism" (p. 81). In sociobiolog-
ical terms, we first evolved parental tendencies, and later these capacities were
recruited in the service of kin altruism and reciprocal altruism. Unlike the
maternal behavior of most other mammals, which consists largely of fixed
action patterns triggered by releasers and primed by hormones, primate
mothering is highly flexible and empathic (Fernald 1992). This capacity for
empathy, a vicarious emotional state, may have provided an emotional impetus
for flexible altruistic behavior toward nonkin as well as kin (Trivers 1971).
Aspects of Pride and Shame 207

Accordingly, cingulate gyrus lesions in rhesus monkeys resulted in a loss of

grooming and of "acts of affection" toward others (Kling & Mass 1974). The
operates behaved as if they were inanimate, walking over them or even sitting
on them.
The prefrontal cortex may also play a role in parental and altruistic behavior.
Animals and people with prefrontal lesions sometimes lose their affection
toward their master or family (Levin et al. 1991), perhaps because of a reduction
in empathy via connections with the anterior cingulate gyrus. For example, a
man and a woman who both had sustained OFC damage in infancy were later
insensitive to the welfare of their own infants and were unable to form
friendships (Moore 1999). Another factor in animals may be loss of fear of the
master resulting from the frontal cortical damage; cf. inappropriate dominance
and submission behavior in OFC-lesioned monkeys. Dogs with prefrontal leu-
cotomies showed a loss of fear for superiors and consequently an instability of
social ranks (Fox 1965).
The OFC and amygdala seem to be involved in another aspect of reciprocal
altruism and dominance hierarchization. Social arrangements such as domi-
nance hierarchies, territories, and the exchanges of reciprocal altruism are
enforced by anger (Trivers 1971). Anger prompts "moralistic aggression,"
which punishes individuals who violate social norms regarding reciprocity,
dominance hierarchy prerogatives, territorial boundaries, possession, and so on.
(Weisfeld 1980, 1994). For example, animals whose dominance prerogatives are
usurped typically react with rage. Prefrontal ablations in apes and monkeys
sometimes result in a decrease in anger when the animal is mistreated (Damasio
1994; Levin et al. 1991), and a decline in gratitude (Bianchi 1922). Likewise,
human frontal lobe patients often do not sustain their anger (Panksepp 1998).
The functionally related amygdala may participate as well. Monkeys and people
with bilateral amygdalar lesions tend to be calmer and less readily angered—the
tameness part of the Klliver-Bucy syndrome (Aggleton 1992). Thus, the OFC-
amygala complex may play a role in the intense aggression that animals and
people employ to protect their dominance status in hierarchies and other social
contracts.

REASON VS. EMOTION: A FALSE DICHOTOMY

Because of the prevasiveness of pride and shame in human affairs, the

human OFC adds a whole new layer of emotionality to our behavior. Pride and
shame are constant, unavoidable considerations in our voluntary, motivated
behavior. When we perform an altruistic deed or avoid committing an antisocial
act, we are driven by a distinct emotion. Under these circumstances, we are not
acting purely rationally. The OFC of the limbic system exercises control even
over these "civilized" behaviors. Consistent with this idea of fundamental
control by the limbic system over the neocortex, there are many more neural
fibers going from the limbic system to the neocortex than the reverse (Panksepp
1998).
208 The Evolutionary Neuroethology of Paul MacLean

In fact, there is no such thing as a rational motive; it's an oxymoron. All

motivation is emotional, even if it entails long-term and calm deliberation (i.e.,
rational support). Our motives are the subroutines for adaptive behavior. There
would have been no adaptive point in evolving a "motive" not to be emotional,
not to strive to fulfill our various biological needs in the most efficient and
assiduous fashion possible. Our powers of rationality, of perception and cogni-
tion, are the servants of our behavioral imperatives. They can never replace or
even suppress our set of motives. If we "control" our impulses long enough to
satisfy our needs more diplomatically or effectively, this only demonstrates the
power of emotion to guide future action. In short, there is no evolved imperative
to guide behavior except for our emotions. Any such force for rationality would
have to negotiate with our affects, and so would have to be emotional itself. The
affects evolved so that the rest of our brain would know what course of action to
pursue, what motive to address next. This requires that the affects be distin-
guishable from each other, which they are, and that they be quantitatively
comparable even though they are qualitatively distinct. Where would "ration-
ality" fit into such a mechanism for comparative measurement? On what author-
ity would it preempt a basic motive such as the need for food or air? There is no
higher priority—no other priority—than fulfilling the imperatives of fitness.
Then too, how would one "learn" to control one's emotions, except through
operant conditioning, the experience of reward or punishment following a
particular act? Again, the role of emotion is inescapable. Perhaps some of this
learning occurs through observational learning, but this probably entails
vicariously experiencing the emotions of the model. Emotion also guides
memory and attention: We preferentially attend to and remember emotionally
salient stimuli. So any rational process is "contaminated" by emotional tone
(Zajonc 1984).
The misconception that rationality guides human behavior has contributed to
neglect of the basic, universal emotion of pride and shame. We need to include
this emotion in the human ethogram; it is omitted from most psychologists' lists
of the basic emotions (as is sex!). It may not be flattering to us as a species to
admit that we are subject to the sin of pride as well as those of gluttony, lust,
sloth, and so on. But it is only realistic to acknowledge this, and to recognize the
adaptive value for our own species, as well as for others, of a motive to compete
with one's rivals.
Despite the fact that we humans retained the dominance motive in evolving
from our primate ancestors, this motive became greatly elaborated in our
species. The increased complexity of our criteria for dominance was probably
related to expansion of the prefrontal cortex and amygdala. We are evaluated for
our accomplishments and contributions as well as for our physical prowess and
mate value.
The neural connections necessary for utilizing all this sociocultural
information in our planning are built up in the prefrontal cortex through various
forms of socialization, just as connections accumulate in the secondary sensory
and motor cortical areas as we acquire various perceptions and skilled move-
ments. This sociocultural information is garnered through individual experience,
Aspects of Pride and Shame 209

exposure to models of successful behavior, formal instruction about proper

behavior such as that provided during puberty rites, and even parables and jokes
that edify us about social foibles to avoid (Weisfeld 1993). We learn to formu-
late courses of action that do not result in cognitive dissonance, in the feelings of
discomfort that occur when our actions compromise our self-esteem. Psycholo-
gists speak of internalization of norms, but this is nothing more than learning
societal values about social behavior just as we learn which foods to eat and
which dangers to avoid.
Another misleading idea is that of conscience, or the superego. There is no
supra-egoistic force that censors our baser instincts, no cultural invention or
product of group selection. Rather, there is a full-fledged instinct, or emotion—
pride and shame—that we seek to fulfill along with all our other emotions. It is
certainly a powerful and pervasive emotion, as argued above. But its adaptive
value lies only in its potential to be redeemed for tangible prerogatives of rank
sooner or later. Therefore, we sometimes sustain a loss of status in order to reap
some ulterior benefit. For example, we may embarrass ourselves in our zeal to
aggress against some tormentor, or we may violate a traffic law in our haste to
get to a movie. If conscience were superordinate over the other emotions, this
sort of result would never occur.
Our kin socialize us to participate in the regulated competition of social
hierarchies and reciprocal altruism, because this is generally the best strategy for
maximizing individual fitness in human society. But our psychological allegi-
ance to these values, our conscience itself, ought not to obscure the fact that this
motive is only one among many. Confusion about the notion of conscience may
also arise because we often pursue two emotional goals at a time, and pride/-
shame is usually one of these emotions. We try to get water on a hot day without
sneaking ahead in the line to the water cooler. We try to steal a nap without
attracting the notice of the lecturer. But, again, the way to make sense of these
processes is to consider all the human emotions, and only them.

TOWARD AN ETHOLOGICAL PSYCHIATRY

In conclusion, an evolutionary approach to neuroscience suggests keeping in

mind the ancestral way of life—adaptive problems—of our species. Naturalistic
tests of neurological functioning might be devised that take into account the
highly social nature of human behavior and the paramount importance of
emotion and motivation. More specifically, it suggests that neurological tests are
needed that assess our evolved emotional capacities. This would lead to a new,
more ethologically valid set of diagnostic categories, one based on the assump-
tion that behavioral pathology usually arises as an aberration from normal,
evolved emotional functioning (see McGuire & Troisi 1998; Nesse & Williams
1994).
Further, an evolutionary perspective fosters a balanced view of the whole
organism. All of the basic human emotions, the building blocks of voluntary
behavior, are assessed. A model of only some of the emotions, such as those in
210 The Evolutionary Neuroethology of Paul MacLean

which expression is prominent, would be as weak as a model of only some of

the endocrine glands, some of the essential nutrients, or some of the bones.
Behavioral disease may seldom resolve itself into a circumscribed malfunction
of a single motive; other neural mechanisms and bodily systems may be affected
also, as in other forms of disease. But for an assessment of the patient's condi-
tion and hence a direction for therapy, it seems sensible to systematically
evaluate the function of each emotion. In particular, the neglected and yet
pervasive emotion of pride and shame needs to be expressly included in any
assessment of psychological functioning.

NOTES

1. When an emotion arises from interoceptors (e.g., hunger and thirst), the pathway
seems to originate in the hypothalamus. Nevertheless, a high fraction of amygdalar cells
in cats and humans respond to visceral information such as blood C O 2 , heart rate, and
respiration rate (Halgren 1992).
2. A possibly related symptom of frontal lobe pathology is Witzelsucht, or facetious-
ness. Although this affliction strikes all of us on occasion, it seems to be related to right
frontal lobe damage (Levin, Eisenberg & Benton 1991). It may be caused by a
combination of social insensitivity (reduced capacity for shame) and mania, which often
results from right frontal lobe lesions, that is, from greater left than right frontal lobe
activity. Clinical series cited by Levin et al. suggest that the right orbital gyrus is
typically involved. Likewise, episodes of ictal laughter apparently can result from a
stimulating lesion of the left orbital area (Loiseau, Cohadon & Cohadon 1971).
Similarly, clinical depression is associated with increased utilization of serotonin in the
lower medial prefrontal cortex, primarily on the left side; experimentally induced
pleasant thoughts are related to reductions in regional blood flow, especially to the right
prefrontal and bilateral tempero-parietal regions (McGuire, Fawzy, Spar & Troisi 2000).
3. It is possible that a lesion sustained before age 3 might not lead to derangement of
the pride/shame system because the latter seems to mature between ages 2 and 5. Other
brain areas might assume the function of the lesioned ones. At age 2 children typically
begin to exhibit concern with personal success and failure, and dominance hierarchies
gradually take shape from 2 to 6 (Weisfeld & Wendorf 2000).
4. Clinical cases such as these suggest that the OFC mediates guilt, shame,
embarrassment, and feelings of occupational failure alike. Therefore, these different
terms may not reflect evolutionarily separate emotions, but merely semantic distinctions.
For example, subjects often refer to experiencing "guilt" when privately contemplating
their transgression of social norms, and to "shame" when the offense is public (Weisfeld
1997a). The affect is likely to be identical in the two situations since apparently it is
mediated by the same neural structure (although Stuss & Benson [1986] suggested that
drive and motivation are disturbed most by pathology involving the [neocortical] medial
convexity and frontal polar structures, whereas social disinhibition seems to be most
pronounced following [limbic] orbital frontal disturbance). Likewise, a multitude of
terms are used to refer to competitive behavior in humans, including social comparison,
self-esteem, power motivation, rivalry, achievement motivation, and approval motivation.
But these terms all involve the affect of pride and shame, whether explicitly referred to or
not. Moreover, the characteristic emotional displays of this emotion—direct gaze, relaxed
demeanor, and erect posture and their antithetical expressions—are typical primate
Aspects of Pride and Shame 211

dominance displays, suggesting a single, common evolved origin for this emotion
(Weisfeld & Linkey 1985). Distinctions among shame, guilt, embarrassment, and the like
may be useful therapeutically, but they probably do not reflect fundamentally different
motives (Weisfeld 1997a). It is unlikely that more than one of these motives exists in our
primate relatives, or that humans evolved any new motives not possessed in rudimentary
form in simians (Panksepp 1994).
5. Obsessive-compulsive disorder also seems to involve the basal ganglia. Recogni-
tion of this fact provides a nice illustration of the benefits of ethological thinking. The
obsessive hand washing of patients is reminiscent of self-cleaning in animals, which
involves the basal ganglia. Rapoport (1989) reasoned that pathological hand washing
might reflect an abnormality in these structures. Indeed, patients were found to have low
levels of serotonin in these areas, and responded therapeutically to serotonin-enhancing
drugs (Wise & Rapoport 1988).
6. Nevertheless, visceral feedback is unlikely to play a major role in these vicarious
affective experiences, any more than it does in directly experienced emotions. These
visceral adjustments to emotional state doubtless evolved to set the body in an appro-
priate pattern of visceral activation, not to provide the brain with belated feedback about
its own output. Additional arguments against the James-Lange theory of the origin of
affects were offered by Cannon (1927) and remain valid. For example, quadriplegics are
not emotionally impaired by their reduced visceral feedback; they do not show affects
that are inappropriate for their situations, for example, they do not feel hungry when they
should be angry, as might be the case if affects depended mainly on visceral feedback.
For further discussion, see Weisfeld (1997b), Panksepp (1998), and Rolls (1999).
7. A recent study has offered some additional details on this capacity (O'Doherty,
Kringelbach, Rolls, Homak & Andrews 2001). Patients with OFC lesions tend to show
deficits on gambling tasks, i.e., being able to make choices based on anticipated gains and
losses. An fMRI study of normal patients revealed heightened activity in the lateral OFC
when they made a choice that caused them to lose money, and deactivation when they
were rewarded. The opposite pattern was observed for activity in the medial OFC. The
magnitude of the change in activation was related to the extent of the gain or loss. Thus,
lesions in this region may affect ability to gauge the consequences of one's actions.

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 12

THE TRIUNE BRAIN AND THE

FUNCTIONAL ANALYSIS
OF ATTENTION

Allan F. Mirsky and Connie C. Duncan

INTRODUCTION

Modern concepts of attention have evolved from earlier notions of attention as a

single monolithic function to that of a group of separate functions, each serving
a specific, articulated role in the organism's interaction with the environment.
Moreover, some theorists have posited that each specific attentional function
depends on the integrity of a distinct brain region, with the regions forming an
integrated system within the intact brain. We have proposed a heuristic model of
1
the factors involved in human attention. Our model is derived in large part from
neuropsychological findings in patients with seizures or other neuropsychiatric
disorders. MacLean's concept of the triune brain provides a remarkable
armature upon which to build a model of the organization and development of
attentional functions in the human brain. The concept of the triune brain also
provides an explanation for how this organization of attention developed from
an evolutionary point of view. In this chapter, we describe our model and relate
it to MacLean's concepts of reptilian, neomammalian, and mammalian brains.

THE EVOLUTIONARY PERSPECTIVE

The theoretical context that guides our conceptual view of the neuro-
psychology of attention is, broadly speaking, evolutionary-developmental. The
basic neural foundation for attention is a brain stem system that has existed for
millions of years, and is still present and functioning in the brains of modern
reptiles.
216 The Evolutionary Neuroethology of Paul MacLean

The model is based on the concept of the triune brain, as delineated by

2,3
M a c L e a n . According to this theory, the brain of higher mammals consists of
three interconnected tissue complexes, corresponding to major evolutionary
developments. The oldest of these is the reptilian or R-complex. Overlaid on
this is the paleomammalian or limbic system complex. The highest develop-
mental complex, manifest in the explosive growth of the forebrain in higher
mammals (and especially primates), is the neomammalian. These three
interconnected tissue complexes are illustrated in Figure 12.1.

Figure 12.1. The Triune Brain (after MacLean)

The R-complex consists of masses of gray matter at the center of the

cerebrum. Included are the basal ganglia (caudate, putamen, globus pallidus)
and their connections to the thalamic, tegmental, and pontine regions of the
brain stem. As illustrated in Figure 12.1, the R-complex is overlaid by and
interconnected with the paleomammalian complex which includes the limbic
system (amygdala, hippocampus, cingulate gyrus, and related structures) and the
more primitive (paleomammalian) cortex. The neomammalian component,
enveloping and extensively interconnected with the earlier structures, comprises
primarily the phylogenetically newer neocortex and the thalamic structures.
MacLean^ has pointed out that the brain of the reptile consists of little more
than a brain stem and several ganglia; the paleomammalian and neomammalian
"brains" are represented only in rudimentary form in the brain of the reptile.
Nevertheless, this reptilian brain supports a complex series of behaviors,
including sustained attention or vigilance. From the point of view of evolution,
therefore, the capacity for sustained attentive behavior may be present in many
species in which there is no more than a rudimentary forebrain or telencephalon.
We define "sustained attention" as the capacity to maintain the focus of sensory
Functional Analysis of Attention 217

receptors on an aspect or aspects of the internal or external environment for an

appreciable interval of time, sufficient to accomplish a task or meet a need
significant to the organism.
MacLean's analysis of the R-complex in the human brain leads to the view
that this clump of ganglia, which constitutes virtually all of the reptilian brain,
can support a variety of behaviors that could be characterized as vigilant,
attentive, and sustained. The following passage illustrates this point dramati-
cally, in the case of a giant Komodo lizard lying in wait to ambush a deer: "He
proceeds to a favored ambush site . . . Well camouflaged by his own colors and
the surrounding herbage, he hides himself about 1 m from the trail where he can
lunge forward and grip the deer . . . he remains so motionless that one might
think that he was asleep or dead . . . Finally the moment arrives! . . . (he) lunges
3 p 131
forward, grabbing a large stag by the hind leg."
As evolution progressed to other species, the brain developed additional
volume and complexity. Augmented capacity for attentive behavior was thus
overlaid on the more primitive, although in many aspects adequate, brain stem
system of the reptile. Therefore, whereas the system for maintenance of attentive
behavior in the human (or higher primate) includes limbic and neocortical
components, the brain stem remains a key component and may be the keystone
of the entire system. Additional evidence of the essential role of brain stem
structures in attention is provided by the capacity of the newborn human for
sustained visual attention, which exists well before the neocortex is fully
4
myelinated (see review by Lipsett and Eimas ); this capacity would therefore
appear to be heavily dependent on subcortical structures in the paleomammalian
and reptilian portions of the human brain.

CONTRIBUTIONS FROM THE STUDY OF EPILEPSY:

CONVERGING CONCEPTS OF THE REPTILIAN BRAIN
AND THE CENTRENCEPHALON

The writings of MacLean have emphasized the critical role of deep subcort-
ical structures in the maintenance and elaboration of numerous behaviors,
including, as we have pointed out, vigilance or sustained attention. A similar
conclusion could have been reached on the basis of an entirely different line of
evidence, namely, the behavioral and electrophysiological signs associated with
various types of seizure disorders, particularly as manifest in the clinical pheno-
menon of petit mal or absence epilepsy.
MacLean took considerable advantage of the knowledge to be gained from
the experiments in nature that comprise seizure disorders. Particularly memo-
rable is his discussion of how elaborate, articulated behaviors might occur in
complex partial epilepsy without any recollection on the part of the patient.
5
MacLean accounted for this by noting that the hippocampus, the master control
mechanism for memory, was inoperative throughout such episodes—in a
seizure-induced bioelectric storm—and thus memory function was temporarily
suspended.
218 The Evolutionary Neuroethology of Paul MacLean

6
As background, it should be noted that Hughlings Jackson enunciated the
principle of three levels of differentiation or integration of functioning of the
central nervous system. The first two levels were concerned, respectively, with
representation of body parts and coordination of movements or sensations. The
highest level of integration was a functional rearrangement of sensory and motor
behavioral components that constitute the neural basis of consciousness. Jackson
suggested that this highest level might reside in the frontal lobes or, to use
MacLean's terminology, the neomammalian brain. In contrast, the neurosurgeon
Wilder Penfield and the neurologist Herbert Jasper proposed that the third level
7
was localized deep within the brain stem or "centrencephalon."
The concept of the centrencephalic system was derived from the results of
numerous experimental studies of the electrical activity of the brain in animals.
The results pointed to a major coordinating role for midline brain stem structures
in the functioning of neural activity in the forebrain, which eventually makes
conscious activity possible. Penfield and Jasper maintained, further, that petit
mal seizures provide an example of a disorder of the centrencephalic system: the
primary manifestation of this type of seizure is a brief interruption of conscious-
ness or attention that occurs in conjunction with bilaterally-symmetrical, three-
per-second E E G discharges. A petit mal seizure was described in 1954 by
7
Penfield and Jasper :

There is a loss of consciousness which may be associated with no other outward

manifestation than a blank stare, an arrest of what one might call voluntary activity. The
return of consciousness may likewise be without sign except for the resumption of his
previous train of thought as shown by speech or action. The patient himself may have no
knowledge of the gap unless he perceives that his position has changed or his surround-
ings have altered . . . Thus, the clinician is brought to a consideration of consciousness
and unconsciousness, in spite of himself and however insecure he may feel, when forced
to pass over so much deep water on the thin ice of his own psychological insight (p. 480).

Figure 12.2 provides an example of the bilaterally symmetrical and synchro-

nous three per-second spike-and-wave E E G seizure discharges that characterize
8
absence epilepsy. These seizures were considered to be "centrencephalic" in
origin, emanating from deep, centrally-located structures with widespread con-
9
nections to both cerebral hemispheres. In Penfield's words:

Interference with the centrencephalic system of the higher brain stem produces loss of
consciousness. In the presence of deep coma due to a small critically placed local lesion
in the higher brain stem, the motor mechanism may seem to remain intact. The patient
lies in bed and moves occasionally as in deep sleep, like the enchanted "sleeping beauty"
of the French nursery tale . . . When epileptic discharge occurs in the gray matter of the
centrencephalic system of the higher brain stem, the patient is initially unconscious
because the discharge interferes with local ganglionic function . . . The system of nerve
fibers and ganglionic centers within the brain stem may be called centrencephalic since,
because of its central position, it provides symmetrical connections with the whole brain.
Through it, one may suppose that this part of the cortex, or that part, could be used
Functional Analysis of Attention

simultaneously or in sequence, depending upon the pattern and the requirements of the
existing state of consciousness (italics added), (p. 1444)

The italicized portion of text suggests that different regions of the cortex may be
implicated in different attentional functions, according to the requirements of the
situation, and relates directly to the theoretical localization of attention functions
1
in cortical areas that we have proposed.

fi
rTTTTTTTTT nnr
Figure 12.2. Bilateral Symmetrical and Synchronous Three per Second Spike-and-Wave
EEG Seizure Discharges (with permission) (see Appendix for more detail).

7
Penfield and Jasper proposed that the diagnostic label petit mal epilepsy be
replaced with centrencephalic epilepsy. In their theorizing, therefore, con-
sciousness was either localized in, or regulated by, deep brain stem structures.
The reasoning is analogous to that used by MacLean in accounting for the
memory blackout during a hippocampal seizure. In the case of an absence
attack, however, the seizure is in the centrencephalon, or, we may say, the
reptilian brain. Thus, attention is temporarily suspended. Figure 12.3 illustrates
the centrencephalic system of Penfield and Jasper, the central integrating
mechanism for coordinating and regulating the activities of the two cerebral
hemispheres.
220 The Evolutionary Neuroethology of Paul MacLean

Figure 1 2 . 3 . The Centrecephalic System of Penfield and Jasper (with permission) (see
also Appendix).

CONTRIBUTIONS FROM THE STUDY OF ATTENTION AND CON-

SCIOUSNESS: CONVERGING CONCEPTS OF THE REPTILIAN
BRAIN: THE CENTRENCEPHALON AND THE ASCENDING RETI-
CULAR ACTIVATING SYSTEM

We are struck by the similarity of views represented by MacLean's reptilian

brain and Penfield and Jasper's centrencephalon. It is also remarkable that these
two approaches converge with that represented by the concept of the "ascending
reticular activating system," originating from the reticular core of the brain stem,
10
as enunciated by Lindsley. The ascending reticular activating system is a deep
subcortical system with widespread connections to the forebrain that are crucial
for the maintenance of alertness and arousal. Figure 12.4 depicts Lindsley's
conceptualization of the ascending reticular activating system, with the reticular
formation of the brain stem forming its base.
10
Based on 30 years of neurophysiological research, Lindsley proposed the
following definition of the organization of attentional functions:

Wakefulness is maintained by excitation of the reticular formation and the ARAS

[ascending reticular activating system] through collaterals from all sensory pathways, by
corticifugal impulses originating in various regions of the cortex and by humoral factors
which affect particularly the rostral portions of the reticular formation...Attention is
closely allied to arousal and wakefulness and, like wakefulness and consciousness,
appears to be a graded phenomenon extending from general alerting, as in the orienting
reflex, to specific alerting, as when attention is focused upon a given sense mode and
dominates sensory input to the point of exclusion of other sense modes. Still higher or
Functional Analysis of Attention 221

more finely focused attention may be restricted to a limited aspect of a given sense mode
(italics added) (p. 1589)

Figure 12.4. Lindsley's Ascending Reticular Activating System (with permission) (see
also Appendix).

9
As in the case of the quotation from Penfield above, the portion in italics
presages the theoretical, functional localization of attention functions in cortical
1
areas that we have proposed.
There is thus considerable overlap among the three concepts of reptilian
brain, centrencephalon, and reticular activating system. Such overlap is to be
expected, as the three concepts all draw from the same repository of data
concerning the organization and development of attentional functions within the
central nervous system.

L O C A L I Z A T I O N O F A T T E N T I O N FUNCTIONS IN T H E BRAIN: T H E
BRAIN S T E M AND BEYOND

Our thesis is that the system responsible for the regulation of consciousness
also supports those aspects of attentive behavior characterized as "sustained."
This view is supported by the results of numerous experiments showing that the
capacity for sustained attention or vigilance is dependent upon the integrity of
the midline brainstem system (reptilian brain, centrencephalon, or reticular core
of the brain stem).
Some of this research involved the development of monkey models that
permitted direct exploration of brain structures and systems thought to be
involved in the maintenance of sustained attention. All of these experiments
involved monkeys trained to perform tests of sustained attention. They comprise
11
lesion studies of the effects of electrical stimulation of subcortical brain
12,lj
regions, and the recording and identification of "attention" cells in subcor-
14, 15
tical and cortical areas of the monkey brain. This work is described in detail
222 The Evolutionary Neuroethology of Paul MacLean

in the original publications; we excerpt here some of the key results indicating
the critical role of brain stem (reptilian brain) structures in the support of
sustained attention.
Figure 12.5 presents sagittal sections of the macaque brain, indicating the
location of electrical brain stimulation-induced effects on a test of sustained
16
attention, a monkey version of the Continuous Performance Test As shown in
Figure 12.5, critical points for inducing lapses of attention (i.e., errors of
omission) cluster in the mesencephalic and pontine reticular formations and in
the pons.
20 __j i i i i l I i

15 -I

10

o -\

lO- Lot 1.0-4.0

15-

'T-
20 IS K> 10 15 20

20 L _i_ _i_

15-

lO-

5 -

O -

5 -

lO -

15 ~i— n—
20 15 10 10 15 20

Figure 12.5. Location of Electrical Brain Stimulation-induced Effects. Macaque

Brain, Sagittal View (with permission) (see Appendix for more detail).
Functional Analysis of Attention 223

Figure 12.6 depicts frequency histograms of task-related neuronal activity in

single cells in the monkey recorded during performance of a similar test of
sustained attention. The animals were trained to respond ("go") to one stimulus,
and withhold a motor response ("no go") to another stimulus. In these exper-
iments, cells that fired only on "go" trials were labeled Type I, and were
considered motor cells. In contrast, cells that fired for both "go" and "no-go"
14, 15
trials were classified as attention-related cells. The Type II cells, such as
those seen in the lower portion of Figure 12.6, were found frequently in the
region of the mesencephalic reticular nuclei. The consensus of the results of the
various experimental approaches was that a critical area for sustained attention
lies in the medial portions of the pontine and mesencephalic reticular formation-
17
the heart of the reptilian brain or centrencephalon.

G 0 T R I A L S
NO GO TRIALS
A B

TYPE I CELL

TYPE II CELL

• A

Figure 12.6. Frequency Histograms of Task-related Neuronal Activity in Single Cells

in the Monkey (with permission) (see Appendix for more detail).
224 The Evolutionary Neuroethology of Paul MacLean

However, in addition to attention functions dependent upon an intact brain

stem, extensive research conducted over the past three decades indicates a major
role of limbic and neocortical structures in the support of attention. We believe
that the various functions of attention have become differentiated and articulated
as the brain has evolved. Our reasoning is similar to MacLean's, in that certain
"limbic" attention functions are overlaid on the reptilian or centrencephalic
brain, and that still others are neocortical and contained within the neomam-
malian brain. These, in turn, overlie the paleo-mammalian brain. Moreover, the
structures supporting these functions are inter-connected.
Figure 12.7 shows some of these structures, along with their tentative
functional roles, as assigned by our model of attentions

Figure 12.7. Structures of Attention and their Functions (with permission) (see Appendix
for more detail).

Our work indicates that it is essential to consider attention as a multi-faceted

process or capacity, and MacLean's work has suggested a model of how these
attention functions may be organized—from an evolutionary point of view. The
figure summarizes our proposal for a beginning taxonomy of attentive functions,
stimulated, in part, by MacLean's model of the behavioral capacities that appear
in the three strata of the triune brain.
Functional Analysis of Attention 225

CONSTRUCTS OF THE ATTENTION MODEL

The primary constructs of our model of attention may be summarized as

follows:
1. Attention is a complex process or set of processes. It can be subdivided
into a number of distinct functions, including sustain and stabilize, encode,
focus, execute, and shift.
2. These functions are supported by different brain regions, which have
become specialized for this purpose, but which are nevertheless organized into a
system. This system has advanced in complexity over the course of brain
evolution.
3. The system organization allows for shared responsibility for attentional
functions. This implies that the functional specialization is not absolute and that
some structures may substitute for others in the event of injury.
4. Sustaining a focus on some aspect of the environment is the major respon-
sibility of the reptilian brain, which comprises rostral midbrain structures,
including the mesopontine reticular formation and midline and reticular thalamic
nuclei. We believe that the function we have labeled stabilize, controlling the
regularity of response, may also be dependent upon midline-thalamic and brain
1819
stem structures. Sustaining a focus of attention is the phylogenetically
earliest attention function.
5. Encoding of stimuli is dependent upon the hippocampus and amygdala.
This function is supported by the limbic or paleomammalian brain.
6. The function of focusing on environmental events is shared by superior
temporal and inferior parietal cortices, as well as by structures that comprise the
corpus striatum.
7. The execution of response depends heavily on the integrity of inferior
parietal and corpus striatal regions. By MacLean's analysis, focusing and execu-
tion are dependent upon both the reptilian and neomammalian brains (corpus
striatum and temporo-parietal cortex as seen in Figure 12.7), but this requires
further study and analysis.
8. The capacity to shift focus from one aspect of the environment to another
in a flexible, adaptive manner is dependent upon the integrity of the prefrontal
cortex, including the anterior cingulate gyrus. This capacity may be a unique
20
function of the neomammalian brain.
9. Damage or dysfunction in one of these brain regions can lead to circum-
scribed or specific deficits in a particular attention function.
These nine points are the primary tenets of our attention model. Ordinarily,
the three brain layers operate together harmoniously, as a system, except when
there is a structural or functional lesion. We have written elsewhere on the use
21
of our model in studies of neuropsychiatric disorders, including schizophrenia,
22 1 23
infantile autism, absence epilepsy, attention-deficit hyperactivity disorder,
24 25
malnutrition, and parasite infection; and we believe that it provides a
valuable heuristic for both theoretical and practical clinical applications.
226 The Evolutionary Neuroethology of Paul MacLean

APPENDIX
DETAILED EXPLANATION OF FIGURES

Figure 12.1. Schematic diagram of the evolution of the human cerebrum. The
brain expands in hierarchic fashion along the lines of three basic patterns that
may be characterized as reptilian, paleomammalian, and neomammalian (after
MacLean).
Figure 12.2. The relation between a burst of spike-and-wave activity and
performance in a patient with petit mal epilepsy. The top six channels in the
tracing represent a standard antero-posterior EEG run, with electrode placements
determined by the 10-20 system. Note the symmetrical and synchronous three-
per-second pattern that characterizes petit mal (absence) seizures. The next
channel is a 1-s time mark. Below this are represented the stimuli presented to
the patient; those that required a response are seen as upward deflections from
the baseline; other stimuli appear as downward deflections. The patient's
responses are shown on the lowest channel, indicated as upward deflections. The
patient failed to respond to the two stimuli occurring during the spike-and-wave
burst, but responded correctly to those before and after the burst. Reproduced
8
from Mirsky and Tecce (with permission).
Figure 12.3. According to Penfield and Jasper, the centrencephalic system is
the chief central integrating mechanism for various areas of cortex. It is defined
as the neuron system, centering in the higher brain stem, having equal functional
relationships with the two cerebral hemispheres. The to-and-fro projection path-
ways are considered as integral parts of the system. Indicated are the connec-
tions involved in making records of past experience available (memory
mechanism) and executing voluntary movements (supra-cortical motor). Repro-
7
duced from Penfield and Jasper (with permission).
Figure 12.4. The ascending reticular activating system projected schemati-
cally on the monkey brain. The reticular formation, consisting of the multi-
neuronal, multisynaptic central core of the region from medulla to hypotha-
lamus, receives collaterals from specific sensory pathways and projects diffusely
10
upon the cortex. Reproduced from Lindsley (with permission).
Figure 12.5. Sagittal sections of macaque brain showing the location of
electrical brain stimulation-induced effects on a sustained attention test (CPT) in
the monkey. Points which when stimulated caused errors of omission on the test
(filled squares) are concentrated in the more medial portions (lateral 1.0-4.0,
upper figure) of the lower brain stem (i.e., reptilian brain). Points which when
stimulated caused errors of commission (Xs) are concentrated more in the lateral
sections of the brain (lateral 4.5-6.5, lower figure). The open circles indicate no
behavioral effect of stimulation. Abbreviations: MRF, mesencephalic reticular
formation; PRF, pontine reticular formation; MED, medulla oblongata; Col s,
superior colliculus; Col i, inferior colliculus; AC, anterior commissure; OCH,
optic chiasm; CC, corpus callosum; TH, thalamus; IC, internal capsule; Rub, red
nucleus; SN, substantia nigra; Caud, caudate nucleus; Pal, pallidum; Put,
12
putamen. Reproduced from Bakay Pragay, Mirsky et al. (with permission).
Functional Analysis of Attention 227

Figure 12.6. Frequency histograms based on the number of spike potentials

recorded during go and no-go trials in three task-related cells in the brain of the
monkey. Each histogram typically summarizes 15 to 20 trials. The black triangle
indicates the onset of the task stimulus; the interval used for summating spikes
was 32 ms. The Type I cell (top row of figure) fires during go trials but shows
no responses during no-go trials; the Type II cell (middle row of figure) is active
only poststimulus; and the Type II Anticipatory cell (bottom row of figure)
begins to fire about 1 s prior to stimulus onset. Type II cells, active in both go
and no-go trials, are thought to form part of an attention system in the brain, and
are found in many locations in the reticular formation (reptilian brain).
17
Reproduced from Mirsky and Duncan (with permission).
Figure 12.7. Semi-schematic representation of the proposed attention system
of the human brain. Functional specializations are tentatively attributed to
distinct brain regions. The assignment of function is not intended to be absolute
or exclusive; moreover, in the case of injury or disease, some functions may be
assumed by the remaining, intact portions of the system. Adapted from Mirsky,
1
et al. (with permission).

NOTES

1. Mirsky AF, Anthony BJ, Duncan CC, Ahearn MB, Kellam SG: Analysis of the
elements of attention: A neuropsychological approach. Neuropsychology Review, 1991;
2: 109-145.
2. MacLean PD: The Brain in Relation to Empathy and Medical Education. Journal
of Nervous and Mental Desease, 1967; 144: 374-382.
3. MacLean PD: The Triune Brain in Evolution: Role in Paleocerebral Functions.
NY: Plenum Press, 1990.
4. Lipsett LP, Eimas PD: Developmental psychology. Annual Review of Psychology,
1972; 23: 1-50.
5. MacLean PD: A mind of three minds: Educating the triune brain. In Chall J,
Mirsky AF (Eds): Education and the Brain. Chicago: University of Chicago Press, 1978,
pp. 308-342.
6. Jackson JH: Selected writings of John Hughlings Jackson. Taylor J (Ed): Volume I,
On Epilepsy and Epileptiform Convulsions. London: Hodder and Stoughton, 1931.
7. Penfield W, Jasper HH: Epilepsy and the Functional Anatomy of the Human Brain.
Boston: Little Brown, 1954.
8. Mirsky AF, Tecce, JJ: The analysis of visual evoked potentials during spike-
andwave EEG activity. Epilepsia, 1968; 9: 211-220.
9. Penfield W: Neurophysiological basis of the higher functions of the nervous
system Introduction. In Field J, Magoun HW, Hall VE (Eds): Handbook of Physiology,
Section J: Neurophysiology, Volume III. Washington, DC: American Physiological
Society, 1960; pp. 1441-1445.
10. Lindsley DB: Attention, consciousness, sleep and wakefulness. In Field J,
Magoun HW, Hall VE (Eds): Handbook of Physiology, Section 1: Neurophysiology,
Volume III. Washington, DC: American Physiological Society; 1960, pp. 1553-1593.
11. Mirsky, AF, Oshima HI: Effect of subcortical aluminum cream lesions on
attentive electroencephalogram in monkeys. Experimental Neurology, 1973; 39: 1-18.
228 The Evolutionary Neuroethology of Paul MacLean

12. Bakay Pragay E; Mirsky AF; Fullerton BC; Oshima HI; Arnold SW: Effect of
electrical stimulation of the brain on visually controlled (attentive) behavior in the
Macaca mulatta. Experimental Neurology, 1975; 49: 203-220.
13. Mirsky AF, Bakay Pragay E, Harris S: Evoked potential correlates of stimulation
induced impairment of attention in Macaca mulatta. Experimental Neurology, 1977; 57:
242-256.
14. Bakay Pragay, E; Mirsky, AF; Ray, CL; Turner, DF & Mirsky, CV Neuronal
activity in the brain stem reticular formation during performance of a "go-no go" visual
attention task in the monkey. Experimental Neurology, 1978; 60: 83-95.
15. Ray C; Mirsky AF; Bakay Pragay E: Functional analysis of attention-related unit
activity in the reticular formation of the monkey. Experimental Neurology, 1982; 77:
544-562.
16. Rosvold HE, Mirsky AF, Sarason I, Bransome ED Jr, Beck LH: A continuous
performance test of brain damage. Journal of Consulting Psychology, 1956; 20: 343-350.
17. Mirsky AF, Duncan CC: Behavioral and electrophysiological studies of absence
epilepsy. In Avoli N, Gloor P, Kostopoulos G, Naquet R (Eds): Generalized Epilepsy:
Neurobiological Approaches. New York: Plenum, 1990, pp. 254-269.
18. Tatman JE: Elements of Attention and Concentration in Normal Aging Adults:
Locus of Decline. Unpublished master's thesis, The American University, Washington,
DC, 1992.
19. Mirsky AF: Disorders of attention: A neuropsychological perspective. In Lyon
GR, Krasnegor NA (Eds): Attention, Memory and Executive Function, Baltimore: Paul H.
Brookes, 1995, pp. 71-95.
20. Goldstein K, Scheerer M: Abstract and concrete behavior: An experimental study
with special tests. Psychological Monographs, 1941; 53: 1-151.
21. Mirsky AF; Yardley SJ; Jones BP; Walsh D; Kendler KS: Analysis of the
attention deficit in schizophrenia: A study of patients and their relatives in Ireland.
Journal of Psychiatric Research, 1995; 29: 23-42.
22. Pascualvaca D; Fantie BF; Papageorgiou M; Mirsky AF: Attention capacities in
children with autism: Is there a general deficit in shifting focus? Journal of Autism and
Developmental Disorders, 1998; 28: 467-478.
23. Mirsky AF; Pascualvaca DM; Duncan CC; French LM: A model of attention and
its relation to ADHD. Mental Retardation and Developmental Disabilities Research
Reviews, 1999; 5: 169-176.
24. Levav M; Mirsky AF; Schantz PM; Castro S; Cruz ME: Parasitic infestation in
malnourished school children: Effects on behavior and EEG. Parasitology, 1995; 110:
103-111.
25. Levav M; Mirsky AF; Cruz ME; Cruz I: Neurocysticercosis and performance on
neuropsychological: A family study in Ecuador. American Journal of Tropical Medicine
and Hygiene, 1995; 53: 552-557.
 PART V

INTERPRETATIONS AND
CHALLENGES
 13

FROM PHYSICS AND EVOLUTIONARY

NEUROSCIENCE TO PSYCHOTHERAPY:
PHASE TRANSITIONS AND
ADAPTATIONS, DIAGNOSIS
AND TREATMENT*

James Brody
INTRODUCTION

This chapter proposes the combining of models from statistical physics with the
evolutionary neuroscience of Paul MacLean. "Chaos," "stasis," and "phase
transition" apply broadly in statistical physics and offer a platform for our
understanding of biological organizations. Darwinian natural and sexual selec-
tion, nature's reliance on two sexes, and the dynamic properties of genes,
families, culture, and morality suggest striking similarities with the phases and
transitions seen in physical systems. There is also a basis through binary and
tertiary models for MacLean's triune brain concept. Integrating these ideas from
physics, evolution, and neuroscience should provide useful insights and lead to a
unified theoretical approach for the diagnosis and treatment of human emotional
disorders.

PHYSICS AND THE REQUIREMENTS FOR EVOLUTION TO OCCUR

Introduction: Coherence and Metaphor

According to a review in Nature, statistical physics has earned 16 Nobel

1
prizes in physics and chemistry. Further, "statistical physics, and more
specifically the theory of transitions between states of matter, more or less

This chapter is based on presentations given in Boston (7/99), Manhattan (11/99) and
Amherst, MA (6/00). Thanks to Howard Bloom, Donald Mender, M.D., Ladislav Kovac,
Ph.D., for their encouragement.
232 The Evolutionary Neuroethology of Paul MacLean

defines what we know about 'everyday' matter and its transformations . . . (and)
. . . is promising to offer insights into phenomena once considered outside the
physicist's domain: traffic flow, economics, cell biology and allometric scaling
1 p 7 4
(the relation of biological functions to body mass), to name a few." '
This chapter attempts to relate a few concepts of statistical physics to the
evolutionary neuroscience of Paul MacLean. The first part establishes the
necessary concepts borrowed from physics. The second part connects these
ideas with MacLean's concepts of the limbic system and the triune brain.
Finally, the integrated model is applied to diagnosis and therapy of emotional
distress. It will be argued here that (1) some models from statistical physics
apply to human groups and individual CNS organization, (2) our developmental
paths are necessarily more channeled than we often realize, and (3) there is a
coherent physical and evolutionary model for our psychological characteristics,
a model that might inform our clinical work. The following sketch, and it is only
that, reaches across customary disciplinary gaps. In addition to bridging from
physics to biology, the following paragraphs jump several more levels to
reconstruct basic aspects of how people weave order in their lives and how we
view psychopathology. It's a stretch!
This discussion incurs the risk of our dealing with metaphors, behavior
patterns that are similar to each other only through our descriptions and
explanations of them. Life grew from simple combinations of molecules to ever
more complex ones that even at the bacterial level seem to parallel human
2, J 4 5
organizations. ' ' These similarities may be independent metaphors or it may
be that they arise from a shared statistical environment that builds and supports
only particular kinds of organizations. The similarities discussed in this
chapter—like those in statistical physics—occur at many levels of inorganic and
biological organization and may be analogous products that were sculpted,
independently at times, from different origins in response to similar environ-
mental contingencies.

Evolution Steers between Stasis and Chaos

Kauffman observes: "a phase boundary separates networks that exhibit

frozen, orderly dynamics from those that exhibit chaotic dynamics. The
existence of this boundary leads us to a very general and potentially very
important hypothesis: Parallel-processing systems lying in this interface region
between order and chaos may be those best able to adapt and evolve. Further,
natural selection may be the force which pulls complex adaptive systems into
6 p 2 1 8
this boundary region." '
Inorganic and organic molecules are not solitary but take part in decision
6, 7 8 9
networks. There are two phases in these networks, static and chaotic. ' '
Chaos is sometimes synonymous with "indecision." A person (or decision unit,
or network of units) participates in several larger networks at the same time but
there are conflicting, unresolved demands from each of them. Phase refers to a
substance's having strikingly different properties in response to just a small
Physics and Evolutionary Neuroscience 233

change in its temperature or some other environmental variable. For example,

water is one phase for groups of the molecule H 0 . Ice and steam are two other
2

phases. Networks are in a static (frozen, ordered, or unchanging) phase if

modifying the activity of a few participants has no impact on the larger network.
Network responses involve only a small part of the organization and are fast,
invariant, and of short latency regardless of the antecedent. They are
independent to the extent that there is no cascading of changes throughout the
entire system. Reflex arcs are a useful example in which the stretch receptor in
the knee triggers leg movement but with no reactions in the neck, arm, or eye.
Static nets do not evolve even if reproduced because there is no variability on
6
which natural selection can act.
In contrast, the decision units—transistors, genes, neurons, or people—in a
chaotic phase are interconnected in a manner whereby changing the activity of
6,7
one unit triggers adjustments throughout the entire network. Chaotic networks
amplify small changes but in unpredictable ways. They appear to be irreversible,
may never repeat themselves, and may never attain a new steady state. The
weather, smoke patterns, the turbulence of a flowing stream, and human lives
often show chaotic effects wherein a tiny difference in the initial conditions
leads to substantially different outcomes that will never be repeated. Chaotic
networks also do not evolve because there is no consistency that can be
reproduced after natural selection has culled some of the variations.
Evolution occurs between stereotypy (rigidity, stasis) and indecision (chaos).
Changing too quickly outruns the niche but changing too slowly entails lost
opportunities; either gambit leads to a childless heap of dried fur and stained
bones. The trick is to stay in the middle, in a phase transition between rapid
stereotypy and indecision, creating and defending linearity and coherence but
also allowing some changes with circumstance, using tricks from past
experience whether such were learned or evolved, taught by our mother or
encoded in our genes.

The Generality of Phase Transitions

Phase boundaries, also called phase transitions, are common. Our most
personal sense of one is when we float in a pool of water, too heavy to rise in the
air and too light to sink. We also find them in magnetism and conductivity and
in fluids and gases. It can be argued that water itself is a phase boundary
between steam and ice, one that is essential in order for complex life to evolve.
The earth's orbit, our atmosphere, average global temperature range, and present
climate all have the property of a phase boundary that separates contrasting and
almost limitless extremes in solidity or temperature.
There are phase transitions in the number of hours that we sleep and in
physiological variables such as heart rate, blood pressure, and in the partial
pressures of oxygen and carbon dioxide in our blood. Neural firing patterns
sometimes exhibit a narrow range of increased sensitivity to small changes in
10
input while being generally resistant to changes on either side of that range.
234 The Evolutionary Neuroethology of Paul MacLean

11 12
Traffic flow, crowd panic, and even hand clapping in auditoriums move
13
between randomness and coherence. Human life occupies a phase boundary
that runs 26,000 miles laterally but from only three miles below to five miles
above the surface of the earth, a distribution like that of a water spider. And most
important for this discussion, we show phase transitions when we organize
ourselves into groups through our logical and social computations}^

Phase Transitions Bring Symmetry to the Neo-Darwinian Model

15
Hamilton explained how selfish genes can evolve altruism, but it is also
evident that, starting with bacterial communities long ago, altruistic genes
evolved selfishness. Species and people can drift to either side of a phase
boundary and, like a tacking sailboat running into the wind, must be able to
come about. Kauffman remarks: "tentative evidence supports the hypothesis that
parallel-processing systems coevolving to carry out complex tasks . . . do in fact
6 p 232
evolve both from the ordered regime and from the chaotic regime''
Speciation itself represents a decision, a movement from a larger group into two
smaller ones and a simplification, an extinction, through the elimination of
intermediate forms.
It is possible to find "simplify" and "complicate" at many levels. For
example, we have opposing muscle groups—extensors that push things away
from us (simplifiers) and flexors that pull us together (complicators). Miller
discusses natural selection and sexual selection as processes for uniformity and
16
variation. Bloom draws a similar model with his concepts of "conformity
2
enforcers" and "diversity generators" in cultures of bacteria and human groups.
Stevens and Price discuss "distancing" of individuals; that is, you can have a
position within a hierarchy but may also participate to varying degrees in that
hierarchy, moving yourself from chaotic to static networks and back again by
17
varying your connectedness.
Thus, we should be able to distinguish processes such as aggression,
migration, abortion, helplessness, and the development of social tools or
technologies that simplify a life or a social organization from those that help it to
become more complex such as bonding, empathy, kin selection, reciprocity,
altruism, and moral codes. Individuals as well as groups and species oscillate
between degrees of connectedness, and it is another stretch but not a leap to
reconsider why moralists sin and sinners periodically hide behind morals.

The Number "3"

Minor shifts in relationships in a phase boundary steer its inhabitants rapidly

into chaos or stasis. Kauffman found that chaotic and static phases are largely a
function of the average number of interconnections between members of the
9
network and not the number of participants Having an average of fewer than
two interconnections in a Boolean net of 100,000 binary units is associated with
Physics and Evolutionary Neuroscience 235

stasis and fast but invariant outcomes from any input; an average of four or more
interconnections produces chaos and decision times of a billion years or more.
The shift between decision and indecision occurs when the average number of
interconnections is between 2.5-3.5. In this narrow range of connectedness, a
^ decision' appears in 317 msec even in networks of 100,000 participants—a
9
time consistent with biological events.
There are some fascinating implications from these effects. They suggest a
reason why we have two sexes (plus 1 dependent child for 4 years) instead of
three sexes or five. Removing or adding connections and tasks between people
will make individual behavior, respectively, more variable or less so. According
to Sigmund, 2 competitors will produce oscillations in the population frequency
18, p 5 6 - 5 9
of each of them. Add a third and the frequencies tend to stabilize for
each of them. It is tempting to speculate that any stable biological system will
have at least three mutually regulatory components such as an activator, an
inhibitor, and a switch. In a variation of this schema, some species have the
same relationships observed in the game Stone-Paper-Scissors. That is, species
18
A dominates species B and B dominates C, but C dominates A ! Increasing the
number, the diversity, of species usually increases the stability of the entire
network.

Triality, MacLean, and Neural Architecture

MacLean's evolutionary triune concept of reptilian (brainstem-striatal),

mammalian (limbic), and neomammalian (neo- or isocortex) reflects this triality
and may indeed be an expression of decision nets within evolved neural
19
architecture. After all triality is common to other psychological concepts, for
20
example, Freud's id, ego, and superego. And clinical research gives us a
tripartite set of responders, possible responders, and nonresponders to nearly any
variable. Triage has been with us since the ancient Egyptians and the concept of
21
a triune deity, a Holy Trinity, perhaps as long. Pythagoras talked about
22 23
triangles, so do modern Bowen family therapists and some ethologists. In
addition psychologists create lots of 2x2 and some 3x3 tables but derive
correlations in order to understand larger ones. We are apparently no different
from primitive peoples, 8-month old human infants, or rhesus monkeys—all of
whom keep exact count of 3 or fewer objects but turn to magnitude estimation
for quantities larger than 6 unless formal training is given in counting, a step that
changes 99 objects into a single one, rank-ordered between the two objects, 98
24
and 100.

COMPUTATIONAL PROBLEMS AND OUR SENSE OF "MAYBE"

I have mentioned examples from physics that involve liquids, magnetism, or

conductivity, parallel phenomenon exists for logical computations, one that
14, 25, 2 6
takes us out of physics and into human social behavior. Consider this
236 The Evolutionary Neuroethology of Paul MacLean

14
example from Hayes of a SAT or "satisfiability" problem: "You are chief of
protocol for the embassy ball. The crown prince instructs you either to invite
Peru or to exclude Qatar. The queen asks you to invite either Qatar or Romania
or both. The king, in a spiteful mood, wants to snub either Romania or Peru or
both. Is there a guest list that will satisfy the whims of the entire royal family?"
Hayes's protocol example translates easily into ones that contain hunter and
gatherer variables such as past resource availability, profitable search tactics
(each member is given assignments that match his or her skills: not everybody
gets to throw a spear!), and the presence of competing demands within and
between groups. Time of year, health of the participants, stockpiles of
equipment, and available technologies are all factors in the computations which
could easily become foundations for selective pressures in human groups. The
anthropologist, Sarah Hrdy, observes: "humans . . . live in families where
mothers simultaneously care for multiple young. Closer birth spacing . . .
exacerbated dilemmas confronted by mothers who must then decide on how to
27, p 2 0 3 - 2 0 4
allocate resources among dependent young with competing needs." It
is easy to imagine that any advantage in negotiating such conflicts would
translate into enhanced reproductive success.
According to Hayes, solution time varies linearly with the number of
participants but shows a phase transition related to the number of demands that
14
each of them makes. One or two demands (variables) from each participant
(clause) can be solved with linear-time algorithms and are trivial. Solution
14,
difficulty increases sharply when there are three or more variables per clause.
2 5 , 2 6
Hayes comments, "there is a critical value . . . below which almost all cases
are (rapidly) satisfiable and above which they are almost all unsatisfiable (at
14
whatever length investment is made)." The really "difficult" problems for
computational scientists or for mothers of three children are in the phase
boundary between possible and impossible, the ones that will take persistence
and cleverness to unravel. Because of conflicting social demands, we cannot
solve them easily but we can not simply walk away from them. Such problems
are the essence of the word "maybe. "

Humans Occupy Decision Networks

7
Langton remarked once that life evolves to the edge of chaos. People and
species are similarly guided. In good times and in moments of speculation we
take on more tasks, but dump the excess in bad. Unlike Kauffman's transistors,
humans move themselves into greater or lesser degrees of involvement with
other humans, serving their own self interest by either maneuver. This steering
is accomplished by genes, receptors, channel capacity, hormones, social
learning, sudden changes in status, and our executive functions. (Further,
blocking these personal maneuvers elicits substantial affective distress!)
Mercenaries, bounty hunters, and outlaws are guided primarily by their
immediate self interest. At the opposite extreme, Hamlet was immobilized, split
between his own ambition and loyalties to other people. He became a western
Physics and Evolutionary Neuroscience 237

icon for chaotic indecision. He has his equals in the anonymous many of us who
dare not act without first consulting every relative and every neighbor or who
are paralyzed by the conflicts between our self-interest and our duties to an
abusive partner. Mothers who do not allow hierarchies between their young
children and women who go directly from child care to attending their ailing
parents also lose themselves in a steel web of conflicting duties and incompat-
ible agendas.
Disconnecting allows an independent decision to do or don't do, one that
occurs without disrupting the rest of an orderly network; chaos and indecision,
however, are characterized by the words "reactive," "convulsive," "unpredict-
able," or "endless." A bias toward indecision is reflected in words such as
"cooperative," "mutualistic," "rule-bound," "traditional," "other-directed," and
"enabler." Sensitive people sometimes immerse themselves in chaotic networks
but feel "ambivalent", "confused," "guilt-ridden," or "helpless." Once people
are wrapped in a network, more extreme conditions of unpredictability elicits
panic and words like "trapped," "overwhelmed," or "paralyzed."

Tracking Our Individual Phase Transitions

Ball remarks, "The point is that phase transitions are global and abrupt—they
show matter behaving at its most nonlinear, with effects quite out of proportion
1
to cause." Given the power of phase transitions, it is small wonder that we pay
so much attention to adjusting our task loads and personal ties, that we generate
so much affect in connection with those adjustments, and that we have such
ambivalence about them and argue forever about free will vs. determinism,
selfishness vs. sharing, and men vs. women.
Events on complexity's scale, like water to a fish, surround us so much that
we must balance our lives within it. Therefore, we have tactics—conscious and
unconscious, volitional and not—that help us to navigate between confinement
and isolation. Such tactics are emergent in our self-talk, our language that
explains to our self what we did. The words "simplify" and "complicate" merely
head the index of a long list of words that describe variations in our
connectedness.
Slack time? Most of us validate the expression "Work expands to fill the
time available" with hobbies, new relationships, and incomplete obsessions. On
the other hand, if we are overwhelmed or short of resources, then our emotions
and our executive functions rearrange priorities, make lists, shunt work off to
other people, or discontinue tasks. Even an essayist straddles a phase boundary
between monotony and circumstantiality when she manages the number of ideas
—probably an average of 2.5—on the page at any one time. If we don't use our
executive functions for these decisions, we feel "overwhelmed" or want time for
ourselves. Anger or depression, guilt, or denial will then automatically adjust
our task list on the basis of immediate self-interest instead of more long term
outcomes.
238 The Evolutionary Neuroethology of Paul MacLean

Isolation increases personal instability. In human lives, impulsiveness and

stereotypy are associated with developmental immaturity, illness and its
residuals, drug or alcohol abuse, senescence, injury, depression, being alone,
having no further resources at risk, being rushed for time or selfish and
overconfident. It is also noteworthy that suicidally accompanies all these
factors. It may be that suicide is best understood both as a form of migration and
as the ultimate simplifies
Many of these phenomena may reflect an erosion of cross-talk between the
various decision units of a human mind. Eibl-Eibesfeldt gives fascinating
examples of these effects, taken from Ertel's study of dogmatism in German
politics during the Nazi era and in Nietzsche's writing during alternating health
28, p p 4 6 - 5 0
and syphilitic crises. Along these lines, solitary confinement in prison is
29
associated with higher risks of psychotic episodes and suicidal attempts.
Jamison records many examples of poets, novelists, painters, and composers
who were unstable to the extent of suicide although it is unclear how much
30
social isolation was a cause or a result of their instability. (Indeed, each factor
may feed the other.) Sensory deprivation research in universities was halted
because of its destabilizing effects on randomly selected college students, effects
29
comparable to those of prisoners in solitary confinement. McGuire and Troisi
also show the frequency of bizarre behavior by a mental patient, displayed as a
29, p 7 6
function of the number of observers. There is, consistent with Kauffman, a
sharp drop between two and three observers! "Independent scholars" demon-
strate some of these effects and social isolation is sometimes associated with
their creativity. Along similar lines, Kuhn observed that paradigm shifts come
1
from either younger scientists or from older ones who are new to a field/

Making a Phase Transition: Our Favorite Tools

Temperature, water availability, and atmospheric gases all vary both

randomly and systematically in relation to their contexts. So do competitors and
predators whether viral or furred and because of high rates of mutation, drift,
migration, and environmental stress, so do genes. This variability must be
managed for the daily pursuit of our self-interests as well as our long-term
survival. Further, survival and evolution require that we seek variety and new
opportunities. Thus, our rudders oscillate between novelty and familiarity and
consist of some evolutionary processes (natural and sexual selection) and some
of their products (alliances and hierarchies; genes, receptors, learning, and
mental executive functions). I suggest that natural and sexual selection operate
at a species level and across generations whereas alliances and hierarchies
achieve for an individual what natural and sexual selection do for a species.

Natural and Sexual Selection: Steering Left or Right Across Generations

Natural selection corrects for mismatch between niches and individual traits.
Therefore, in a stable niche it eventually reduces differences between indivi-
Physics and Evolutionary Neuroscience 239

duals. Small differences in traits for obtaining food or avoiding predators lead to
cumulatively greater numbers of offspring who carry the more advantageous
characteristics.
On the other hand, sexual selection increases variation and operates in a
different niche, one that consists of the receptors of possible mates. Receptor
systems are sensitive to small differences between individuals of the same sex.
Small gradations are magnified as only one participant successfully mates out of
32
10 or a hundred contenders in each generation.
Receptors alert predators as well as mates and predation helps ensure that
costumes (size, brightness and contrast, symmetry), activity level, and resources
16
are correlated with both survival and with healthier children. If you draw atten-
tion to yourself and are clumsy, you will probably die sooner. It is, therefore, no
surprise that displays interact with niche abundance and with predators. Safer,
richer environments and high population turnover lead to both fancier costumes
and greater behavioral variability that explores settings to their limits. Bad times
erode the advertising budget and we all slink when in dangerous neighborhoods.

Alliances and Hierarchies Manage Individual Differences within a

Generation

The structural variability of the brain does not usually affect gross anatomical features
that are characteristic for the animal species. But the size and position of cortical areas,
the distribution of neurotransmitters, and peptides, the thickness of fiber tracts, the
number of neurons constituting a nucleus, the recruitment of muscles during stereotyped
behaviors such as locomotion, and particularly the microanatomy of neurons and
neuronal circuits vary significantly from individual to individual in virtually all animal
3 3 p 10
species. '

One part of the brain, the anterior commissure...varies seven-fold in area between one
person and the n e x t . . . the massa intermedia . . . is not found at all in one in four people.
The primary visual cortex can vary three-fold in area . . . our amygdala . . . can vary two-
fold in volume—as can our hippocampus . . . Most surprising, our cerebral cortex varies
34, p 143
in non-learning impaired people nearly two-fold in volume.

35
It appears likely for many reasons that a "universal human nature" is an
assembly of traits that does not exist in an individual human or perhaps even
within groups of them. Alliances and hierarchies manage differences between
people within each generation; they make corrections that correspond to those
made between generations by natural and sexual selection.
One explanation for hierarchies is that they minimize spilled blood within a
36
group; dominance and priority are decided by ritualistic displays. Hierarchies
also, like sexual selection, magnify differences in the consequences experienced
by each participant. Small disparities in ability have large effects on differential
reproductive success because dominant members inhibit reproduction by
subordinates. However, a third explanation can be offered.
240 The Evolutionary Neuroethology of Paul MacLean

We are genetically and psychologically different from each other and, like
bacteria who swap packets of DNA when distressed, we help each other.
Differences between people lead to economic and social exchanges. As Krebs
and others have pointed out, we offer things that are easy for us to make in
37 38 39
return for goods and services that are difficult. ' '
While alliances allow mutual aid, they also slow things down. As in
Kauffman's simulations, organizational slowing will occur as soon as 2 parties
begin to work as equals for a common goal. Further, decision times will
accelerate indefinitely as you include a 3rd, 4th, or more members, each with
conflicting demands. (The same temporal changes are also seen in SAT
problems.) Humans make hierarchies within a few moments after a social
contact is made and prevent an explosion in the latencies of decisions made by a
group. Seven individuals take the lead from one or two. Debate shortens in
primate troops, human regiments, academic committees, and families. Amy tells
her little brothers what to do and life continues with less interruption for her
mother.

Weaving Self-interest and Morals at the Edge of Chaos

Ed Wilson commented to Bob Wright, "I've always wanted to transform

40 p 138
messy subjects into scientifically orderly subjects." ' It is perhaps no
coincidence that Ed has been fascinated with weaver ants for much of his life.
Like Ed and his ants, we each weave our own structures by exploring,
collecting, and modifying the things around us in a process of active Darwinism,
41 4 2
' one that also glimmers in the phrase "free will." Even singletons and
hermits walk this same course, filling their worlds with pets, collections, and
dreams when other people do not fit in.
Stasis and chaos are managed by cooperative or selfish gambits in searches
for a balance of variation and linearity. Genes and receptor systems are one
foundation of that search. However, some new toys—learning, our mental
executive functions, culture, and morals—allow humans and chimps to speed
their experiments, conduct them more systematically and retract bad ideas
without fatalities. Our sense of maybe is one result, science is another. While
female ducks might grow iridescent feathers through sexual selection over a
hundred generations, some hominid women can change lipstick twice in 3
minutes for the same reasons. The ducks may go extinct in order to shed their
markers, women usually do not.

Genes

Genes are an accumulation of receptors and strategies that worked in our past
and that may be needed again in our futures. They stabilize us across niches and
generations and narrow the range of our likely responses so that we are less
random and more apt to use behaviors that have worked for us in the past. Genes
Physics and Evolutionary Neuroscience 241

are functional parallels to a weaver, taking nucleotide fibers and aligning them
into a single experience that can be acted upon by other experiences. Because of
genes our future behavior is less chaotic and more orderly than might be
expected otherwise.
Linearity is observed in physical development as well in the behavior of
identical twins, but it is true that different outcomes can be elicited by varied
43
environments from a common set of genes. Skomer voles will be aggressive or
tame as a function of their rearing and some grasshoppers will be fat and
10
wingless or lean and winged as a function of their diet. It is as if the same
genes can work either side of a phase transition. However, genes have a range of
normal variability that is often small or that leads to very predictable bifurca-
tions, not purees, in response to variations in niche conditions. As Darlington
observed, genes will give you a stomach in one place and a liver in another but
44
never produce "stiver" in between.

Receptors

There is some evidence that receptor characteristics—whether for serotonin

or for sparkles of light—are more stable than effector sequences. C.U.M. Smith
describes approximately 14 types of serotonergic receptor and dates them back
45
700 million years and their precursors back perhaps 2.5 billion years. The
receptor characteristics of our ancestors, mates, and predators shaped and shape
us three times—once through long intervals of phylogeny, again through the 9
months after our personal conception, and again every day between our birth
and death.
Receptors, whether for glucose levels, a suitable mate, or an insect automati-
cally make priorities for us, anchoring us to tasks and locations through
neurochemistry and conditioning. Satisfying our receptors often "feels good"
and guides us on searches in a manner that underlies active Darwinism. Given
the conservatism of receptor systems and the variability seen in genetically
based response sequences, careful study of receptor mechanisms may be a more
reliable cue to our phylogeny than any schema founded on either bones or
behavior "modules. "

Executive Functions

Executive functions are the most newly evolved, most variable between
individuals, and most newly analyzed tool that we have for pursuit of our long
term self-interests. Working memory, word retrieval, a sense of time, task
prioritization, regulation of affect, and our ability to sit under a tree while we
analyze situations and synthesize novel solutions—all are thought to be aspects
46 47
of human executive functions. ' We make a stack of tasks to be done, arrange
them in temporal priority, and return to our stack if we are interrupted. An
infinite array of stimuli are filtered and organized and reactions are delayed or
242 The Evolutionary Neuroethology of Paul MacLean

implemented in a process of continuous negotiation between self interest and

external demands.
Abrupt, go/no-go decisions are inhibited as a wider array of inputs is
considered. We discover "maybe" as we accumulate memories, experiences and
consequences, form alliances and with all of these aids, look at more options
before making an irretrievable commitment. On the other side, we do not spend
so long pondering all likely outcomes that we fail to make any response at all.
Thus, we steer along the phase boundary of maybe but from two directions,
whether we are with no obligations or mired in the affective slop and goo of
primate reciprocities.

Strategic Bias: Men Scatter, Women Gather?

Although there is overlap between human males and females in every

48
behavior including lactation, there are also differences in the average
49
performances shown by each group, perhaps hedging our species' bets by
exploring "maybe" along parallel tracks. One explanation for two sexes is that
they follow opposite boundaries of a phase transition while collecting resources
and scattering gametes but with complementary tactics, sharing their respective
gains. The partnerships between men and women, however contentious, could
mean that whenever one sex is successful, the other benefits. (And so does our
species.)
Axons: Males and tools—jokes to slogans. Allman points out that neurons
reduce information: many influences are carried into the dendritic tree and
50
condensed into a do or don't-do by a uniform pulse down the axon. We can
expect that any single neuron will simplify a decision network just like, as
50
Allman points out, a bacterium or a stock broker. This same process is
reflected in the aggregate behavior of males and females!
Males are usually more active and independent than females all through
school and their reproductive years. Males hold an order of magnitude more
51
records in literature, music, the arts, and athletics from mutual competition. It
could be said that males are biased towards impulsiveness and motor output
rather than towards motor inhibition. Some of this outflow is verbal. Younger
males interrupt in class and older males tend to dominate politics and religion,
transforming the jokes of youth into slogans that may achieve goals of
dominance and popularity, the same goals originally met by the jokes. Males
often interrupt and emit more words but females are usually superior in both
9
receptive and expressive abilities* The interesting possibility exists that males
make announcements to other males that neither the sender nor the receiver
comprehends fully and women listen not for content but for thought order, word
flow, and hints of sincerity and kindness.
"Making a mark" means exerting leadership in the arenas of religion,
politics, the arts, or law. It is plausible that much of our legal edifice, tax codes,
political traditions, scientific, and religious beliefs are a byproduct of guys
showing off against each other. There are also significant implications not only
Physics and Evolutionary Neuroscience 243

for creativity and invention but also for the opposite phenomenon of
organizational incompetence in which males exaggerate personal assets but
51
minimize those of their competition, a strategy that closely parallels the lies
that we tell in courtship, politics, and sometimes before armed conflicts.
Dendrites?: Females—rules and networks. Females appear to have a bias
towards monitoring environmental details, reflected in their superior incidental
52
memory and recognition for subtle cues from other people. Their sense of
smell is keener than that of a male and they are usually better at recognizing
53
discord in the facial expressions of other women. Females are usually more
compliant than males and better able to sit at desks and follow teachers'
directions through school. While human females take in a wider spectrum of
influences before acting, both verbal rules and social networks limit chaotic
outcomes for them. This "bias towards chaos" is honored in recognition of
feminine sensitivity but ridiculed with talk about their shopping, driving, and
changing their minds.

Learning, Family, and Culture

Learning tracks the environment more immediately and specifically than if

we relied solely on genes or hormones. The memory from a half second ago
guides our next response as we search for linearity, whether in a fight or a
banquet.
Family and peers are sometimes considered to be in opposition to one
47
another but both confer stability either across generations or within a group of
the same chronological age. Parents and peers do complementary things; they
can also substitute for each other but with more static or chaotic outcomes,
respectively, and encourage the chances of survival should either one be
missing.
The tools and rules of culture are functionally the same as genes, family, and
peers but work over intermediate amounts of time. All guide us to use first the
solutions that appear to have worked in our pasts. All stabilize the behavior of
individuals and groups of individuals across time and niche changes.

Morality

Chaos and stasis helped structure our genome and became unrecognized
pillars for our conduct and how we view it. Moral codes are a spun web that
sanctions both initiative and restrictions on it. In human relationships and
cultures the fences around personal action include tradition, rules, memories,
and fears about pain, sickness, or confinement. They also include spite, guilt,
shame, and worry about what might happen to our children.
People who are surrounded by reactive networks but ignore them see
themselves as independent or self-actualizing but may be punished as
"impulsive," "unilateral," "inconsiderate," "egoistic," "narcissistic," "selfish," or
244 The Evolutionary Neuroethology of Paul MacLean

"uncooperative" by the other members. On the other hand, that same individual
will appear average in a disconnected network where he bothers very few people
at any one time. There can also be an overly cooperative individual in a static,
disconnected network, distressed by the lack of reciprocity but working
excessively to create and maintain it by complicating everyone else's lives!
Constrained actions and actors generally receive greater social approval in
such words as "responsible," "dependable," "cooperative," "thoughtful," and
"mature." We each find exactly these sentiments in our personal Greek chorus
that prompts, praises, and scolds us. There is also a tendency for the dissipation
of human and natural resources to be judged as bad except in displays such as
weddings and holidays.

KAUFFMAN'S PHYSICS AND MACLEAN'S EVOLUTIONARY

NEUROSCIENCE: TOWARD DIAGNOSIS AND THERAPY

The power of Kauffman's analysis lies in the generality of the phenomena

that it describes, whether in computer simulations or in personal dilemmas.
Thus, we can have unstable networks in human groups or within a human mind;
the rules should be the same in either world. The model also combines nicely
with a sketch of MacLean's model of the phylogenetic changes in the ways
species solve adaptive problems. When extended to humans, a coherent "DSM
5 4
V " may result!

Diagnosis and a Foundation for DSM V?

Modularity—the concept that we have specialized routines for accomplishing

survival tasks such as hunting, mate selection, managing plants, rearing children,
and other chores—will some day lead to an appreciation that every human has a
unique mosaic of traits. We not only look different, we act different. Such an
appreciation will enrich both our labels and the assistance that we given to each
client. However, I ignore the intricacies of "modules" in order to simplify the
description as presented in Table 13.1. The 3 columns in the table correspond to
(1) immobility, (2) stereotypy, and (3) the transition between them. The rows
attempt to arrange our miseries in a plausible phylogenetic order and to the right
or left side of the center column as a function of relative impulsiveness or
constraint. (Please note the order is approximate and applies within mammals).
 T A B L E 1 3 . 1 : A P h a s e Transition and P h y l o g e n y
Chaos | Phase Transition | Stasis
Paralysis from indecision. W N L re a d a p t i v e c h a l l e n g e s Unilateral, stereotyped, short
Rapidly shifting incomplete latency behavior
strategies, excessive response
inhibition after minor inputs
Hypochondria, free-floating Self-maintenance: Specific phobias: Poison,
anxiety, Cleaning, movement animals, insects, e x c e s s heat,
helplessness, feeding/hunting, c o l d , fire, w a t e r .
illness/waiting. self-defense. Escape.
1
" D e p r e s s i o n ' s e c o n d a r y to Variable activity level H y p e r a c t i v i t y in n o v e l o r r i c h e r
illness settings, mania. O C D ?
R-complex?
Withdrawal, submission. Self D e f e n s e , territory, Assault
E x p e c t a t i o n s of task failure. dominance, submission, short Excess displays (dominance &
Social phobia, term mating, escape, migration mating).
D e p r e s s i o n f r o m territory or Agonic hierarchies T e r r i t o r i e s e x c e e d ability.
mating defeats Migration/suicide
Limbic?
E x c e s s Guilt. Peer & family bonding, long- Antisocial PD, borderline PD,
Dependent PD, term mating. O C P D , narcissistic P D .
avoidant PD, Alliances/hedonic hierarchies. Grandiosity, spite,
"enabler," Delayed reciprocity, raise-the- selfishness, rejection sensitivity.
e x c e s s i v e humility. stakes. Depression, suicide
D e p r e s s i o n (social failure, Child investment,
a n t i c i p a t e d r e s o u r c e loss) Economic swaps
T e a m hunting & gathering
Neocortical/Orbital
Inconsistent use of routine Executive functions refine paleo Excess reliance on a few
behavior, highly "other-directed" tasks via language. adaptations
"To be or not to be," an endless Delayed gratification, task Narcissistic P D
question sequencing, affect regulation, OCD
planning. T a s k s p e c i f i c , rigid i n h i b i t i o n s .
Social e x c h a n g e of information Residuals of infection
Senescence
246 The Evolutionary Neuroethology of Paul MacLean

Column on the Left: Creatures of "Us"

Anxiety and social confinement are associated with fretting, worry, and
generalized inhibition of coherent behavior. We can be indecisive or we can
revert to more primitive thinking, becoming even more helpless and forgetful
and failing to make subtle distinctions or to engage in problem solving. We look
for allies to protect us, to arrange our lives, or to pick up our load. Constrained
behavior—anxiety disorders, many depressions, and some of the personality
disorders—nest with the "internalizing" ones.

Column on the Right: Creatures of "Me" and of the Moment

Impulsive behaviors—defined not on the basis of speed but of inaccuracy

and a failure to consider other people and delayed consequences—include
mania, dysthymia, some of the personality disorders, and some aspects of
ADHD. They generally overlap with "externalizing" disorders. Injury, immatur-
ity, aging, infections and their aftermath, developmental arrest, depression,
grandiosity, and genomic imbalances are plausible foundations for impulsive,
ratcheted behavior. Small children and childish adults (some of the personality
disorders, some criminals, and people in a manic state) tend to sever reciprocal
ties, exerting unilateral initiative while minimizing concern for other people or
the environment.
Some drugs simplify the user's life, either by eroding worry, guilt, and spite
(alcohol and cannabis, the benzodiazepines, the antidepressants and mood
stabilizers) or by increasing initiative and improving sustained attention (the
stimulants, mood stabilizers, and one of the atypical "neuroleptics,"
risperidone). The more primitive expressions of this bias may be reflected in our
experience of traumatic avoidance learning, food poisoning, PTSD, OCD
(safety, hoarding, and cleansing rituals), or escape (migration and suicide).

Alternating from Center to Left or Right and Back Again

Miller discusses "protean behavior," nearly random sequences of behavior

that are useful for escaping predators, developing novel solutions, or for
55
exploring new settings. Creative brainstorming, daydreams, and moments of
hypervigilance and racing thoughts are momentary trips further into chaos;
utility depends on aligning their content with practical requirements. Doing so
can produce new art forms or advertising campaigns or the invention of
56
polymerase chain reactions.
Physics and Evolutionary Neuroscience 247

The Rows: A Phylogenetic Sketch; Behavior We Share with Bacteria

We are still tubes that follow our mouths. Even before we were worms,
however, we were viruses and bacteria. We were active or waiting, advancing or
retreating. We signaled success and replicated or after a failure, waited for better
times or explored another niche. We also formed organizational nets with
impressive capacity for parallel information processing and collective problem
2
solving. Thus, activity level, initiative, sleep and appetite, and avoiding the
stench of death are all recursive elaborations of very old mechanisms. The same
holds true for our reactions to allergens, poisons or to a glut of food. Depression
may well have started as being poisoned, hungry or thirsty, too hot or too cold or
too alone. Imagine salmonella discovering thawed hamburger after a period of
starvation. Would they have a manic episode? Probably. And lithium would
probably calm them down.

Structure and Variation in Mammals

MacLean defined a triune brain in which the brain stem and striatum, the
limbic system, and the neocortex are seen as three stages in the evolution of the
19
human brain. It seems reasonable to expect different behaviors from each of
them. Erratic sleep cycles, helplessness, deep pain, nausea, and physical harm
disturb insects, lizards, mice and men. It is tempting within mammals to extend
this analysis to reproduction, mother-infant attachment, grooming, social
alliances, and economic swaps. However, pioneering analyses such as
MacLean's have some dangers.
First, our common sense will mislead us about physical and behavioral
relationships. For example, the geneticists have found that whales and hippos
are siblings! This kind of surprise is also seen in clinical research. An array of
behavioral problems from depression to guilt to grandiosity to OCD to weight
and sleep regulation all respond to changes in serotonin. A family of discomforts
has been defined by their responses to a single medicine and we, after listening
57
to Prozac now have the concept of serotonin spectrum disorders that provide a
single umbrella for our emotional whales and hippos. This is not a unique tale.
For millennia we considered illness to be an outcome of damnation rather than
of germs and contaminated water. As with Prozac and depression, a new tool—
the microscope—ended a superstition and a stack of books, written by the
authorities who practiced it, moved to the history section in the library.
Second, evolution is disorderly. It is noted for redirecting an existing
structure rather than designing something from scratch for a new purpose.
Further, we are just beginning to unravel the extent to which retroviruses and
reverse mutations scribbled freely in genomes. This latter phenomenon makes it
possible for a physical trait to appear, then disappear back to an earlier form, and
then reappear. Thus, tracing a reflex through time and arranging a phylogenetic
order for it becomes very difficult since those traits are usually more labile than
58
sensory or physical ones.
248 The Evolutionary Neuroethology of Paul MacLean

Third, overlaying and highly interconnected evolutionary elaborations such

as the striatum, limbic system, and neocortex are not surprising when evolution
refines basic interrelated components that have been there for a long time.
Capping the entire striatum with a cortex could have resulted from a change in a
homeobox regulator gene, one that operates early in ontogeny and affects many
cell types and physical structures but now operates one more time, one step
further removed from the brain stem. It is possible that such a genetic change
would be relatively simple, one that does not instruct the creation of entirely
new systems. Epigenetic instructions might need merely to state "do it again one
more time" after elaboration of the limbic areas. In another section of the
ectoderm, our fingers, hand, wrist, and forearms can be seen as the repeated
splitting of an upper arm bone—a process mirrored in our legs, ankles, feet, and
59
toes. Our cortical layers may allow an increase in resolution similar to what we
observe in our fingers because the cortex is a step or two after the decisions that
first sculpted a brain stem. Did we get fingers at about the same time that we got
a cortex?
One result is that we can expect highly similar modules at all levels of the
CNS; any new ones may come from doing old things in a more elaborate way,
possibly the product of genetic instructions that add a layer to old neural
structures and, via local decisions between the layers, connect them in a more
complex way, almost inevitably slowing decisions while enhancing the
emergent qualities of thoughtfulness, cooperation, and a sense of maybe. At the
same time, global diagnoses for one disorder or another will fragment into more
modular, more specific ones. The refinements that we see in learning disabilities
will also be discovered in characteristics, and possible adaptations, such as
mating, spatial orientation, child care, plant awareness, and so on.

MacLean's R (protoreptilian) Complex

The R-complex, which designates the forebrain striatum as integrated with

the neural chasis (midbrain, hindbrain, and spinal cord), may govern much of
our ancestral behavioral repertiore. Our sensitivity to personal helplessness, the
rustles and scent of a predator or of a lover, the salty velvet liquor of blood, the
distressed look of an infant—all possibly started about the same time that we
gained fur and feathers. We might expect such old stimuli to elicit fear
sequences that condition quickly, extinguish slowly, and are not particularly
open to verbal interventions. Pavlov's results with interoceptive conditioning
had many of these characteristics. So do the traits associated with post traumatic
stress disorder.
60 61
Biologic motion, sensory filters, and fragmented Jungian evolutionary
62
research findings all suggest that innate stimuli exist for humans, stimuli also
powerful in other creatures and that, after a single reinforced trial, may elicit
disproportionate waves of fear, immobilization, anxiety, disgust, or anger in one
direction; elation, silliness, curiosity, pride, and arrogance in another. Some of
us exclaim "gross" or "I'm going to throw up" at the thought of a news item
Physics and Evolutionary Neuroscience 249

about water leaking from coffins that were removed from an old cemetery. If we
consider that we share receptor mechanisms, there is less surprise that most of us
will nurture a helpless chick or baby squirrel or that one species may protect the
young of another.
It is a step from sensory guides to the motor and communication sequences
that satisfy them. Our daily posturing, our advances and retreats, and many of
the large motor sequences that we display when making a sale or standing in line
for a cup of coffee are recognizable by our dog or cat and possibly by a lizard.
Reptiles may share our foundations for assertion, claiming territory, courtship,
and submission, finding a home, establishing and defending territory, ritualistic
displays for dominance, defense or surrender, triumph, hoarding, greeting, social
19
groups, flocking, and migration. (Any temptation to include lizards in our
lineage is often panned. However, mice—a close genetic relative to humans—
6
have homeobox regulator genes that are similar to drosophila and to humans! ^
6 4
If we share these fundamentals with drosophila and other bilaterally symme-
trical species, we may as well include Komodo Dragons in our family!)
Despite the wired characteristics of the brain stem, it is open to definition by
outer experiences. Because of this feature, we can travel a life course of either
impulsiveness or stability as a function of early events. And more immediately
from moment to moment, we repeat whatever it was that we were thinking or
doing when we got a reinforcement. Outside consequences turn neuromotor
randomness into routines; each of us solves a problem with whatever systems
were active when it was first solved. Thus, it becomes certain that with
increased neural complexity and increased environmental variability, no two
creatures will ever use identical neurological structures in order to solve the
4
same external problem. Individual differences in brain structure^ are consistent
with this speculation; so is the analysis presented in a recent book by Edelman
65
and Tononi.

The Limbic System or MacLean's Paleomammalian Complex

The limbic system, a designation given this tissue complex by MacLean in

1952 and also included in his paleomammalian complex, introduced a new level
of persistence to striatal routines as emotion led to increased duration and
amplitude of overt behaviors. Limbic intensity and persistence formed enduring
pair bonds and allowed differential investments in their young on the basis of
size, liveliness, emotionality, and impulsiveness. Between adults or children,
within or between generations, emotions amplify selfishness and feuds or
protect reciprocity, bonding, and investment. Disruptions in nursing, infant care,
peer relationships, or the loss of a close ally or a lover might shift whole theaters
66 67
of behavior for long intervals. (Or might not. See Cohen and Harris for a
review of findings that children can have great resilience to parental aber-
rations.)
250 The Evolutionary Neuroethology of Paul MacLean

The Neocortex or MacLean's Neomammalian Complex

The neocortex, included in MacLean's neomammalian complex because of

its conspicuous development in the higher mammals, is the most newly refined
section of our brain and depends on extensive interconnections with as well as
the integrity of many older systems. Thus, we can expect it to be less predictable
(more chaotic) in comparison with either the limbic system or brain stem
(reptilian complex).
Indeed, there is such extensive connectivity within the brain that it would
appear to be an exception to Kauffman's findings that large arrays of units can
work quickly—again, 100K units can have a coherent output within 300 msec—
9
// they are sparsely connected It may be that each neuron participates in
thousands of different networks in the CNS but is directly influenced by only a
few other neurons in any particular decision. Thus, you can get many decisions
per unit of time and by large arrays but by a different array from instant to
instant. Learning, when it involves increased speed and lessened response
variability, may involve simplification in neural networks as much as it may
involve making new connections and maturation may involve the pruning of
inactive cells by a similar process. While we acquire some capacities as we
mature, we appear to lose the potential for many, many others.
The chaos in neural organization, however, becomes a strength when it
allows equivalencies between formerly arbitrary stimuli and the creation of
distinctions between cues that are physically very similar. It also allows the
loose, sometimes misleading, attachment of language as both an excuser and an
68
instructor for behavior. Language and negotiation are essential components of
socialization and have enormous advantages for the cohesion of highly variable
individuals who then make up for each other's deficits. Because of their
evolutionary complexity and late maturation, we can expect greater variability in
69
language and planning functions than in our other abilities. And because of
cultural demands on us—i.e., SAT computations and our dependence on
communication skills—there will not only be more deficits in these areas but
their impact will be more severe. It follows that problems in socialization can be
more of a personal handicap than is a missing limb. In addition to expecting
greater variability in linguistic and executive functions, we will have to listen
carefully to our clients both to understand their unique ways of analyzing and
solving problems and to adapt our suggestions to their particular skills. Special
education teachers have attempted this chore for a decade; therapists may soon
emulate them.
Refinement of our psychological adaptations, reciprocity computations, and
social networks seems to have accompanied the elaboration of our executive
functions. The prefrontal area appears essential for our executive functions that
let us make agendas, stack our priorities, segment time, swap plans, and use our
47,69
imaginations to solve p r o b l e m s . These capacities depend upon the integra-
tion of data from many other cortical and subcortical layers.
Physics and Evolutionary Neuroscience 251

THERAPY

First, because of genes and early developmental tuning, resilience blesses

some of us and curses others. A client with a productive history will recover
quickly from a crisis almost regardless of what a therapist does to him but a
history of systematic deterioration is less often consistent with recovery. Thus, it
may be that, like major universities, successful practitioners recruit successful
clients.
Second, the abruptness of switching between chaos and stasis, immobility
and stereotypy, can be modulated as when an ordinary electric switch becomes a
dimmer switch and complicates a circuit. Increasing the number of interconnec-
tions in parts of a human network—through experience, alliances, or
maturation—will slow the action. Decrease those connections by injury,
intoxication, or social isolation and decisions speed up, becoming both more
staccato and more stereotyped. Thus, clients with intact executive functions (or a
recent history of such) will be more deliberate, needing us less and discovering
their own solutions. Such clients will better share plans and integrate the
information from talk therapy. On the other hand, clients who have difficulty
with planning, constructive imagination, self-observation, and systematic
problem solving are often less able to apply methods recommended in therapy
and more reactive to environmental changes in their job, sleep pattern, family
status, friends, and seasonal activities. Such people will need our help to
discover effective changes and help from other allies to maintain them.

Constraint, Impulse

We need to "keep our act together" at the same time that we want to have fun
and most of us negotiate this conflict from moment to moment with our
children, peers, spouses, and employers. We also negotiate with our pet, our
lawn, automobile, and the wiring in our basement that consistently blows out a
fuse when we most need to use our computer. Our clients often represent one of
two kinds of negotiator, internalizers and externalizers, and treatment consists of
moving either strategist towards the middle. We seek more freedom for the
internalizers who are frightened and trapped but some limits, boundaries, and
complications for the externalizers, whom we call impulsive, selfish and
thoughtless. (Successful treatment will also produce freedom for the wives,
parents, teachers, and parole officers who originally sent them our way!)
Simplifiers can be interchangeable and include allies who do things for you,
lessened guilt (including tools such cognitive therapy or fluoxetine), forming
lines and hierarchies, making lists, delegating tasks, breaking chores into smaller
segments, putting things off, and old memories of being safe and in control.
Chain saws and bulldozers, assertion training and visualization, Prozac and
alcohol, cannibis, or cocaine are simplifiers just as are fungi, bacteria, and
neuronal apoptosis. Complicators can also be interchangeable, and include
allies who force you to stay out of trouble, bosses, mates, teachers, parents,
252 The Evolutionary Neuroethology of Paul MacLean

contracts, ministers, legal authorities, moral codes, deadlines, rules, and lawyers
who are working for someone else. Cement, fences, signs, and walls are
complicators and so are pets, school, and television shows.

Tuning

Age, reproductive standing, access to resources, seasons of the year, and

significant niche changes (divorce, empty nest, job changes, moving) will have
enduring effects on the client perhaps by altering the particular set of genes that
are active! Explanations can reduce anxiety that the client may have about
"losing their mind" as they become a different "person." Therapy can provide
information about tactics in a current relationship or job. However, it can
encourage changes in activities, perhaps the client's returning to arenas of earlier
success or to those wherein family members were successful. Study the client's
victories and repeat them; avoid battles entirely or engage them in an order in
which they can be won.

Active Darwinism

We seek and build niches that give us more choices. The label Active
Darwinism describes this process by which organisms select and modify their
41,42,70,71
environments. Furthermore, we apply a Darwinian consequence to our
worlds when we choose homes, toys and tools, plants and pets that suit us and
duplicate them with saws and hammers or with selective breeding of other
creatures. To the extent that humans are selective factors, environments compete
for human approval; environments and creatures in them that meet human
demands are kept and multiplied.
Despite structural order from phase transitions and from phylogeny,
j 3 , 3 4
development makes no two brains identical in neuroanatomical detail or in
their tricks that acquire food, partners, or possessions. While evolution specifies
reinforcement systems and environment offers choices, we differ in the
strategies and neuroanatomy that we use to achieve those rewards, in our
72
selecting and arranging environments, and in our explanations for what we d o .
Thus:

1. No single template defines our clients. Their assets and liabilities,

freckles, smiles, and PET scans will be unique for every one of them.
2. Whatever other natures our clients may have, the moment-to-moment
effort to regulate complexity will be a part of their every struggle and
their every satisfaction.
3. Each client is on a quest for experiences that meet her particular
allotment of psychological adaptations; each therapist also has her own
quest. Therapists and clients recruit each other for their own purposes. It
follows that in therapy as in marketing, practitioners who carefully
respect their client's individual nature will be more popular and possibly
Physics and Evolutionary Neuroscience 253

more effective than those who do not. (Some of this respect for the
client's individual nature will entail breaking current practices and
recognizing the sometimes identities of traits and circumstances between
that client and members of his immediate biological family.)
4. Clients will always pick among the therapist's offerings whether or not
that is the therapist's intent. The richer the menu offered, the greater the
chance for client satisfaction and clients will reinforce therapists for
developing suitable menu options.
5. There will be some conflict of interests to the extent that client and
therapist characteristics do not match. However, greater similarity
between client and therapist might predict stronger alliances between
u
them. This one REALLY understands me!" Active Darwinism will be
reflected in our picking friends who agree with us but listening to
contrary advice may be a violation of our instincts. Seeking conflicting
opinions may be newly evolved, easily impaired, and an important
diagnostic marker of its own.
6. While there will be substantial uniformity of automatic thoughts—
perhaps because, as MacLean approach suggests, we all started with the
same "lizard"—there will also be substantial variability between people.
The array of automatic thoughts available to the client will vary with his
or her age, reproductive standing, access to resources, seasons of the
year, and significant changes in his or her niche.
7. To the extent that language reflects evolved sensory and motor conflicts
with regard to chaos and stasis, stereotyped client verbal patterns will
73
sometimes reflect conflicts between genes.

CLOSING

This brings to a close my efforts to indicate how combining elements of

statistical physics with the evolutionary perspective of Paul MacLean can throw
light upon aspects of evolutionary theory and phenotypic development. For
clinical applications, I have suggested that such insights can lead in the direction
of a more coherent diagnostics and therapy and a model that is uniform for
physical systems as well as for human dilemmas. It will take time, opportunity,
talent, and effort to pull this structure together.
Ball cautions, "Despite the proven value to cell biology of some concepts
from the study of phase transitions . . . there remains much scepticism as to
whether any biological phenomena can arise from the sort of collective,
emergent behavior of statistical, interacting ensembles rather than the closely
1
controlled protein relays to which cell biologists are accustomed." But, I look at
a crouching cat and a modern sports car, note the similarities in their proportions
and their suspensions, and "know" that the same physical and statistical rules
guided the evolution of each. The role of phase transitions in human conduct has
a similar quality of obvious truth for anyone favorably disposed to the concepts.
However, there is a second group of analysts—often composed of scientists and
254 The Evolutionary Neuroethology of Paul MacLean

engineers in stasis—who will insist on knowing the formulae for attraction and
repulsion and the variables that participate in each one. (Perhaps of necessity,
there's also a third group, one chaotic in circumstances and ideas, who doesn't
believe numbers and graphs!)
A similar skepticism will exist for applying phase models to such evolu-
tionary human behavioral features as ambivalence, impulsiveness, and guilt-
until some tools for prediction and manipulation are created. T-mazes and
operant chambers, stop watches and microswitches, lab assistants, and electro-
mechanical programming gadgets made it possible for nearly anyone to observe
similar functional relations in the behavior of a wide array of birds and
mammals. Likewise, data from population biology and math from Haldane,
74
Pearson, and Sewall Wright revived Darwinism. Systematic awareness of
phase transitions in human conduct awaits a tinker and mathematician as well as
a rat and pigeon to uncover them.
Some theoretical issues for research to explore include: (1) our emotional
reactions to inter- and intrapersonal chaos, order, and phase transitions, (2) the
role of natural and sexual selection and of alliances and hierarchies in life's
oscillation between chaos and stasis, and (3) the possibility of sexual roles
allowing a species to pursue risk and constraint at the same time. More
clinically, and as sketched in Table 13.1, I would (4) rearrange how we view
pathologies and (5) incorporate the formal recognition of various constraints and
simplifiers that we offer to our clients and the complementary roles of such. We
might also formalize (6) the idea that more primitive threats and rewards will
override newer ones, and (7) the probability that response competition, through
reciprocal inhibition, will occur in a hierarchic manner between our varied
75 76 77,78
psychological a d a p t a t i o n s . ' ' Finally, we can begin to align clinical views
with those of common sense, that the striking behavioral similarities found in
twins reared apart will also be found between generations in a family and that
such patterns can more deliberately inform the choices that each of us makes.
79
Karl Pribram asked, "How is it that I can sense so much and do so little?"
As Pribram himself taught us, one of the important decisions for life is that of
20 46 47 50 8 0
go/no-go, the cueing of action or inhibition. ' ' ' ' Along these lines,
50
Allman reminds us that an E. coli merges the influences from a dozen
receptors but its motor, its flagellum, turns either clockwise or counter-
clockwise. Neurons take in a wide array of information but generate relatively
few outputs. A floor trader in the stock market considers a lot of factors but
u
compresses them into b u y " or "wait" while he adjusts his course from moment
50
to moment. His decisions are an adaptive walk between chaos and stasis, taken
in the same manner as a bacterium, a neuron, a bird, a species, a diagnostician,
or a scientist like Karl Pribram or Paul MacLean.
Physics and Evolutionary Neuroscience 255

NOTES

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2. Bloom H: Global Brain: The Evolution of Mass Mind from the Big Bang to the
2Jst Century NY: Wiley, 2000.
3. Smith CUM: Elements of Molecular Biology. (2nd Ed.). NY: Wiley, 1996.
4. Haig D: The Social Gene. In J R Krebs & N Davies (Eds.) Behavioral Ecology: An
Evolutionary Approach. London: Blackwell Science, 1997, pp. 284-306.
5. Wright R: Nonzero: The Logic of Human Destiny. NY: Pantheon, 2000.
6. Kauffman S: Origins of Order: Self-Organization and Selection in Evolution. NY:
Oxford, 1993.
7. Langton C; Taylor C; Farmer J D; & Rasmussen S: (Eds.) Artificial Life II :
Proceedings of the Workshop on Artificial Life. Held February, 1990 in Santa Fe, New
Mexico (Santa Fe Institute Studies in the Sciences of Complexity), vol. 10. Redwood
City, CA: Addison Wesley, 1992.
8. Waldrop M: Complexity: The Emerging Science at the Edge of Order and Chaos.
NY: Touchstone, 1992.
9 Kauffman S: At Home in the Universe: The Search for the Laws of Self
Organization and Complexity. NY: Oxford, 1995.
10. Fentress J: Personal communication.
11. Casti J: Complexification. New York: Harper Collins, 1994.
12. Glausiusz J: Joining hands. Discover, July, 2000; 32-34.
13. Helbing D, Farkas I, & Vicsek T: Simulating dynamical features of escape panic.
Nature, 2000; 407: 487-490.
14. Hayes B: Can't get no satisfaction. American Scientist, 1997; 85: 108-112.
15. Hamilton W: The evolution of altruistic behavior. American Naturalist, 1963; 97:
354-356. Reprinted in Hamilton, WD Narrow Roads of Geneland: The Collected Papers
of WD Hamilton, Vol I, Evolution of Social Behavior. NY: Freeman, 1996; pp. 6-8.
16. Miller G: How mate choice shaped human nature: A review of sexual selection
and human evolution. In Crawford C & Krebs D (Eds) Handbook of Evolutionary
Psychology. Mahwah, NJ: Erlbaum, 1998; pp. 87-130.
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 14

EVOLUTIONARY AND PHILOSOPHICAL

1
ISSUES IN TRIARCHIC THEORY

Seymour W. Itzkoff

INTRODUCTION

MacLean is a pioneer in his endeavor to show that human behavior is substrated

by neurological structures inherited from our ancient reptilian and mammalian
ancestors. He must be seen as a trailblazer in attempting to link human behavior
with the varying levels of phylogenetic structures that are part of our evolution-
ary inheritance. In this chapter I argue, that contrary to MacLean, the selective
power of humans considered from the evolutionary standpoint does not lie in the
various R-complex and limbic system heritages of behavior, even though they
constantly erupt from the depths of our neurological past to dominate individual
and social actions. Rather the selective power of humans is rooted in the
isocortex which hosts our ability to think, reason, and to create laws and
principles to guide the future of our society as well as prevail over all other
living species.

CONCEPTUAL PERSPECTIVE AND ITS LIMITATIONS

"The focus of the present book will be on protoreptilian and paleo-

mammalian formations and their role in nonverbal aspects of mentation and
2
behavior." MacLean thereby endeavors to show that human behavior is
composed of neurological structures inherited from our ancient reptilian and
mammalian ancestors. In this he is close to contemporary sociobiological
thinking. He must be seen as a trailblazer in attempting to link human behavior
with the varying levels of phylogenetic structures that are part of our evolution-
ary inheritance. In this neuroarchitectural endeavor he is even more of a pioneer.
His research reveals the actual morphologies and patterns of structural
interactions inherited from this reptilian and mammalian base. Naturally he is
260 The Evolutionary Neuroethology of Paul MacLean

concerned to connect the past with the neo-pallium and modern human
isocortical structures and behaviors.
Even given MacLean's recognition of the crucial role of causal thinking in
the powerfully selective rise of humans to dominance, his acceptance of the role
of language in coordinating the higher integrative conceptual powers of modern
humans, the paleoneurological substrate nevertheless interests him most as he
explores the morphological and neurological heritages that underlie all human
behavior:

the phenomenology of psychomotor epilepsy suggests that without a co-functioning

limbic system, the neo-cortex lacks not only the requisite neural substrate for a sense of
self, of reality, and the memory of ongoing experience, but also a feeling of conviction as
to what is true or false. This presents a problem of crucial epistemological significance
because there is no evidence that the limbic structures of the temporal lobe are capable of
comprehending speech, nor is there any basis for inferring a capacity to communicate in
verbal terms. Hence, it would appear that the manufacture of belief in the reality,
importance, and truth or falsity of what is conceived depends on a mentality incapable of
verbal comprehension and communication . . . it is one thing to have a primitive, illiterate
mind forjudging the authenticity of food or a mate, but where must we stand if we must
3
depend on that same mind for belief in our ideas, concepts, and theories?

He should be puzzled, for here his empirical research and theoretical

conclusions are less developed. But he brought about a phenomenal achieve-
ment: the revealing of our phylogenetic morphological and psychological
heritage structurally embedded in the R-complex and then in the limbic system,
then as these interact with the recently developed brain structures. Throughout
his writings MacLean shows an intimate knowledge of evolutionary research,
using it often to guide his own technical analyses of the various dimensions of
brain organization. As such, in viewing the sigificance of what he has learned,
and what he is about to embark on in pursuing this research, the evolutionary
perspective is both an enhancement and a limitation of his and others' research
to come. Because, without the most accurate interpretations describing the
significance and placement of these structures in light of the evolutionary facts,
his interpretations will be both limited and inhibitory. His states his perspective
clearly in the following passage:

In its evolution the human forebrain expands along the lines of three basic formations that
anatomically and biochemically reflect an ancient relationship, respectively to reptiles,
early mammals, and late mammals. The three formations are labeled at the level of the
forebrain that constitutes the cerebral hemispheres comprised of the telencephalon and
4
diencephalon.

MACLEAN'S EVOLUTIONARY FULCRUM

A critical evolutionary issue could affect our understanding of the signifi-

cance of MacLean's research as it concerns the internal paleoarchitectural
relationship of the three phylogenetic layers of brain function. This lies in the
role of the cortex in the shaping of the structures, and the cortex's evolutionary
Issues in Triarchic Theory 261

role in the positive selection of the vertebrate tetrapods. Throughout MacLean's

work he continuously refers to the ostensible adaptive functioning of these
structures, thus their role in natural selection. If these assumptions are not
accurate, or if they need significant modification, we will see the human brain
and its ostensible sociobiological imperatives in a wholly new light. MacLean
committed himself to the task of showing a line of continuity between the
development of each new tetrapod neuromorphological structure as it evolves
concomitantly with the Darwinian behavioral enhancements reflective of this
shift. Yet in the end it is this continuity, even dominance, of the past over the
present that holds the central role in MacLean's evolutionary drama.

In summary, except for their derivation from the original stock (the stem reptiles), all
extant reptiles have a lineage entirely separate from the therapsids. For comparative
neurobehavioral studies on reptiles I chose to focus on lizards because as will be
explained, they suggest a closer resemblance to early mammal-like reptiles than other
existing forms . . . it is requisite to characterize the structures of the basal forebrain that
represent a common denominator in reptiles, birds, and mammals, and finally to
comment on the long-standing, enigma regarding their functions. In regard to the
question of correspondence of structures in the three classes of animals, the evidence
5
rests on phylogenetic, embryological, neuroanatomical, and neurrochemical data.

The basic thrust of MacLean's evolutionary interpretation therefore places

human functioning at the causal beck and call of the prior established brain and
neurological structures. The evolutionist is enjoined to view the behavioral
power of the R- (striatal) complex and the limbic system as central to the
adaptive and selective destiny of the line leading to humans. The dimensions of
inductive thought, prediction, anticipation, organization and assimilation of
perception through memory, epitomized in cortical functioning, for him fade in
evolutionary significance when compared to the evidence of the modern
reification of more ancient brain and neurologically-rooted behavioral patterns.
For example, MacLean takes up the so-called challenge displays in various
animal lines, including humans, to show this continuity, the carry-over from
animals to humans. MacLean sees Diane Fossey's research on silverback
gorillas as close to the display of lizards. Jane Lawick-Goodall's description of
the chimpanzee "bipedal swagger," also reminds MacLean of reptile behavior.

As in the case of lizards, the stilted, staccato steps of the displays of the great apes seem
to carry the message of a series of exclamation marks. The Schragstellung gait of the
Komodo dragon . . . calls to mind the goose step of a military parade. The question
naturally arises as to whether the striking similarity between the challenge displays of
animals as diverse as lizards and gorillas represent "convergent" or "parallel" evolution.
Among different species the sideways presentation and the stilted, staccato steps have
such an uncanny resemblance that it would almost seem that the challenge display had
6
been genetically packaged and handed up the phylogenetic tree of mammals.

To argue that R-complex and limbic system functions are subordinate in an

evolutionary sense to the basic function of cognitive and intellective assimilation
would give an entirely differing cast to MacLean's research. Perhaps the
262 The Evolutionary Neuroethology of Paul MacLean

enormously complex reptilian and mammalian brain and neurological functions

in fact accompany the true, the core selective dynamic in the evolution of the
vertebrates. Such a central evolutionary process involves cognitive brain func-
tion. The R-complex and limbic system structures and functions in reality
constitute ancillary adaptive elements varying in their expression among a wide
7
variety of vertebrate forms, on land, in the seas, and in the air.
The evolutionary question thus remains: which of the three systems was the
crucial selective element driving the succession of land tetrapods? How did
these elements become morphologically and physiologically assimilable, beha-
viorally adaptively coordinated with the decisive selective factor? How do we
evaluate each of these structural and behavioral elements in their furtherance of
the general homeostatic success of the line? Finally, where should we look to
discover the more progressive and decisive selective dimension, that which took
us from the waters to the air and land, finally to the sweeping vertebrate
s
dominance of Homo sapiens sapiens (Hss)?
Differing answers to this question result in differing perspectives on
contemporary human behavior, altruistic or aggressive patterns, hierarchy,
dominance/submission, obsessional behavior, magic and superstition, even the
variety of language functions, song, poetry, declamation, and narrative.
A critique of MacLean's evolutionary perspective stems from Hss' para-
digmatic intellective behavior. It focuses, by contrast, on a triarchic theory
centering on the brain's increasing cortical discriminations, first in the
vertebrates, then in the land-roaming tetrapods, integrating information,
expanding the time zone of prediction and survival. Rather, in the contemporary
culmination of this one-billion year evolutionary romance glows a neglected
"nova," the iso- or neo-cortex. This brain structure can both regulate and domi-
nate the functions and behaviors of the R-complex and limbic system. To
understand human behavior—whether "primitive," pathological, or civilizat-
ional, we must look to the evolutionary meaning of the brain and intelligence.
And we must examine how both the reptilian and mammalian systems have been
systemically reincorporated as buttresses for the adaptive and selective survival
of the line.

WHAT EVOLUTION TELLS US ABOUT TRIARCHIC THEORY

Taxonomy establishes vertebrates within the over two dozen animal phyla.
The subkingdom of animals now compares to the subkingdoms of plants, fungi,
and various protozoa subkingdoms, fellow participants in the eukaryote
kingdom of complex sexually reproducing unicellular and multicellular life
forms. Finally, taxonomy includes the so-called prokaryote kingdoms, the
eubacterial and archaebacterial worlds, from which the eukaryotes separated
9
unknown billions of years ago. The distinctions are clear. Our line consists of
life forms with characteristics that include motility, heterotrophy (herbivores and
carnivores), that become environmental and ecological chance takers in highly
variable spatial and time frames. We are movers and opportunists, feeding on
Issues in Triarchic Theory 263

sessile, embedded opters for the status quo of momentary spatio/temporal

success.
A 4-billion-year time scale, allows for much Darwinian innovation. At each
point in the evolutionary progression, those who have peeled off for the good
life have by and large distinguished themselves evolutionary-wise from the
unstable by their high rates of extinction. Evolutionary instability, animal lines
ever at the edge of annihilation, takers of chances with change, became the
10
theme of the successful from the standpoint of our own evolutionary destiny.
In this time-deep zone of adaptation, biochemical and temperature parameters
remained conducive to multicellular eukaryote heterotrophic life and thereby
provided a selective groove of ever-increasing positive value given to creatures
able to negotiate dangerous and variable ecologies requiring movement and
11
change. These circumstances produced an internal guidance system selected
for its adaptation to instability through phenotypic, behavioral means, a slow
genetic pathway strewn with intergenerational boulders. Environmental, ecolo-
gical, and organic change often happened quickly and radically. The brain fur-
nished the adaptive means for momentary avoidance and survival, in contra-
11
distinction to a gradualism selectively culling existing genetic diversity.
The basic eukaryote cell is a highly complex energy machine with an internal
homeostatic structure that enables it to traverse diverse environments and to feed
upon victims randomly encountered, and then enveloped by the never-ending
12
explorations of their cilia and undulipoda. The chordates and, later, true
vertebrate fish continued that mainline adaptive tack. Concomitantly, vast
numbers of conservative stay-at-home-lancelets and tunicates, armored bottom-
dwelling Agnathans were either eliminated or permanently consigned to the
periphery as "things" changed.
The brain so became the preeminent adaptive and selective dimension
instrumental in the flowering, diversification, and maintenance of the vertebrates
in the front ranks of animal phyla. Jerison views brain size in relation to body
size as the desideratum of intelligence in the vertebrates. He maintains that no
real advance in intelligence emerged even when the proto-amphibians came onto
the land surfaces some 370mya and quickly radiated and evolved into the stem
13
reptiles. Certain visual specialization in the advanced Dipnoi seemed to
produce an expanded cerebellum beyond that of most other fish families. The
sharks and skates, ancient and only partially evolved vertebrate forms, possess
relatively large brains in comparison with the vast panorama of the sea denizens.
This argues for the relative indifference of the oceans, seas, and lakes to body
structure/brain-intelligence relationships, once a basic adaptive surge of its
14
original inhabitants had occurred.
Of course the land surfaces then uninhabited by animals could provide a
barrier to intelligent behavior. But the brain rapidly opened the door to a
dominant highly visual reptile brain outfitted with a number of ancillary
neuro/morphological and behavioral functions. The striatal or R-complex of
brain-behavior structures inherited from an ancient vertebrate body plan
underwent a long perfecting in the seas, but then showed evidence of existing on
land and in the air, from c.500-200mya. The R-complex fixed connections
264 The Evolutionary Neuroethology of Paul MacLean

among phenomena-temporal-momentary, conformity or nonconformity with

precedent conditions, ritualistic displays and changes in behavior, hunting,
homing, mating, selecting homesites, establishing territory, engaging in various
types of display, breeding, imprinting, forming social hierarchies, and selecting
leaders.
MacLean, of course, recognized that the transition from reptile to mammal
did not represent a mere superimposition of mammalian accretions onto
preexisting reptilian structures. Existent reptilian morphologies reorganized and
expanded. MacLean based his analysis of the shift between reptile and mammal
neurologies on the evolutionary transition between still reptilian therapsid
cynodonts and the earliest mammal, "Morganucodon," c.220-200mya. In all
likelihood this transition took place gradually, for, several cynodonts, dog-like
or larger in size, lived into the Jurassic alongside the now mouse-sized early
mammals. More orthodox Darwinian branchings could have the proto-animals
already separating from the therapsid/cynodont line during the mass extinctions
of the Permian (250-245mya), both groups the remnants of a once-luxuriant
synapsid/therapsid reptile clade. The latter were to be supplanted by the visually
vigorous archosaurs, parallel in the time to the first mammal appearance, c. 220-
15
200mya.
MacLean's evolutionary interpretation centers on the formation of the limbic
system, and not on the selective impact of cortical expansion. According to
Jerison, the earliest mammals already had a brain-body ratio 5-10 times what
existed in the classic fish/amphibian/reptile brain. The lower multiple might also
be applied to the therapsid cynodonts. MacLean: "the widening of the brain seen
in the therapsid-mammalian transition might be interpreted as a reflection of the
development of limbic parahippocampal cingulate, and entorhinal cortex, rather
16
than of the neocortex." Clearly this represents an important and controversial
issue.
MacLean included in the limbic system the olfactory bulb, septum, fornix,
hippocampus, amygdala, and cingulate gyrus. Indeed, he superceded in his
analysis the neocortex, represented in all vertebrates, by emphasizing the unique
17
expansion and reorganization of the limbic system of the mammalian line.
What MacLean interprets as an evolutionary advance provided by the limbic
system has to be seen in the context of a proliferating extroverted reptilian
evolutionary thrust, as compared with a clearly defensive mammalian posture.
The question concerns the evolutionary context during which the limbic system
began to be shaped away from traditional reptilian morphological patterns. In
the competitive contexts of the late Triassic, c.220-190mya, the developing
mammalian suite of limbic system adaptations was generally homeostatic and
defensive rather than exemplifying an expansive adaptive and thus demographic
trend.
It is difficult not to factor in as part of the expansion of the mammal brain the
basic neocortical values that instrumentally reorganized these innovative mam-
malian limbic structures. During the c.l50my of mammalian evolution under the
shadow of the dinosaurs, intensive selective dynamics were taking place.
However, once the mammalian suite of adaptations had carved out its life space,
Issues in Triarchic Theory 265

it is doubtful that this evolutionary trend was in large part shaped by the
pressures of the reptilian hordes. The original Permian climatic and ecological
crisis (250-45mya) more than likely shaped the mammalian body plan.
Miniaturization was probably a defensive preadaptation along with internal
homeothermy, nocturnal vision, and exploration. Useful, too, for some mam-
mals, was the ancient placental pattern of internal gestation.
Besides the archosaurs/dinosaurs, mammals likely needed to defend
against other cynodonts. So opportunity arose for these then-tiny creatures, c.
200mya, when the visually adapted and energetically mobile archosaurs pressed
the therapsid cynodonts into extinction. Jerison, but not Quiroga, for example,
believed that the therapsid/cynodont brain was more reptile than mammal-like,
therefore implicitly arguing, as I do here, for a longer period of separated if
parallel evolution of the two lines. "Although there may have been some
expansion of the cerebellum . . . (T)he mammal like reptiles, in short were
18
reptilian and not mammalian with respect to the evolution of their brains." I
find it persuasive that intraspecific adaptive and selective dynamics pushed
much of mammalian evolution c. 215-65mya. This early 5-10 times expansion
in brain/body ratios may have resulted from this earlier post-Permian ( 2 4 5 -
15mya) evolutionary dynamic. Not the limbic system so much as the expanding
cortex perhaps comprised the locus of their powerful adaptive and selective
19
thrust into dominance.
It is often thought that the suzerainty of the placental mammals over a wide
variety of other mammal lines, marsupials, multituberculates, and monotremes
stemmed from a new reproductive innovation late into mammalian history, c.
100-65mya. Yet placental reproduction can be traced back to sharks and skates
20
living in the seas some 400mya. Today there are many forms of fish that
reproduce in the viviparous and oviparous manner, as any aquarium lover can
testify. The advantages of viviparity cannot be assigned merely to reproductive
efficiency. Ultimately, placental reproduction gave increased opportunity for the
extension of fetal brain growth within the womb as compared with brain
truncated fetal birth in marsupial young. Many evolutionists see the reproductive
patterns of the marsupials as an insignificant advance beyond other vertebrate
oviparous reproductive patterns. Note, in addition to the monotreme's ancient
reproductive structures, they possess comparative cortical impotency at
21
maturity. The final phase of brain-body ratio growth, 10-30X the classic
reptile brain, led to the dominance of the placental mammals by the KT
boundary in the Paleocene, c. 65mya. The power of the mammals cannot be
argued to lie within R-complex/limbic system functionalities. Rather the
dominating feature stemmed from neocortical capacity linked to the reconsti-
tuted 150my-heritage of existing mammalian morphologies and behaviors.
Isaacson phrases the evolutionary implications of the accretative mammalian
defensive morphological suite as follows:

Another way to conceptualize the limbic system may be to see it as a regulator of the R
complex. On the basis of behavioral analysis, this regulation seems to be inhibitory in
nature. Stimulation of the limbic system often produces a suppression of ongoing
266 The Evolutionary Neuroethology of Paul MacLean

behavior, and lesions made within it often seem to "release" various activities . . . The r
complex is necessary for ritualistic displays and the averbal communication associated
with them. At the human level, MacLean believes that certain behavioral tendencies are
due to an inheritance of dispositions mediated by this same, primal brain region. These
include certain violent reactions, the preference for routine or 'ritualistic' actions, and
22
some form of displacement activities.

In the evolutionary tradition that spans the period from the eukaryote impact
on the evolutionary flux of life to the vertebrate land living tetrapods, mammals
and primates inherited the line of succession of this time-deep adaptive tradition.
From about the period of presumed placental diversification, evidence, mole-
cular as well as fossil/geological, c.l00-90mya, the primates exemplify this
adaptive trend: motility, adaptability to variable environments, omnivorous food
habits, defensiveness, nonspecialized behavior, higher-than-average body-brain
ratios, and high intelligence.
The particular specialized adaptive niche occupied by the primates took a
long time to be grooved into the genetic morphological and behavioral memory
bank. Much contemporary controversy concerns the place of Homo and its
immediate antecedents. To be fair with the history of these controversies over
human evolution, we ought to place the various positions on these issues into the
hypothetical. On the basis of modern Darwinism, the roots of the hominids will
likely be found on an outer branch, as with the mammals and their most ancient
23
aqueous progenitors, the Osteolepiforms.
It thus took c.l50my, from c.365-215mya, for the power of higher intelli-
gence to make its first land-adaptive impact, meaning the survival of the
remnant products of the reptile, synapsid, therapsid, cynodont line. The sur-
vivors probably represent a long deviant proto-mammal branch. Then, another
125my allowed the higher brain-to-body ratio of the placentals to demonstrate
its adaptive and selective power. The primates were a not hidden peripheral
spiral of this ancient defensive, intelligent, outlander tradition. But they did not
make their ultimate taxonomic success until the coming of Hss, with that
creature's devastating selective power over almost all of animal and plant life.
The primates needed some 75-80my to effect this most recent impact of
intelligence and adaptability over other distant taxa. The hominids themselves
needed 35-30my from the time of their most probable separation from the
various anthropoid branches in the Oligocene to establish the power of their
enveloping isocortex.

THE SOCIOBIOLOGY OF THE LIMBIC SYSTEM

Paul MacLean discusses the impact of the neopallium on human behavior.

He is an especially clear and honest scientist when he demurs from the
possibility of exploring the full role of Homo's new brain in its interaction with
the older levels. His continuing focus on the supposedly dominating role of the
older structures, however, raises questions both of balance and realism. Are we
humans truly in the thrall of the striatal complex and the limbic system in
Issues in Triarchic Theory 267

cultural behavior, given that our uniqueness as mammals is characterized by the

vast expansion of the new brain, the isocortex? I quote again from MacLean:

Recalling that in this chapter (#28 "Special Role of Prefrontal Neocortex") our primary
concern is with paleopsychic processes, we focus in this final discussion on human
evolution as it pertains to (1) shedding of tears with crying; (2) the role of play in
acculturation and creativity; and (3) the "memory of the future" All of these topics reflect
in some degree the concurrent evolution of a sense of empathy and altruism. Since they
are conditions that appear to depend particularly on the linkage of the frontal neocortex
with the thalamocingulate division in the limbic system, it is relevant as background to
summarize what is known about the time course of the evolution of the present-day
human cranium with its distinctive elevation of the brow overlying the prefrontal region
24
of the brain.

MacLean's discourse involves a highly technical analysis of the morphologies

of the human brain as they impact on the above typically sociobiological, limbic
system behaviors: laughing, yawning, courtship, submissive behavior, territoriality,
challenge displays, deceptive behavior, routinizing behavior, reenactment behavior,
perseverative behavior, epilepsy, dejection, fear, desire, anger, gratulant (gratifying,
triumphal, successful, ecstatic) exhultation, affection, searching behavior, protec-
tive, aggressive or caressive behavior; handedness, sound communication and
speech, weapon and child carrying, the evolution of tearing, play, and laughter.
At core, MacLean's argument places the locus of certain basic and untutored
responses in the limbic system. The human limbic system becomes the regulator
that prevents or shapes those earlier rigid, stereotyped, and autonomous drives
centered in the reptilian complex: amygdaloid area-aggressive behavior; septal area
sexual function. MacLean notes that sexual behavior in the paleomammals
25
originated in rhinencephalon and the olfactory structures.
In an important interpretation of the implications of MacLean's theory, two
scholars at the University of Palermo, M. Ernandes and S. Giammanco, probe the
powers of the R-complex and the limbic system in order to clarify human hierar-
chical institutions, both religious and political. In concordance with MacLean, the
R-complex fixes connections among phenomena-temporal-momentary; conformity
or nonconformity, with precedent conditions, ritualistic changes in behavior. The
limbic system adds an emotional element, producing relaxation when activities are
completed, anxiety when they are brusquely interrupted or changed. The neocortex
possesses "induction" capacity from particular phenomena with causal connections
felt in all perceptual experience. In humans, R-complex factors lead to obsessional
and magical behavior and compulsions. In humans a language factor adds to these
26
R-complex elements.
Underneath these behaviors certain brain structures provide a level of biological
causation. In the R-complex, neurons form masses, nuclei or ganglia. The limbic
system includes pallial or cortical structures in addition to nuclei. These include: (a)
paleopallium-piriform cortex; (b) medial pallium, (i.e., hippocampus-archipallium);
and (c) dorsal pallium-neopallium. The isocortex possesses 6 layers. Biochemi-
cally, all three brain types exhibit acetylcholine and dopamine typical of R-
27
complex, and serotonin. Ernandes and Giammanco write: "Following MacLean's
268 The Evolutionary Neuroethology of Paul MacLean

model, in the serotenergic system we can distinguish a reptilian part (i.e., of the R-
omplex) and a mammalian part (i.e., of the limbic system), the latter being formed
in particular by raphes obscurus and dorsal raphes nuclei. Ascending fibres extend
from the pontine nuclei (MRN and DRN) to several telencephalic regions, among
28
which are basal ganglia."
Reduction in serotenergic action leads to (a) increase of intraspecific compet-
ition; (b) increase of magical thought; (c) temporal epilepsy. Reduction in
serotenergic function weakens the limbic system's ability to resist hierarchy-
29
making structures, as well as obsessive-compulsive disorders.
Although inhibited by the limbic system, the human brain's R-complex
preserved and still preserves the structures and hierarchy-forming functions that
give rise to submission to leaders. MacLean sees "the immensely powerful
being" as created by the action of the R-complex on the neocortex. Ernandes and
Giammanco see the weakening over the span of human evolution of the
inhibitory influence of the limbic system on the R-complex's influence over the
30
neocortex.
The question is, why did this happen, why the weakening? They answer that
the brain makes causal connections between temporally variable inputs of
perceptual information in a rationally verifiable and experientially adaptable
manner, if the cortex can find the cause. In the case of magical thought, when
inputs cannot be organized cortically in rational verifiable behavior, the result is
nonfunctional illogical responses, that is, faith. Magical thought thus stems from
its unconscious origins in the R-complex. The neocortex makes this conscious
and tries to give it an appearance of rationality by embedding these emotions
31
(limbic system) in a nexus of associated symbolism.
Such symbolic systems lead to the acceptance of powerful human gods, as
well as supernatural forces and gods. "Initiatory rites occur at critical ages of
individual development with emotional involvement. They mainly operate on
the limbic system and the r-complex. The limbic system provides the ingredients
for the strong affective feeling of conviction attached to beliefs, while the r-
complex is the seat of 'imprinting,' until religious beliefs as to the existence of a
32
supernatural Powerful Being become strong and well established."
From Desmond Morris: "in a behavioral sense, religious activities consist of
the coming together of large groups of people to perform repeated and
prolonged submissive displays to appease a dominant individual. The dominant
individual takes many forms in different cultures, but always has a common
33
factor of immense power."

EVOLUTIONARY CRITIQUE

Because MacLean always followed the mainline evolutionary perspectives of

the Darwinians, the direction of his highly technical and specialized morpho-
neurological research on the brain adhered closely to the accepted evolutionary
perspective. He colored his evolutionary interpretation, however, with the
comparative functions of the so-called striatum or R-complex and the more
Issues in Triarchic Theory 269

recently evolved limbic structures. Even more MacLean saw the behavioral
impacts of these latter systems on human life, considering but not emphasizing
the impact of Homo's cortical accretions. So, too, in turning to the evolutionary
record, he tended to view mammal evolution as adaptively and selectively
defined by the behavioral impact of limbic system structures. To MacLean, they
provide definition, in contrast with the underlying reptilian R-complex, and thus
have been decisive in the selective sense.
We have here the traditional chicken-or-egg argument. Which element,
traditional limbic structures or cortical causal and evaluative factors, tilted the
selective equation? The debate transitions into the evolution of the hominids.
Here the isocortical growth explosion unanimously seems the reason for
hominid and Hss success. MacLean understandably pointed to the ongoing
impact on behavior of these phylogenetically ancient structures. Compared to
the base primates, they possess inordinate prominence in Homo's brain. Still, the
isocortex maintains its roles as the decisive selective element in human evolu-
tion. The isocortex seeks out causes, relationships, and ventures predictions of
the future. In its hyper-corticality linked with the ancient mammalian structures,
this brain structure discovered the keys to mastering the physical and biological
world.
MacLean, as we have noted above, viewed the innovative mammalian
physical and brain structures—lactation, the protective nursing mother, the
audio-vocal cries of protection and defense, play—as crucial adaptive factors
that allowed for the positive selection of this class of animals. These led to their
eventual domination over the other tetrapods, reptiles, and amphibians. The
more contextual evolutionary perspective would place a much greater emphasis
on the larger cortex of the mammalian brain, as compared with the reptiles,
because it fostered the adaptive efficacy of these animals. Indeed, as MacLean
notes, a number of these adaptations may already have been part of the
therapsid/cynodont suite of adaptations (homeothermy, internal gestation) before
the evidentiary extrusion of the mammals 215-200mya.
Most have conceded that, compared with the extroverted visual and
energetically dynamic reptile adaptive patterns, the mammalian suite of
brain/behaviors originally had defensive functions. But without the suzerainty of
a larger cortex to coordinate such defenses behaviors, their selective impact on
the evolutionary destiny of the mammals would have been marginal, as evident
in a number of marsupial and monotreme lines. These lines, without the
competitive pressures exerted by placentals would have held their own against
existing reptile forms, and, indeed, with a limbic brain, did proliferate.
Emotional control epitomized in the limbic areas without the coordinating
powers of the neocortex, however, would have never won the selective battle for
the placentals.
And, of course, the primate line, once an intelligent, defensive, side branch
of the placentals, made its living by "staying out of the way" through protective
brain-power. Eventually, use of that brainpower linked to a powerful and
energetically dynamic limbic system, destroyed innumerable long prospering
species that existed to that point. MacLean admits the closely linked morpho-
270 The Evolutionary Neuroethology of Paul MacLean

logical and behavioral connections in the human brain between the various parts
of the limbic system and the isocortex. So much so, it is difficult to see where
one function ends and the other kicks in. Still, the following quotation reflects
the deep impression of the power of the limbic system on human behavior.

[T]he complete lack of memory for what happened during automatisms (psychomotor
epilepsy) is primarily owing to a disturbance of limbic function and a resulting failure of
the integration of internally and externally derived experience, upon which a sense of
reality of the self depends. Without an integrated sense of self, there is, so to speak, no
place to deposit a memory of ongoing experience . . . [T]he limbic cortex receives more
extensive input from interoceptive systems than the neocortex and, also of crucial
importance, receives input from the various exteroceptive systems. It should be recalled
at this point that psychomotor epilepsy provides evidence that the limbic system is
involved in self-realization, as evident by such experiences during the aura as feelings of
enhanced feelings of reality, increased awareness, or self-duplication ('mental diplopia')...
the phenomenology of psychomotor epilepsy reveals that even the least obtrusive feelings
generated by limbic activity are tinged with some degree of affect...the saying that
'something does not exist until you give it a name': Something does not exist unless it is
34
imbued with an qffective feeling, no matter how slight.

An intimacy between feeling and thought in human interpersonal and cultural

behavior has long been commented upon. A seeming axiom holds each issue
from a differing dimension of the human psyche. Yet emotions cannot be
individually suppressed in our living actions without human suffering. The
artist, scientist, musician, even the philosopher, needs the juices of affect to
undergird, to give spirit to, his mentation. This completely concords with
MacLean's views. At the same time, the raw feelings of "blood," of nationalism,
of power, of love and sex, religious or ethnic zealotry without the rigor and
restraints of thought or reason, become inchoate and animalistic. Eventually,
without cognitive discipline, they turn any human activity into "blind obedience
to powerful beings."
The selective power of humans considered from the evolutionary standpoint
does not lie in the various R-complex and limbic system heritages of behavior,
even though they constantly erupt from the depths of our neurological past to
dominate individual and social actions. True human power is rooted in the
isocortex, our ability to think, reason, analyze, abstract from momentary
perception, and create laws and principles whose impact on other humans and
the world beyond may not be evident for weeks, months, years.
Sociobiological fascination, clearly influential in MacLean's metainterpret-
ations, derives from a need to search for a unity of derivation in our biological
nature. But such reductionist views miss the great biological story in the "super-
primate" revolution heralded in the isocortex of Homo. The missed "story!" can
be found in the evolutionary processes that created this unprecedented brain.
Such conceptual myopia is exemplified in the quickness of reputable scientists
to swallow "humans-as-third-chimpanzee" science fiction.
The hegira leading to Hss has been long in coming. The hominids in all
likelihood expelled and pushed the African anthropoids into extinction, except
Issues in Triarchic Theory 271

for the peripheral and now highly specialized chimpanzees and gorillas. Indeed,
it is likely that much of African ape evolution since the Miocene, 20mya, has
been selectively influenced by the increasingly successful australopithecines and
then their supplanters, Homo. Only recently has the weight of evidence replaced
the lineal view of the fossil record with a new awareness of the long-in-process
branching nature of hominid evolution.
Scientific opinion has now solidified the awareness that the first truly
modern humans were the Cro-Magnons, Hss, of Europe and West Asia. The
power of their ballooning cortex is revealed in the spontaneous symbolic
effusions of their technology, art, and social discipline. In the richness of their
cultural productions, we can envision the workings of the paleoneurological
structures. But they are filtered through and disciplined by the isocortex. There
had been, before this bursting of traditional hominid boundaries c.45,000 B.P.
many forms of Homo. It is difficult to know what their cultural potential could
have been were they to have lived within the protective bosom of the Cro-
Magnons. The Neanderthals, a primitive progressive erectine type with a large
brain, are increasingly viewed as having lived side by side with the Cro-
Magnons in Europe and West Asia, and for at least 10,000 years. Perhaps they
were even protected by the moderns. Certainly, much interbreeding took place.
Skulls as far back as 90,000 B P—Qafzeh, Skuhl. in the Near East, later,
Predmost and Mladec in Moravia, 35,000 B.P—reveal such a relationship. Most
recently discovered is an apparently post-Neanderthal hybrid child, at about
23,000 B.P.
In addition, large populations of humans lived away from the center of this
final evolutionary thrust that received, though only gradually and variably, the
genetic biochemistry that produced the modern cortex. Our contemporary
inheritance, then, is mixed in terms of the cortical and cultural assimilation of
these evolutionary dynamics. But, the ancient paleoneurology exists in all
humans, an inheritance dated in the tens and hundreds of millions of years. And
it shows itself in the variety of human interpersonal behaviors, as well as
cultural and civilizational life-styles. Some of us can fall under the thrall of R-
complex and limbic passions of allegiance to human tyrants, religions that
demand the debasement of human reason to myth, magic and superstition.
Weak cognitive profiles are victimized by the devotional totems emanating from
Hollywood or Yankee Stadium. Highly intelligent and educated peoples, such as
the Germans or Japanese, can surrender their rationality to "the myth of the
35
state." The Cro-Magnons, at 30,000 B.P, evidence in their art, monuments, and
technology little mythology or violence. The classical Greeks and the early
modern Europeans were intellectually moved to draft written constitutions in
which democratic practices acted to nullify the sway of the ancient neurological
regime. This represents strong evidence for the latent powers of the neocortex in
human sociobiological affairs.
272 The Evolutionary Neuroethology of Paul MacLean

PHILOSOPHICAL INJUNCTIONS FOR RESEARCH AND POLICY

The 20th century witnessed a powerful resurgence in the glorification of

"paleocerebral functioning." From the throwing off of Victorian behavioral
modalities for the freedoms of sexual as well as cultural expression, cinema,
literature, and so on, the frontal brain areas of restraint and discipline ceded their
suzerainty to the "let-it-all-hang-out" expressivity of the older behavioral
regime. In addition, the susceptibility of the masses, ceding their rationality to
the unlimited god-like powers of tyrannical leaders such as Hitler and Stalin, the
toleration for the massive genocides unleashed by these human animals, allows
us to witness at first-hand the paradoxical character of the human brain.
Paul MacLean sees opportunities for a higher form of animal behavior
through the union of limbic and cortical functioning in the human animal:

The possibility is suggested that through the neofrontal connections with the thalamo-
cingulate division, a parental concern for the young generalizes to other members of the
species, a psychological development that amounts to an evolution from a sense of
36
responsibility to what we call conscience.

What is substantially new in the known history of biology is that this concern extends not
only to the human family, but to all living things—an evolutionary turnabout that could
affect a turnabout in what has heretofore seemed a vicious life-death struggle long
37
recognized as the struggle between good and evil.

It is well and good to identify the source of so-called human altruism in the
nurturing concern of parents for their young. This sense of responsibility,
however, is not strictly rooted in the genetics of neofrontal/ thalamocingulate
maternity. Nurturing is now a freely chosen behavior, and, equally, discarded in
neglect and cruelty. We human beings can extend our sense of "responsibility"
and "conscience" toward the young of others. In similar cognitive acquiescence,
we can act to destroy the children of strangers. The puzzling voluntarism of
human intraspecific violence finds a parallel in the mystery of mental dysfunc-
tion. We human animals uniquely display this. Some would place a sociobio-
logical tonality onto these malfunctionings as heralding defeat and biological
ostracism. Yet the behaviors seem to have persisted over long spans of time.
The biochemistry that we now see as complicit, at least in part, has not been
expelled from the genome. In fact, many individuals afflicted with bipolar
syndrome are socially successful and creative persons.
Hans Eysenck hypothesized a close relationship between schizophrenia and
genius; they seem to occupy different sides of a sometimes permeable brain
behavioral membrane. The genius sees in the given symbolic structure possi-
bilities inherent in the fluid malleability of factual reality. The schizophrenic
envisions possibilities that are beyond the facticity of the given. The sense of
possibility in one grows out of a sense that the real is never permanently
embedded. In the other there is no public facticity from which to envision real
38
possibilities. Who can say where in triune brain structure this fluidity of
thought is made possible?
Issues in Triarchic Theory 273

MacLean often points to epileptic seizures as revealing the interdependence

of the new brain on the older morphologies. So, too, we can view the charis-
matic demagogue transformed into the tyrant as an exemplar of the "demonic"
power pathologies inherent in the ancient structures when allied with humans in
crafty and unscrupulous intelligence.
What we see in the historical working out of an extremely variable, yet
radically new set of brain structures in this interbreeding super-species, Homo
sapiens, is the slow, variable, and inexorable march toward domination of the
dictates of cortical intelligence in human behavior. We cannot depend on
inchoate instinctive mammalian motivations to direct us into the future. The
neocortex must not suppress, but rather discipline those paleoneurological
juices, our evolutionary vertebrate heritage. Intelligence and rationality need to
consolidate, if not establish their suzerainty in our thinking and behaving. It is to
be hoped that this process will define the internationalization of the larger
human community.

NOTES

1. Triarchic rather Triune because the former reflects the semi-independent variability
of the three morphological structures in terms of their behavioral correlates. Triune
implies as with the "Trinity" a merging of three factors in a unity of expression.
2. MacLean, P. D. 1990. The Triune Brain in Evolution, NY: Plenum, p. 10.
3. MacLean, 1990. pp. 578-579.
4. MacLean, P. D. 1968 "Alternative neural pathways to violence," in Alternatives to
Violence, L, Ng., ed., New York: Time-Life Books, pp. 24-34.
5. MacLean, 1990, pp. 33-35.
6. MacLean, 1990, pp. 232-233. See also Gadjusek, D. C. 1970. "Physiological and
psychological characteristics of Stone Age Man," in Symposium on Biological Bases of
Human Behavior, Eng. Sc., 33: 58-59.
7. Janvier, P. 1984. "The relationship of the Osteostraci and the Galeaspida," Journal
of Vertebrate Paleontology, 4: 344-358; Long, J. 1995 The Rise of the Fishes, Baltimore:
Johns Hopkins University Press, pp. 30, 32, 34.
8. Radinsky, L. 1987. The Evolution of Vertebrate Design, Chicago: University of
Chicago Press, pp. 50-52.
9. Woese, C. R., Kandler, O., and Wheelis, M. L. 1990. "Towards a Natural System
of Organism: Proposal for the Domains Archae, Bacteria, Eucarya," Proceedings.
National Academy of Science, 87: 4576-4579; Kandler, O. 1993. Progressive Botany,
54: 1-24; de Duve, C. 1995. Vital Dust, NY: Basic Books; Sogin, M. 1991. "Early
Evolution and the origin of the Eucaryotes," Current Opinion Genetic Development, 1:
457-463.
10. Henderson, L. 1913 The Fitness of the Environment, NY: Macmillan.
11. Nisbet, E. G. 1991 Living Earth, New York: Harper Collins, p.l 11; Dawkins, R.
1995. River Out of Eden. NY: Basic Books.
12. Margulis, L. 1992. Simbiosis and Cell Evolution, 2nd edition. San Francisco: W.
H. Freeman; Wilford, J. N. 1996. "First Branch in Life's Tree Was 2 Billion Years Old,"
The New York Times reported in Science, 1/30/96.
13. Jerison, H. 1973. Evolution of the Brain and Intelligence, NY: Academic Press.
274 The Evolutionary Neuroethology of Paul MacLean

14. Smith, H. 1961. From Fish To Philosopher, New York: Anchor-Doubleday, pp.
120-121; Long, J. 1995. The Rise of the Fishes, Baltimore: Johns Hopkins Press, pp. 201,
209; Jerison, H., 1973, op. cit, p, 28.
15. MacLean, 1990, pp. 95-97.
16. MacLean, 1990, p. 257; Jerison, H. 1973.op. cit.
17. Radinsky, 1987, The Evolution of Vertebrate Design, op. cit.
18. Jerison, H. 1973. Op. Cit, p 154; Quiroga, J.C. 1979. "The brain of two
marnmal-like reptiles (Cynodontia-Therapsida)," Jnl. Hirnforsch, 20: 341-350; Quiroga,
J. C. 1980. "The brain of a mammal-like reptile Probaingnathus jenseni (Therapsida,
Cynodontia). A correlative paleo-neurological approach to the isocortex at the reptile-
mammal transition," Jnl. Hirnforsch, 21: 299-336.
19. Jerison, H. 1982. "The Evolution of Biological Intelligence," in R. J. Sternberg,
ed., Handbook of Human Intelligence, Cambridge, Eng.: Cambridge University Press, pp.
723-791; Jerison, H. 1977. "The Theory of Encephalization," Annals of the N Y Acad, of
Sciences: 299: 146-160.
20. Bone, Q., Marshall, N., Blaxter, J. 1995. Biology of Fishes, London: Blackie
Academic and Professional, pp.178, 180-182.
21. MacLean, 1990, p. 92; Gadow, H. F. 1911. "Reptiles-Anatomy" in Encyclo-
paedia Britannica, 11th ed., New York: Cambridge University Press, v. 23, p. 170.
22. Isaacson R. L. 1982. The Limbic System, 2nd ed., NY: Plenum Press, p. 246.
23. Ahlberg, P. E., and Johanson, Z. 1998. "Osteolepiforms and the ancestry of tetra-
pods." Nature, Vol. 395, 10/22/98, 792-794.
24. MacLean, 1990, p. 552.
25. Ernandes, M. and Giammanco, S. 1998. "MacLean's Triune Brain and the Origin
of the 'Immense Power of Being' Idea," Mankind Quarterly, Winter 1998, Vol. 39: 2,
173-201 (184).
26. Ernandes, M. and Giammanco, S., 1998, p. 184.
27. Ernandes, M. and Giammanco, S., 1998, p. 180; see, Voogd, J. R., et. al. 1998. in
Niewenhuys, R., et al., eds., The Central Nervous System of the Vertebrates, Berlin-
Springer-Verlag, pp. 1636-2097 (p. 1872).
28. Ernandes, M. and Giammanco, S., 1998, p. 191.
29. Ernandes, M. and Giammanco, S. 1998, p. 192; Rapoport, J. L. 1989. "The
Biology of Obsessions and Compulsions," Scientific American, 260:3: 62-69.
30. Ernandes, M. and Giammanco, S. 1998, p. 187.
31. Ibid, p. 184.
32. Ibid, p. 188.
33. Morris, D. 1994. The Naked Ape, London: Vintage/ Random House, p. 121.
34. MacLean, 1990. p. 578.
35. Cassirer, E. 1945. The Myth of the State, New Haven: Yale University Press.
36. MacLean, 1990. p. 562; MacLean, P. D. 1985a. "Brain evolution relating to
family, play, and the separation call," Archives General Psychiatry, 42: 405-417.
37. MacLean, 1990. p. 562.
38. Eysenck, H. 1995. Genius: The Natural History of Creativity, Cambridge: Cam-
bridge University Press.
 15

MACLEAN'S EVOLUTIONARY
NEUROETHOLOGY: ENVIRONMENTAL
POLLUTION, BRAIN CHEMISTRY, AND
VIOLENT CRIME

Roger D. Masters*
INTRODUCTION
The evolutionary perspective in the study of the brain and social behavior is the
hallmark of Paul MacLean's science. His limbic system and triune brain
concepts have been among the most influential in neuroscience over the most
recent decades. The full significance of the evolutionary neuroethology which
he so tirelessly championed, however, has yet to be felt within the social
sciences and even less yet in areas of social policy where it potentially
illuminates some important, even urgent areas of concern. This chapter reports
the results of findings in environmental pollution, specifically the effects of
heavy metals upon violent social behavior, and emphasizes the necessity for
bringing the perspective of evolutionary neuroscience into our social sciences
and our social policy-making.

ENVIRONMENTAL POLLUTION, NEUROCHEMISTRY, AND

BEHAVIOR

Building upon the work of such pioneering figures as Ramon y Cajal,

Hughlings Jackson, C. Judson Herrick, Karl Pribram, Paul MacLean and others,
evolutionary neuroscience continues to transform our understanding of human
behavior. It has revealed not only the evolutionary history of our neural
architecture but also anatomic structures and chemical mechanisms underlying
emotion, cognition, and motor coordination (e.g. MacLean 1990; Purves et al.

* The research on silicofluoride toxity reported here was suggested by and conducted in
collaboration with Myron J. Coplan (PE, Intelliquity consulting, Natick, MA), whose
expertise and precision have been invaluable.
276 The Evolutionary Neuroethology of Paul MacLean

1997; Gazzaniga, Ivry & Mangun 1998; McGuire & Troisi 1998). However, for
most social scientists, following Locke and the behaviorist tradition in
psychology, the brain remains a black box responding to environmental stimuli.
This outdated view of the brain as a tabula rasa still resonates in the widespread
assertions of the "social construction" of human cultural and political behavior.
Although many traditional assumptions about the human brain are clearly
false, the social sciences remain dominated by a generation totally unaware of
neuroscientific research. As a result, it is commonplace to "explain" learning
deficits, substance abuse, and antisocial behavior solely by such factors as
poverty, socioeconomic status, and racial or sexual prejudice. Of course, these
conditions greatly influence all of us. But their effects are mediated by each
individual's central nervous system, a product of millions of years of species
evolution, that processes similar information in varying ways due to differential
genetic propensities, fetal and neonatal development, diet, maternal and paternal
bonding, early learning and social experience—along with myriad other inputs
to the human brain. To understand how such complex factors contribute to
violent behavior, an understanding of the revolutionary advances in neuro-
science becomes both invaluable and indispensable (Raine 1993; Wilson &
Petersilia 1995; Niehof 1999). We begin this discussion by considering the
effects of environmental elements that are toxic to the proper functioning of our
evolved neural architecture.

Neurotoxins and Their Effects

Neurotoxins are among the factors that can change brain function and thus
alter behavior (on the following, in addition to Aschner & Kimelberg 1996;
Purvis et al. 1997; and Gazzaniga, Ivry and Mangun 1998; see esp., Lippard &
Berg 1994). The central nervous system (CNS) is perhaps the subtlest and most
sensitive chemical system in the human body—as most of us learned the first
time we drank too much alcohol.
Mere environmental exposure to toxic chemicals is, however, not the whole
story. Evolution has also built in a degree of protection for the nervous system.
Given the complexity of neurochemistry, it should hardly be a surprise that
natural selection has to some extent buffered the central nervous system against
potentially harmful chemicals in the environment.
If a toxin is swallowed, its effects depend on whether it crosses the gut-blood
barrier. Once in the bloodstream (whether from ingestion or wounds), toxins
must also cross the blood-brain barrier before they can influence brain function
and behavior. However, because the selective passage of many toxic chemicals
through cell membranes is determined by a variety of physicochemical variables
including size, charge, hydrophilicity, lipophilicity, etc., toxicologists have
focused on toxin-induced health risks such as cancer and birth defects rather
than on social behavior.
Despite its buffering effect against certain elements, the blood-brain barrier
does, however, possess channels that function to allow the passage of essential
Pollution, Brain Chemistry, and Violence 277

elements that play a regulatory role in cellular function. These elements are
sometimes positively charged ions ("cations") and sometimes negatively
charged ones ("anions"). Many essential elements, including calcium, iron, and
zinc, are called divalent cations because they have an electrical charge of 2+.
Individuals deficient in these elements are more likely to absorb toxic heavy
2+ 2+ J+
metals that are also cations, including lead (Pb ), manganese (Mn , M n ,
4+ 2+ 3+
M n ) , cadmium (Cd ), or aluminum (Al ). These toxic elements can cross the
acetylcholine channel, that allows only positively charged ions to pass into cells
with little discrimination between cations (Lippard & Berg 1994: 159). Inhala-
tion of toxins provides a more direct and more dangerous route, because some
molecules can move through the nasal cavity to the brain directly, bypassing the
blood-brain barrier altogether.
Within the brain, another mechanism of detoxification can sometimes fail,
leading to unwanted behavioral effects. Glial cells function to absorb the products
of chemical reactions in the brain and release them to the bloodstream (Aschner &
Kimelberg 1996). But this process is subject to a number of biochemical constraints
that sometimes do not effectively remove toxins. For example, the cellular surface
of neurons normally maintains a net electrochemical balance between positive and
negative charges—the so-called Donnen Equilibrium. If this balance is disturbed
with a resulting net negative charge, uptake of positive cations increases without
regard to the toxicity of the elements involved. As a result, the combination of an
imbalance in normal chemical elements plus exposure to such toxic metals as lead,
manganese, cadmium, or aluminum can easily result in brain uptake (Lippard &
Berg 1994: ch. 6).
Based on these considerations, we hypothesize that such heavy metals more
likely influence behavior than do many industrial neurotoxins. To be sure,
endocrine disruptors (Coburn, Dumanoski and Myers 1997) can also have
important effects on behavior, as is suggested by recent findings linking them
with a preference for same-gender sexual partners (Crews et al. 2000). Despite
these facts, traditional studies of the toxicity of many elements including
cadmium (Ashner & Kimelberg 1996: Ch. 11) and fluoride (e.g., Dunipace et al.
1989, 1996; Jackson et al. 1997), have continued to focus almost entirely on
cancer and similar diseases.
One difficulty in studying the effects of heavy metals on behavior is that
exposure does not alone account for dysfunctional outcomes. Neuronal uptake
of heavy metals largely depends on other factors such as dietary deficits, stress,
or exposure to substance abuse, which damage the brain's normal mechanisms of
defense against toxins (Bryce-Smith 1983, 1986; Ashner & Kimelberg 1996).
Hence the poor, with diets lacking sufficient calcium, iron, or zinc, are at higher
risk for the negative effects of heavy metals. Likewise affected are those persons
with hypolactasia or other genetic conditions that predispose toward diets low in
calcium and other essential minerals.
Of the heavy metals harmful to normal learning and behavior, lead is the best
known (Needleman, ed. 1991; Needleman 1998). Its effects were noted long ago
by Benjamin Franklin, who wrote a friend: "the Opinion of this mischievous
Effect from Lead is at least above Sixty Years old; and you will observe with
278 The Evolutionary Neuroethology of Paul MacLean

Concern how long, a useful Truth may be known and exist, before it is generally
receiv'd and practic'd on." (Masters, Hone and Doshi 1998:13). Manganese and
cadmium have also been associated with increased aggressiveness or hyper-
active behavior and learning, deficits. In addition, long-term exposure to manga-
nese or to organophosphates has been implicated in a form of Parkinsonism
(Dicalzi et al. 2000; Pryadarshi et al. 2000; Weiss 2000). Some researchers
believe aluminum is a risk factor in Alzheimer's Disease although evidence is
lacking.
Environmental exposure leading to uptake of heavy metals can therefore
contribute as a co-factor to many behavior deficits and social dysfunctions.
Among the conditions that have been studied are learning disabilities (Bryce-
Smith 1983, 1986), low IQ (Needleman, ed. 1991), attention deficit disorder
(ADD) as well as hyperactivity (ADHD) (Tuthill 1996; Manuzza 1989, 1998),
teenage pregnancy, alcoholism, drug abuse, and crime (Masters, Hone and
Doshi 1998). In each case, neurochemical imbalances that interfere with normal
information processing and impulse control number among the risk-factors
associated with dysfunctional or anti-social behaviors.
Specific mechanisms underlying these findings have been studied at the
neuroanatomical level. For instance, attentional focusing, and behavioral inhibi-
tion represent functions regulated by circuits in the basal ganglia (structures
deep in what MacLean called the R-complex). Two inhibitory circuits in this
structure, regulated by the neurotransmitters dopamine and GABA (gamma-
amino butyric acid), facilitate continued information search and optimize
responses to environmental stimuli (Purvis et al. 1997: 348-349; Gazzaniga,
Ivry and Mangun 1998: 412-420). By reducing the levels of these neuro-
transmitters, lead or manganese can produce defects in inhibition (Masters,
Hone and Doshi 1998). Not surprisingly, therefore, recent studies have shown
substantial numbers of hyperactive (ADHD) children with elevated levels of
lead (Tuthill 1996) or manganese in head hair. Masters, Hone and Doshi. have
compiled data revealing that head hair has been used as a marker of heavy metal
uptake over the preceding 2-3 months (1998: 13-48).
Other factors that contribute to observed correlations include vulnerability of
neuroanatomical structures to heavy metal toxicity. One important structure for
learning, whose functions are only now being understood by neuroscientists is
the hippocampus. There CA1 and CA3 neurons establish lasting connections
between synaptic firing patterns through longterm potentiation (LTP), that
increases responses when paired stimuli are perceived, as well as long term
depression (LTD), which reduces associative responses as part of habit forma-
tion. These basic mechanisms for learning and habituation depend on calcium,
magnesium, and the neurotransmitter glutamate (Purvis et al. 1997: 440-451;
Gazzaniga, Ivry and Mangun 1998: 285-287). Lead can both lower levels of
glutamate and replace calcium, thereby disrupting the normal regulatory
functions of ion channels. Such neurotoxic effects may explain why lead uptake
so widely correlates with lower IQ and other learning disabilities (Bryce-Smith
1983; 1986; Needleman, ed. 1991; Needleman 1998).
Pollution, Brain Chemistry, and Violence 279

EMPIRICAL EVIDENCE LINKING NEUROTOXIC METALS AND

BEHAVIORAL DYSFUNCTION

No single risk-factor explains everything in human antisocial behavior. Poor

impulse control and low IQ can be traced to factors other than toxic metals,
ranging from genes to sociocultural backgrounds (Masters and Coplan 1999b).
However, the contribution of heavy metals can be disentangled from these
factors by three types of findings. First, body levels of lead, manganese, or
cadmium can be measured among persons with specific behavioral dysfunc-
tions—ranging from hyperactivity to violent criminal records—and compared to
comparable individuals who do not exhibit the behavior in question (e.g.,
Walker 1998). Second, geographic levels of the same behavioral dysfunctions
can be compared in communities that do and do not have sources of environ-
mental pollution with heavy metals (e.g., Masters, Hone and Doshi 1998). Third,
time-series data can be examined to assess whether changes in levels of
pollution influence rates of learning disabilities and antisocial behavior (e.g.,
Masters 2001). At all three levels, evidence shows heavy metal neurotoxicity to
be a significant risk-factor contributing to problems of learning and self control.

Heavy Metals as a Risk Factor to Individuals

As noted, studies over the last decade in the U.S. and Europe repeatedly
found a linear inverse relationship between individual lead levels (as measured
in blood or head hair) and IQ (Bryce-Smith 1983, 1986). Some critics have gone
to extreme lengths to challenge these findings—for example by claiming that
because impulsive children eat lead paint that, in turn, causes low IQ, impulsi-
vity rather than lead toxicity represents the root cause (Juberg 1977: 9). In a
series of carefully controlled studies, Herbert Needleman and his colleagues
(Needleman, ed. 1991; Needleman et al. 1996) have demonstrated the error of
this hypothesis. Most recently, this research team has compared infants at birth,
showing that there were no early differences in the response patterns of children
subsequently found to have higher lead uptake and attention deficit disorder
(Needleman 1999).
Poor impulse control apparently contributes to the learning deficits
associated with heavy metal toxicity. This finding is plausible on neuro-
ethological grounds. For example, ritalin, the most widely used medication for
hyperactivity, increases dopamine—a neurotransmitter with inhibitory functions
whose levels are reduced among individuals who absorb too much lead. Indeed
Walker (1998) has reported that removing lead is an effective therapy for
hyperactivity and notes that, since cocaine and ritalin have similar effects on
dopamine, drugging ADHD children to make life easier for parents and teachers
is both medically unwise and ethically unsound.
Given an association between poor impulse control during childhood and
subsequent violent behavior (Manuzza et al. 1989, 1998), others focused on
levels of lead and manganese in the head hair of criminals. Seven different
280 The Evolutionary Neuroethology of Paul MacLean

groups of violent offenders were compared to those in the same prison convicted
of property crime. This provided a valuable test. Robbery and theft are more
likely to be preceded by planning than barroom brawls. Hence these studies
provide an assessment of impulsiveness that takes into consideration other
factors leading to criminal behavior. In all seven samples, the violent offenders
had significantly higher levels of either lead and cadmium or manganese
(Masters, Hone and Doshi 1998).
Two prospective studies confirmed these findings by showing that children
with early evidence of high lead uptake more likely exhibit later behavioral
dysfunction (Denno 1993; Needleman 1996). The larger of these samples, based
on data from the Philadelphia Biosocial Study, revealed that blood lead levels at
age 7 significantly predicted juvenile and adult crime (Denno 1994).

Environmental Pollution with Heavy Metals: a Geographic Risk Factor

A second approach analyzes the extent that heavy metal pollution associates
with geographical areas at risk for higher rates of behavior dysfunction.
Although anecdotal data are risky, it may be worth noting that a numberof the
major school shootings in the United States over the last two years have
occurred in communities that are Superfund sites. Only in Springfield, Oregon—
where Kip Kinkle acted alone—is there no evidence of industrial releases of
heavy metals. Springfield is about 40 miles from the nearest Superfund pollution
site. In all other cases—most notably Littleton, Colorado, where the Superfund
site was ignored by all the journalists—there is striking evidence of toxic
pollution with heavy metals and other toxins (Rymer and Alpert 1999).
The Environmental Protection Agency's Toxic Release Inventory for lead
and manganese, two of the principal heavy metals implicated in poor impulse
control, provided more convincing statistical data for these heavy metals.
Comparing all counties in the United States on over twenty socio-economic and
demographic measures, including income levels, population density and size,
racial composition, and education, industrial releases of heavy metal pollution
were a statistically significant risk factor for higher rates of violent crime (Table
15.1). Lead or manganese pollution interact with each other and with above
average rates of alcoholism. Communities with any two or all three of these risk-
factors have signficantly higher rates of violent crime than those with only one
(Masters, Hone & Doshi 1998).
Pollution with neurotoxins like lead can, moreover, last for many years
(Bailey et al. 1994). Indeed, although forest areas may be able to recycle toxic
metals quickly, some estimates suggest that in an urban soil, lead toxicity may
last for up to fifty years. Because children play in the dirt and lick their
fingers—a behavior increased by the sweet taste of lead—neighborhoods
adjoining heavily used urban highways represent areas of risk. Within a number
of American urban communities, including cities as different as Milwaukee and
New Orleans, careful studies by Howard Mielke and associates found that areas
along highways that were heavily traveled when automobiles used leaded
Pollution, Brain Chemistry, and Violence 281

gasoline have higher levels of lead in the soil around housing units (Mielke
1998).

Table 15.1. Factors Associated with U.S. Crime Rates, 1985-1991

All U.S. Counties Reporting Data from 14 Independent Variables

Violent Crime - Violent Crime Increase 1985 to

1985 1991 1991
Stan. t- Probability Stan. t- Probabilit Stan. t-value Probabil
Coeff. value Coeff. value y Coeff.
Demographic Variables
Population 0.178 4.047 0.0001 0.199 4.528 0.0001 0.121 2.161 0.0306
Population Density 0.171 8.433 0.0001 0.150 7.441 0.0001 0.046 1.811 0.0730
%Black 0.230 13.1 0.0001 0.298 17.21 0.0001 0.237 10.785 0.0001
%Hispanic 0.141 8.818 0.0001 0.144 9.045 0.0001 0.092 4.516 0.0001
Socio-Economic Variables
Per Capita Income n.s. n.s. n.s. n.s. n.s.. n.s. n.s. n.s. n.s.
Black Poverty 0.399 9.851 0.0001 0.425 10.51 0.0001 0.219 4.26 0.0001
Hispanic Poverty -0.056 1.645 0.1001 n.s. n.s.. n.s. n.s. n.s. n.s.
Median Grade 0.054 2.913 0.0036 0.082 4.473 0.0001 0.070 3.032 0.0025
Completed
Public Policies
Welfare Per Capita -0.316 5.717 0.0001 -0.396 7.184 0.0001 -0.260 3.711 0.0002
Police/Capita 0.145 8.267 0.0001 0.089 5.077 0.0001 n.s. n.s. n.s.
Public Water/Capita 0.091 5.515 0.0001 0.089 5.427 0.0001 0.059 2.807 0.0050
Toxic Metals
Lead Toxic Release 0.043 2.633 0.0085 0.038 2.275 0.0230 n.s. n.s. n.s.
Manganese Toxic 0.047 2.901 0.0037 0.078 4.792 0.0001 0.077 3.741 0.0002
Release
%Pre-1939 Houses -0.143 8.460 0.0001 -0.158 9.509 0.0001 -0.091 4.298 0.0001

number of counties 2881 2754 2659

Adjusted r-squared 0.418 0.445 0.146
F-test 148.97 159.468 32.405
Q
y
probability 0.0001 0.0001 0.0001

Note: Compiled from EPA and FBI data.

Temporal Effects of Pollution from Leaded Gasoline

As Mielke's work suggests, environmental pollution can continue to

influence behavior long after the original release of the toxins. In addition to
prolonged exposure, toxins can produce delayed effects because exposure of the
fetus or infant often produces lasting damage to normal brain structure and
chemistry (Wong et al. 1992; Aschengau, Ziegler and Cohen 1993; Levitt 1999).
In humans, delayed behavioral dysfunctions due to low-level exposure to lead
and other heavy metals show as subtle effects (Mendlesohn et al. 1998) and may
not become readily apparent until manifested in anti-social behavior in teenage
years (Needleman, ed. 1991, esp. Ch. 11-12; Denno 1993; Needleman 1996).
The national phase-out of leaded gasoline provided an interesting way to
study such a proposed delayed effect of lead on behavioral dysfunction for two
reasons. First, longitudinal studies have shown striking declines in lead levels in
children since the ban on sales of leaded gas, indicating that in this case public
282 The Evolutionary Neuroethology of Paul MacLean

policy significantly reduced exposure and uptake of a dangerous neurotoxin.

Second, since humans absorb 40 to 50% of inhaled lead as compared to only 5
to 15% of ingested lead (Needleman ed. 1991: 81), effects of nasal exposure to
leaded gasoline likely have been especially great. Whereas uptake of ingested
toxins is thought to be dependent on dietary deficits, fumes of tetraethyl lead
from gasoline pumps could even harm pregnant women and their fetuses as well
as infants with diets not deficient in calcium and other essential minerals. If so,
one can hypothesize that the long-term effects of exhaust from lead gasoline on
fetal and infant development could have been responsible for behavioral
problems when those affected reached teen-age and early adulthood.
The recent decline in violent crime rates in the United States provides a way
of testing this hypothesis. While correlation does not prove causation, it can
suggest possible risk-factors that deserve further analysis. The continuous fall in
rates of murders and other violent crimes since 1991 has elicited many explana-
tions from social scientists and criminologists (Wilson and Petersilia 1995), but
only one seems to have looked at leaded gasoline sales (Nevin 2000). This
should not be surprising, since the contemporary sales of leaded gas are
negatively related to rates of crime. From the perspective of brain development,
however, attention should focus instead on prenatal and neonatal neuronal
damage that is only manifest years later. It appears conceivable that the harmful
effects of leaded gasoline were temporarily delayed until those exposed before
the age of 2 grew up.
Time-series data for all violent crime and for the sales of leaded gasoline 17
years earlier show roughly parallel down-turns in the early 1990s (Warren,
Silverman and Sonnenborn 1999). A similar analysis of homicide and lagged
rates of leaded gas sales is more useful, however, because it permits an assess-
ment of effects that differ due to the age of the offender. Lagged gasoline sales
not only track murder rates during their rise for 15 years prior to the 1977 ban,
but in the five subsequent years for which we have data. But while gasoline
consumption peaked at 1.7 times the baseline level, the homicide rate by 14-17
year olds peaked at over 3 times the baseline. The peak rate for the 18-24 age
group was clearly not as high, suggesting greater impulsiveness among the
younger cohort. That this difference might stem from the combined effects of
pre-natal and neonatal exposure to particulate lead in gasoline exhaust is
reinforced by the more precipitous decline in crime among younger offenders
once rates began to fall in 1993 (see tables and figures in Masters 2001 for
detail).
These findings add weight to the hypothesis that the strongest long-term
effects of exposure to residues of tetraethyl lead were due to prenatal and
neonatal development, reflecting the importance of long-term body stores of
lead in current neurotoxicity (Gulson et al. 1995). To be sure, many factors
contribute to crime (Wilson and Petersilia 1995). But because most socioe-
conomic and cultural variables usually invoked to explain crime either did not
change in a manner that could explain the data or are themselves in need of
explanation, the ban on leaded gas seems to have played an unexpected role in
the sudden drop in criminal violence 17 years later (Nevin 2000).
Pollution, Brain Chemistry, and Violence 283

It might be objected that the number of years chosen for the lagged variable,
while based on the lag needed to track prenatal exposure of those 14 to 17 at the
time of FBI crime reports, is arbitrary. Alternative explanations, however, are
not entirely satisfactory. For example, some experts have claimed that the
decline in violent crime since 1991 is due to the falling demand for crack
cocaine. But this merely displaces the problem, since one has to ask why the
demand for crack declined. This is particularly important because lead down-
regulates dopamine whereas cocaine up-regulates dopamine—in that respect
cocaine acts on dopamine the way Prozac acts on serotonin (cf. Martin 1983;
Dewey 1986; Cook et al. 1995). Moreover one factor associated with enhanced
lead uptake (silicofluoride usage in public water supplies, discussed in detail
below) is correlated with increased levels of cocaine use at the time of arrest in
an NIJ study of over 30,000 criminals in 24 cities. Because this effect was
predicted by our research (Masters, Coplan & Hone 1999b) whereas it does not
follow from traditional socioeconomic or racial models of substance abuse and
crime, changes in cocaine usage cannot be invoked as a cause that is unrelated to
absorption of lead from the environment.
Given linkages between lead and deficits in impulse control based on the
neurochemical mechanisms outlined above, the hypothesis of a lagged positive
effect from removing lead gasoline could be further tested by looking at
additional measures that reflect impulsive behavior (Nevin 2000). One report
suggests, for example, that sales of leaded gas highly correlate with the
consumption of alcohol (DelRosso et al. 1999). Another tentative study suggests
that rates of teen-age pregnancy were weakly correlated with leaded gasoline
sales, albeit with a lag time of 14 years (Lauer et al. 1999). While both drinking
and sexual promiscuity seem at first connected to impulsiveness, alcohol
consumption provides an especially interesting test because the genetics and
biochemistry of alcoholism gained wide study over the last decade.
Whereas the effects of lead neurotoxicity described above concern behaviors
associated with dopamine, the consensus of recent scholarship points to crucial
deficits in another neurotransmitter, serotonin (Masters & McGuire 1994: Ch.
6). Little evidence links lead toxicity to abnormal serotonergic function, whereas
manganese clearly down-regulates serotonin levels (Ashner & Kimelberg 1996).
In addition, data on crime indicate that rates of alcoholism influence behavior
independently of industrial releases of either lead or manganese, reinforcing the
belief of many researchers that alcoholism is strongly influenced by genetic
factors. It follows from this as well as the diverse socioeconomic and cultural
factors influencing alcohol consumption that the pattern of correlation between
leaded gas sales and alcohol consumption should differ from that observed for
homicides by young males.
The data confirm this hunch, pointing to puzzling associations that might
further implicate lead neurotoxicity in social behavior. The correlation between
leaded gasoline sales in the 1960s and 1970s and alcohol consumption 17 years
later is negative (r = -.307). Nor do leaded gasoline sales strongly associate with
the same year's alcohol consumption (r = .228). Oddly enough, however, if
statistics are matched with a lag of 5 years, there is a stronger association (r =
284 The Evolutionary Neuroethology of Paul MacLean

.689). This suggests that recent lead exposure may influence some aspect of
alcoholic consumption, since a lag of 5 years means that when leaded gasoline
sales ended, the principal effect probably concerned children between the ages
of 8 and 13 (the average age when teenages first start drinking [Masters and
Coplan 1999a]).
Because alcoholism is primarily associated with serotonin, a neurotransmitter
that is not a primary target of lead toxicity, these data suggest that the influence
of lead on drinking behavior might concern the impulsivity with which people
consume alcohol rather than the fact of consumption itself. If so, we might
expect differences in the kinds of alcohol consumed to be more susceptible to
lead toxicity than the overall consumption patterns.
When alcohol sales are broken down into beer, wine, and spirits (hard
liquor), this is precisely what we find. If each year's sales of leaded gas are
correlated with contemporary sales of each type of beverage, it becomes obvious
that leaded gasoline was associated with a shift from beer and wine to distilled
spirits as the drink of choice. The correlation between sales of spirits in years
between 1949 and 1993 and sales of leaded gasoline during, the same year is
.811 (p = .000), whereas both beer and wine sales are negatively and weakly
correlated with leaded gas.
Unlike crime, the effect of exposure to leaded gasoline on alcohol seems to
be a breakdown of aversion to the effects of rapid inebriation, at most triggered
by lowering inhibition in late childhood. The correlation implies that the effect
may have been strong, but many other cultural factors could also have
contributed to the growing market for beer and wine. However that may be,
since the brain dysfunction associated with alcohol consumption differs from
that underlying homicide, it is not surprising that the precise pattern of
association with exposure to fumes from leaded gasoline is also different.
These temporal relationships need further study. Although it is necessary to
control for diverse social and geographic factors, the differences noted above are
consistent with other data showing the behavioral effects of lead intake. If
confirmed, such complex findings as the lagged effects of banning leaded
gasoline on homicide and a markedly different pattern of influence on drinking
patterns would constitute additional evidence for the neurotoxicity hypothesis
(Masters 2001).

INDIRECT FACTORS ENHANCING LEAD UPTAKE

In some respects, the most intriguing and important analyses concern factors
that enhance the uptake of lead. While pollution in the form of leaded gasoline
fumes that are inhaled by pregnant mothers and infants would directly impact
the developing brain, uptake of other sources of heavy metals may be enhanced
by additional risk-cofactors in the environment.
Research with Myron Coplan and Brian Hone focused on one such factor,
the use of silicofluorides in the fluoridation of public water supplies. Virtually
all testing of fluoridation chemistry (with the exception of several early studies)
Pollution, Brain Chemistry, and Violence 285

has focused on the efficacy of sodium fluoride (NaF) in preventing caries. More
recently, a few studies have considered the health effects of NaF—but none
consider fluosilicic acid (H SiF ) and sodium silicofluoride (Na SiF ) and
2 6 2 6

compare them to sodium fluoride (Coplan, Hone & Masters 1999a). EPA
officials admit that they have no data on health or behavior effects of these
chemicals (Fox 1999). Because the silicofluorides are used in the water
treatment for over 90% of Americans receiving fluoridated water, this failure to
study them is all the more surprising (Coplan, Masters & Hone 1999).
These chemicals deserve study because, in a sample of 250,000 children in
Massachusetts, those living in communities using silicofluorides had signifi-
cantly higher average blood lead levels than those in communities that do not
fluoridate at all or that use sodium fluoride (Masters & Coplan 1999).
Multivariate analyses shows that lead uptake from known environmental sources
of pollution, such as average lead levels in 90th percentile first draw water and
percent of housing built before 1940, was significantly higher in communities
that also use SiF in water treatment (see Figure 15.1).

4.00 -i-

15 15 15 15
pbb ppb ppb ppb

Lead in Water

Houses p r e 1940 Houses pre 1 9 4 0

Less than 2 9 . 5 % Over 29.5%

ANOVA Significance:
Main EFFECTS
% Houses pre 1940: p = .00901, F 21.17
90th percentile 1st Draw Lead > 15ppb: p = .0101, F 6.75
Silicofluoride use: p = .0177, F 5.63

Interaction effect
silicofluoride use * 1st Draw Lead in Water: p = .0422, F 4.18

Note: Derived from EPA and state data.

Figure 15.1. Factors Associated with Childrens' Blood Levels. Massachusetts.

Moreover, using a matched set of towns that do and do not fluoridate with
these chemicals, SiF is associated with higher rates of crime and higher
educational expenditures.
286 The Evolutionary Neuroethology of Paul MacLean

These associations between SiF and higher percentages of children with lead
in excess of lOmcg/dL have been confirmed in studies of rural counties in
Georgia and Wisconsin as well as in the 35 urban counties sampled in the
National Health and Nutrition Evaluation Survey or NHANES III (Masters,
Coplan & Hone 1999b). While these national data from NHANES III do not
include counties with populations under 500,000, they show graphically that the
greater vulnerability of racial minorities to higher lead uptake—long noted in
studies of lead toxicity—is enhanced in communities using silicofluoride in their
water (see Figures 15.2a and 15.2b).

Fluoridation and Race as Factors In Blood

Lead of Children 3-5, NHANES III

• Black, Non-H
• Mexican
0 Other
• White, Non-H

H i g h Fl M e d Fl Low Fl Unknown

% of Population with Fluoridated

Water

Source OF Sum of Mean F Value Pr^ F

Squares Squares
Mode! 15 4113.841 274.2561 0.0001
Error 1811 31628.18 17.46448
Corrected Total 1826 35742.02

Source DF Type III SS Mean F Value Pr > F

Square
FLJ3ROUP 3 769.5048 256.5016 14.69 0.0001
RACE 3 1215.789 405.2629 23.2 0.0001
FL GROUP^RACE 9 427.3706 47.48563 2.72 0.0038

Source: NHANES (National Health and Nutrition Evaluation Survey (NIH).

Figure I5.2a. Fluoridation and Race as Factors in Blood Level of Children 3-5
Pollution, Brain Chemistry, and Violence 287

Fluoridation and Race as Factors in Blood

Lead of Children 5-17, N H A N E S HI

• Black, Non-H
D Mexican
B Other
• White, Non-H.

High F Med F Low F Unknown

% of Population with Fluoridated
Water

Source DF Sum of Mean F Value Pr > F

Squares Squares
Model 15 5672.469 378.1646 44.58 0.0001
Error 6106 51799.4 8.483361
Corrected Total 6121 57471.87

Source DF Type IK SS Mean F Value Pr > F

Square
FLJ3ROUP 3 982.8809 327.627 38.62 0.0001
RACE 3 1385.593 461.8644 54.44 0.0001
FL G R O U P ' R A C E 9 673.1287 74.79207 8.82 0.0001

Source: NHANES (National Health and Nutrition Evaluation Survey (NIH).

Figure 15.2b. Fluoridation and Race as Factors in Blood Level of Children 5-17

These findings have been further confirmed by comparable statistical

analyses of venous blood lead levels in a sample of over 150,000 children in
New York state communities of 15, 000 to 75,000 population (Masters, Coplan,
Hone & Dykes 2000). Once again, ethnic minorities were a substantially higher
risk if exposed to SiF treated water, especially if other environmental sources of
lead (such as old housing) were also prevalent in the community. All told,
therefore, data in these three studies confirm the effects of silicofluoride in tests
of blood lead for over 400,000 children.
In addition, we found behavioral correlations between SiF usage and
antisocial behaviors otherwise associated with lead neurotoxicity, not only in
county-level data for 1985 and 1991 (Tables 2a,b; Figures 3a,b), but in the
288 The Evolutionary Neuroethology of Paul MacLean

alcoholism and cocaine consumption of over 30,000 criminals tested for drug
use by the NIJ in 24 large cities (Masters, Coplan & Hone 1999a). The effect of
SiF on cocaine usage—noted above in passing—was predicted as a behavioral
correlate of lead neurotoxicity because cocaine, unlike the other drugs tested
(which did not show higher usage in SiF communities) is a nonselective
dopamine reuptake inhibitor (see Tables 15.2a, b; Figures 15.3a, b).

Table 15.2a. Multiple Regression-Causal Factors Associated with Rates of Violent

Crime in All U.S. Counties, 1985

Variable: Coefficient: Std. Err.: Std. Coeff.: t-Value: Probability:

INTERCEPT -0.005056
**%SiF 0.000368 0.000133 0.044933 2.779132 0.0055
UNEMPLOYMENT.. 0.000076 0.000013 0.106014 5.988623 0.0001
PC INCOME BL... -9.92E-09 5.69E-09 -0.028883 1.742151 0.0816
PC INCOME 9.53E-08 1.91E-08 0.115025 4.989345 0.0001
MEDIAN GRADE... 0.000205 0.000069 0.081833 2.971707 0.003
MEDIAN YEAR... 0.000003 0.000004 0.01226 0.719065 0.4722
% BLACK 0.00005 0.000003 0.313211 17.565442 0.0001
% GRADUATE ... -0.000022 0.000007 -0.096468 2.965084 0.0031
% RURAL -0.000027 0.000001 -0.349944 18.728391 0.0001

CONFIDENCE
INTERVALS
Variable: 95% Lower: 95% Upper: 90% Lower: 90% Upper: Partial F:
INTERCEPT
"%SiF 0.000108 0.000628 0.00015 0.000587 7.723575
UNEMPLOYMEN... 0.000051 0.000101 0.000055 0.000097 35.863607
PC INCOME BL... -2.11E-08 1.25E-09 -1.93E-08 -5.50E-10 3.035O91
PC INCOME 5.78E-08 1.33E-07 6.39E-08 1.27E-07 24.893561
MEDIAN GRADE... 0.00007 0.00034 0,000091 0.000318 8.831041
MEDIAN YEAR... -0.000005 0.000011 -0.000004 0.00001 0.517055
% BLACK 0.000044 0.000056 0.000045 0.000055 • 308.544769
% GRADUATE ... -0.000036 -0.000007 -0.000034 -0.00001 8.791723
% RURAL -0.00003 -0.000024 -0.000029 -0.000024 350.752619

Note: Again, presence or absence of silicofluorides is a significant predictor of violent crime.

Interestingly, in this group of nine predictive variables, only the median year of house construction is
NOT significant. Compiled from EPA and FBI data.
Pollution, Brain Chemistry, and Violence 289

Table 15.2b. Multiple Regression-Causal Factors Associated with Rates of Violent

Crime in All U.S. Counties, 1991

Variable: Coefficient: Std. Err.: Std. Coeff.: t-Value: Probability:

INTERCEPT -0.026874
**%SiF 0.000922 0.00019 0.076136 4.847215 0.0001
UNEMPLOYMEN... 0.000064 0.000017 0.062928 3.693542 0.0002
PC INCOME BL... -3.96E-09 8.09E-09 •0.007926 0.489639 0.6244
PC INCOME 1.28E-07 2.63E-08 0.108872 4.869223 0.0001
MEDIAN GRADE... 0.000504 0.000095 0.140963 5.304905 0.0001
MEDIAN YEAR... 0.000014 0.000006 0.039495 2.4115640.0159
% GRADUATE... -0.000058 0.00001 -0.178521 5.719072 0.0001
% RURAL -0.000041 0.000002 -0.376415 20.749842 0.0001
% BLACK 0.00008 0.000004 0.351002 20.358866 0.0001
CONFIDENCE
INTERVALS
Variable: 95% Lower: 95% Upper: 90% Lower: 90% Upper: Partial F:
INTERCEPT
"%SiF 0.000549 0,001295 0.000609 0.001235 23.495494
UNEMPLOYMEN... 0.00003 0.000098 0.000035 0.000092 13.642253
PC INCOME BL... -1.98E-08 1.19E-08 •1.73E-08 9.36E-09 0.239747
PC INCOME 7.65E-08 1.80E-07 8.48E-08 1.71E-07 23.70933
MEDIAN GRADE... 0.000317 0.00069 0.000347 0.00066 28.142022
MEDIAN YEAR... 0.000003 0.000026 0.000004 0.000024 5.81564
Variable: 95% Lower: 95% Upper: 90% Lower: 90% Upper: Partial F:
% GRADUATE ... -0.000078 -0.000038 -0.000075 -0.000041 32,70778
% RURAL -0.000045 -0.000037 -0.000044 -0.000038 430.555948
% BLACK 0.000072 0.000088 0.000074 0.000087 414.483444

Note: In 1991, silicofluorides are again a significant predictor of violent crime controlling for eight
other variables. Unlike 1986, in 1991 age of housing is a significant predictor whereas per capita
income among blacks is no longer significantly associated with rates of violent crime in the U.S.
Compiled from EPA and FBI data.
290 The Evolutionary Neuroethology of Paul MacLean

SilicofluorideWater&Lead Pollution as
Predictors of 1985 Violent Crime Rate
(All US Counties, n = 2871)
0.005 l 1
•i

<10% >11%<79% >80%

% of Population with Water Treated
with Silicofluorides
Signif. SiF: p <.0001; Pb: p<.0001; Interaction:
n.s.

Source: Lead Pollution: EPA Toxic Release Inventory

Figure 15.3a. Silicofluoride Water and Lead Pollution of Predictors of 1985 Violent
Crime Rate
Pollution, Brain Chemistry, and Violence 291

S i l i c o f i u o r i d e W a t e r & L e a d P o l l u t i o n as
P r e d i c t o r s of 1991 V i o l e n t C r i m e
R a t e (All U S C o u n t i e s )

0.008 -l 1

<10% >11%<79% >80%

% of Population with Water Treated
with Silicofluorides
Signif: SiF: p< .0001; Pb: p<.0001;
Interaction p=.067

Note: Derived from EPA and FBI data.

Figure 15.3b. Silicofluoride Water and Lead Pollution as Predictors of 1991 Violent
Crime Rate
292 The Evolutionary Neuroethology of Paul MacLean

The time-series data showing the lagged effects of leaded gasoline sales
suggest another manifestation of SiF enhancement of anti-social behavior due to
lead neurotoxicity. Leaded gas sales were virtually the same in 1960 and in
1980, three years after the peak sales in 1977. But 17 years after the second of
these dates, the 14-17 and 18-24 homicide rates had only fallen from their peak
values to 1.5 times their earlier base rates. Although other factors contribute to
rates of violent behavior, the impact of socioeconomic or demographic causes of
homicidal behavior seems to have been strengthened at the same time due to
increasing SiF usage. Combined with other evidence presented here, this
suggests that violent crime rates peaked around 1992-94 and subsequently
declined in part due to the changing sales of leaded gasoline, with effects
modified by other likely environmental influences such as SiF usage as well as
more conventional socio-economic or cultural factors.
Finally, since lead neurotoxicity has also been implicated in ADHD and
other learning disabilities (Tuthill 1996; Needleman 1999), we have also begun
to explore the possibility that rates of these learning problems are higher in
communities that treat water supplies with silicofluorides. A first test, using an
informal survey in a set of small New York cities with populations between
40,000 and 70,000 with and without SiF treated water, showed risk ratios of
about 1.38 both for high school students coded with a learning disability and for
students receiving medication for ADD/ADHD.
These findings are congruent with data linking environmental pollution,
alcoholism, and substance abuse to crime (see Wilson and Petersilia 1995, Ch.
13). Diverse research perspectives are thus consistent with neurotoxin-induced
dysfunctions that increase alcohol and drug usage as a crude form of self-
medication. Because substance abuse can in turn exacerbate learning deficits
and antisocial behavior, this perspective suggests that neurotoxicity may be one
of the triggering factors in a multifactorial system leading to increased risks of
anti-social behavior (Masters, Coplan & Hone 1999b).

TOWARD THE SOCIAL SCIENCE OF THE FUTURE

Paul MacLean's evolutionary neuroscience and its applications illuminate a

deep flaw in conventional social science: the attempt to study human social
behavior in abstraction from the way the brain evolved and how it actually
works in contemporary environments. Our industrial and technological civili-
zation adds elements into the environment that the brain did not confront and to
which it did not adapt in its long process of evolution. Significant among these
elements is industrial pollution of the environment with heavy metals. The
analysis of this heavy metal pollution as a risk co-factor in learning disabilities,
substance abuse, and crime shows that linkages go far beyond merely insightful
historical footnotes. Indeed, this approach touches the very heart of many vital
public policy debates.
Pollution, Brain Chemistry, and Violence 293

It should be obvious that examining the possible behavior effects of lead and
other toxic elements is far from a "reductionist" approach to human behavior.
Many other factors, including genes, diet, socioeconomic status, demography,
and technology come into play. While the ban on the sale of leaded gasoline was
based on a general notion of the dangers of lead toxicity, political dialogue,
prudent judgment, and effective decision-making—not some automatic effect of
heavy metals themselves—were the basis of this public policy. Indeed, the
toxicity of leaded gasoline was well known to those who introduced it, and the
original approval of its use rested on economic and political interests rather than
science.
Integrating environmental factors such as pollution with evolutionary
neuroscience in the study of behavior adds something of great importance to our
knowledge. The data presented above, for example, suggest that the public
policy decision to ban leaded gasoline may have been far more effective than
even its most fervent supporters have imagined.
These effects also cast new light on the political bias that surrounds many
environmental issues. On the left, social ills are often blamed on economic or
cultural factors that have been described as "socially constructed." On the right,
the costs of environmental legislation have often been said to exceed its benefits
by far. If our data are valid and predictive, neither side has even begun to under-
stand the true dimensions of our social problems and the gains from dealing with
them in a scientifically effective manner.
Whether we are assessing the consequences of established policies or
proposing new initiatives, it is increasingly necessary to follow Paul MacLean's
footsteps into the challenging, complex, and utterly fascinating terrain that links
disciplines that have too long been ignored by conventional social scientists. In
the long run, such interdisciplinary perspectives must transform the insularity of
academia if our civilization is to survive the technological changes that will
continue to assault us in the 21st century.

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 PART VI

SOCIAL PSYCHOLOGY A N D
SOCIAL THEORY
 16

REIFICATION AND HEGEMONY: THE

HUMAN BRAIN AS THE LINKAGE
BETWEEN MACRO AND MICRO LEVEL
POLITICAL PHENOMENA

Steven A. Peterson

INTRODUCTION

One of the most interesting of human phenomena is the tendency of people to

give their beliefs superordinate status over those ideas' creators. This is often
termed reification (sometimes hypostatization) when those ideas are taken as
"givens" and as being external to the individuals who created those ideas. This
chapter explores the psychobiological bases of human reification. It also
discusses how the individuals' tendency to reify can produce social stability. To
use Antonio Gramsci's (1957) terms, if individuals within a society have similar
reifications and accept these, then a society wide hegemony can develop. One
important contributor to the development of this project has been Paul MacLean.
His research and theoretical work both inform much of the argument developed
below. While one may disagree with aspects of MacLean's thought, his body of
research provides valuable insight into a psychobiology of reifying.
In this chapter, we consider the following: A. The nature and underlying
psychobiology of reification; B. The nature of hegemony and how the tendency
to reify can support the development of hegemony; C. The extent to which
people can come to be less subservient to their own creations and live in, for
want of a better term, a more "authenticated" world; D. The value of the work of
Paul MacLean in illuminating various aspects of this project.

REIFICATION DEFINED

A common human phenomenon is holding fiercely to a deeply held view,

value, concept, or idea and, perhaps, accepting this as "outside" ourselves and a
guide to our behavior. In the process, one comes to perceive this as a "given" or
300 The Evolutionary Neuroethology of Paul MacLean

as "in the nature of things." Philosophers have referred to this as reification or,
perhaps more accurately, hypostatizing, attributing "a separate or higher reality
to something, thus abstracting it from its relationship of dependence on other
things." (Clark 1976: 6). Reification is a process by which values, beliefs, and
other human "creations" become transmuted into "things-in-themselves," and
are considered apart from the human activity that actually created them. Berger
and Luckmann define reification in much the same terms, when they note that
this is "the apprehension of human phenomena as if they were things, that is, in
non-human or possibly suprahuman terms . . . [R]eification is the apprehension
of the products of human activity as if they were something else than human
products—such as facts of nature, results of economic laws, or manifestations of
divine will." (1966: 89).
The irony of the human ability to create a conceptual world is that its
products may be accorded superordinate status over their creators—perhaps as
the delusions of schizophrenics become seen as "outside" them (for more
complete discussion of this analogy, see Peterson with Sicherman 1995) It
seems very easy for people to come to accept living in a world of abstractions,
which they consider as guides to their behavior.
Only when there is questioning of the dominant, reified values guiding the
1
people are there likely to be significant prospects for change. One must no
longer view the totality of reigning values, products of human relations, as
things-in-themselves, as eternal verities, as superordinate guides to behavior.
One must discern that these things are actually creations of human activity, not
2
separate from that activity, and, therefore, changeable or endable.

NEUROPHYSIOLOGICAL BASES OF REIFICATION

Reification is a complex phenomenon; few such behaviors are going to be

localized in a single area within the brain. Uttal has summarized the implication
nicely when he states that (1978: 342): "almost all complex behaviors can be
affected by almost any part of the brain and that the sort of localization that
occurs must be interpreted more in the form of a system of interconnecting
nuclei than in terms of any theory of sharply demarcated functions of single
centers." The psychobiological roots of reification are important to consider,
since their very existence indicates that part of the human condition is an ease of
creating abstractions which then escape our control, being transmuted into
things-in-themselves, and which ultimately lead us to accept the transcendence
of our own creations. That is, it is easy for us to overconceptualize the world and
create and accept grand explanations. It is as if we are designed to search for a
faith, for concepts to subordinate ourselves to (on the evolutionary advantage of
this, see Peterson 1981. On pathologies associated with this, see Peterson with
Sicherman 1995).
Reification and Hegemony 301

ORGANIZING CONCEPT: THE SCHEMA

Arbib, Erdi, and Szentagothai (1998) have argued that the concept of the
schema is central to linking brain function with brain structure. A schema is the
brain's internal representation of "reality" "out there." These structures help
make sense of a complex world, a world producing a wide array of stimuli
which impinge upon the individual. Morton Hunt notes (1982: 173):

Our method of making categories has a simple and obvious biological rationale: it is
the mind's way of representing reality in the most cognitively economical form. In the
real world . . . traits occur in 'correlational structures'; observable characteristics tend to
go together in bunches . . . We may not have innate ideas . . . but our minds filter and
compile incoming data in such ways that we tend to form prototypes and categories
without help or instruction.

The basic idea of schema theory is that much of what people see and
comprehend about the world is more closely tied to the internal schema than to
the external stimulus itself. As a theory of comprehension, schema theory states
that we often understand only those events that are consistent with our schemata,
and that we either ignore or misunderstand those events that are not. As an
orientation toward memory, schema theory states that enduring memory does
not typically occur independent of schemata. If our comprehension of things is
guided and organized by schemata, so is our memory.
Arbib et al. claim that their (1998: 35) "contribution has been to provide a
schema theory that can bridge from the external characterization of function to
the interactions of brain regions and the inner workings of neural circuitry."
They consider two categories of schema—a perceptual schema and the motor
schema. In the process, they attempt to, then, link perception and action. In the
final analysis, they note that through the schema (Arbib et al. 1998: 344), "The
brain 'models' the world so that when we recognize something, we 'see' in it
things that will guide our interaction with it." Ulric Neisser, a leading cognitive
psychologist, speaks generally of the psychobiological roots of schemata (the
plural form of the term schema) (1976: 54):

From the biological point of view, a schema is part of the nervous system. It is some
active array of physiological structures and processes: not a center in the brain, but an
entire system that includes receptors and afferents and feed-forward units and efferents.
Within the brain itself there must be entities whose activities account for the modifiability
and organization of the schema: assemblages of neurons, functional hierarchies,
fluctuating electrical potentials, and other things still unguessed.

G. J. Dalenoort (1982) has suggested that cell assemblies underlie schemata.

Representations are stored in dispersed cell assemblies in humans' long term
memory (LTM). Reifications are one subspecies of schemata. They are internal
representations of ideas that people transmute into reality "out there." Thus, one
part of a psychobiology of reification is to explore the neurological roots of
schemata.
302 The Evolutionary Neuroethology of Paul MacLean

THE NEUROPHYSIOLOGY OF REIFICATION

In the following paragraphs, we consider the following brain areas: the basal
ganglia, the thalamus, the hypothalamus, the limbic system, the neocortex (is
there hope for creating a more authentic world here?), and an internal reward
system based upon either (both) endogenous opiates or (and) dopamine. (For a
detailed atlas of the human brain, see Mai, Assheuer, and Paxino 1997.)
To help guide the discussion of a neuropsychology of reification, Figure 16.1
outlines a circuit diagram suggesting the substrates for reifying; text elaborating
upon this model is presented below (the author freely notes that experts advance
somewhat different sets of afferents and efferents to each of the brain structures
in the circuit diagram; thus, the diagram in Figure 16.1 is something like a
"consensus" version).

Figure 16.1. Circuit Diagram for Reification

Basal Ganglia

Key structures in the basal ganglia include the substantia nigra (very
important for producing a key neurotransmitter, dopamine), the neostriatum
(composed of the putamen and caudate nucleus), and the globus pallidus.
The basal ganglia have traditionally been looked at as central to motor
control (e.g. Arbib et a l l 9 9 8 ; Cote & Crutcher 1991; Denny-Brown 1962;
Beatty 1995; Rolls & Williams 1987). However, studies suggest that these
Reification and Hegemony 303

centers can have a measurable impact on aggression (Senault 1979), arousal

(Hornykiewicz 1966), learning and memory processes (e.g., Crosson 1990,
1997; Gambarian, 1979; Gambarian et al. 1979; Middleton & Strick 1994; Kolb
& Whishaw 1996), species-typical (or, in more common terms, "instinctive")
behavior (Murphy et al. 1981), neglect (Heilman, Watson, & Valenstein 1997)
language (Crosson 1990), and some cognitive functions (Beatty 1995; Cools &
van den Bercken 1977; Middleton & Strick 1994; Oberg & Divac 1979).
Among the very young, the basal ganglia may even substitute somewhat for
damaged or not yet developed functions of the neocortex (Teuber 1976;
Buchwald et al. 1975).
What of reification or hypostatization? Paul MacLean argues, based upon his
experimentation across a range of animal species, that:

The reptilian brain [neostriatum and pallidum] seems to be hidebound by precedent.

Behaviorally, this is illustrated by the reptile's tendency to follow roundabout, but
proven, pathways, or operating according to some rigid schedule. Customs of this kind
appear to have some survival value and raise the question to what extent the reptilian
counterpart of man's brain may determine his obeisance to precedent in ceremonial
rituals, religious convictions, legal actions, and political persuasions (1973: 10).

Repetitiveness appears to be one behavior associated with this (MacLean

1990: 150, 236-238). That is, abstract ideas as guides to behavior may be
elemental products of the operation of the basal ganglia. People can, as a result,
come to cling jealously and zealously to tradition and habit and this might be
generalized to ideas, beliefs, and values (and see MacLean 1990; Keyes 1992).
In another essay, MacLean elaborates (1972: 146-147):

Is it possible that through these neural elaborations nature has revamped the striatal
complex so that it serves as a playback mechanism not only for ancestral behavior, but
also currently learned performance? We close with one more thought. It is traditional to
belittle the role of instincts in human behavior. But how should we categorize those
actions that seem to stem from a predisposition to ritualistic, compulsive, or imitative
behavior . . . or to a propensity to seek and bow to precedent?

The extension to hypostatizing is obvious. Afferents (incoming nerve fibers

to a particular brain structure) to the neostriatum (NS) come from all areas of the
cerebral cortex, from various nuclei in the thalamus, and from the substantia
nigra (e.g., Cowan & Powell 1966; Peele 1977). Efferents from the NS (fibers
leaving a brain center) project to both the substantia nigra and the pallidum
(Carpenter 1991; Beatty 1995). The pallidum receives projections from the
cerebral cortex, the thalamus, and the substantia nigra (Peele 1977). In turn, it
projects nerve fibers to several nuclei in the thalamus, in particular, the lateral
ventral, anterior ventral, and centrum medianum nuclei (Kemp & Powell 1971;
Peele 1977).
304 The Evolutionary Neuroethology of Paul MacLean

Thalamus

The thalamus receives afferents (incoming nerve signals) from the pallidum
and substantia nigra in three of its nuclei—the lateral ventral, anterior ventral,
and centrum medianum. Additional relevant afferents for these nuclei include
the neocortex and other thalamic nuclei, making them uniquely situated to
correlate and integrate input from a wide variety of brain centers. The lateral
ventral and anterior ventral nuclei project to both motor and sensory areas of the
neocortex (Peele 1977). The centrum medianum projects to the neostriatum
(NS), completing a neostriatum - > pallidum - > thalamus - > neostsiatum loop.
It also projects to other thalamic areas, such as the dorsomedial nucleus which,
in turn, has nerve connection to the hypothalamus and amygdala, the latter a key
center in the limbic system (Peele 1977: 291-294). Peele has suggested that
(1977: 293) "the dorsomedial nucleus would appear to be involved in
mechanisms underlying emotional expression" and that this nucleus projects to
both the neostriatum and the pallidum. This series of connections may provide
the link between "affect" (centered to a large extent in the limbic system, the
seat of emotions) and "rigidification" (centered to some extent in the basal
ganglia).
Functions of the thalamus vary across nuclei, as implied in the previous
paragraph. The dorsal tier nuclei seem associated to some extent with the
"mobilization of mental energy," speech, and memory (Fuster 1973; Bennett
1977: 202-205). Some studies have indicated that lesions in the anterior nuclei
are related to diminished emotional reactivity in some animal species. The
dorsomedial nucleus appears to have both inhibitory and initiating centers for
emotional behavior (Bennett 1977: 143-144). The latter nucleus, once more,
projects nerve fibers to both NS and pallidum, linking the basal ganglia to the
thalamus.
The thalamus is apt to be a part of the system involved in organizing the
propensity to take part in reifying or hypostatizing because of its role as a relay
station to the neocortex. It is centrally located so that it can collate information
from a variety of areas that send data to the neocortex through thalamic nuclei
(Clark 1975; Kelly 1991; Kelly & Dodd 1991; Lezak 1995).

Limbic System

Some experts argue that the limbic system is a basic center for species-
specific behavior. Schmidt, for instance, has claimed that for humans this would
translate into "'emotions,' 'affective behavior,' 'feelings'. . . In this sense one
function of the limbic system would be to control the expression of the
emotions"(1978: 266). Thus, the limbic system—and especially the amygdala
and septum—is key to understanding emotion (Beatty 1995; Lezak 1995).
MacLean has applied this general perspective to the expression of affect
toward values and beliefs. He notes (1977: 319):
Reification and Hegemony 305

It is of special epistemological interest that at the beginning of a limbic discharge, a

patient may have an intense free-floating feeling of what is real, true, and important or
experience eureka-type feelings such as occur in mystical revelation or under the
influence of psychedelic drugs. Ironically, it seems that the ancient limbic system has the
capacity to generate strong affective feelings of conviction that we attach to our beliefs,
regardless of whether they are true or false!

Elsewhere, MacLean has noted that sensations associated with epileptic

seizures—associated with limbic discharges—include (1990: 48) "the feeling
that what is happening or what one is thinking at the moment is all important;
feelings of certainty and conviction; and feelings of revelations of the truth." If
he is correct, this would seem to link the limbic system with affective coloration
of reified values or concepts; that is, the limbic system adds emotion to reified
values and beliefs (and see Isaacson, 1982; on questions about the limbic system
concept, see LeBar & LeDoux 1997).

Neocortex

People view the neocortex as the seat of higher cognitive and intellectual
functions. This view, as we have already seen, is oversimplified, since other
brain centers are also involved in such functions. Nonetheless, as Gardner has
put it: "Human behavior is correlated to a large extent with the relatively
massive size of the forebrain. Here reside most of the mechanisms governing
learning, memory, intelligence, language, emotion, and behavior" (1975: 3 7 4 -
375).
Different areas of the neocortex have extensive connections with many of the
structures thus far noted. Efferents from all parts of the neocortex project to the
basal ganglia, the thalamus, the limbic system, and—indirectly—the hypothala-
mus. In turn, the neocortex receives nerve messages directly from the limbic
system and thalamus and indirectly from the basal ganglia and hypothalamus
(Gardner 1975; Peele 1977). This set of connections raises the possibility that
there can be a cortical overriding of holding fiercely to ideas. Schmidt, for
instance, has noted that (1978: 306) "one of the roles of the frontal lobes is
related to the learned control of innate behavior pattern."
The neocortex has an important role in emotional processes. The limbic
system does not work alone to produce affect. Connections between the neo-
cortex and the limbic system suggest that (Schmidt 1978: 266) "it is in the
neocortex that environmental events receive their affective coloration and thus
their 'meaning' to the organism." In short, the limbic system produces primitive
emotions and the neocortex interprets these. Extensive reciprocal connections
between the frontal lobes of the neocortex and the limbic system indicate that
this neocortical area has as one role the learned control of species-specific
behavior patterns and emotions (Schmidt 1978: 305-306). Clinical findings,
indeed, show that frontal lobe problems are associated with difficulty in
controlling behaviors and emotions (e.g., Beatty 1995).
306 The Evolutionary Neuroethology of Paul MacLean

Randall Sengel (1979) has linked memories with emotion in his delineation
of a neurological basis for cooperative behavior (For political applications, see
Davies 1976). His central hypothesis is that (1979: 49) "during human
evolution, the emotional states associated with defense, competition, and
hunting could reinforce successful cooperative behavior through the influence of
the limbic system and/or emotionality for social behavior." The author notes that
the limbic system links affect with memory and learning. Sengel asserts that
(1979: 50): "It is assumed that any perceptual experience which acquires an
emotional connotation during memory storage will, upon recall and comparison,
endow current experience with emotional and motivational significance." In like
fashion, learning of ideas or concepts can, through limbic system connections,
cloak these abstractions with affect. (For an argument which relies on
holological theory and comes to similar conclusions, see G. Schubert 1983.)
Sengel's argument is a good base upon which to elaborate some of the
cognitive functions of the CNS. Incoming information is processed and may be
stored in long-term memory. Preexisting schemata help to shape how memories
are stored. Information may be either assimilated (fit into an existing schema) or
lead to accommodation (in which a schema changes somewhat to take into
account new information). Assimilation is likely to take place under normal
circumstances, as we tend to be conservative with our schemata. That is, we tend
to assimilate information to fit with our existing schemata. And, to complete the
argument with respect to hypostatizing, a reification is simply a schema, a
mental representation of a concept, value, or belief.
Returning once more to Sengel's argument, these reifications would be
linked with the limbic system and, hence, affect. It is also easy to see how these
reified notions could be linked to the neostriatum where "rigidification" takes
place.

BIOCHEMISTRY OF REIFICATION (THE INTERNAL

REWARD SYSTEM)

The actual motivation to reify ideas and beliefs may be a product of what
James Danielli (1980) once referred to as the "internal reward system." Danielli
asserts that his overall argument becomes more plausible in light of recent work
on CNS opiate peptides-enkephalins and endorphins, substances which have
both analgesic (pain-reducing) and euphoric effects. Studies suggest that such
substances could underlie this reward system. Others have suggested that
dopamine, another significant product of the basal ganglia (especially the
substantia nigra), could be associated with reward (Depue & Collins 1999). The
naturally occurring opiates are concentrated in the pallidum, caudate nucleus,
hypothalamus, thalamus, and amygdala and affect the firing of neurons in other
areas of the brain such as the hippocampus and neocortex (e.g., Guillemin 1978;
Pert 1978).
Solomon Snyder has said of the opiates' functions: "The dorsal medial
thalamus is strongly associated with frontal and limbic cortical areas involved in
Reification and Hegemony 307

emotional regulation and so may relate to the euphoria produced by opiates."

(1978: 307). His contention suggests a tie-in between orchestration of affect by
interacting brain centers and enkephalin neurons in the thalamus. Very specifi-
cally, Stein and Belluzzi say that endorphins may serve as transmitters in neural
systems for the mediation of pleasure and reward (1979: 375). Their work
indicates that the endogenous opiates serve as reinforcers. Significantly, though,
we also find that dopamine may serve some of the same functions (e.g., see
Lippa et al. 1973; Rolls et al. 1974).
Danielli has speculated that analogous processes underlie small-group and
large-group social activities. In both instances, release of the opioid peptides
would subserve motivation to carry out specific behaviors related to small
groups (e.g., play or social grooming) and large groups (e.g., religious rituals or
spectator participation at football games and other "mob activities").
It is logical to extend Danielli's argument into the realm of ideas and beliefs.
Danielli has asserted, in short, that humans do certain things because it feels
good to do so. The mechanism for this could be the opioid peptide-rooted
reward system or a dopamine-based one. Just so, such a system could also
encourage people to think certain things because it would feel good to do so.
Therefore, the hypostatizations which people learn (rigidified through the basal
ganglia and charged with affect through the limbic system) may upon their
exercise activate the internal reward system and reinforce, by the "pleasure" thus
induced, their continued acceptance by the individual and behavior consistent
with these.

SUMMARY

Reifying and the brain may thus be wed. Social conditioning brought on
through a concurrence of messages transmitted and reinforced by influential
agencies of socialization (e.g., religion, the family, the media, schools, and so
on) leads to an increased probability of individuals learning appropriate sets of
values and beliefs. Mechanisms underlying learning and memory would process
these and then store them in long-term memory. Coupling these values with the
internal reward system would provide a motivation for adherence to these values
and behavior consistent with them. The euphoria associated with deeply held
values would lend these great potency (through the release of endogenous
opiates or dopaminergic reinforcement). Corticostriatal connections, in turn,
would rigidity these values, possibly through dopaminergic (e.g., Broekkamp et
al. 1977) and/or endorphinergic reinforcement. Extensive reciprocal cortico-
limbic and indirect pallido-limbic links through the thalamus would provide the
means whereby values stored in long-term memory and rigidified by neostriatal
processing would be clothed in affect, once more, through the reinforcing effects
of dopamine and/or endorphins.
Finally, cortico-striatal, corticothalamic, and cortico-limbic pathways would
allow for the conscious override of hypostatized values and beliefs and their
effects. How easy or difficult the override would be is a function of the extent to
which the values have been conditioned and reinforced in the first place.
308 The Evolutionary Neuroethology of Paul MacLean

Nonetheless, cortical efferents from integrative centers provide a theoretical

basis for positing this override potential. Thus, there is a place for human will
within this model.

T H E C O N C E P T O F H E G E M O N Y : ITS P O L I T I C A L S I G N I F I C A N C E

The Italian Marxist Antonio Gramsci elaborated the idea of hegemony in the
early part of the twentieth century; his views represent the starting point for
analysis. Gramsci's hegemony emphasizes how values supportive of dominant
interests in society get passed on to the masses and thereby, once accepted by
the multitudes, come to reinforce the domination of the existing elite. Dawson,
Prewitt, and Dawson state that (1977: 26):

Hegemonic theory starts with the assumption that government would not be possible
unless the strains and tensions associated with the unequal allocation of values in society
were somehow muted . . . Unless the losers come to see that the way things are is
'natural' or 'appropriate' or 'legitimate,' social disruptions are likely. Socialization is
viewed as the learning that leads the losers to accept the way things are, even to think that
the way things are is in their best interests.

Normally, citizens come to accept things the way that they are—as benign,
useful, legitimate, and "right." As Gramsci puts it, "humans are (1957: 59)
conformist to some conformity." This supports the continuation of the status
quo—and, by definition, those who benefit from the current state of affairs
maintain their sway with this sort of mindset. Those who are powerful and
wealthy will stay that way, in part, because the bulk of the people accept this
situation. How do the mass of people come to accept values that lead to their
continuing status as losers in the struggle for life and reward? Williams,
summarizing Gramsci, states that hegemony is: "an order in which a certain way
of life and thought is dominant, in which one concept of reality is diffused
throughout society in all its institutional and private manifestations, informing
with its spirit all taste, morality, customs, religious and political principles, and
all social relations, particularly in their intellectual and moral connotations"
(1960: 587).
The basic premise is that those in power who control the economic and
political structures also control the transmission of messages, the views of
reality, to the masses. In a capitalist society, those who are not wealthy are
continually told that (a) if they work really hard, they can make it and get rich—
so do not rock the boat and jeopardize your chances of joining the elite; (b) if the
elite get wealthier, then this will trickle down and benefit those who are not in
the ranks of the well-to-do. By being told this over and over, the mass of people
come to accept their status in society and allow the powerful to stay powerful,
the wealthy to stay wealthy.
Hegemony, according to Gramsci, is the result of a bloc of interests united
behind a common set of values and norms, which—upon being transmitted to
Reification and Hegemony 309

the mass of people through the many institutions of society—reinforce the

power of that bloc. Although a hegemony tends to be stable, change can take
place, perhaps through the emergence of a politically conscious working class.
The power of hegemony is illustrated by what did not happen during the
1930s. Think about this for a moment. At the depth of the Great Depression,
nearly one quarter of the American work force was unemployed. That rate was
still in the upper teens later in the 1930s. Should one not have expected a
growing and radicalized American working class demanding major changes in
the system? Obviously, a working class movement demanding major changes
did not develop.
Hegemony may help to explain this. Polls from the late 1930s asked a sample
of Americans the extent to which they supported the free enterprise system. A
clear majority of every social group examined supported capitalism—even
among the unemployed working class. More telling, only a minority of
unemployed working class people had anything like "class consciousness," a
sense of themselves as workers having an interest in opposition to a capitalist
class.
Why did a working class consciousness and support for radical change not
emerge among the unemployed working class? Poll data show, simply, that the
working class—including those who were unemployed—accepted individualist
and liberal ideals. In short, those workers most likely, one would think, to
challenge the legitimacy of the system accepted the key tenets of liberalism; as a
result, they did not develop a class consciousness. Liberal hegemony dampened
the chances of a major working class movement to challenge the system (Verba
& Schlozman 1977).

SOCIOBIOLOGY OF REIFICATION: THE LINK TO HEGEMONY

One argument advanced in this chapter is that the individual's tendency to

reify may be linked to the society wide hegemony that can develop. What
mechanism is available to explain this link between the micro and the macro
levels? Sociobiology appears to provide an explanation.
One requirement for reproductive success in social species is group stability
and social order. Alexander states that humans accept limitations (in the form of
justice, ethics, and morals—all reified notions) on absolute freedom. He
suggests (1975: 96) that "individual humans tolerate such restrictions because it
has for millions of years been less profitable reproductively to go it alone."
Edward O. Wilson elaborates in his discussion of religious beliefs:

The extreme plasticity of human social behavior, Bergson notes, is both a great strength
and a danger. If each family worked out its own rules of behavior, the society as a whole
would disintegrate into chaos. To counteract selfish behavior and the dissolving power of
high intelligence and idiosyncrasy, each society must codify itself. Within broad limits
any set of conventions works better than none at all. Because arbitrary codes work,
organizations tend to be inefficient and marred by unnecessary inequities . . . .
 The Evolutionary Neuroethology of Paul MacLean

But the arbitrariness of sanctification engenders criticism, and within the more liberal
and self-conscious systems visionaries and revolutionaries set out to change the system.
Their ultimate purpose is to elevate codes of their own devising. Reform meets
repression, because to the extent that the reigning code has been sanctified and
mythologized, the majority of people regard it as beyond question, and disagreement is
defined as blasphemy (1978: 185-186).

Here, Wilson is working at the society wide level of analysis. The important
point is that even arbitrary codes may be sanctified. When these systems of
sanctification exist and are accepted pretty much as given by the mass of people,
then the odds of social order are much increased providing, in the final analysis,
an environment more conducive for individuals' reproductive success.
Conformity to sanctifications (which are, to use our terminology, reified values)
confers, then, reproductive advantage to individuals. Wilson further states:

The ability of individuals to conform [recall Gramsci's phrase: "conformist to some

conformity"] permits them to enjoy the benefits of membership with a minimum of
energy expenditure and risk, and their behavior is sustained over long periods of time as
the norm. Although the rivals of the conformists in the society may gain momentary
advantage through selfishness and irreverence, it is lost in the long run through ostracism
and repression (1978: 187).

The key point is that when individuals accept certain values within a society
as given—as they reify these values—this influences social stability which, in
turn, affects individuals! reproductive success. Thus, through inclusive fitness
doctrine, we can hypothesize that there is a selection advantage for people to see
the world populated with reifications standing apart as "ideas become real."

DISCUSSION

Is it possible to live in a world without the dominating presence of reifica-

tions as guides to human behavior? Martin Heidegger warns against over-
theorizing and overconceptualizing. For Heidegger, the study of phenomenology
"expresses a maxim which can be formulated as T o the things themselves.' It is
opposed to all free-floating constructions and accidental findings" (Heidegger
1967: 295). For humans to understand what it is that is "out there," we should
try to prevent our preconceptions and problematic methodologies from obscur-
ing the nature of the things themselves that we are observing. As Calvin Schrag
puts it, "The data are always prior to man's logical and epistemological theories
concerning them." (1967: 279).
Following Heidegger, one might argue that we need to prevent overtheor-
izing and overconceptualization and to get back to "the real," to the things of life
themselves. Of course, this is too easy, since it is pretty clear that humans'
preconceived notions inevitably shape their interpretation of the world around
them. Human cognition and the human brain probably make this so (Peterson
1981). However, human "will" can play a role in at least reducing the
Reification and Hegemony 311

unthinking tendency to act almost delusionally in accepting reified values and

beliefs without much question (on the analogy between accepting reifications
and schizophrenia, see Peterson with Sicherman 1995).
Recall the argument that the neocortex is in a position to override unthinking
adherence to reifications. "Normal" people are in a position that schizophrenics
are not—in a position to will themselves back to "reality" and out of the dream
world of reifications.
To live in a de-reified (or, perhaps, more positively stated—an "authentic"
world) world would be difficult to achieve and even more so to sustain. Berger
and Pullberg (1965) argue that while something like widespread de-reification
might take place, new sets of rigidified values would normally rather quickly
spring up to take their place. Anthropologist Vernon Reynolds has said:

It is because the norms of social life are taken by people as givens that they react to them,
whether by conformity or deviance, in such powerful ways. Once their arbitrariness is
grasped they lose their power, and the individual is 'free.' Once the 'implicit' becomes
'explicit' we see it for what it is—an idea, a construct in the minds of those around us
that earlier we shared.
But, in de Musset's words, 'qui s'eleve, si'sole.' The price for standing apart, for
observing, for ceasing to be engage is the very price of freedom—a falling apart of the
security structures of the mind, a frightening took into the unknown . . . (1976: 206, 209):

What sociologists have called "reification" of social norms and situations,

i.e., the process by which the individual comes to believe in the reality and fixity
of social forms, can be seen as a sanity-promoting process. Reynolds, it follows,
concludes that de-reification would be most difficult to sustain.
What would an "authenticated" world look like? A Hobbesian war of each
against all, without commonly held values to maintain social order? A world in
which people would learn to appreciate the myriad different understandings of
different people with differing experiences? Or is the question absurd, given that
humans are likely programmed to view the world in a reified manner? These are
the key, larger issues that future discussion ought to focus upon.

NOTES

1. Of course, as Donald Keyes reminds us (personal communication), there may be

benign hypostatizations (or reifications which actually serve useful social purposes. He
suggests a project of differentiating benign from non-benign reification. Indeed, this
distinction probably calls for elaboration, but that is beyond the scope of this paper.
2. There is an interesting analogy between hypostatizing and certain schizophrenic
symptoms (For full argument, see Peterson and Sicherman 1995) Believing that the
products of human activity are outside of human control and are "given" to us, is on its
face, delusional—just as DSM suggests for religious and other cultural groups with
strongly held beliefs. In such cases, people's sense of identity gets lost and overwhelmed
by the values that they have adopted—they become playthings of a higher or external
force (witness David Koresh's acolytes, willing to burn to death to follow him in their
delusion that he was the Messiah come back). This is, in form, little different than the
312 The Evolutionary Neuroethology of Paul MacLean

delusions and hallucinations that can drive the behavior of schizophrenics. The question
is: who's normal and who's crazy?(see Rosenhan 1973). Individuals will become guided
by higher values or beliefs, and one continues to behave, perhaps appropriately, when
there are abundant data that one is following the wrong course of action. Obviously,
when one meets a schizophrenic in the acute stage of the problem, one knows that a
schizophrenic is not a normal person. But is it so very different in kind (albeit it is in
degree) to see a true believer in action, ignoring facts from the surrounding world in order
to promulgate and continue supporting his or her religious values? Or political views? Or
personal philosophy? This is a question worthy of serious refection.

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 17

UPSHIFTING AND DOWNSHIFTING THE

TRIUNE BRAIN: ROLES IN INDIVIDUAL
AND SOCIAL PATHOLOGY

Kent Bailey*

INTRODUCTION

This chapter represents the most current application of phylogenetic regression-

progression theory. I introduced my approach to phylogenetic regression over 20
years ago (Bailey 1978) and subsequently addressed it in several publications
(Bailey 1985, 1987a, 1988, 1991). The regression-progression approach has,
from the outset, drawn heavily from MacLean's triune brain formulation (Bailey
1987b). This chapter refines and extends my general theory and details how the
vagaries of human experience may be construed in terms of dynamic patterns of
regression and progression. Finally, the theory is applied in a brief analysis of
the Columbine killings in April 1999 where two young men—Eric Harris and
Dylan Klebold—killed 12 classmates, a teacher, and themselves in an "inexpli-
cable" act of violence.

HIERARCHIES OF MODULES AND ADAPTATIONS

Modern evolutionary psychology views the human brain as a collection of

highly specialized neuromodular coordinations that evolved to solve specific
fitness problems in the environments of evolutionary adaptation (EEAs) of
human evolution. Various deep-structure modules subserve fundamental pro-
cesses of memory, sensation/perception, spatial orientation, nonverbal and
verbal communication, behavioral coordination and output, intuitive processes,

* I wish to thank Valerius Geist for his personal support and for his clear delineation of
"classic regression." Thanks also to the many people who provided helpful feedback
including Patrict Callahan, Paul Gilbert, and Bill Tillier.
318 The Evolutionary Neuroethology of Paul MacLean

and cognition (Matlin & Foley 1992); these co-integrate in numerous ways to
form complex motivational/emotive/behavioral/conceptual adaptations of the
human mind (Kendrick, Sadalla & Keefe 1998). The Swiss Knife metaphor
(Cosmides 1994) is frequently used to characterize the specificity/functionality
of module-based adaptations such as male jealousy, kin recognition, space
preference and territoriality, sexual orientation and mate preference, strategies
governing reciprocity (Cosmides & Tooby 1992), balanced social relations
(Bailey 2000), and so on (see Pinker 1994). Unfortunately, we do not have a
reasonably complete neurohistological, neurochemical, or neurofunctional
understanding of any single module, and integrated adaptations are even more
elusive. We are even more in the dark regarding how various modules/
adaptations excite, inhibit, complement, or otherwise interact with each other.
The implicit hierarchical arrangement of the various modules and adapta-
tions adds another important level of complexity. Clearly, modular processes/
adaptations differ in ancestral history and complexity ranging from the wood
tick's reaction to a single molecule of bombykol (see Bailey 1987b), to the
specialized bug detector units in frog's brains (Lettvin et al. 1959), to the highly
integrated hormonal and neural mechanisms underlying maternal behavior in
rats (Fahrbach & Pfaff 1982), to the neurologically circumscribed lateral hypo-
thalamic stalk and attack patterns in cats (Moyer 1976), and, finally, on to the
neocortically mediated conceptual modules of human beings. The brain and its
functions have been viewed hierarchically over most of the history of neuro-
science (Smith 1992), and it is important to focus on how ancestrally older and
newer motivational/behavioral/cognitive systems operate in the vertical dimen-
sion.
Neuroscientists are making steady progress in mapping complex functional
relationships across vertical levels of the brain. For example, Le Doux's (1996)
model of fear and aversive conditioning features hierarchical co-integration of
phylogenetically older and newer brain systems that govern processes of learn-
ing and extinction, escape responses, memory of past fear experiences, and, in
humans, various subjective meanings associated with threatening and dangerous
events. At the simplest level of Le Doux's model, the amygdala identifies and
processes potentially dangerous stimuli quickly, reactively, and nonconsciously
in a strict stimulus-response or releaser-action pattern. The amygdala represents
a kind of "triggering device for the execution of survival functions" (Le Doux
1996: 224), and, under circumstances of extreme threat or when higher functions
(e.g., the hippocampus or prefrontal circuits) are disabled, the amydala can
operate essentially on its own. In humans, emotional reactivity and response to
threat typically operate within a complex, hierarchical feedback system involv-
ing the amygdala, the hippocampus, and the prefrontal neocortex where the
latter two systems exert modulatory control over the automatic and quick-
reacting amygdala. Given that connections "down" from the higher two centers
are weaker than connections "up" from the amygdala (Le Doux 1996), fairly
frequent neurological regression or shortcircuiting of the more advanced
amygdala-hippocampus-prefrontal neocortex would be expected: "This may
explain why it is so easy for emotional information to invade our conscious
Upshifting and Downshifting the Triune Brain 319

thoughts, but so hard for us to gain conscious control over our emotions" (Le
Doux 1996:265).

THE BRAIN AS AN O R G A N OF INHIBITION

The human brain operates primarily as an organ of inhibition (see Smith

1992). With the brain's 100 billion or so neurons and the possibility that any one
neuron can have synaptic connections with perhaps ten thousand others (Wilson
1999), the possibilities for neural outputs far outnumbers the particles in the
universe (Restak 1984). Moreover, Restak (1984) states that the brain's potential
for creating and transmitting information is vastly greater than that of the entire
5 15
genotype (approximately 10 for genetic possibilities and 10 for neuronal
possibilities). Without a rigid and extensive system of internal inhibition
governing these synaptic possibilities, the brain would degenerate into chaos and
disorder. The schizophrenic's "word salad" is viewed as a major departure from
the norm, but idiosyncratic word sequences are trivial compared to the brain's
potential for disorder. The integrity of organs, organ systems, and behavior all
are premised on small streams of excitation amid oceans of inhibition within the
brain, and failures of inhibition go to the heart of matters of normality and
abnormality from the individual cell to the individual self to society at large.
Neuropsychology and psychology in general basically study the dynamics of
inhibition and release in the brain. Aside from the ongoing activation of vital
metabolic systems that maintain life, the stream of human behavior is a function
of the selective activation of a few single or several interactive modular systems
and the simultaneous widespread inhibition of all other competing modular
systems. Paul MacLean and many others in the history of neuroscience have
emphasized both the hierarchical and the inhibitory natures of the brain in
producing orderly and functional behavior. These concepts underpinned the
studies of the great English neuroscientist John Hughlings Jackson on epilepsy
and the mind in general (Taylor 1932).
In Human Paleopsychology (1987b), I suggested that pathological releases of
function in epileptic and epileptoid conditions could serve as a model for many
forms of individual and social pathology above and beyond epilepsy per se.
That is, many forms of pathology reflect the release of unwanted and socially
inappropriate material into consciousness, feelings, fantasy, and/or overt
behavior, and often this release is of evolutionarily older systems that fit poorly
with or interfere with the situation at hand. MacLean's triune brain theory fit
perfectly with this line of reasoning, and it seemed intuitively appealing to me to
speak of progressing up (upshifting) and regressing down (downshifting) the
triune brain system that begins with the most ancient R-complex and proceeds
up through the newer paleomammalian level, and, finally, on up to the newest
level of functioning in the neocortex.
320 The Evolutionary Neuroethology of Paul MacLean

THE PROCESS OF REGRESSION (DOWNSHIFTING)

The phylogenetic progression-regression theme is widespread in the litera-

ture on human paleopsychology, evolutionary psychopathology, and related
areas, but is seldom addressed directly. Indeed, most evolution-based models
implicitly revolve around the fundamental assumption that all human behavior
constantly fluctuates between evolutionarily older and newer levels of function-
ing where the "primitive" gains ascendance one moment, the phylogenetically
"advanced" at another, or the two levels blend or intermix in some way.
Unfortunately, little attention has been paid to the specifics of this process, and
my phylogenetic progression-regression model represents one attempt to address
the dynamics of movement and inhibition/release between the older (primitive)
and newer (advanced) poles of human response. Most simply, any discernible
movement toward the lower pole would constitute phylogenetic regression,
whereas analogous movement toward the higher pole would constitute
phylogenetic progression. Table 17.1 summarizes several direct and indirect
attempts to define phylogenetic regression, and it is clear that "regression down
the triune brain" is an especially meaningful variation on the theme.

Table 17.1. Variations on the Phylogenetic Regression Theme

The main point here is that in a matter of seconds, a culturally refined, controlled
individual can regress to the emotionality characteristic of his evolutionary
forebears, and at that moment he is little different from them . . . under severe
stress, threat, provocation, or loss of "control" through alcohol ingestion, drugs, and
so forth, we temporarily lose our humanity, our culture, our rationality (Bailey
1978:22).

Although a variety of ecological pressures may move a culture away from its
ancestral form, the existence of innate biases with respect to human behavior will
produce a tendency for us to return to ancestral ways of behaving. This process is
called ancestralization (Crawford 1998: 292; emphasis in original).

At heart we are still a primitive people. We evolve far more slowly than our culture
. . . Culture may dress up the appearance of people, but it seems to be too shallow to
affect their nature deeply. In crises our natures reverts (Edey & Johanson 1990:
389).

Some of the pathologies of sexual behavior observed can be explained as phylo-

genetic regressions to an archaic agonistic sexuality . . . we can state that sexuality
without love and affiliation is a pathological regression to an archaic reptile stage
level of sexuality (Eibl-Eibesfeldt 1989: 259).

[Circumstances] . . . which could, ideally, lead to nurturance and growth, leads

instead to conflictual, agonic interactions. We are thrown back in time, as a kind of
Upshifting and Downshifting the Triune Brain 321

Table 17.1, continued

phylogenetic regression, where the attachment and hedonic modes were yet to
evolve (Gilbert 1989: 196).

Thus we have the phenomenon . . . that I have called "downshifting." When the
individual detects threat. . . full use of the great new cerebral brain is suspended,
and faster-acting, simpler brain resources take larger roles (Hart 1983: 108;
emphasis in original).

We overcome this [xenophobia and aversion to outsiders] to some extent through

cultural learning . . . But put stress on the system, and the age-old dispositions are
dominant (Holloway 1974: 8; emphasis added).

[In regression] both the phylogenetic and ontogenetic clocks are turned back
(Meerlo 1962: 79) . . . regressive behavior is so much more seductive and
contaminating than civilized, restrained behavior (p. 78).

Most of us today seem to have a latent emotional affinity with members of our
groups . . . our own kind collectively; such feelings show up in times of crisis, or
in evocative situations (Mellen 1981: 273).

In mammals, the autonomic nervous system response to challenge follows a

phylogenetic hierarchy, starting with the newest structures and, when all else
fails, reverting to the most primitive structural system (Porges 1997: 66).

Indeed, grand mal epilepsy can . . . be described as a disease in which the cognitive
drivers are all turned off because a kind of electrical storm in the brain, and the
victim is left momentarily with nothing operative but his neural chassis. This is a
profound impairment, temporarily regressing the individual back several hundreds
of millions of years (Sagan 1977 57-58; emphasis added).

In man, the neocortical mantle is thought to be the seat of logical and mathematical
reasoning, knowledge and understanding, analytical and synthetic processes,
invention and fantasy, philosophy and religion, meditation and intuition. However.
. . some behaviors and aspects of mental disease suggest a regression of brain
functioning to a predominantly paleomammalian (limbic) or reptilian level. In this
last instance . . . the breakdown of social, familial, parental behavior, and personal
care is often accompanied by the emergence of asocial, hostile, and aggressive
behaviors, and "reptilian" man emerges (Valzelli 1981: 38; emphasis added).

Each of the quotes in Table 17.1 proceeds from a basic "return to animality"
metaphor, but from there each approach develops its own distinctive emphasis:
Bailey emphasizes loss of control over emotionality, Meerlo the "seductive"
nature of regression, Eibl-Eibesfeldt the re-activation of older agonic and sexual
mechanisms, Eibl-Eibesfeldt and Gilbert the de-activation of affectional
systems, Edney and Johanson the thin veneer of culture, Crawford a return to
earlier ancestral patterns, and most imply some form of neurological regression
from higher to lower centers (especially Bailey, Hart, Sagan, and most notably
322 The Evolutionary Neuroethology of Paul MacLean

Valzelli). Note the number of quotes that emphasize danger, stress, or privation
as the primary elicitors of the regressive process (Bailey, Hart, Holloway,
Mellen; see also Geist 1978). The proposed stress-regression linkage will be
discussed further in the next section.
In a recent personal communication subsequently excerpted in the ASCAP
Newsletter (January 2000a), Valerius Geist described the "classic" form of
phylogenetic regression whereby a member of a particular species
occasionally—when under stress—will activate patterns of behavior distinctive
to closely related ancestral species:

I will illustrate a classical regression I witnessed in the Munich zoo in Siberian

elk [wapiti] . . . Red deer males advertise via vocalizations, attracting females and
then trying to keep them close by . . . To keep his harem together, the rutting stag
herds his harem using threats, even violence. He also has the problem, of course,
of approaching females in order to breed. So his courtship posture and behaviour
is the antithesis of his herding postures and behaviour . . . The female when the
male approaches in courtship posture, lowers her head, while opening and closing
her mouth rapidly. That stops the bull, he turns, and roars or bugles away from
the female. That is, he lets her know that he obeyed her cut-off signal.
In a pen was a deantlered Siberian elk bull, a female and a calf. The bull had
just killed female No. 4, whereupon the staff, belatedly, sawed off his antlers. He
had [previously] controlled a harem of five cows. The bull, seeing only one cow
assumed the herding posture towards her and continually followed, even rushed
her, wanting her back in the "harem." This went on unendingly so the female by
this time was haggard, skin and bones, not able to escape the bull. By the time I
saw her, she no longer used the species-specific "cut-off signal," rather, she
squatted trying to urinate while opening her mouth as if vocalizing—except no
sound emerged. She was trying, therefore, exactly what [primitive] Old World
Deer females do upon courtship of the male: they squat to urinate, and head
lowered, they vocalize. A perfect, most meaningful regression (Geist 2000a: 6 -
7).

DEFINING ASPECTS OF REGRESSION IN HUMANS

Several core assumptions follow from the phylogenetic progression-

regression model (see Bailey 1978, 1985, 1987b). First, it is far easier and
simpler to regress than to progress phylogenetically—regression merely requires
reactivation or passive release of previously evolved motivational, emotional, and
behavioral coordinations, whereas progression requires years of cultural
programming to effect context-appropriate outputs.
Second, phylogenetically older coordinations stored lower in the triune brain
are more quickly and efficiently activated (e.g., the fast-acting amygdala
previously discussed by Le Doux) than are more phylogenetically recent, neocort-
ically mediated outputs involving large amounts of cultural content. Gilbert (1989)
discussed how quickly lower psychoneural functions can be brought into action,
and Bailey, Tipton, and Taylor (1977) provided empirical support for the
hypothesis that "instinctual stimuli" such as a threatening stare are processed more
Upshifting and Downshifting the Triune Brain 323

quickly in profoundly retarded subjects than in presumably more cognitively

oriented mildly retarded subjects.
Third, reactivation of previously evolved coordinations, patterns, and systems
is inherently pleasurable in many instances (Bailey 1987b; Hernnstein 1977),
whereas activation of "higher" neural coordinations, patterns, and systems
subserving progression are more often hedonically neutral, unpleasurable, or even
aversive. Bailey, Burns and Bazan (1982) found that college students reported
considerably more subjective pleasure for visceral experiences such as eating,
drinking, having sex, receiving a back rub, and so forth, than for neocortical ly
mediated activities such as studying, writing a computer program, attending a
lecture, or writing a term paper. The pleasure/regression link is not a hard and fast
rule, however, for a number of ancient adaptations are clearly unpleasurable when
activated (e.g., anger, rage, fear, jealousy, envy, submissiveness, and the like
Gilbert 1999). Thus, when species-typical approach kinds of adaptations are
regressively activated the rule seems to hold, but it breaks down where avoidance,
loss, and pain-related systems are involved.
Fourth, individual differences are systematically reduced in regression but may
be either reduced (conformity) or augmented in progression (individualism; "free
will"). Generally, individual differences (and "free will") are smoothly and
progressively reduced with regression down the triune hierarchy, but gender
differences represent a special case. Whereas males and females show typical
patterns of reduced inter individual differences for regression within their
respective genders, patterns are more complex between the genders. Human
gender differences tend to be augmented in regression to lower mammalian levels
of the MacLean hierarchy but such differences tend to disappear at the lowest
levels of the reptilian brain. For example, men and women tend to easily fall into
their ancestral gender patterns when under stress, high sexual arousal, or in
producing and parenting offspring (Bailey 1987b). But gender differences may be
negligible or absent in reptilian rage reactions or screams of anguish during
serious injury. Obversely, human gender differences tend to be recovered as a
function of the reptilian-to-paleomammalian progression, but such differences
may be either neutralized, reduced, or augmented in progression to higher levels
of the neocortex where cultural mandates require certain gender styles or where
"free will" allows a range of choices in gender style.
Fifth, any stimulus condition that compromises or nullifies neocortical
control over lower systems may incite regression, but stress—especially stress
related to survival of self or kin—is fundamental to the process. In my model,
the stress ^ regression intercoordination is viewed as an evolved
adaptation that assures that ancestrally proven coping mechanisms are readily
accessible when needed (as in Geist's classic regression above). Geist (1978)
suggests that stress in the form of high arousal and/or extreme privation (i.e.,
hunger and starvation) may actually reduce blood flow to the neocortex and thus
leave the lower centers to their own "older" devices. Natural selection is both
efficient and economical, and it makes sense that frequent reactivation of
species-typical adaptations and even prehuman adaptive patterns would be
324 The Evolutionary Neuroethology of Paul MacLean

generally preferable to the creation of novel solutions for each challenge

encountered.
Sixth, phylogenetic regressions may be either passive or active. Passive
regression "refers to an uncontrolled or dyscontrolled loss of neocortical ability to
inhibit archaic impulses and imperatives. Here one effortlessly slips back, often
unconsciously, into species . . . patterns of behavior" (Bailey 1987b: p. 99). This is
the most common form of phylogenetic regression and may be set into motion by
any internal condition or external circumstance that weakens, compromises, or
immobilizes rational, conscious, culturally targeted, and neocortically mediated
controls over the far more ancient, powerful, and fitness-targeted reptilian and
paleomam-malian systems. Internal eliciting conditions for regression include brain
damage/ dysfunction, physical disease and illness, alcohol, and other drugs, fatigue,
activation of internal stress mechanisms and so forth; certain of these internal
conditions appear to encourage regression to the lower centers by occupying
neocortical resources that would be otherwise used for inhibition (e.g., coping with
serious disease), others directly interfere with or compromise neocortical inhibitory
processes (e.g., brain damage or alcohol intake), and in some cases the ancient
systems of response just simply overwhelm the neocortex as in a powerful stress
response that forces phylogenetically newer responses into the background.
External primers and elicitors of regression are even more numerous than
internal ones, and reflect any and all stimuli and situations that lead to regression
through the weakening of neocortical inhibitions, the activation and amplification
of lower systems, or, most probably, some concurrent combination of neocortical
inhibition and reptilian/paleomammalian activation (Bailey 1987b). Examples of
the latter combinatorial type include being provoked into an angry fight even when
one is a "pacifist" neocortically. We shall see later that the "inexplicable" behavior
of Eric Harris and Dylan Klebold in the Columbine tragedy conforms to this model
quite well. On the fateful morning of their attack, there was a mighty release of
primitive emotion from the lower levels of the brain, on the one hand, and a
complete renunciation of morality, culture, rationality, and higher things, on the
other.
Whereas passive regression represents a kind of yielding or surrender to lower
and more powerful systems of the brain, there are times when consciousness,
rationality, culture, and self-perceived morality side with ancient imperatives and
even aggravate and amplify them. In active regression, the culturally programmed
neocortex fans the flames of regression by providing dissonance-reducing rationali-
zations and justifications for primitive eruptions and outpourings of ancient
adaptations and coordinations. The more pernicious forms include ideology-based
warfare, terrorism, ethnocentrism, racial prejudice, political jingoism, religious
cultism, and fear and hatred of any and all things different. However, mild and
even neutral forms may be seen in advertising, the media, entertainment, education,
and even science when neocortical propaganda and high-sounding self-delusion
serve to amplify and mask "true" underlying concerns with sex, dominance, rank,
and general selfishness regarding the individual and his or her inclusive fitness
system. Indeed, the history of science is rife with dramatic stories of warfare, spite,
revenge, and even physical violence between scientists over matters of priority,
Upshifting and Downshifting the Triune Brain 325

rank, recognition, money, and sometimes minute differences in theory or ideology.

A quick read of Roger Lewin's (1988) wonderful Bones of Contention will leave
little doubt on this point.

THE REGRESSION-PROGRESSION CONTINUUM-

THE SPECIES CONTINUUM

All behavior in a species population may be seen as falling somewhere on a

theoretical species continuum proceeding from the most phylogenetically
primitive to the most phylogenetically advanced patterns of response for the
species in question (Bailey 1987b). Phylogenetically ancient and simple species
such as bacteria, trilobites, or the wood tick have little or no neural tissue; this is
reflected in their truncated species continua. Such organisms are at the mercy of
their few, simple, invariant, and species-specific patterns of survival and reproduc-
tion, and they fit the deterministic "selfish gene" model very well (Dawkins 1976).
Such patterns are subserved by very simple modular processes composed of highly
specific neurostructural, neurophysiological, and behavioral components, or what
Gardner (1988, 1996) calls basic plans] motivational, emotional, and cognitive
components will be added in later and more complex species. In essence, these
simple organisms carry out the fundamental adaptational thema of their species
and do little or nothing else.
By contrast, phylogenetically more recent and complex species such as
reptiles, early mammals, early primates, and modern humans have extended
continua that reflect both the total number of adaptations available, the levels of
complexity of available adaptations, and the degree of plasticity or malleability
of available adaptations in response to environmental inputs (e.g., see Geist
1978 on alternative responses to differing ecological pressures). Simple
organisms (e.g., bacteria) are characterized by few adaptations of low complex-
ity, whereas complex organisms such as apes and human beings are character-
ized by numerous in-built and highly complex hardware and software programs
that dramatically widen respective species continua at the upper end.
As the species continuum widens, behavioral possibilities widen
accordingly—including enhanced individual differences in pursuing survival
and reproductive fitness, occasional moments of detachment from strict
biological imperatives, and complex and highly integrated adaptations may
sometimes be deconstructed into their separate behavioral, motivational,
emotional, and cognitive components. Thus, with wider species continua, the
response outputs of particular species members may deviate somewhat from
those of other members, and brief periods of "individual freedom" may be
interspersed among the more fixed, automatic, and species-specific patterns of
adaptation to environmental demands.
Given that natural selection operates primarily by building onto and
extending pre-existing systems or primitive characters, the extended continua of
more recent and complex species reflect derived characters (Martin 1992) or
accretions primarily at the upper or progressive end of the scale. Thus, the
326 The Evolutionary Neuroethology of Paul MacLean

lower segments (and perhaps mid-segments) of closely related species continua

(e.g., chimpanzees versus humans) tend to overlap greatly due to shared ancestry
going back to a common ancestor. Indeed, given the logic of the species
continuum, it follows that the wider continua of more phylogenetically recent
and complex species in a genus or family (e.g., apes and humans) are
determined mainly by newly evolved neurostructures and associated physiolog-
ical and componential functions (viz., behavior, motivation, emotion, and
thought) that provide some adaptive advantage in progressively complex and
demanding environments. In those instances where natural selection more or
less substitutes one adaptation for another at essentially the same point on the
species continuum, some degree of evolution has occurred but the continuum
itself has not been extended appreciably. Moreover, when a new but lower level
reptilian or paleomammalian adaptation evolves into the system, the organism
may be accorded more physiological or behavioral options, but again, little in
the way of continuum extension. In sum, continuum extension occurs mainly by
virtue of accretions at the uppermost end of the scale where significantly
modified preexisting adaptations (i.e., derived characters) or new adaptations
extend the system.

THE HUMAN SPECIES CONTINUUM

For human beings, the species continuum forms, in theory, from n number of
subcontinua representing motivational, emotional, behavioral, and fantasy compo-
nents operating at a given moment in time. Such subprocesses are few in simple
animals and are highly integrated and firmly directed toward fitness goals, but
dissonances between subprocesses may be seen in conflict situations (Hinde 1970),
displacement activities (Eibl-Eibesfeldt 1989), or deceptive behavior (Eibl-
Eibesfeldt 1989). Deception is especially widespread in birds and mammals and
Geist (1978; 2000) discusses many rich examples including mountain sheep
"lying" about their intent to clash to catch the opponent unawares; young male
mountain sheep faking estrus to gain acceptance of older males; the broken wing
display of plovers and other birds to lure predators away from young; sham feeding
by ungulates as a means of catching predators off guard; and so on.
With more complex and highly evolved mammals and primates, some
control over the interaction of subprocesses is possible, and human beings are
masters of the capacity to feel one way and act another or to wish for one thing
yet pursue another. Nevertheless, most human behavior is species-congruent,
orderly and goal-directed, and significant decomposition of complex adaptations
is the exception rather than the rule. Ultimately, however, humans are blessed
and burdened with the freedom to not only temporarily de-couple from the
evolutionary process, but to manipulate the subprocesses underlying response
output as well. Thus, one might be smiling at a person while simultaneously
harboring hatred and perhaps imagining harm coming to the person; essentially,
several regressive and progressive subprocesses may be simultaneously active
with momentary placement on the continuum roughly reflecting the algebraic
Upshifting and Downshifting the Triune Brain 327

average of the subprocesses at any one point in time. Practically, however, it is

probably best to assume that the overall progression-regression continuum
reflects more or less congruent subprocesses under normal conditions, but
careful analysis of continuum dynamics requires close attention to possible
dissonant and conflicting processes, especially where pathological reactions are
concerned.
Whereas the normal person exerts considerable control over activation/
deactivation of component processes, the mentally ill person often fluctuates
between extreme eruptions of "pure" regressive and context-inappropriate material
(e.g., strangers may be seen as prey, predators, tribal enemies, close kin, inviting
sex objects, territorial interlopers, etc.), or, contrariwise, day-to-day adaptations
(especially social ones such as a brief conversation on today's news with a family
member or friend) may decompose into internally dissonant hodgepodges of
feelings, perceptions, behaviors, verbalizations, and fantasies. Hallucinations,
delusions, conftisional and obsessional states, phobic and anxiety states, bizarre and
inappropriate behavior, and numerous other pathological manifestations may be
seen as problems of phylogenetic progression-regression and disintegration of
subcomponential processes.
Judith Rapoport is chief of child psychiatry at NIMH, and her biological model
of obsessions and compulsions is remarkably similar in form to my more general
formulation (Rapaport 1989). A key feature of her model is the idea that certain
behavioral subroutines such as grooming and territoriality have been programmed
into the human brain over the course of evolution, but they typically remain
suppressed in everyday affairs. Put pressure on the system, however, and these
ancient modular processes re-activate or "release" with a vengeance and may be
replayed repeatedly much like a tape in a broken VCR. The patient is at the mercy
of her circumscribed, irrational, and commanding obsessions (dirt, germs, toxins,
bodily wastes, etc.) or compulsions (excessive bathing and grooming, contaminant
avoidance/removal, checking, hoarding, etc.), that emanate primarily from the basal
ganglia (basic structures in MacLean's reptilian brain). Whether released by stress
or brain malfunction, these remarkably uniform "fixed action patterns" spring into
action when higher brain centers fail in their modulatory and suppressive functions.
Rapoport suggests that many other psychiatric problems ranging from nail biting
and phobias to a variety of impulse disorders may fit the model as well.

THE PRIMITIVE POLE ON THE HUMAN CONTINUUM

In theory, the overall human species continuum is anchored by the least

cognitive, least consciously self-controlled, least culturally conditioned, most
blindly motivated and most psychoneurally ancient response ever experienced/
emitted by a member of the species (Bailey 1987b). In the MacLeanian sense, the
lower pole would be anchored by the most reptilian response ever experienced by
any member of species Homo sapiens. In modern humans, the most primitive
response of a Ted Bundy (e. g., vicious biting of a victim's buttocks as she was
being killed), Jeffrey Dahmer (numerous brutal murders and body mutilations,
328 The Evolutionary Neuroethology of Paul MacLean

storage of body parts, and cannibalism) or Gary Heidnik (even more cannibalism
than Dahmer) would seem to plumb depths of prehuman animality, but we can only
surmise what the "most primitive" of all humans responses might be in the abstract.
Practically, however, the idea that atavistic predatory tendencies lie in the deep
recesses of the reptilian brain which can erupt into overt patterns of stalking, brutal
killing, and cannibalism serves as a meaningful baseline for "deepest levels of
primitiveness" in this chapter.
When in the hypothetically deepest of regressive states, primitive emotions and
drives of the subcortical centers are in full control (see Bailey 1987b; Buck 1999;
Geist 1978; Le Doux 1996); psychological functions are dominated by unconscious
(Le Doux 1996), narcissistic, selfish (Buck 1999), and opportunistic themes; finer
linguistic outputs, future projections, self-control, and abstract problem-solving are
muted or lost; and the motive apparatus is dominated by the "selfish gene," kin-
selective processes, and current and/or ancestral fitness-targeted imperatives. At
such times, the person truly is not himself or herself but is rather a temporary
creation of past evolutionary processes. Once the state passes, the person may feel
shocked and dismayed by his or her loss of humanity.

THE ADVANCED POLE ON THE HUMAN CONTINUUM

By contrast, the mirror-image advanced pole on the human species continuum is

anchored theoretically by the least animalistic, least evolutionarily programmed,
least motivational-emotional, most coolly rational, and most cognitively complex
response ever emitted by any human being in the modern era. The most phyloge-
netically advanced level is reached when motivation/emotion processes are
minimal and rational thought is maximized to the fullest (see Bailey 1987b; Bailey
Burns, & Bazan 1982). "Distance-from-the-genes" (see Scheller & Axelrod 1984;
Symonds 1979) is maximal and the person is essentially distanced from the
resources of his or her primitive self. Thought can occur for thought's sake with
minimal interference from the lower centers and some freedom of choice enters the
picture. To quote Dabrowski (1972), "By higher level of psychic development we
mean a behaviour which is more complex, more conscious and having greater
freedom of choice, hence greater opportunity for self-determination" (p. 70).
As with the primitive pole, it is not possible to identify any single "most
advanced response," but the great physicist and cosmologist Stephen Hawking
illustrates our general points very nicely. He was unremarkable as a student and
only began to have his momentous insights about the universe after suffering the
crippling and deadly disease amyotrophic lateral sclerosis (Boslough 1984).
Although confined to a wheelchair and dependent on others for his daily needs,
Hawking's mind seemed to stretch to greater heights as the disease, for all practical
purposes, nullified the body and much of the motivational and emotional processes
(Bailey, 1987b). He has been described as the nearly perfect "cerebral being"
(Boslough 1984), who may spend more time at the highest and most creative levels
of human cognitive functioning of any person on earth. Indeed, as Einstein's heir
apparent, he may be the first theoretical physicist to reconcile the twin pillars of
Upshifting and Downshifting the Triune Brain 329

modern physics—Einstein's theory of general relativity and modern quantum-

mechanics theory (Boslough 1984). At his best, Stephen Hawking would certainly
be near the apex of human abstraction and complexity of thought, and at those
times the farthest from his animal nature.
Psychological health and happiness, however, requires much more than pure
cerebrality. Indeed, personal spontaneity, emotional warmth, sexiness, assertive-
ness, and being "real" require some degree of regressive access to our
paleomammalian selves. Much of the practice of psychotherapy (Bailey, Wood
& Nava 1992) is salubriously regressive in this respect. From the standpoint of
mental health, the goal would be to avoid disruptive and regressive psycho-
pathology on the one hand (excess responsivity toward the primitive pole) while
simultaneously avoiding constricting and suprarational fixation at the advanced
pole. Normal, healthy, and happy human behavior is typically found somewhere
well within the polar extremes—that is, within the human species modal range
of response.

THE SPECIES MODAL RANGE

Each species continuum has its hypothetical modal range of response, or a

preferred zone of species-specific or species-typical response output. In ex-
tremely ancient and simple organisms, the species modal range of response is
essentially the same as the overall species continuum. In more phylogenetically
advanced species, the modal range of response is considerably narrower than the
overall species continuum, with a relatively large submodal residue at the lower
end of the continuum (the zone of regression) and a relatively small supramodal
residue (zone of progression) at the upper end. Of course, the more advanced the
species (e.g., human beings), the greater the width of the supramodal zone of
accretion and the greater the potential to phylogenetically progress beyond the
modal zone when opportunities arise.
The species modal range represents a kind of species comfort zone or ecolo-
gical niche wherein the organism experiences its greatest degrees of physio-
logical homeostasis, reproductive viability, and fidelity to its species mandates.
When a species or species member stays appropriately within its "normal" zone
of response, biological and reproductive fitness are maximized, but when
organisms stray too far below (regression), or above (progression), their modal
zones, individual and inclusive fitnesses may be diminished accordingly. Thus,
movement out of the species modal zone is, by definition, not typical or fre-
quently sought, but it does allow additional options for dealing with unusual or
rare challenges and demands. For modern humans in advanced societies, one
such demand is to "progress at all costs" in the domains of self-control, good
citizenship, education, and occupation in order to successfully compete in a
world far different from ancestral ones.
The species modal zone is not to be confused with the so-called EEA or
environment of evolutionary adaptation, first suggested by John Bowlby.
Indeed, they are quite different. The species modal zone is the medium within
330 The Evolutionary Neuroethology of Paul MacLean

which previously evolved adaptations are "proximally" activated in the pursuit

of survival, whereas the EEA is a special species-deviant medium within which
special ecological pressures lead to new adaptations that will "ultimately" lead
to higher survival rates in new species variations or entirely new species. For
example, Geist's (1978) privation- stressed maintenance phenotype is subjected
to significant evolutionary pressures and is, thus, a variation of the EEA
concept, as is his dispersal phenotype, which is subjected to the ecological
"pressures" of superabundance "that are normally found during the colonization
of vacant habitats"(Geist 2000b). By contrast, the prosaic species modal zone is
particularly well defined in stable populations characterized by evolutionary
stasis, phylogenetic inertia, and the constant repetition of previously proven
behaviors. Once new and different ecological pressures are brought to bear on
stable modal zones, they will then resemble or become EEAs or zones of
evolutionary change. Nature resists change, however, and it is doubtful that most
members of most species are significantly involved in the evolutionary process-
that only occurs over vast expanses of time to a relatively few mutant
individuals. Indeed, the great masses of living beings inhabit their species modal
or comfort zones and not zones of evolutionary change.
Although complex animals have the option to move out of the species zone,
they seldom do so. Herrnstein (1977; see also Bailey 1987b) argues that
individual deviations from species norms is experienced as aversive in higher
animals, whereas conformity to species mandates is experienced as subjectively
pleasurable. These dynamics of pleasure and displeasure appear to be nature's
way of keeping species members within their appropriate species ranges of
response.
Some degree of continuum movement occurs within a given species modal
range, but the more interesting forms are those from the species modal zone to
lower and more ancient forms of response (regression) or to newer and higher
forms of response (progression). Thus, the species modal zone serves as a kind
of broad baseline from which deviations down or up constitute regression or
progression respectively. Further, this logic leads to what might be called the
hegemony of regression; that is, given that all animals (including humans) have
far wider submodal than supramodal ranges of response, it follows that when
deviations from species norms do occur, they are far more likely to occur in the
regressive direction. This makes sense evolutionarily, for an animal under stress
or environmental challenge has far more to gain in fitness by recovering tried
and proven old adaptations than by gambling on new accretions with little
record of success (see Geist 1978).

THE INDIVIDUAL CONTINUUM

Each member of a particular species has its own individual continuum and
individual modal range of response. This is where behavior of living beings
occurs. The actual individual continuum is embedded within its hypothetical
species continuum and, by definition, cannot be wider than that continuum. In
Upshifting and Downshifting the Triune Brain 331

simple animals, the individual and species continua overlap greatly, the
individual modal range of response and the species ranges of response overlap
greatly, and there is relatively little variation in adaptational processes either
within or between members of the species. The effects of what Wilson (1975)
calls phylogenetic inertia is especially evident in simpler species; that is, simple
organisms seldom stray from their evolved genetic programming that is,
ultimately, targeted toward species-defined fitness imperatives.
As more complex organisms evolved, both within-individual and between-
individual sources of variation entered the picture. Rather than all members of
an ancient species carrying out species mandates in virtually the same way,
where individual and species continua and their respective modal ranges were
virtually identical, many new possibilities entered the equation. For example,
human beings vary greatly in the respective widths of their personal continua
(e.g., a regressed schizophrenic versus Stephen Hawking), in the dynamics of
movement on their individual continua (patterns of progression-regression), in
the width and placement of their modal ranges of response on their individual
continua, and in the congruence between personal modal ranges and the
hypothetical species modal range of response. All of this potential for variation
does not imply limitless personal freedom or even the probability that most
human beings will deviate all that much from species mandates to survive and
reproduce; indeed, even though people have the potential for vast amounts of
variation due to high intelligence, accumulated knowledge, cultural program-
ming, and various environmental pressures, phylogenetic inertia and the
pleasure of acting "normally" as a species member keeps most individual zones
of response near the species one.

CONTINUUM DYNAMICS AND MISMATCH THEORY

In 1995, I outlined the basic principles of mismatch theory in a symposium

chaired by Charles Crawford at the Human Behavior and Evolution Society
meeting at Santa Barbara. Mismatch theory is based on the following funda-
mental assumptions: (1) human morphology and behavior evolved in zones of
time called EEAs; (2) the human species ceased to evolve, in any great degree,
beyond late Homo sapiens some 40,000 years ago; (3) massive cultural and
environmental changes have occurred since that time; (4) current human beings
often find their naturally evolved selves mismatched or at odds with current
physical, social, and cultural environments; and (5) the frequency and magnitude
of such mismatches for a given person are positively correlated with both
physical disease and psychopathology. Essentially, many modern human beings
in highly technological societies are much like "fishes out of water" ecologically
(Ahern & Bailey 1997), and their bodies and minds yearn unconsciously for
enough phylogenetically regressive "matches" and "rematches" to make life
fulfilling, pleasurable, and secure (Bailey 1996 ASCAP series).
Although the term mismatch is not always used, this line of reasoning has
been productively applied to the genesis and treatment of physical disease
332 The Evolutionary Neuroethology of Paul MacLean

(Eaton, Shostak, & Konner 1998; Lappe' 1994; Nesse & Williams 1995;
Williams & Nesse 1991) including reproductive cancer in women (Coe &
Steadman 1995; Eaton et al. 1994), the problem of drug addiction (Nesse &
Berridge 1997), the practice of psychotherapy (Bailey 2000; Glantz & Pearce
1989), modern angst and despair (Wright 1995), problems in the classroom
(Bernhard 1988) and the workplace (Bernhard & Glantz 1991), and the
problems of modern life in general (Tooby & Cosmides 1990). The strengths
and weaknesses of mismatch theory have been discussed at length by Crawford
(1998; see also Geist 1978), and he calls for both more rigorous theory and more
rigorous research paradigms for assessing EEA-current environment differences.
Continuum theory construes mismatch as a condition in which the personal
modal range of response sufficiently differs from the hypothetical species modal
range so as to induce dishomeostasis physically and internal tension and
subjective discomfort psychologically. In theory, the species modal range in
current humans overlaps greatly with that of Homo sapiens 40,000 years ago, for
only so much disparity can be tolerated at the population level; thus, most
human beings of the world are expected to "match" species requirements well
enough to avoid pathological effects. Individual modal ranges, however, can be
all over the place, and many individuals—especially those who have progressed
highly in modern technocracies—find themselves estranged and distanced from
nature (Bailey 1996 ASCAP series; Wright 1995). Many of the various
"diseases of civilization" (Eaton, Shostak, & Konner 1988; Nesse & Williams
1995), including cancer, heart disease, and many other medical conditions,
crime and drug addiction, anxiety and depression, anorexia and bulimia, and so
on, reflect major disparities in the species and personal modal ranges.
Treatment and therapy for such conditions—whether they are primarily medical
or psychological—often feature various back-to-nature themes that implicitly
encourage increased congruence between the species and individual modal
ranges of response.

SPECIES CONTINUA IN EARLIER VS. MODERN HOMO SAPIENS

A brief comparison of the species continua and modal ranges for Homo sapiens
(just following the "great cultural leap forward" [Diamond 1989] around 40,000
years ago) and modern human beings will help to illustrate continuum dynamics
and the regression-progression model. Prior to the great leap, our hunting and
gathering ancestors were essentially the same as moderns in the genetic, neurolog-
ical, and behavioral potential for speech and language, complex kinship and social
relations, tools and technology, and culture in general, but the Rubicon had not yet
been crossed. No one knows exactly why, but relatively conservative and stagnant
cultural patterns suddenly gave way in the Late Paleolithic to the creation and
storage of new ideas that were the seeds of modern civilization. In Valerius Geist's
(1978) terminology, the privation-stressed, static, and survival-obsessed mainten-
ance phenotype of early Homo was more or less permanently supplanted by the
growth, future-oriented, and resource maximalization policies of the dispersal
Upshifting and Downshifting the Triune Brain 333

phenotype. During the last 20-35 thousand years new tools of bone, antler and
ivory appeared, and other innovations included spear throwers, needles and sewing,
more elaborate personal adornments and decorations, endowed burials (e.g., various
materials were interred with the deceased), complex art forms, and progressively
more elaborate habitation sites (Shick & Toth 1993). Kinship patterns were leading
to stronger, more well-defined sexual contracts, a firmer sense of family that
included a greater proportion of fictive kin and in-laws as well as genetic relatives,
more complex coalition-building made possible by marriage across previously
isolated or antagonistic groups, and the burgeoning of trade and reciprocal relations
among unfamiliars and people from distant locales (see Shreeve 1995 for an
excellent discussion).
Once the great leap forward had occurred, both the species continuum and the
species modal range were extended considerably over those of Homo erectus (see
Walker & Shipman 1996) and the earlier versions of Homo sapiens. With little in
the way of new phylogenetic adaptations, Homo now surged forward by virtue of
exaptation (viz., the exploitation of old adaptations for new purposes, see Gould &
Vrba 1982; see also Femald 1992) and processes of cultural evolution subserved by
fast-paced positive feedback mechanisms that contrasted with the vastly slower,
negative feedback processes of organic evolution. Once cultural material could be
stored permanently in the form of cave art, stone and metal tools and artifacts, and
later writing, culture could feed on itself and grow at a geometric rate. It is these
forms of social, technological, and cultural growth that have produced the modern
human society with its staggering advances in knowledge, technology, and control
over Mother Nature. Aside from these mighty cultural advances, the human being
of today is little different emotionally or motivationally from the earliest Homo or
even from other animals for that matter: otherwise "why do we continue to do the
things other animals do?" (MacLean 1978). In sum, the wider species continuum
and the wider modal range in modern humans reflect a small number of phylo-
genetic accretions at the progressive-cognitive of the scale that allow for seemingly
limitless generation, storage, and application of complex cultural information.
Figure 17.1 compares earlier Homo sapiens with modern human beings in terms
of continuum dynamics and MacLeanian processes of progression and regression.
The species continua and modal ranges are estimated but hopefully provide reason-
able approximations of those that characterize early and modern human beings.
Note first that both the species continuum and modal range of response is
appreciably wider in modern humans, as are both the submodal zone of regression
and the supramodal zone of progression. In sum, modern human beings have far
more options for response outputs both within and out of the species modal range
of response, and the options are particularly rich at the neocortically-mediated
progressive end of the scale.
Although the theoretical options for response available to moderns are vast,
their modal range of response is only marginally wider than that of earlier Homo.
However, the modern modal range has shifted in toto toward the progressive pole
by virtue of presses to master a highly complex culture and compete in highly
aggressive economic and informational meritocracies.
334 The Evolutionary Neuroethology of Paul MacLean

Early Homo sapiens

Primitive Advanced
Pole Pole

Modal Range

Modern Homo sapiens

Primitive Advanced
Pole Pole

Modal Range of Response

Progression

Reptilian System Paleomammalian System Neocortical System

Regression
Figure 17.1. Species Continua and Modal Zones for Homo Sapiens

In advanced societies, the daily life of people is dominated by preparation (e.g.,

formal education) for such competition in the early years and pressure to produce
culturally, materially, and intellectually in young adulthood, mid-life, and increas-
ingly in the later years. When given the chance, however, most people prefer to
"regress" toward the low end of the modal range for dinner with friends, relaxation
and recreation, sexual activity, or a walk in the mountains, and at those times—
aside from the trappings of culture—they are not very different motivationally and
emotionally from earlier Homo. As Figure 17.1 shows, such benign regressions
"matches" today's person very closely with the middle area of earlier Homo's
modal zone of response. Theoretically, that should be the area on the modern
species continuum that produces the greatest subjective pleasure, sense of security,
and salubrious effects. Indeed, that is basically the area on the continuum that we
evolved to occupy. It should be no surprise then that when the smoke and fire of the
workday subsides, we long for the archetypal "hunting and gathering" experience
of our ancestors.

OVERVIEW OF THE MODEL:

MOVEMENT ON THE CONTINUUM

In phylogenetic progression-regression theory, a given individual is character-

ized by the range of his/her primitiveoadvanced response continuum, by the
modal region of response (e.g., whether typical behavior is generally nearer the
Upshifting and Downshifting the Triune Brain 335

lower or higher pole), and by the frequency and amplitude of movement on the
continuum. Most normal persons in modern technological cultures have wide
primitive-advanced continua due to educationally and culturally extended upper
poles, and, given numerous social presses for appropriate culturally "advanced"
behavior, they tend to operate publicly well above their species modal range mid-
points. However, lower points would be expected on respective continua for private
behavior, private feelings, and private fantasies, where cultural pressures to
conform are diminished or nullified. Of all expressions, fantasies would seem to
most freely reflect the inner world of feelings, motives, and fleeting images that
have been carried over in the evolutionary process (Bailey, Burns & Bazan 1982).
Public behavior, by contrast, is typically least connected to the older systems, and is
more likely to follow the immediate mandates of group process, social etiquette,
and rule of law.
Clearly, issues of normality/abnormality, social propriety, conformity/noncon-
formity, hypocrisy, deception, and realness as a person revolve around the dyna-
mics of progression-regression and the congruence and noncongruence of compo-
nent subsystems operating at any one time. Our selfish, inherently amoral and
potentially brutal natural selves must always be tidied up for culture, and much of
this involves hiding, repressing, rationalizing, and sublimating the socially unaccep-
table outward aspects of our ancient adaptations. That is, one set of continuum
dynamics may characterize presentable behavior while an entirely different and
even contradictory set may characterize the inner world of self, motives, and
feelings. For example, sociopaths who have the benefits of reasonably high
intelligence and a charming social presentation are often able to manipulate and
victimize others through guile, deception, and subtle forms of intimidation
(Cleckley 1976; Mealey 1995; Meloy 1988; Tillier 2000). By misrepresenting his
true motivations of selfishness, greed, and predation, the skillful sociopath is able to
play his ancient regressive games with impunity.
The complexity of continuum dynamics is evident in the truncated or phylo-
genetically fixated behavior and reliance on subneocortical mechanisms seen in the
mentally retarded (Bailey, Tipton & Taylor 1977; Hereford, Cleland, & Fellner
1973; Mac Andrew & Edgerton 1964), the highly variable regression-progression
patterns of the schizophrenic, the inwardly regressive yet outwardly progressive
behavior of the manipulative sociopath (Meloy 1988), the regressive limbic disturb-
ances in severe depressives (problems in eating, sleeping, pleasure-unpleasure,
sexuality, aggression, and sociality in general) in conjunction with progressive
neocortical inputs such as guilt and self-recrimination, the sudden regressive,
epileptoid discharges of aggression in otherwise normal persons (Bailey 1987b),
and so forth. As we will see, the epileptoid, fundamentally predatory, and appar-
ently pleasurable actions of Eric Harris and Dylan Klebold at the Colombine High
School rampage on April 20, 1999, are explicable from the progression-regression
standpoint as well.
336 The Evolutionary Neuroethology of Paul MacLean

BRIEF ANALYSIS OF THE COLUMBINE KILLINGS:

THE FATEFUL TUESDAY MORNING

On Tuesday morning, April 20, 1999, Eric Harris and Dylan Klebold,
unloaded two black duffel bags filled with guns and bombs and began to shoot
their classmates at Columbine High School in Littleton, Colorado. Four hours
later, twelve students and a teacher had been killed and Harris and Klebold were
found in the school library dead from self-inflicted gunshot wounds.

Eric Harris

The parents, older brother and Eric lived in an upper-middle class subdivision
on the outskirts of Littleton, Colorado. The father was a highly decorated Air Force
officer, the mother was well-liked in the neighborhood, and the older brother was a
successful athlete. Overall, the family appeared normal to neighbors and friends.
Eric was extremely shy but bright and capable in school. He had a talent for
computers, loved violent video games, and assumed a leadership role among his
small circle of friends. He seldom had a girl friend and was often lonely and
depressed. He sought sanctuary in the Trenchcoat Mafia from the taunts and abuse
from the "jocks" at school.
Although Eric was probably clinically depressed, extremely angry, and socially
alienated, no one would have deduced beforehand that he or Dylan Klebold were
capable of their vicious killing spree. However, there were a number of aggravating
circumstances in Eric's background that probably contributed to—but did not
directly cause—his "inexplicable" behavior. Included among these were frustration
and anger due to his role as "social outcast"; being bullied and humiliated by
athletes at school; frustration, anger, and thoughts of revenge toward various
"enemies"; violent fantasies and racist ideology expressed on a personal website;
fascination with guns, killing, military violence, and Adolph Hitler; fascination with
violent video games such as Doom and Duke Nukem; use of alcohol, prescription
drugs, and the serotonergic antidepressant Luvox; concerns over his sick dog;
rejection from the Marine Corps five days before killings; and the recent breakup of
close friendship with male neighbor Brooks Brown.

Dylan Klebold

Dylan Klebold was loved and doted upon by his liberal and affluent parents.
They feared problems with older brother Byron but never with the quiet, shy, and
accommodating Dylan. The mother came from a wealthy and prominent Jewish
family and the father was a successful geophysicist before going into real estate.
The Klebolds looked like the perfect family to neighbors and friends. Dylan was a
tall, extremely bright, and quiet kid with a knack for math and computers. He
towered over others physically, but tended to lack motivation and direction. He was
lonely and insecure and would often hand out cookies to classmates to make a good
Upshifting and Downshifting the Triune Brain 337

impression. Dylan seemed like a basically normal person whose most fateful
personality trait was his willingness to follow others, especially Eric Harris.
Whereas Eric Harris suffered from depression, chronic rage, and possible
pharmacological complications, Dylan Klebold was essentially a normal young
man. However, he appeared to identify with and model after Eric's anger, violent
and paranoid obsessions, and, subsequently, phylogenetically downshifted right
along with him to the point of killing his classmates. Indeed, while in the regressive
state during the killings, Klebold appeared every bit as vicious and inhuman as the
instigator Eric Harris. Dylan Klebold personifies what Joost Meerlo (1962) calls the
"seductive" and "contaminating" nature of such regression. Not only is phylo-
genetic regression easy to elicit, inherently pleasurable, and responsive to stress, it
is also extremely easy to effect through processes of identification and modeling.
Psychological research has shown that modeling disinhibition is far easier than
modeling inhibition (Bandura 1969), and passive phylogenetic regression is a form
of disinhibition involving loss of neocortical control over the reptilian and
paleomammalian centers (Bailey 1987b). The Columbine killings show that even a
normal person such as Dylan Klebold can do the most horrific things while under
the influence the "modeling" influence of someone in a deeply regressive state of
mind.

THEORETICAL OVERVIEW

The Columbine killings illustrate a number of major theoretical points

discussed in this chapter. First, the human triune brain is composed of extremely
ancient, primitive, selfish (Buck 1999) and nonrational reptilian neurostructures
at the first level (e.g., "self-preservational programming," Cory 1999), moder-
ately ancient, primitive, and often irrational paleomammalian neurostructures at
the second level (e.g., motivation, emotion, concrete empathy and "affectional
programming," Cory 1999), and, finally, relatively new, sometimes rational
neocortical capacities for language communication, abstract empathy and
otherness, foresight, self-reflection, personal choice, and unprecedented techno-
logical achievements (e.g., "executive programming" in Cory's 1999 system).
For better or worse, human beings can downshift or upshift within the triune
system, and the Columbine killings were extreme examples of downshifting or
phylogenetic regression.
Second, the human brain is composed of supernumerous modular processes
and various coordinations of modular processes that generally work in a smooth
and integrated way. In the EEAs of human evolution, these processes were targeted
toward individual and inclusive fitness, but that is not always the case today (Tooby
& Cosmides 1990). Orderly behavior and adaptive outputs of the brain are
determined by exceptionally complex processes of inhibition and release that
operate within the overall triune system. Epilepsy (see Sagan 1977), epileptoid
dyscontrolled behavior (Monroe 1978), and sudden forms of phylogenetically
regressive behavior reflect a temporary breakdown of inhibitory processes where
338 The Evolutionary Neuroethology of Paul MacLean

older, often ego-dystonic motivational/behavior/cognitive intercoordinations are

"released" from their neocortical bondage.
The evening and early morning before the Columbine attack, the behavior of
Eric Harris and Dylan Klebold was unremarkable, but as the attack began their
actions resembled the epileptoid dyscontrol syndrome of violent criminals (see
Monroe 1978) and the arousal, stalk, and kill predatory behavior of animals (see
Bailey 1987b; Fox 2001; Meloy 1997; Miller 2000)—with astonishing rapidity,
ancient "reptilian" and predatory coordinations essentially co-opted and over-
whelmed the thinking part of the brain as the attack progressed over a two-hour
period. Eric Harris and Dylan Klebold were, indeed, "not themselves" during the
attack, for their actions came more from ancient predatory reptilian and mammalian
tendencies programmed into the triune brain than from their own personalities,
temperaments, environmental backgrounds, or moral training. Had they lived, they
would have been as puzzled as anyone as to why they performed such vile
misdeeds (as was the case with Ted Bundy, see Michaud & Aynesworth 1983).
Third, the Columbine attack showed the ease with which ancient and culturally
repulsive processes can be suddenly re-activated, especially in young males of the
species. Moreover, the young killers gave every evidence of enjoying the killing
spree, and the event was a kind of killing festival for them. This disturbing fact
cannot be explained by any existing sociocultural theory, and the "pleasure" aspect
of the killings forces us to acknowledge the predatory nature of the attack (see Fox
2001; Meloy 1997; Miller 2000). Indeed, predatory aggression is the only form of
aggression that appears pleasurable in animals (Moyer 1976), and we recall
Washburn and Hamburg's (1972) admonition that "man has been a predator for a
long time and his nature is such that he easily learns to enjoy killing other animals
. . . (and) . . . man easily learns to enjoy torturing and killing other human beings"
(p. 294).
Fourth, almost all mass and serial murderers are men, and Eric Harris and Dylan
Klebold regressed not only to predatory violence but to "phylogenetic maleness" as
well. I have argued (Bailey 1987b) that phylogenetic maleness often plays a part in
most forms of human violence, crime, and mayhem, including rape, murder, sexual
deviations, and even vandalism (Bailey 1988, 1991). More recently, Wrangham
and Peterson (1996) have discussed the "demonic male" from the evolutionary
standpoint, and they describe the twin pillars of predatory maleness, male bonding
and the lethal raid. Certainly, male bonding played a central role in the "lethal raid"
of Eric Harris and Dylan Klebold, as well as a more general "dark side" of male
violence goes far back into human ancestry (Ghiglieri 1999). As Ghiglieri (1999)
says, "We live in a world in which cheaters, robbers, rapists, murderers, and war-
mongers lurk in every human landscape" (p. 246). Many males—such as Harris
and Klebold—seem ready to downshift to such predatory or demonic maleness
with astonishing ease and rapidity.
Fifth, a long-term accumulation of stresses, hassles, frustrations, and humilia-
tions can set the stage for a sudden regressive release of sometimes murderous and
deadly predatory violence. In my paleoanalysis of the serial murderer Ted Bundy, I
outlined the numerous conditions that helped to "prime" and "elicit" his stalking
and killing behavior (see Bailey 1987b, Table 9.2). These included an illegitimate
Upshifting and Downshifting the Triune Brain 339

birth, ambivalence toward the mother, rejection by his foster father, confused self-
identity, rejection by women, fascination with pornography, use of alcohol and
marijuana, fantasies about killing, and a host of other variables. In my view,
however, these conditions could never lead to murderous sexual aggression without
the existence of sexual and predatory centers deep in the brain that are accessible
via phylogenetic regression. The killing sprees of Ted Bundy or Eric Harris and
Dylan Klebold are not directly caused by stress or an accumulation of stressors,
although they no doubt help to set off the reaction. It is the readiness of the reptilian
and paleomammalian systems in the brains of human males to be "set o f f that
more accurately captures the asocial behavior of the Bundys, Harrises and
Klebolds.
Sixth, there was a significant element of active or neocortically augmented
regression in the months leading up to and during the Columbine killings. Racist
philosophy, hatred of enemies, thoughts of revenge against the jocks, and a sense of
self-as-victim made it that much easier for Harris and Klebold to dehumanize their
enemies and turn them into prey to be brutalized and killed in the most cold-
blooded fashion. This form of regression lies behind the most demonic and
depraved aspects of the human condition, including racism, genocide, war, and
hatred of all things different from one's self and kin.
Seventh, lethal regressions of the Harris and Klebold type involve a deact-
ivation of higher affectional, empathic (MacLean 1977), prosocial, moral and
prefrontal processing of future consequences (see Buck 1999) simultaneous with
the activation of subcortical predatory, rage, and violence areas of the brain
(Valzelli 1981). As Harris and Klebold gleefully and brutally killed their school-
mates, the warmth, love, and kinship areas of the brain were completely shut down,
and people became mere objects or "prey." MacLean's (1982) more phylogenet-
ically advanced third or thalamocingulate division of the limbic system governing
"family-related behavior" was clearly deactivated, as was any indication of
attachment or love (Buck 1999), friendship, caring or altruism, or even the barest
traces of kinship (see Bailey 2000). Adding fuel to the fire was the deactivation of
fear, aversion, and punishment processes that typically inhibit aggression and
violence (and psychopathy, see Mealey 1995); this probably involved selective de-
activation of the amygdala/hippocampus/prefrontal fear axis (see Le Doux 1996)
where fear functions were more or less shut off and defensive functions were
subdued (Harris and Kelbold were not subjected to counterattack by their victims),
but predatory attack and generalized aggression functions of the amygdala were left
unconstrained (see Bailey 1987b: 365-372).
Lastly, Eric Harris and Dylan Klebold were essentially normal but somewhat
evolutionarily "mismatched" members of species Homo sapiens whose individual
species continua were extended due to education and privilege, whose modal
ranges of response were similarly extended, and whose supramodal or progressive
ranges were extended quite above the norm. They were highly educated and intelli-
gent young men whose frustration and anger set them on a path of regression that
ultimately nullified all of their cultural achievements and led to the deaths of 15
people, including themselves.
340 The Evolutionary Neuroethology of Paul MacLean

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 18

ALGORITHMS OF N E U R A L
ARCHITECTURE, HAMILTON'S RULE,
A N D THE INVISIBLE H A N D OF
ECONOMICS

Gerald A. Cory, Jr.

INTRODUCTION

This chapter builds upon the triune modular brain concept of Paul MacLean to
create a new model of our neural architecture called the conflict systems
neurobehavioral (CSN) model. It develops reciprocal algorithms of behavior,
involving the tug and pull between ego and empathy, neocortical representations
of phylogenetically established self-preservation and affectional brain structures.
These algorithms are applied to the ubiquitous phenomenon of social
reciprocity. The same fundamental algorithms are further shown to be the
underlying dynamic of social exchange as well as the transactional market
governed by the so-called laws of supply and demand. The reciprocal algorithms
are offered as the evolved mechanism complement to Hamilton's rule of
inclusive fitness. The linkage of their mathematical expressions is demonstrated.
The neural algorithms are also expressed in the invisible hand concept of Adam
Smith, which, as a basic economic concept, has been the source of much
theoretical speculation in microeconomic theory. The linkage of Hamilton's rule
with the reciprocal neural algorithms combined with the sourcing of economic
and social exchange in the neural dynamic allows a theoretical basis for the
integration of evolutionary psychology with evolutionary neuroscience as a
foundation for economics and the social sciences.
To proceed with developing the conflict systems neurobehavioral (CNS)
model, I begin with the work of Paul D. MacLean. MacLean, who was founder
and longtime chief of the Laboratory of Brain Evolution and Behavior of the
National Institutes of Health, is our leading evolutionary neuroscientist.
MacLean's triune brain concept has been one of the most influential ideas in
brain science since World War II (e.g., see Durant in Harrington 1992: 268).
1
Nevertheless, it has also been criticized in some quarters of neuroscience.
346 The Evolutionary Neuroethology of Paul MacLean

Although much of this criticism has recently been shown to be inaccurate and
2
based upon misinterpretations of MacLean's position, the presentation in this
chapter is adjusted to accommodate those criticisms where clarification is
indicated. In his encyclopedic summary of the last fifty years of brain research,
MacLean (1990) documents the human brain as an evolved three-level
interconnected, modular structure (see Figure 18.1). This structure comprises a
self-preservational, maintenance component inherited from the stem reptiles of
the Permian and Triassic periods (between 225-250 mya), called the
protoreptilian complex, a later modified and evolved mammalian affectional
complex, and a most recently modified and elaborated higher cortex.

Figure 18.1. A Simplified, Modified Sketch of the Interconnected Modular Triune Brain
Structure. After MacLean. As represented here the three brain divisions do not constitute
distinct additions but rather modifications and elaborations of probable preexisting homo-
logues reflecting phylogenetic continuity.

As brain evolution progressed in the branching vertebrate line ancestral to

humans, simple protoreptilian brain structure was not replaced, but provided the
substructure and homologues for subsequent brain development while largely
retaining its basic character and function. Accordingly, the brain structure of
early ancestral vertebrate life forms (i.e., early fishes, amniotic anapsid reptiles)
became the substructure and provided the homologues for the mammalian
modifications and neocortical elaborations that followed and which have
reached the greatest development in the brain of humankind. Appreciating the
qualitative differences of the three levels is important to understanding the
dynamics of human subjective experience and behavior.
The protoreptilian brain tissues in humans are proposed, as they did in the
stem vertebrates, to govern the fundamentals, or the daily master routines, of our
life-support operations: blood circulation, heartbeat, respiration, basic food-
getting, reproduction, and defensive behaviors, which were functions and
behaviors also found in the ancient stem reptiles. Located by MacLean in what
Neural Algorithms, Hamilton's Rule, and Economics 347

are usually called the hindbrain and the midbrain (i.e., the brain stem) as well as
in certain structures at the base of the forebrain (i.e., the basal ganglia), this
primal and innermost core of the human brain made up almost the entire brain in
ancestral fishes, amphibians, and amniotes (although not necessarily their
modern representatives).
The next developmental stage of our brain, which comes from rudimentary
mammalian life and which MacLean called the paleo- or "old" mammalian
brain, is identified with the structures designated collectively as our limbic
system. Developing from homologues preexisting in the protoreptilian brain,
these newly elaborated limbic tissue clusters included such physiological
structures as the amygdala, the hypothalamus, the hippocampus, the thalamus,
and the limbic cingulate cortex. Behavioral contributions to life from these
modified and elaborated paleo-mammalian structures, or limbic system,
included, among other things, the mammalian features (absent in the stem
vertebrates) of warm-bloodedness, nursing, infant care, and extended social
bonding. These new characteristics were then neurally integrated with the life-
support functional and behavioral circuitry of the protoreptilian brain tissues to
create the more complex life form of mammals.
The neocortex, which MacLean called the neo- or "new" mammalian brain,
is the most recent stage of brain modification and elaboration. This great mass of
hemispherical brain matter that dominates the skull case of higher primates and
man, by elaborating the preexisting homologues present in the brains of early
vertebrates, overgrew and encased the earlier ("paleo") mammalian and
protoreptilian neural tissues, but essentially did not replace them. As a conse-
quence of this neocortical evolution and growth, those older brain parts evolved
greater complexity in support of these new tissue structures and in response to
the behavioral adaptations necessary to life's increasingly sophisticated circum-
stances.

TOWARD A NEW BEHAVIORAL MODEL

The unique features of the human brain evolved over a period of several
million years in a primarily kinship based foraging society where sharing or
reciprocity was essential to survival and which reinforced the adaptive evolution
3
of the mammalian characteristics of self-preservation and affection. Ego and
empathy, self-interest and other-interest, are key features of our personal and
social behavior. To relate these to MacLean's concept we need a subjective/
behavioral rather than a neurophysiological vocabulary—one that will express
what the presence of our protoreptilian and paleomammalian brain structures
mean with regard to our day-to-day, subjectively experienced, behavioral initia-
tives and responses to one another and the world we live in. In computer-related
vocabulary, familiar to us all through cognitive psychology and artificial
intelligence, I use the software designer's vocabulary of programs and program-
ming. I will speak of our three developmental brain levels as behavioral pro-
grams or sets of programs that subjectively drive and generate specific, and
348 The Evolutionary Neuroethology of Paul MacLean

4
objectively observable, behaviors.
From the predominantly survival-centered promptings of the ancestral proto-
reptilian tissues, as elaborated in the human brain, arise the motivational source
for egoistic, surviving, self-interested subjective experience and behaviors. Here
are the cold-blooded, seemingly passionless, single-minded behaviors that we
have generally associated with the present-day lizard, the snake, and that most
5
maligned of fishes, the shark.
Here is a world revolving almost exclusively around matters of self-preser-
vation. The protoreptilian brain structures, then, will be referred to as our self-
preservation programming.
From the infant nursing, care-giving, and social bonding initiatives and
responses of the mammalian modifications and elaborations arise the motiva-
tional source for nurturing, empathetic, other-interested experiences and
behaviors. Here are the warm-blooded, passionate, body-contacting, bonding
6
behaviors that we've come to identify with the lion, the wolf, the primates.
Here is a world in which nearly single-minded self-preservation is simul-
taneously complemented and counterpoised by the conflicting demands of
affection. The early mammalian modifications, then will be referred to as our
1
affectional programming
Before I go on to discuss the neo-mammalian neocortical structures in
behavioral terms, I wish to pause to consider how these first two sets of pro-
grams function together.

Our Evolved Brain and the Sources of Subjective/Behavioral Conflict

These core behavioral program modules, composed of (or served by) sets or
subsystems of modules, of our brain structure serve as dynamic factors of our
behavior. They are energy-driven by our cellular as well as overall bodily
processes of metabolism as mediated by hormonal, neurotransmitter, and neural
architecture. Each is an inextricable part of our makeup, because each is "wired
into" our brain structure by the process of evolution. The degree of genome
control seems, however, to vary with the mechanism. Older brain parts like the
hindbrain and parts of the limbic system, phylogenetically old and necessary for
survival, seem to be more closely under genetic control. Other more recent
tissues in the neocortex depend also on development and environmental
experience. Damasio (1999, 1994) uses the terms preset and preorganized,
apparently (and appropriately, I think) to avoid the implication of an overly
deterministic prewiring in some brain regions. Behavioral conflict exists, then,
simply by virtue of the presence of these two large-scale energy-driven modular
program sets in our lives—up and running even prior to birth. Their mere
physiological presence sets us up for a life of inner and outer struggle, as we are
8
driven by and respond to their contending demands. Conflict is more than an
externalized, objective ethical, moral, or decision-making dilemma, however.
Subjectively, feelings of satisfaction occur when we can express our felt motives,
while feelings of frustration occur when either our self-preservational or
Neural Algorithms, Hamilton's Rule, and Economics 349

affectional impulses cannot be expressed in the behavioral initiatives and

responses we wish to make.
Behavioral tension then arises. Experienced as subjectively defined variants
such as frustration, anxiety, or anger, behavioral tension occurs whenever one of
our two fundamental behavioral programs—self-preservation or affection—is
activated but meets with some resistance or difficulty that prevents its
satisfactory expression. This subjective tension becomes most paralyzing when
both programs are activated and seek contending or incompatible responses
within a single situation. Caught between "I want to" and "I can't"—for
example, "I want to help him/her, but I can't surrender my needs"—we agonize.
Whether this tension arises through the thwarted expression of a single impulse
or the simultaneous but mutually exclusive urgings of two contending impulses,
whenever it remains unresolved or unmanaged it leads to the worsening
condition of behavioral stress.

The Blessing of Tension and Stress

The evolutionary process by which the two opposite promptings of self-

preservation and affection were combined in us enhanced our ability to survive
by binding us in social interaction and providing us with the widest range of
9
behavioral responses to our environment. Our inherently conflicting programs
are a curse, then, only to the degree that we fail to recognize them as a blessing.
Our self-preservation and affection programs allow us a highly advanced
sensitivity to our environment, keeping our interactive social behaviors within
survival limits as well as enabling us to perceive and appreciate the survival
requirements of others. Ironically, the accompanying behavioral tension—even
the stressl—is an integral part of this useful function, for it allows us to more
immediately evaluate (a subjective function) our behavior and the effect it is
10
having on ourselves and others.
Behavioral tension serves as an internal emotional compass that we can use
to guide ourselves through the often complicated and treacherous pathways of
interpersonal relations.
Behavioral stress tells us that we are exceeding safe limits for ourselves and
others, and for our larger social, economic, and political structures.
Behavioral tension and stress are, at this point perhaps needless to say,
inherently and necessarily subjective. But of course all of this requires a certain
level of consciousness, perhaps best designated self-aware consciousness,
coupled with the ability to generalize our internally experienced motives. If all
we possessed were the conflicting programs of self-preservation and affection,
we would, be among the life forms whose behaviors are governed by instinct.
We would be driven by the urgings of fight, or flight, or bondedness; and every
so often—like the legendary mule who, thirsty and hungry, looked back and
forth between water and hay, unable to move—we would be caught in the
indecision of those urgings.
But whether or not other mammals with paleomammalian brain structures,
350 The Evolutionary Neuroethology of Paul MacLean

with self-preservation and affection programming, experience conscious conflict

from these two behavioral priorities, we certainly do. We can reflect and genera-
lize not only upon our choices, but upon the meanings they have for our
personal as well as our species' existence and significance. And it is in that
capacity to reflect, to self-consciously experience, generalize, and decide upon
the tug-and-pull of our conflicting urgings, that we come to the third stage of
brain development in MacLean's model: the neomammalian or "new" mammal-
ian brain structures—what I have designated the executive programming.

T H E C O N F L I C T S Y S T E M S N E U R O B E H A V I O R A L (CSN) M O D E L

The neural substrate of consciousness is still a matter of considerable specul-

ation and debate (e.g., see Edelman & Tononi 2000; Damasio 1999, 1994; Cory
2000a; Searle 1997; Smith 1996). Although the emerging mechanisms are still
somewhat unclear, I follow the position here that there is no homunculus (little
person) or other Cartesian dualistic process involved. Nevertheless, it seems that
our expanded and elaborated neocortex (or isocortex), anchored in and
interconnected with our earlier mammalian and protoreptilian brain systems, is
part of the "dynamic core" (Edelman & Tononi 2000; cf. Dennett 1998) neces-
sary to our self-aware or self-reflective consciousness. As well, our elaborated
neocortex provides us with the evolutionarily unique and powerful ability to use
verbal and symbolic language to create concepts and ideas by which to interpret
our consciousness, to describe the feelings, motives, and behaviors that arise
11
within us and in response to our social and environmental experiences. It is
with this so-called executive programming that we acquire the ability to name,
12
to comment upon, to generalize and to choose between our contending sets of
behavioral impulses: self-preservation, commonly called, at a high level of
cognitive generalization, "egoistic" or "self-interested" behavior, and affection,
which we call, at an equally high level of cognitive generalization, "empathetic"
or "other-interested" behavior. Empathy allows us the critical social capacity to
enter into or respond emotionally to another's self-interest as well as other
13
emotional states.
Although the positioning of ego and empathy in Figure 18.2 (facing the
reader) is primarily for illustrative purposes only and is not intended to suggest a
definitive lateralization, there is some evidence to suggest that the right
hemisphere is favored for emotion and the left for more analytical self-
preserving behaviors (e.g., see Damasio 1994; Tucker, Luu, & Pribram 1995;
Brownell & Martino 1998). However, Heller et al. (1998), after noting that it is
well established that particular regions of the right hemisphere are specialized to
interpret and express emotional information, argue that the total experience of
emotion is not lateralized but involves dynamic interactions between forward
and posterior regions of both hemispheres as well as subcortical (limbic)
structures. Such complex, highly generalized capacities as ego and empathy
should more safely be thought of as engaging the interaction of both hemi-
spheres. Davidson (1995), for example, hypothesizes that the left and right
Neural Algorithms, Hamilton's Rule, and Economics 351

anterior regions of the brain are key components of an affective regulatory

system for approach and avoidance behaviors.

Figure 18.2. The Conflict Systems Neurobehavioral Model. A simplified cutaway

representation of the brain showing the behavioral programs and the derivation of
Ego/self-interested and Empathy/other-interested motives and behaviors. I should note
that earlier models, e.g., Freud (id, ego, and superego) postulated three-part conflictual
models. Freud, however, was unable to tie his model to brain circuitry and it remained
ungrounded in neural science because brain research had simply not advanced to that
point.

14
In other words, our executive programming, especially our frontal cortex,
has the capability and the responsibility for cognitively representing these limbic
and protoreptilian brain connections and inputs and making what may be
thought of as our moral as well as rational choices among our conflicting,
impulsive, and irrational or nonrational motivations. This self conscious, gene-
ralizing, choosing capacity accompanied, of course, with language, is what
differentiates us from even closely related primate species and makes findings in
primate behavior, although highly interesting and unquestionably important,
insufficient in themselves to fully understand and account for human behavior.

EXECUTIVE PROGRAMMING AND NEURAL NETWORKS

According to Joaquin Fuster, of the Neuropsychiatric Institute, UCLA, the

frontal cortex constitutes the highest level of a hierarchy of neural structures
(reaching down to the motoneurons and anterior roots of the spinal cord), that
represents and executes the actions of the organism. Because of its topmost
position in this neural hierarchy, the frontal cortex has been named the
"executive of the brain and the organ of creativity." (1999: 187; see also
Goldberg 2001).
Fuster, thus, designates the frontal neocortex as the neural substrate for
executive functioning (cf. Pribram 1973, 1994). There are, however, a number
of competing models for executive functioning, some tied to neural substrate,
some not. Bernard Baars and colleagues of the Wright Institute have proposed a
352 The Evolutionary Neuroethology of Paul MacLean

Neural Global Workspace Model (GW), which combines the concepts of

attention, working memory, and executive function into a theater metaphor.
Baars and colleagues (Newman et al. 1997; cf. Harth 1997) review other
neuroscience and neural network models that deal with attention, binding,
resource allocation, and gating that share significant features with their own GW
model for conscious attention (for an alternative model based on an evolutionary
and clinical approaches and which draws upon MacLean's triune concept, see
15
Mirsky 1996). The authors acknowledge that the models they present imple-
ment only partial aspects of their GW theory. Notably neglected are the
influences of memory and affective systems upon the stream of consciousness
(1997: 1205). The CSN model presented in this paper attempts to incorporate
the affective (generalized into empathy) neural substrate necessary to initiate
and maintain sociality.
It is noteworthy that distributed artificial intelligence (DIA) models more
closely approximate interpersonal behavior in that they seem to reflect an effort
at intelligent balance between the competitive self-interest and cooperation
which is necessary to the operation of complex social organizations (Newman et
al. 1997: 1196;Durfee 1993).
Underpinning the CSN model, the neural substrate for self-survival
(generalized as ego) mechanisms may proceed from circuits in the basal ganglia
and brain stem (protoreptilian complex) through connections with the amygdala,
other limbic structures (early mammalian complex), and probable cortical
representations which add emotion or passion (see Kandel et al. 1995: 595-612),
ultimately to be gated into the frontal cortex by thalamocortical circuitry (e.g.,
see LaBerge 1995; Crick 1994; Baars 1997, 1988; Sherman & Guillery 2001).
Likewise, the mammalian nurturing (affectional) substrate and its associated
motivation, a fundamental component underlying empathy, may originate in the
septal and medial preoptic limbic (see Fleming et al. 1996; Numan 1994, Numan
& Sheehan 1997) areas, proceed through hippocampal and amygdaloid circuitry
(Brothers 1989; Bachevalier 2000) as well as other limbic structures, and in turn,
be gated into the orbital and frontal cortex by neuromodulating thalamocortical
circuits (to include the cingulate cortex), where the conflict with egoistic imputs
is resolved in the executive or Global Workspace of conscious self-awareness.
The neuromodulating and gating of affect as well as cognition by the thalamo-
cortical circuitry is supported by neurologists Devinsky and Luciano (1993),
who report that the limbic cingulate cortex, a cortical structure closely
associated with the limbic thalamus, can be seen as both an amplifier and a
filter, which joins affect and intellect interconnecting the emotional and
cognitive components of the mind (1993: 549).
Tucker, Luu, and Pribram (1995) speculate that the network architecture of
the frontal lobes reflects dual limbic origins of the frontal cortex. Specifically,
the authors speculate that two limbic-cortical pathways apply different motiva-
tional biases to direct the frontal lobe representation of working memory. They
suggest that the dorsal limbic mechanisms projecting through the cingulate
gyrus may be influenced by hedonic evaluations, social attachments, initiating a
Neural Algorithms, Hamilton's Rule, and Economics 353

mode of motor control that is holistic and impulsive. On the other hand, they
suggest that the ventral limbic pathway from the amygdala to the orbital frontal
cortex may implement a more restricted mode of motor control reflecting the
adaptive constraints of self preservation (1995: 233-234). The orbital frontal
cortex via its connections to the anterior cingulate gyrus, amygdala and other
limbic structures seems especially important to the interaction of ego and
empathy (Damasio 1994; Schnider & Gutbrod 1999; Fuster 1999; see also
Weisfeld, this volume). Such findings are consistent with the CSN model in
which ego and empathy represent conflicting subcortical inputs into the cortical
executive. Several researchers have posited the dynamic of conflicting modules,
vying for ascendency in behavior and consciousness (e.g., Edelman & Tononi
2000; Edelman 1992; Dennett 1998; Pinker 1997).
Although it is beyond the scope of this chapter to attempt to deal with the as
yet partially understood detailed electrochemical physiology of such egoistic/
empathetic conflict, it is appropriate to acknowledge that such behavior is made
possible in part by the complex electro-chemical excitatory and inhibitory
interactions among groups of interconnected neurons (e.g., see the discussions in
Koch 1999; Cowan et al. 1997; Fuster 1997: 102-149; Gutnick & Mody 1995).
The role of hormones and neurotransmitters must also be acknowledged in
any complete analysis. For instance, from the egoistic perspective, testosterone
is associated with competitiveness and power urges. Serotonin levels in humans
seem related to confidence and self-esteem. On the empathetic side, oxytocin,
arginine vasopressin, and prolactin are important to pair bonding and maternal
as well as paternal caring behavior. Opioids (endorphins and enkaphalins) seem
important to positive social relationships. For readers interested in more detail,
two recent and wide-ranging volumes update the research focusing specifically
on affiliation and affection: Carter et al. (1997), The Integrative Neurobiology of
Affiliation, and Panksepp (1998), Affective Neuroscience. Panksepp especially
speculates on the contrast between testosterone-driven power urges and oxytocin
and opioid mediated affectional behavior (1998: 250-259; see also Toates
2001). Damasio reminds us, however, that there is a popular tendency to
overemphasize the efficacy of hormones by themselves. Their action depends
upon neural architecture and their effects may vary in different brain regions
(1994: 77-78).

THE MAJOR RANGES OF RECIPROCAL BEHAVIOR

The two master, inclusive and modular programs of self-preservation and

affection that have been wired into our brain structure operate dynamically
according to a set of subjectively experienced and objectively expressed beha-
vioral rules, procedures, or algorithms. Understanding the workings and applica-
tions of these algorithms is the key to grasping the role of dialectical conflict,
tension, and stress in our personal and interactive lives.
The major ranges of the conflict systems neurobehavioral behavioral model
(Figure 18.3) illustrate the features of this ego-empathy dynamic. In the display,
354 The Evolutionary Neuroethology of Paul MacLean

subjectively experienced internal as well as interpersonal behavior is divided

from right to left into three main ranges called the egoistic range, the dynamic
balance range, and the empathetic range. Each range represents a varying mix of
egoistically and empathetically motivated behaviors. The solid line stands for
ego and pivots on the word "ego" in the executive program of the brain diagram.
The broken line stands for empathy and pivots on the word "empathy" in the
diagram.

EMPATHETIC RANGE DYNAMIC BALANCE EGOISTIC RANGE

self-sacrifice compromise power-seeking
submission fairness domination
responsiveness justice assertiveness
supportiveness competitiveness
others over self self over others

Figure 18.3. The Major Ranges/Modes of Behavior. To simplify the graph, the three
points are intended to mark the center points of each range, with varying mixes of ego
and empathy on either side of each point. The graph thus intends to communicate, not a
zero-sum, either/or set of behavioral options or expressions, but a spectrum of the
increasing or decreasing (depending on direction of movement) proportions of ego and
empathy in behavior (see note 16). The graph represents only what may be thought of as
central tendencies of interactive behavior and is far too simple to represent all the
shadings of emotion and motivation.

The Egoistic Range

The egoistic range indicates behavior dominated by self-preservation

programming. Since the two behavioral programs are locked in inseparable
unity, empathy is present here, but to a lesser degree. Behavior in this range is
self-centered or self-interested and may tend, for example, to be dominating,
power-seeking, or even attacking, where empathy is less. When empathy is
increased, ego behavior will become less harsh and may be described more
moderately as controlling, competitive, or assertive. As empathy is gradually
increased the intersection of the two lines of the diagram will move toward the
Neural Algorithms, Hamilton's Rule, and Economics 355

range of dynamic balance. Ego behavior will be softened as empathy is added.

But the defining characteristic of the egoistic, self-interested range is self-over-
others. Whether we are blatantly power-seeking or more moderately assertive, in
this range we are putting ourselves, our own priorities, objectives, and feelings,
ahead of others.

The Empathetic Range

The empathetic range represents behavior weighted in favor of empathy.

Ego is present, but is taking a back seat. When ego is present to a minimal
degree, empathetic behavior may tend to extremes of self-sacrifice and
submission. When ego is increased, empathetic behaviors become moderated
and may be described as supportive, responsive, or any of a variety of "others
first" behaviors. As the influence of ego is gradually added, empathetic behavior
will approach the range of dynamic balance. In the empathetic range, the key
phrase to remember is others-over-self or others first. Whether we are at the
extreme of self-sacrifice or more moderately responsive, we are putting the
priorities of others ahead of our own.

The Dynamic Balance Range

The range of dynamic balance represents a working balance between ego and
empathy. At this point our behavioral programs are operating in roughly equal
measure. I speak of "working," "rough," or "dynamic" balance because the tug-
and-pull between the two programs continues ceaselessly. The dynamic nature
of the programming means that "perfect" balance may be a theoretical point,
unattainable in practice. Our more balanced behavior tends to be characterized
by equality, justice, sharing, and other behaviors that show respect for ourselves
and others. In fact, respect for self and others is the keynote of the range of
16
dynamic balance.

Energy or Activity Level

The extent to which the programs of self-preservation and affection, ego and
empathy, are out of balance, or pulling against each other, is a measure of
behavioral tension. We experience this behavioral tension both internally and
between ourselves and others, in any relationship or interaction. Unmanaged or
excessive tension becomes, of course, behavioral stress. But that is not all.
Important also is the degree of energy we give to the interaction or the
relationship. The amount of energy we put into any activity depends mostly
upon how important we think it is or how enthusiastic we feel about it. In
competitive sports or contests, qualitative differences in energy are easily
observed. In intellectual contests, like chess, the energy invested may be intense,
356 The Evolutionary Neuroethology of Paul MacLean

but much less obvious.

THE PROPOSED ALGORITHMS OF INTERPERSONAL BEHAVIOR

From the dynamic interplay of ego, empathy, and activity level come the
following algorithmic rule statements which may be considered a research
program to be tested empirically.

1. Self-interested, egoistic behavior, because it lacks empathy to some degree, creates

tension within ourselves and between our selves and others. The tension increases from
low to high activity levels. And it increases as we move toward the extremes of ego.
Within ourselves, the tension created by the tug of neglected empathy is experienced
as a feeling of obligation to others or an expectation that they might wish to "even the
score" with us.
Within others, the tension created by our self-interested behavior is experienced as a
feeling of imposition or hurt, accompanied by an urge to "even the score."

Children often reveal the dynamic of such behavior in a clear, unsophis-

ticated form. Imagine two children playing on the living-room floor. One hits
the other. The second child hits back, responding in kind. Or the children may
not hit each other at all. One might instead call the other a bad name. The second
child reciprocates, kicking off a round of escalating name-calling. One child
may eventually feel unable to even the score and will complain to a parent to
intervene. Most of us have experienced such give-and-take as children and have
seen it countless times in our own children and grandchildren. Similar behavior
is embarrassingly observable among adults. It can be seen in husband- and-wife
arguments, bar fights, hockey games, political campaigns, even in sophisticated
lawsuits. The rule operates not only in such highly visible conflict situations, but
also in very subtle interactions—in the small behavioral exchanges, the ongoing
give-and-take of all interpersonal relations.
Expressive of the underlying conflictual excitatory/inhibitory dynamic of the
neural architecture, we can say that

The reactions that build in ourselves and others do so potentially in proportion to the
behavioral tension created by egoistic, self-interested behavior.

That is, the harder I hit you, the harder you hit me in return. Or the fouler a
name you call me, the fouler a name I call you in return. Or perhaps with more
sophistication, I resolve the tension in me by an act of visible "superiority." I
ignore you—although I could call you an even fouler name, if I chose.
Behavior on the other side of the scale is described in the second rule
statement:

2. Empathetic behavior, because it denies ego or self-interest to some degree, also

creates tension within ourselves and others. This tension, likewise, increases as activity
levels increase and as we move toward extremes of empathy.
Neural Algorithms, Hamilton's Rule, and Economics 357

Within ourselves, the tension created by the tug of the neglected self-interest (ego) is
experienced as a feeling that "others owe us one" and a growing need to "collect our
due." This tension, especially if it continues over time, may be experienced as resentment
at being exploited, taken for granted, not appreciated, or victimized by others.
Within others, the tension created is experienced as a sense of obligation toward us.
The reactions that build in ourselves and others, again, are in proportion to the
behavioral tension created. And again, the unmanaged, or excessive tension is exper-
ienced as behavioral stress.

When we do things for others—give them things, make personal sacrifices

for them—it can make us feel righteous, affectionate, loving. But we do want a
payback. That's the tug of self-interest. It can be very slight, hardly noticeable at
first. But let the giving, the self-sacrifice, go on for a while, unacknowledged or
unappreciated (that is, without payback to the ego), and see how we begin to
feel. The tension, the stress, starts to show. We complain that others are taking
advantage of us, taking us for granted, victimizing us. Self-interest cannot be
long short-changed without demanding its due. We may eventually relieve the
stress by blowing up at those we have been serving—accusing them of
ingratitude, withdrawing our favors, or kicking them out of the house. Or we
may sandbag the stress, letting it eat away at our dispositions, our bodies.
On the other hand, when we do things for others, they often feel obliged to
return the favor in some form to avoid being left with an uneasy sense of debt.
Gift-giving notoriously stimulates the receiver to feel the need to reciprocate.
Think of the times when you have received a holiday gift from someone for
whom you had failed to buy a gift. Sometimes the sense of obligation prompted
by the empathetic acts of others can become a nuisance.
The third rule statement describes the relative balance between the contend-
ing motives:

3. Behavior in the range of dynamic balance expresses the approximate balance of ego
and empathy. It is the position of least behavioral tension. Within ourselves and others, it
creates feelings of mutuality and shared respect.

For most of us it is an especially satisfying experience to interact with others

in equality, with no sense of obligation, superiority or inferiority. To work
together in common humanity, in common cause, is to experience behavioral
dynamic balance. Of course, there are many versions of the experience of
dynamic balance: the shared pride of parents in helping their child achieve, the
joy of athletes in playing well as a team, the satisfaction of coworkers in
17
working together successfully on an important project.
358 The Evolutionary Neuroethology of Paul MacLean

RECIPROCITY THROUGH CONFLICT

These algorithms of behavior operate in the smallest interactions, the
vignettes, of everyday personal life. The dynamic of behavioral tension provides
that for every interpersonal act, there is a balancing reciprocal. A self-interested
act requires an empathetic reciprocal for balance. An empathetic act, likewise,
requires a balancing self-interested reciprocal. This reciprocity goes back and
forth many times even in a short conversation. Without the reciprocal, tension
builds, stress accumulates, and either confrontation or withdrawal results. If not,
and the relationship continues, it becomes a tense and stressful one of inequality
or domination/ submission, waiting and pressing for the opportunity for adjust-
ment.
These, then, are the proposed basic interpersonal algorithms of our three-
level brain. These algorithms show how we get to reciprocity through conflict. I
propose that they shape the conflict and reciprocity, the give-and-take, at all
levels of our interactive, social lives.
Overemphasis on either self-interest or empathy, exercise of one program to
the exclusion of the other, creates tension and stress in any social configu-
ration—from simple dyadic person-to-person encounters up to and including
interactions among members of the workplace, society at large, social groups,
and entire economic and political systems.

THE QUESTION OF SCIENCE: PHYSICS VS. SOCIAL

The algorithmic rules of reciprocal behavior proposed here, as central tend-

encies of behavior, operate very imperfectly. I suspect that this will be true of
any behavioral algorithms or principles proposed at this level of generalization
(cf. Maynard Smith 2002). The proposed algorithms, then, can only approxi-
mate, but not fully achieve, the precision of the laws of classical physics or even
quantum mechanics. This is in part because they are achieved through the
process of organic evolution (which involves some random processes and
natural selection) and therefore cannot operate as immutable universal physical
laws but as generalized algorithms with degrees of variation.
The idealized, or rather statistically generalized, tug and pull of ego and
empathy presented here may be further probabilized in actuality by genetic,
gender and developmental, individual experience and learning, and other
environmental shaping and reinforcing factors. In other words, genetically
speaking, given the individual differences in genetic inheritance that we see in
such obvious things as in hair, skin, or eye color, some individuals behaviorally
may be more or less as strongly wired or preorganized for self-preservation and
affection as others. But granting gender and developmental differences, every
human being is, nevertheless, similarly wired or preorganized with the
fundamental brain architecture unless he/she has very serious genetic defects
indeed. Influential developmental psychologists like Jean Piaget (1965) of
Switzerland and Lawrence Kohlberg (1984) of Harvard, operating from a
Neural Algorithms, Hamilton's Rule, and Economics 359

behavioral perspective, have constructed and tested theories of childhood moral

development. In the theories of both men moral stages of development emerge
much the same in all cultures when the child experiences anything approaching
a normal family life. Such generalized moral stages could not be found across
cultures if they were not genetically based on the species-wide brain structure
and its associated behavioral potentialities.
From the standpoint of individual learning, socialization, and other
environmental factors, modifications in biological structures and potentialities
occur in early development and throughout life. As writers such as G. H. Mead
(1934) have assured us long before the emergence of evolutionary neuroscience,
life or the brain develops in an interactive social context. Individual life exper-
iences may facilitate, suppress, strengthen, or otherwise modify the expression
of these inherited biological programs. Environmental factors, to include
physical constraints as well as our socially and scientifically accepted institu-
tions and paradigms, may also shape and reinforce the expression of the evolved
algorithmic dynamic. Individual learning experience or environmental factors of
the individual life cannot, however, eliminate the genetic structure and
programming of the brain; that is, not without radical injury, surgical, or genetic
intervention. And the behavioral tension will be there to both resist the changes
and to shape the experience, even shape the environment itself, in a dynamic
manner.
Because of these factors, the behavioral algorithms are statistical—much in
the same way as are the second law of thermodynamics and quantum theory of
physics. That is, they do not allow precise prediction of specific behavior at the
basic unit of analysis—the individual, molecular, or subatomic level respec-
tively—but only on the aggregated basis of statistical probability. The proposed
algorithmic rules of reciprocal behavior, as here presented, may nevertheless
very well prove to be equally as valid and useful to social science as the laws of
physics are to physical science. They do not and cannot, however, have the
immutable quality of physical laws such as gravity. As products of organic
evolution and developmental processes, they inevitably involve more probab-
ilities because of individual differences, genetic and learned, in the evolved
basic units.
An admittedly loose, but perhaps interesting, analogy can be made between
the inclusive spectrum of possible behaviors of the conflict systems neuro-
behavioral model and the particle wave function of quantum physics. As the
wave function of a particle is defined to include all the possible values of a
particle according to probability, the "wave" function of behavior can be thought
to include all possible internal and interpersonal behavioral probabilities (mixes
of ego and empathy) extending across the egoistic, empathetic, and dynamic
balance ranges. Externally, observed behavior is predictable from the model, as
is quantum behavior, only on a probability basis specified by the metaphorical
wave function. The behavioral "wave" function, like that of particle physics,
collapses or reduces to one behavior in a decision, action, or observation. If it
doesn't collapse, we see frustration, tension, and indecisiveness—ambiguous
behavior stalled in uncollapsed waveform.
360 The Evolutionary Neuroethology of Paul MacLean

Upon observation by an external observer, the wave function of behavior can

be considered to collapse to a specifically observable behavior on the part of the
individual and that is the end of it. But this would be an overly simplistic
"objective" perception somewhat more characteristic of the now largely
superceded radical behavioristic perspective. Internally, subjectively, we
experience a much more complex process because we have conscious access to
the dynamic. We know in our conscious awareness the tension, the difficulty,
the struggle we go through in important issues of ego and empathy conflict.
Even yet, in the surely much simpler processes of quantum physics we still do
18
not fully understand what set of dynamics leads to the wave function collapse.
In behavior, the dynamic lies in the complexities of subjective preconsciousness
and/or self-aware consciousness.

THE UNIVERSAL NORM OF RECIPROCITY

The norm of reciprocity has long been a major theme in anthropology and
sociology (e.g., see Gouldner 1960; van Baal 1975; Bowles & Gintis 1998: esp.
Ch. 17) and more recently in economics (e.g., Fehr & Gachter 2000). This
universally observed norm, found in all societies, primitive and modern, has
been accounted for, or shown to be possible, in evolutionary theory by such
concepts as kin selection, inclusive fitness (Hamilton 1964), reciprocal altruism
(Trivers 1971, 1981; Alexander 1987), and game theory (Maynard Smith 1982;
Axelrod & Hamilton 1981). These efforts draw upon gene-centered perspec-
tives, which see such reciprocity as basically selfish. More recently, extensive
reciprocity seen as based not upon selfishness, but empathy, has reportedly been
observed in the behavior of rhesus monkeys (de Waal 1996). F. de Waal's
approach is a welcome departure that tries to escape the selfishness of gene-
centered approaches and looks to the implied motivational mechanisms. All
these approaches, however, to include that of de Waal's, have been based on the
external observation of behavior. They have not attempted to identify or even
speculate upon the neural mechanisms within the organism that must necessarily
have been selected for by the evolutionary process to accomplish the functions
of motivating, maintaining, and rewarding such observed reciprocal behavior.
I suggest it is time now to consider fully what the newer findings of
neuroscience add to the discussions from the gene-centered and ethological
perspectives. I think that at this time in our evolutionary thinking, it has been
established beyond any reasonable doubt, by the work of Hamilton, Trivers,
Alexander, Maynard Smith, et al., that even from the most hard-core selfish
gene perspective, the basis for the closely related behaviors of reciprocity,
cooperation, and altruism has, from the Darwinian or the Neo-Darwinian
perspective, been established in the human genome (e.g., see the summary in
Corning 1996). The presence of these behaviors has further been confirmed by
quantities of observational data in primates, even in studies of early protohuman
hominids (Isaac 1978), and by extensive anthropological and sociological obser-
vation.
Neural Algorithms, Hamilton's Rule, and Economics 361

In other words, we now know that we must have, wired into our brain and
nervous system, the neural mechanisms that make such behaviors possible. It is
time, therefore, with the full emergence of neuroscience, to make every effort to
identify and specify these brain mechanisms and extrapolate the implications of
their presence and functioning for our personal and social lives. Although it has
failed to adequately incorporate the literature of evolutionary neuroscience, this
is, in fact, the thrust of the emergent subdiscipline of evolutionary psychology
(Cosmides & Tooby 1989; Tooby & Cosmides 1989; Barkow, Cosmides, &
Tooby 1992; Crawford & Krebs 1998; Buss 1999).

THE EVOLUTION OF THE MARKET

To understand the behavior of the modern day free enterprise market as it is

shaped by our inherited brain structure and behavior, it is helpful to go back to
early times—to reconstruct as best we can the days before the market appeared.

The Family or Group Bond

In those times, when people consumed what they produced, the excess that
they shared with, gave to, or provided for the needs or demands of the family or
community was in the nature of natural affection or empathy. The reward for the
empathetic, supplying act was emotional—there was not a specific, but a diffuse
value assigned to it. It also had social effects—the givers, providers gaining
status in the group. The emotional and the social effects were both directly
governed by the reciprocal algorithms of behavior.
Let us look more closely. The provider, say the warrior brought meat from
the hunt or the wife brought berries and fruits from the field, tanned skins, and
so on, to give to the family or group (cf. Willhoite 1981: 242). The act of
providing, giving, created behavioral tension in the giver, who acting empathet-
ically denied ego to some degree and required a response of acknowledgment,
gratitude, respect, affection, or some other reaffirmation of ego. This providing
or giving also created behavioral tension in the receivers. It was a service to
their ego, their needs or demands—to their own preservation—which created
tension requiring an offsetting empathetic response, a thank-you, an expression
of appreciation or respect. In any family or close group, even now, this dynamic
flows constantly, even in the smallest activities. In the small group the rewards,
the reciprocations, are largely not quantified, but are diffuse. They become
obligations—bonds—that hold the group together for protection or mutual
survival. Nevertheless, they must achieve some approximation of balance or the
unresolved tension will build within the group and become disruptive. Expres-
sions for thank you and you 're welcome, found in all known human languages,
reflect this reciprocity.
362 The Evolutionary Neuroethology of Paul MacLean

The Gift

From these early, primitive behavioral exchanges, emerged the gift: an

empathetic act of providing or serving that followed the same algorithmic
behavioral rules that governed provision for survival. It created tension in the
giver—an expectation of reciprocity—and tension in the receiver, who was
bound to reciprocate. The rewards associated with the gift were diffuse,
unspecified, unquantified—except by some subjective measure of feeling,
emotion, or behavioral tension. A gift to a warrior or chief might vaguely
obligate his protection. A gift to a prospective mate might vaguely obligate his
or her attentions.

From Gift to Transaction

From the gift evolved the transaction—namely the gift with the reciprocal
specified or quantified. The transaction is the beginning of the contract, perhaps
of the market itself. The transaction operates, however, by the same algorithms
of behavior as the gift—except that it attempts to head off the residual,
unresolved behavioral tension that creates a condition of obligation or bonding.
After all, in the market, we may be dealing with strangers not to be seen again.
Nevertheless, it retains its essential mammalian characteristics as an act of
empathy, of nurturing, which requires a balancing reciprocal act in payment to
ego.
When we encounter its equivalent in the impersonalized market economy of
today, how often do we feel the subjective experience of the transaction? We
take our sick child to the doctor, who empathetically and carefully applies the
knowledge it took 10 years and a fortune to gain. We pay the bill—that is, we
make a return gift with money that represents a portion of our accumulated
education and labor. The scenario is repeated in transactions with the plumber,
the carpenter, the computer maker. The behavioral algorithms still apply, but the
feeling, the subjective experience has to a large degree been lost.

Behavioral Tension Yet Drives the Transaction

But wait! Let the transaction go wrong, the expected reciprocals not be
forthcoming and the behavioral tension becomes immediately and personally
felt. The reality of the transaction—the market—reveals itself with clarity and
intensity. No one likes to be cheated or short-changed. And most will be moti-
vated to take some action to correct the imbalance in expected reciprocity or
harbor the behavioral tension indefinitely to be acted upon in the future.
The evolution of the transactional market (demand and supply) as shaped by
neural architecture can be summarized in Figure 18.4.
Neural Algorithms, Hamilton's Rule, and Economics 363

STRUCTURE OF RECIPROCAL EXCHANGE

BY BRAIN ALGORITHMS
(NEURAL ARCHITECTURE)

E m e r g e n c e o f

MARKET &
S U P P L Y
D E M A N D

< 3. TRANSACTION RECIPROCAL

(IN EARLY STATES) SPECIFIED

2. GIFT RECIPROCAL
ANTICIPATED
(INTRATRIBAL)
RECIPROCAL
1. SHARING
D I F F U S E
(HUNTING & GATHERING (PERSON TO PERSON
BANDS-KIN) EMPATHY & EGO INTERPLAY
BONDING)
* SUPPLYING DEMANDING
EMPATHETIC RANGE DYNAMIC BALANCE EGOISTIC RANGE
self-sacrifice compromise power-seeking
submission fairness domination
responsiveness equality assertiveness
supportiveness competitiveness
others over self self over others

Figure 18.4. Evolution of Market Exchange Based on Dynamics of Neural Architecture

364 The Evolutionary Neuroethology of Paul MacLean

METAECONOMICS AND MULTIPLE-UTILITY

From the transactional perspective, the CSN model also provides under-
pinning for what is called metaeconomics and the question of multiple utilities
(Lynne 1999, 2000; Lutz 1993; Etzioni 1986). The CSN model shows that the
tug and pull between ego and empathy goes on constantly within us and between
us as we interact socially. To the extent that our economic transactions or
choices are social, and they inevitably are, they will involve the tug-and-pull of
ego and empathy to some degree. The very nature of social or market exchange
is transactional or interpersonal. The idea that we make independent choices
separate from interpersonal or social concerns is largely illusional. The transac-
tional atom when opened up is shown to be composed of ego and empathy in a
state of negotiated tension (Cory 1999: 77-78). There is therefore some degree
of behavioral tension from the tug and pull of ego and empathy, an implicit, if
not actual, dual or multiple motive or perhaps utility on both sides in every
social or market choice or transaction. The degree of tug and pull or behavioral
tension will depend upon the triviality or significance of the transaction—
something neoclassical theory does not discriminate.
The confounding of self-reference with self-interest is a fundamental fallacy
of the neoclassical approach that allows the subsuming of all motives under the
rubric of self-interest and obscures the roughly equal role of empathy. Taking
the individual as the starting point, microeconomic theory mistakenly transforms
this individual or self-referential perspective into an all-inclusive motive of self-
interest. From this logically unwarranted transformation any other motive is
seen as proceeding from self Therefore empathy (and its derivatives of cooper-
ation and altruism, even love) can be trivialized as tastes or preferences indis-
tinguishable in significance from coffee, tea, or milk. But the hidden duality of
ego and empathy is seen in every demand curve and supply curve, especially
when both are combined to show price equilibrium. The dual roles are always
present implicitly if not explicitly. The supplier performs the empathetic role;
the demander performs the egoistic role. (See Appendix 18.1 for examples of the
hidden duality of ego and empathy within the customary self-referential neo-
classical perspective.)
In terms of physics, the neural network architecture of ego and empathy may
be seen as interlocked, often conflictual motive forces, each with its own moti-
vated vector, which in their interactional dynamic produce a resultant vector that
determines choice. But the organic, neural dynamic is more complex than the
representation as forces of physics suggests. The choice does not necessarily
mark the once and for all release or resolution of behavioral tension, as assumed
in the mathematical representations of classical economics. Owing to the neural
capacity for memory combined with emotion, important choices may carry a
residual of behavioral tension that may be cumulative in its social effects. And
the organic social algorithm is, further, homeostatic in its function—like other
algorithmic physiological regulatory processes of the body (e.g., blood sugar,
body temperature) that serve to adjust function and behavior to keep us, for the
most part, within survival limits.
Neural Algorithms, Hamilton's Rule, and Economics 365

T H E I N V I S I B L E H A N D IN T H E S T R U C T U R E A N D B E H A V I O R OF
THE MARKETPLACE

To understand the function of the invisible hand in the socio-economic

market, it helps to maintain a clear distinction between structure and behavior.

Structure

The invisible hand as the tug and pull of ego and empathy is expressed in the
market structure as demand and supply. The reciprocal dynamic tends to work
despite the unidimensional overemphasis on self-interest in classical economics
by the fallacy of self-reference. This is because the very structure itself of the
market is the institutionalized product of the ego/empathy dynamic of our
evolved neural architecture. Our self-survival ego demands are rooted ultimately
in our ancestral protoreptilian or vertebrate neural complexes. Contrastingly, the
act of providing or supplying, is fundamentally an act of mammalian nurturing.
The market exchange system originated from this dynamic. The market could
never have evolved or been maintained on the basis of ego or self-interest alone.
Without empathy we would not know how or what to do to respond to the needs
of others.

Behavior

Behavior, in individual choices and transactions within the above

institutionalized structure, may vary considerably in the mix of ego and empathy
motives on both the demand and supply sides. Nevertheless, even in the most
ego-skewed (or self-interested) market behavior, the overall tendency of the
market will be toward a balance of ego and empathy. Individual and collective
actors, whether seemingly motivated primarily by self-interest or not, will be
compelled by the very evolved and institutionalized market structure itself—to
survive in the market—to perform the structural equivalent of empathy. That is,
they will be required to provide (supply) a proper service or product to fill the
needs (demand) of others.
To the degree, however, that empathy is a consciously included and recog-
nized behavioral motivational component within the market structure, the
product or service provided may be enhanced in quality and the emergence of
trust in market relationships will be facilitated. Conversely, the overemphasis on
self-interest in the neoclassical paradigm tends to vitiate the development of
quality and the emergence of trust in the market. Aside from the scientifically
inaccurate concept of the market in neoclassical economics, this vitiation of
quality and trust is one of its greatest drawbacks, in practice.
Reciprocity through conflict is achieved in the range of dynamic balance
where behavioral tension operating freely tends to pull us. In dynamic balance,
ego and empathy provide for the emergence of cooperation and fairness, trust
366 The Evolutionary Neuroethology of Paul MacLean

and morality, in interpersonal, social, and economic exchange activities. Taking

the dynamic balance range to be approaching or approximating the equilibrium
of ego and empathy as driven by behavioral tension, we can derive the formula:

19
BT (behavioral tension) = Ego/Empathy = ±1 (as dynamic equilibrium or
unity, dynamic balance)
or
BT = Ego = ±1 (approx. equilibrium or unity)
Emp dynamic balance

The above formula (with either ego or empathy as the numerator or

denominator to avoid the inconvenience of fractions) gives basic mathematical
expression to interaction of ego (demand) and empathy (supply). As the two
motives intersect freely in the marketplace, we tend to have equitable
exchange—or in the case of specific products and services, we tend toward
equilibrium price, or fair price. (See Appendix 18.2 for the clarifying effect of
the above formula on the standard treatment in calculus for demand and supply.)
Since the evolved algorithmic dynamic works imperfectly, I use the word tend.
The formula or equation proceeding out of our evolved neural network
architecture thus provides the unifying linkage between neuroscience and
economics or social exchange theory. The behavioral tension driving toward the
proximate dynamic balance between demand and supply in the marketplace
accounts for the motive force for the venerable Invisible Hand—that illusive
dynamic previously accounted for variously by the hand of Deity, Newtonian
mechanics, or other inappropriate physical processes (see Cory 1999: 92-95;
Ingrao & Israel 1990).
The marketplace is thus clearly a product of the dynamic of our evolved
neurological architecture. The same dynamic formula can be shown to underlie
not only market and social exchange but also power relationships, social
stratification, relations of inequality, and even cost-benefit analysis. Kept free
(by appropriate institutions) of the skewing effects of excessive wealth
accumulation and the pressure of powerful special interests, both a democratic
free enterprise system and a democratic political system will, in accord with the
neural architecture, tend toward a dynamic equilibrium which minimizes
economic and political inequalities.
On the other hand, the behavioral tension or inequality within a market
system or a political system may be indexed by the same dynamic formula to the
extent that it departs from dynamic equilibrium and the ratio begins to diverge
increasingly.

THE SOCIAL BRAIN, INCLUSIVE FITNESS, HAMILTON'S RULE,

AND THE EQUATION OF OUR NEURAL ARCHITECTURE

I suggest that the equation developed from our neural architecture expresses
the central tendency of the social brain proposed by the Group for the
Neural Algorithms, Hamilton's Rule, and Economics 367

Advancement of Psychiatry (GAP) (Gardner, this volume) as well as represent-

ing the motivating mechanism anticipated by the concept of inclusive fitness so
central to evolutionary psychology. W. D. Hamilton (1964), in his kin selection
model, formalized the issue of how genes for cooperation and altruism could
evolve in his kin selection model. The core of this inclusive fitness model is that
it weighs the effect of genes not only on the individual that carries them but also
on kin individuals who share the same genes. According to what has come to be
called Hamilton's rule, genes coding for cooperation, reciprocity or altruism
could evolve if the costs of cooperative behavior to the individual were
outweighed by the benefits to related individuals carrying the same genes.
Hamilton's rule is expressed varyingly as

rb - c > 0 or c < rb

In this formula r is the coefficient or degree of relatedness or kin, b is the

benefit of the cooperative or altruistic behavior to the kin, and c is the cost of the
behavior to the individual. The equation predicts that as r increases, benefits will
exceed costs and cooperation, reciprocity, or altruism would be favored by
natural selection. Hamilton's rule gives the basic formula for inclusive fitness
from the external gene's eye view. Hamilton did not speculate on the actual
mechanisms created by the genes to motivate and/or sustain such behavior. The
formula of our social neural architecture derived from the CSN model expresses
this motivating mechanism and establishes linkage with Hamilton's formula. In
other words the equation deriving from the CSN model expresses the function of
the neural architecture which the genes actually did produce under the terms of
Hamilton's rule. The proposed social brain formula can, in fact, be expressed in
the same cost/benefit terms that Hamilton uses. Empathy can be considered the
cost to the behaving individual, ego can be benefit to the survival requirements
of the recipient. Substituting cost and benefit into the formula, we get the gene-
based operational mechanism for Hamilton's rule (see Cory 1999: 97-100).

BT = Benefit = ± 1
Cost

According to the algorithms of our social neural architecture, any empathetic,

cooperative, or altruistic behavior will serve to improve the odds of survival of
self plus others inclusively over purely egoistic or self-interested behavior. This
is compatible with Hamilton's rule which says that as long as the benefit to
related individuals exceeds the cost to the behaving individual, the genes
supporting such behavior can be favored by natural selection. Of course, once
the neural mechanism, the social architecture, is in place, as it has been for
thousands of years, the empathetic or altruistic behavior may be extended to
nonkin—even the universe itself—by appropriate education and socialization
through the medium of language that draws upon, modifies, and elaborates the
existing neural substrate (e.g., see Buss 1999: 228; cf. MacLean 1990: 562).
368 The Evolutionary Neuroethology of Paul MacLean

CONCLUSION

In conclusion the neural algorithms of our social brain function as competing

or conflicting neural networks, both excitatory and mutually inhibitory, interact-
ing with each other within homeostatically prescribed limits (see Levine & Jani
this work for a neural network model of the ego/empathy dynamic; cf Leven
1994). They represent the gene-produced operational mechanism predicted by
Hamilton's external gene's eye rule of inclusive fitness. Their interactive
dynamic can be mapped on to mathematical operations or formulas identifiable
with social stratification and inequality as well as the invisible hand of economic
supply and demand. As the ratio diverges from approximation to plus or minus 1
or unity, it serves to index the behavioral tension and stresses among ourselves
and within our social and political structures. The equations expressing their
dynamic interactions approaching equilibrium or unity as reflected in exchange
and political economy are as follows:

Neuroscience:
BEHAVIORAL TENSION = EGO = ±1 (approx. equilibrium or unity)
EMPATHY dynamic balance

Social Psychology:
INTERPERSONAL TENSION - EGO - ± 1 (approx. equilibrium or unity)
EMP dynamic balance

Economics:
EQUILIBRIUM PRICE - DEMAND = ± 1 (approx. equilibrium or unity)
SUPPLY dynamic balance

Political Economy:
POLITICAL TENSION = DOMINATION = ±1 (approx. equilibrium or unity)
SUBORDINATION dynamic balance

Invisible Hand
Of economics:
Of politics:

BT = EGO = ±1 (approx. equilibrium or unity)

EMP dynamic balance

The CSN model, emerging from evolved neural architecture, not only offers
a mathematically represented mechanism for the social brain of psychiatry, it
permits the unifying of evolutionary neuroscience with the central inclusive
fitness concept of evolutionary psychology. Further, it anchors market theory
firmly in neuroscience and supports the introduction of the moral component of
Neural Algorithms, Hamilton's Rule, and Economics 369

empathy into the rational calculus of economics and other social sciences. The
model supports on-going efforts in economics and sociology to introduce
cooperation and fairness, trust and morality into the neoclassical calculus and
definitively counters the long-prevailing, inaccurate, and troubling self-
interested bias of received microeconomic theory. The CSN model provides the
basis for a new research program to develop and test the hypotheses proceeding
therefrom and to explore the potential implications for rethinking aspects of
contemporary economic and political policy.

APPENDIX 18.1
NEURAL ARCHITECTURE AND THE DUALITY OF THE MARKET

The Demand, Supply, and Equilibrium curves that follow are presented in very
simplified form. They, nevertheless, illustrate the essential features of all such curves.

I. The Demand Curve

Price Quantity Price per unit

$50 1 unit

$30 3 units

$10 5 units

0 1

The demand curve slopes downward because as price increases on the y-axis, the quantity
people are willing and able to buy generally decreases (x-axis). Even the single actor
perspective of the demand curve shows the duality of exchange expressive of our neural
architecture: Price = give = empathy; Quantity = take = ego. In other words, price is what
we give, quantity is what we take. The demand curve, therefore, illustrates the reciprocal,
give-and-take, empathy-ego social exchange relationship.
370 The Evolutionary Neuroethology of Paul MacLean

II. The Supply Curve

Price Quantity Price per unit

$50 5 units

$30 3 units

$10 1 unit

0 1

The supply curve slopes upward because as price increases (y-axis) suppliers are willing
and able to provide more units. The supply curve, like the demand curve, shows the
duality of exchange expressive of our neural architecture. From this perspective: Quantity
provided = give = empathy; Price = take = ego. Again, the supply curve illustrates a
reciprocal, give-and-take, empathy-ego social exchange relationship.

III. Equilibrium in the Market

0 1 2 3 4 5
Neural Algorithms, Hamilton 's Rule, and Economics 371

The duality of exchange expressive of our neural architecture is most clearly seen in
the graph of demand and supply curves combined to show their equilibrium point. The
supplier performs the empathetic structural or institutional role; the demander performs
the egoistic structural or institutional role. In standard economics the demand and supply
curves are related only at the point of equilibrium.

The formula derived from our neural architecture provides a significant insight:

BT = EP (equilibrium price) = Demand = ±1 ( approx equilibrium or unity)

Supply dynamic balance

In economics price is treated as exogenous. That is, demand and supply curves are
related only at the equilibrium price. Price as an exogenous variable draws them together
but remains essentially unexplained. The formula from neural architecture demonstrates
the continuing relationship between demand and supply and the source of motivation for
change that brings demand and supply into equilibrium—behavioral tension that
motivates buyers and sellers to change their behavior. Thus, all points on the demand and
supply curves that do not match the equilibrium point are indicators of behavioral
tension. This effectively unifies the dynamics of neural architecture with economics.

The Problems with Empathy as a Preference or Taste

Currently economics proceeding from the self-reference perspective treats self-

interest as the only primary motive. Empathy is treated as a taste or preference. The
problems with such treatment are:
1. Empathy becomes optional. You may have such a taste or preference or
not. This is distorting because empathy is not optional but a fundamental
motive of our neural architecture roughly equal with self-interest or ego.
2. It trivializes empathy. Empathy as a preference or taste is indistin-
guishable from a taste or preference for Fords or Mercedes or for tennis
shoes or sandals.
3. It distortingly forces a rational self-interested perspective.
4. It misconstrues the real nature of the market.
5. It obscures the dynamic shaping effect of the ego/empathy interplay in all
social exchange.
6. It is not consilient with evolutionary neuroscience—a more fundamental
science.

APPENDIX 18.2: CALCULUS IN PRICE THEORY

As represented in standard texts (e.g., see Landsburg 1992) on price theory, demand
and supply are functions that convert prices to quantities.

D(P) = Quantity demanded at price P

S(P) = Quantity supplied at price P

372 The Evolutionary Nenroethology of Paul MacLean

Derivatives are expressed as follows:

The fact that the demand curve slopes downward is expressed by the inequality

D'(P)<0 OR dOd < 0

dP

The fact that the supply curve slopes upward is expressed by the inequality

S'(P)>0 OR dQs > 0

dP

Equilibrium price is the price at which

D(P) = S(P)

Equilibrium quantity is the common value.

Again, in this case as well as in the illustrations of the demand, supply, and
equilibrium curves, when treated in the standard manner demand and supply are related
only at the point of equilibrium—the equilibrium price. Price, again, is an exogenous
variable that brings them together but remains essentially unexplained. Demand and
supply are treated separately prior to the equilibrium point. The calculus model used in
economics as reflected above does not represent the relationship of behavioral tension
that exists at all other points. The formula from neural architecture does this:

BT = EP = DEMAND - ± 1 (unity, approx. equil.)

SUPPLY dynamic balance

This reinforces or confirms the previous insight that all other points (prices) on the
demand and supply curves are indicators of behavioral tension. Behavioral tension in
equilibrium, then, equals price in equilibrium, and price or behavioral tension not in
equilibrium is what motivates demanders and suppliers to alter prices or respond to them.
Such is the essence of any negotiating process in the market, no matter how formalized. It
is seen clearly in domestic flea markets and in many similar institutions (e.g., bazaars)
around the world. Price, thus, becomes an endogenous variable; that is, one that we can
explain or account for (Cory 2001a, b).

NOTES

1. See Reiner (1990) and Campbell (1992). A great deal of unreflective and inaccurate
criticism of MacLean's position by Reiner and Campbell is obviated by a close reading of
MacLean's recent work.
2. Cory (1998, 1999) documents in detail the inaccuracies and misrepresentations of
MacLean's work in the reviews by Reiner (1990) and Campbell (1992), which have been
relied on by other scholars. Cory concludes that the triune brain concept, when properly
represented, is soundly grounded in evolutionary neuroscience, and with some
clarifications, is the most useful concept for linking neuroscience with the more highly
integrated concepts of the social sciences. Although the concept may lack the desired
Neural Algorithms, Hamilton's Rule, and Economics 373

precision for some neurophysiological researchers, as modified in this paper it is totally

adequate and useful for the behavioral propositions put forth here.
3. For example, see Humphrey (1976), Isaac (1978), Erdal and Whiten (1996),
Cummins (1998), and Tooby and DeVore (1987). Cosmides and Tooby surmise that
cognitive development in humans allowed a widening and diversification of items of
social exchange (1989: 59).
4. For earlier versions of the behavioral model developed here see Cory (1974, 1992,
1996). Also compare the model of human communication by Dingwall (1980) based in
reflexive(striatal or reptilian) affective (limbic or paleo mammalian), and cognitive
(neocortical or neomammalian). Dingwall draws upon Lamendella (1977). See also
Leven(1994).
5. Experimental work in animals as diverse as lizards and monkeys shows the reptilian
complex is involved in displays of agonistic and defensive social communication. Also it
is noteworthy that partial destruction of the reptilian complex eliminates the aggressive,
territorial display (MacLean 1993: 108).
6. The division of function between the protoreptilian complex and the limbic system
is not clear cut, but rather entangled. The lower structures of the limbic node have been
shown to augment the self-preservational behavior of feeding, fighting, and self-
protection (MacLean 1990, 1993: 109), adding passion or emotion to them (Kandel, et.
al. 1995: 595-612). The newer structures in the upper half of the limbic node, especially
the septal, including the medial preoptic area, and thalamocingulate division, are involved
in the affectional, family-related behavior (Panksepp 1998; Numan & Sheehan 1997;
Fleming et. al. 1996; MacLean 1993: 109).
7. Positing the affectional programming draws not only upon current neuroscience but
also the extensive literature on the concepts of social bonding and attachment, especially
the work done on higher primates and man. For fundamental work on lower animals see
the pioneering work of the Austrian ethologist and Nobel prize winner Konrad Lorenz
(1970 & 1971). Particularly relevant here would be the work of psychologist, Harry F.
Harlow on the nature of love and attachment in rhesus/macaque monkeys (1965, 1986).
Harlow described five affectional systems in monkeys—maternal, mother-infant, age-
mate, heterosexual, and paternal (1986). In this chapter I have proposed one all- inclusive
affectional program. It is personally interesting to me that Crews (1997) argues that
affliliative behaviors evolved from reproductive behaviors. This is a position that I took
in 1974 in the first version of the conflict systems neurobehavioral model (Cory 1974)
presented in this chapter. There has been a recent resurgence of interest in the evolu-
tionary biological basis of affection and empathy, especially in primates (e.g., Goodall
1986; de Waal 1996). In the case of humans, the work of Spitz (1965) and British
psychiatrist John Bowlby (1969, 1988) is of special interest. All the foregoing reflect
field observations, experimental behavioral observations and clinical work. None of them
penetrate the brain itself. More recent work in computer modeling of neural processes has
focused primarily on cognition and avoided dealing with the more complex issues of
affiliation and emotion. For example, Churchland and Sejnowski in their extensive and
well known work on the computational brain acknowledge the neglect of these critical
areas (1992: 413). From the standpoint of neuroscience, it is also notable that Kandel,
Schwartz, and Jessell, authors of the most widely used text on introductory neuroscience
also show this neglect (1995). See also Damasio 1999. Extensive research has been done
on the role of the amygdala in emotion, but such research has generally focused on the
emotion of fear (LeDoux 1997). The neglect is not difficult to explain. Research on such
complex pathways within the brain, in spite of great progress in recent years, is still in its
very early stages. The unknowns are still very vast. Currently the best summary of
research in neuroscience on the nurturing, caring, family-related behavior are contained
374 The Evolutionary Neuroethology of Paul MacLean

in Panksepp (1998); Numan and Sheehan (1997); Fleming et al. (1996); MacLean (1990:
380-410; 520-562). For a popular treatment see Taylor (2002)
8. In cognitive neuroscience brain modules are commonly seen as competing and also
cooperating (e.g., see Crick 1994, Baars 1997). The idea of competing or conflicting
modules contriving behavioral tension is also acknowledged by Pinker (1997: 58, 65).
9. The evolution of the neocortex, our big brain, was in all probability greatly
enhanced by the tug and pull of our conflicting programs. Humphrey (1976) sees the
function of the intellect providing the ability to cope with problems of interpersonal
relationships. See also the discussion in Masters (1989: 16-26) and Erdal and Whiten
(1996). Cummins (1998) argues that interpersonal relationships, competing and cooper-
ating with conspecifics for limited resources, is the chief problem confronting social
mammals. Cummins concentrates on dominance hierarchies which she sees as dynamic
rather than static.
10. Damasio's "somatic marker" hypothesis by which emotions become connected by
learning to certain behavioral scenarios is an example of a functional mechanism for
producing behavioral tension/stress (1994: 165-201). Also see the comment on chronic
mental stress (1994: 119-120). Tension and stress are mediated by hormones and neuro-
transmitters acting within neural architecture, rather than through the so-called hydraulic
pressure model of earlier psychodynamic models.
11. A language module did not, of course, pop out of nowhere and appear in the
neocortex. The capacity for spoken language involved modifications of supporting
anatomical structures including the laryngeal tract, tongue, velum (which can seal the
nose from the mouth) and the neural connections that tied in with motor areas necessary
for the production of speech. These all evolved relatively concommitantly from the
hominid ancestral line and, combined with the elaboration of the neocortical structures of
thought and syntax, made language possible. This example of the complexity of language
development provides a caveat to avoid overly simplistic one for one specialized module
for specific behavioral or functional adaptation positions. The work of Philip Lieberman,
a linguistic psychologist at Brown University, is especially relevant for the understanding
of this very complex language capability. See the up-to-date treatment of these issues in
Lieberman (1998, 2000).
12. The ability to self-consciously generalize is apparently a unique gift of the
neocortex with it billions of neurons interconnected into hierarchical networks. The level
of generalization issue in all our disciplines likely springs from this. That is, we can move
from parts to wholes in generalizing and from wholes to parts in analyzing freely up and
down throughout our neural networks. Generalizing (and implicitly analyzing) been
recognized by scholars in many disciplines as perhaps the defining characteristic of the
human brain (e.g., Hofstader 1995: 75; Einstein 1954: 293). This generalizing capacity
loosens up the tight wiring of routines and characteristics of earlier brain structures and
allows us to manage and, to some degree, overcome the mechanisms that we inherited in
common with kindred species (e.g., see Panksepp 1998: 301). In other words, the
generalizing, analyzing capacities of the neocortex change the rules of the game for us
humans by freeing us up from the blind tyranny of primitive mechanisms. This capacity
must always be weighed when trying to apply findings in, for example, even primate
ethology to humans. One of the reasons our feelings and motives are so difficult to
verbalize and communicate to others is probably because the earlier evolved brain
(reptilian and limbic) systems are nonverbal. Their input enters the neocortex through
neural pathways as inarticulate urgings, feelings. It falls to the neocortex with its verbal
and generalizing ability to develop words and concepts to attempt to understand,
represent, and convey these inarticulate urgings. MacLean (1992: 58) states that the
Neural Algorithms, Hamilton's Rule, and Economics 375

triune brain structure provides us with the inheritance of three mentalities, two of which
lack the capacity for verbal communication.
13. My use of the term empathy here includes the affectional feelings of sympathy
which are dependent upon empathy, plus cognitive aspects (Hoffman 1981, 2000). Losco
has noted that empathy, amplified by cognitive processes, could serve as an evolved
mediator of pro-social behavior (1986: 125). Empathy and sympathy are frequently used
inclusively, especially in more recent writing (Eisenberg 1994; Batson 1991). For this
reason, in order to suggest the inclusion of sympathy, I have chosen to use the term
empathetic rather than the more usual empathic. The positing of the ego and empathy
dynamic goes back to the historical juxtaposition of self-interest or egoism and sympathy
or fellow feeling of in the thought of David Hume, Adam Smith, and Schopenhauer
(Wispe 1991). The present articulation goes back to my doctoral thesis done at Stanford
University (1974). The conflict systems neurobehavioral model was applied in several
programs which I authored for corporate management training through the education and
consulting corporation United States Education Systems during the period 1976-85.
Recently Roger Masters (1989) has also noted the possible innate roots of contradictory
impulses to include selfishness and cooperative or altruistic behavior in human
nature.Trudi Miller (1993) has also drawn our attention to this historical duality and
suggested its applicability for today. Neither Hume, Smith, Schopenhauer, Wispe,
Masters nor Miller, however, attempted to articulate a model of behavior based upon this
duality, or as MacLean calls it "triality", acknowledging the role of the neocortex in
articulating the otherwise nonverbal urgings (1993).
14. The frontal neocortex especially has long been recognized to be involved in
executive functions. See the excellent summary and discussion of findings in Miller and
Cummings (1999), Fuster (1997: 150-84). See also Pribram (1973; 1994). Although
executive function is frequently equated with frontal cortex function Eslinger (1996)
reminds us that the neural substrate of executive functions is better conceptualized as a
neural network which includes the synchronized activity of multiple regions, cortical and
subcortical (1996: 392). Eslinger also notes the usual neglect of critically important
affectively based empathy and social and interpersonal behaviors in neuropsychological,
information-processing, and behavioral approaches (390-391).
15. Levine (1986) has also considered MacLean's triune modular concept as a useful
tool in network modeling.
16. The dynamic of the model, the tug and pull of ego and empathy, self- and other-
interest allows the expression of the mix of motive and behavior as a range or spectrum.
The usual dichotomizing of self-interest and altruism is seen only at the extremes of
ranges. All or most of behavior is a mix of varying proportions. Jencks (1990: 53-54)
also notes that every motive or act falls somewhere on a spectrum or range between the
extremes of selfishness and unselfishness. Teske (1997) sees a blend of self-and other-
interest in his identity construction concept.
17. See Eckel and Grossman (1997). Without making any connection with brain
science or the reciprocal algorithms of behavior, the authors use a typology of fairness
(for me, for you, for us) which expresses the conflict systems model and the reciprocal
algorithms of behavior.
18. That is, in physics it is not known exactly why and how wave function collapses or
reduction occurs and how eigenstates are determined (e.g., see Hameroff & Penrose
1996: 311). The standard Copenhagen Interpretation sees collapse as occurring at
randomly measured values when the quantum system interacted with its environment,
was otherwise measured, or consciously observed; (e.g., see Stapp's 1972 well-known
article on the Copenhagen Interpretation). Penrose (1994) and Hameroff and Penrose
(1996) introduce a new physical ingredient they call objective reduction (OR), which
376 The Evolutionary Neuroethology of Paul MacLean

become guided and tuned into orchestrated OR, in which quantum systems can self-
collapse by reaching a threshold related to quantum gravity. Harth notes, in summarizing
his sketchpad model, that "the transformation from the extended activities in the
association areas and working memory to specific mental images may be likened to the
collapse of a wave function in quantum mechanics." He does not, however, imply any
quantum effect (1997: 1250).
19. Since the formula represents a reciprocal tug and pull dynamic of neural
architecture in which the deviation from equilibrium indexes behavioral tension, either
ego or empathy may be expressed as numerator or dominator for convenience sake to
keep the quotient a whole number and not a fraction (see Cory 1999: 97-100).

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 19

T O W A R D A N E U R A L NETWORK
THEORY OF THE TRIUNE B R A I N

Daniel S. Levine and Nilendu G. Jani

INTRODUCTION

From the viewpoint of the computational modeler and systems theorist, Paul
MacLean's major contribution to behavioral and cognitive neuroscience is not
so much his evolutionary perspective. In fact, his great work entails a view of
1,2,J
human nature that includes motivations other than mere survival. Rather, his
modular approach commands attention. The functional division of the brain into
a part related to habits and instinctive behavior, a part related to emotional and
social behavior, and a part related to higher cognitive and semantic processing
provides a useful basis for modeling, even if the assignment of brain areas to
these parts turns out to differ somewhat from what MacLean has exactly
4
proposed. Many neural network modelers, including the authors of this chapter,
have devoted much of their careers to trying to understand what MacLean called
5
the "man, horse, and crocodile" within us and the brain systems that subserve
communication between these three "animals." This chapter reports on these
efforts.

AN INTELLECTUAL MOVEMENT ABOUT EMOTION

Like many other scientific pioneers, MacLean anticipated an intellectual

movement not prominent until years after his major work was published.
Emotions are now in vogue, not just in psychology and neuroscience but also in
neural network theory and even in artificial intelligence. Many engineers and
computer scientists as well as biologists now realize that human and animal
emotions represent, among other things, a source of positive and negative
values. Such a value source, rather than interfering with rational decision-
6
making, actually facilitates decision-making, as Antonio Damasio showed with
384 The Evolutionary Neuroethology of Paul MacLean

his studies of patients whose valuation is blunted through damage to the

orbitofrontal cortex.
Before Damasio's book and a few others appeared, emotion often seemed a
7
"dirty word in science," regarded as inferior to reason, and indeed as a "lower
animal" heritage interfering with higher cognition. Yet MacLean is numbered in
a relatively small group of behavioral neuroscientists who forthrightly spoke of
emotion as an integral part of all decision making. Another, Walle Nauta,
anticipated Damasio's "somatic marker" hypothesis as he noted that frequently a
plan we decide on rationally does not get implemented if thinking about it
8
makes us feel sick. Still another was Karl Pribram, who did a long series of
studies relating arousal and various midbrain and limbic system functions to
9
attentional processing.
While neural networks and artificial intelligence in the early years tended
toward the primacy of rationality, several important modelers as early as the
1970s also insisted on the importance of emotional (and instinctive) processes in
any theory of biological intelligence. These included Stephen Grossberg, Harry
Klopf, Paul Werbos, and Gershom-Zvl Rosenstein.

WHAT NEURAL NETWORKS ARE AND ARE NOT

Neural networks, now a fad, exude a mystique. Yet their study is really
nothing more than the quantitative theory of how neural and cognitive systems
10
are organized. (While neural networks are used for engineering purposes as
well as biological modeling, the biologically relevant sort are essentially
indistinguishable from the large system aspect of computational neuroscience.
The distinction between those two terms is more sociological than it is
scientific.)
Many people upon hearing the term "neural network" think of a very specific
three-layer structure, variously called back propagation networks or multilayer
11
perceptrons, developed by Paul Werbos and popularized by David Rumelhart
12
and James McClelland. This is in fact the type of neural network that has had
the widest engineering applications so far because it has some intriguing
mathematical properties that enable it to solve a wide class of input-output
mapping problems. Yet this is only one of many types of neural networks in the
current literature, and not generally regarded as the type closest to the actual
architecture of the brain.
So neural networks are not a particular narrow class of structures. Yet, what
are they? No definition has gained universal agreement. The closest is probably
one developed in 1988 by a team of experts commissioned by the United States
Department of Defense:

a neural network is a system composed of many simple processing elements operating in

parallel whose function is determined by network structure, connection strengths, and the
processing performed at computing elements or nodes . . . Neural network architectures
Neural Network Theory 385

are inspired by the architecture of biological nervous systems, which use many simple
13
processing elements operating in parallel.

The specific type of structures used in neural network models depend on the
class of cognitive and behavioral functions they are trying to reproduce. For
example, it has been argued that sensory pattern categorization and motor
14
control require fundamentally different types of neural network architectures.

EARLY NEURAL NETWORK MODELS

OF EMOTION, DRIVE, AND REINFORCEMENT

Several early neural network models derived from first principles included
drive or motivational representations, particularly models of classical (Pavlo-
vian) conditioning. Grossberg, building on his own previous network models of
pattern learning, asked how a network exposed to two or more patterns can learn
both patterns without confusing them or learning a meaningless mixture of
15
them. For example, animals can learn that one stimulus predicts food
reinforcement and another stimulus predicts sexual reinforcement. Grossberg
found that this type of learning was facilitated by having nodes in the network
that represent drives such as the hunger and sex drives, in addition to the sensory
and motor representations that were included in earlier versions of his network.
He postulated these drive sources as analogous to hypothalamus or limbic
system areas. Further extensions of this network included both positive and
negative drive loci, and opponent processing of changes in affective value of
16
events.
2 17
Motivation also played a prime role in the model of Klopf, ' who for a short
time worked in the same laboratory as MacLean at Poolesville, Maryland.
Klopf regarded the seeking of pleasure and avoidance of pain as the force
driving every organism's behavior, and indeed regarded survival (or homeo-
stasis) as a subgoal of net pleasure maximization (for which he coined the term
heterostasis). This type of "hedonism," Klopf believed, also occurs at the level
of single neurons, which "try" to maximize depolarization from other neurons
and minimize hyperpolarization. The theory integrated aspects of the triune
brain, in that each of the three parts of the brain tries separately to maximize its
own positive stimulation. The reticular formation, part of the reptilian brain, is
the final arbiter of decisions, and the limbic and neocortical systems have
specific functions in implementing those decisions. As with Grossberg's work,
this theory evolved into a computational model of the time course of Pavlovian
18
conditioning.
Similar ideas for quantitative representation of emotional variables deve-
loped independently in Russia, largely in isolation from Western scientists.
There Pavlov's tradition dominated in science, and was encouraged as socially
useful by a repressive government interested in emotional control of its people.
In this framework Rosenstein developed an abstract neural network model
based, as was Klopf s, on the notion that organisms seek to optimize the level of
386 The Evolutionary Neuroethology of Paul MacLean

a certain variable. ' By analogy to economics, where such optimization

models have always been popular, Rosenstein called this variable Income. He
related Income to dopamine level, and explained schizophrenic systems in terms
of a tendency to seek Income not available from other sources.
The connections with economics are also prevalent in the work of Werbos,
whose back propagation network was motivated in part by efforts to develop
better and more brain-related predictors of economic time series than were then
11,21,22
available. The basic back propagation model was but one of a series of
network architectures Werbos developed, architectures that were designed to
maximize (positive) reinforcement. This was done through learning, and an
essential feature was to monitor which connection strengths should be changed
at any time to most efficiently increase reinforcement. His work and others' led
to principles that are known both in biology and in engineering as reinforcement
learning or adaptive critic design.

TRIUNITY IN MODELS OF COGNITIVE TASKS

The last section shows that biologically motivated neural network principles
have a longer history than generally believed. Yet another 10 to 20 years would
transpire before networks had evolved to the point of modeling anything close to
the "triune brain" at a system level. This scientific evolutionary process is still
underway.
A first example includes the model by Daniel Levine and his colleagues of
24 25
the effects of frontal lobe damage on the Wisconsin Card Sorting Test. ' On
this test, the subjects have to figure out the criteria for classifying cards based on
the experimenter saying "right" or "wrong" without saying why. At various
points the experimenter changes the classification criterion (which could be
color, shape, or number of the designs of the card faces) without warning.
Errors made by people with dorsolateral prefrontal damage on this test are
mainly of a perseverative nature; that is, they classify cards by criteria that were
formerly, but are no longer, correct.
The card-sorting model of Levine and his co-workers is not neuro-
anatomically correct but includes subnetworks conceived as analogous to the
triune brain. The network includes two layers coding features (color, shape, or
number) and card categories, considered analogous to parts of the "neomam-
malian" visual neocortex. The interactions between feature and category layers
are modulated by signals representing attentional biases toward one or another
of the three feature classes. These biases are in turn influenced by two sets of
signals, one connoting positive or negative valuation (from the experimenter),
the other connoting cognitive habit based on previous responses. Prefrontal
damage is mimicked by weakening of the influence of the "paleomammalian"
valuation signals (based on the strong connectivity between prefrontal cortex
and various limbic and hypothalamic areas). In the absence of strong effects of
negative feedback, a positive feedback loop develops between the categori-
zations, the attentional biases, and the "reptilian" habit signals. Mortimer
Neural Network Theory 387

Mishkin and his co-workers confirmed this in a study of the dissociable

influences of motor habits, mediated by the "reptilian" basal ganglia, and
26
memory of rewards, mediated by the "paleomammalian" limbic system.
The interactions among rewards, penalties, habits, and biases have been
extended to models of other prefrontal-related cognitive tasks, such as verbal
27 28 29
fluency and sequence learning and classification. ' Also, several more recent
models of the Wisconsin Card Sorting Test have incorporated more detailed
anatomy and physiology of the prefrontal cortex and its interactions with the
basal ganglia and limbic system. The most detailed of these models so far is that
30
of Oury Monchi and John Taylor, which is based on the structure of loops
between the frontal (both motor and prefrontal) cortex, basal ganglia, and
31
thalamus. Lateral inhibition between different cell populations in the basal
ganglia mediates competition between different attracting states of the network
that represent choices (in this case, categorization criteria). These choices are in
turn influenced by reward and penalty via signals to the prefrontal cortex from
the amygdala via the anterior cingulate gyrus (a part of the Papez circuit for
representing emotions). Another variant of the Monchi-Taylor network has been
utilized to model recency discrimination, and there are extensions in progress to
a model of delayed matching to sample.
Jose Contreras-Vidal and Wolfram Schultz included all three parts of the
triune brain in a model of how dopamine influences the acquisition of
32 30
conditioned responses. Their model, like that of Monchi and Taylor,
depends on interactive loops between cortex, basal ganglia, and thalamus, with
different parts of the basal ganglia (and associated areas of prefrontal cortex)
responsive to the timing of the reward and to its occurrence or nonoccurrence.

MODELING RECIPROCITY

The models discussed in the last section are steps toward unified, biolog-
ically realistic models of interactions among the three parts of MacLean's triune
brain. They are not so much the separate biological computers MacLean
5
described as they are functional modules in an overall dynamical system for
making flexible responses to a nonstationary environment. Each of the models
so far includes only parts of the overall picture. Other parts of the picture have
so far been modeled only at the macro or cognitive level, and not yet mapped in
detail to brain areas.
For example, the two authors are currently developing a neural network
model based on the social and economic theory of the reciprocal modular brain
33
propounded by Gerald Cory. Cory argued, and we agree, that current economic
theories have tended to overemphasize the self-interested side of economic
behavior. In fact, he went on, people are equally motivated by the need to help
and empathize with others, in part because social systems are based on
reciprocity and people need to give benefits to others in order to receive benefits
in return. Hence his socioeconomic model is based on a tug-of-war between the
claims of self-interest, mediated roughly by MacLean's reptilian brain, and of
388 The Evolutionary Neuroethology of Paul MacLean

empathy and social bonding, mediated by MacLean's old mammalian brain. If a

person denies either selfish or empathic claims for too long, she or he experi-
ences discomfort and attempts to reestablish some degree of balance between
the two.
We modeled this tug-of-war using a neural network in which nonlinear
dynamics represented competitive interactions between neuron populations
(represented as network nodes) each coding different criteria or feature classes,
and variable attentional biases toward one or another of these criteria. This was
part of the foundation of the Wisconsin Card Sorting model of Leven and
24
Levine. It was also studied mathematically by Grossberg and Levine in a
34
general setting with an arbitrary number of nodes. Grossberg and Levine
showed that if the attentional biases remained the same over time, the system
always reached a steady state, and the numerical variables in the steady state
represented which features were retained in short-term memory. However, we
asked, what happens if the two nodes represent "selfishness"and "empathy," and
the attentional biases between them vary over time? Is it possible to oscillate
between one or another of those criteria being more dominant, in either a
periodic or chaotic fashion? If the network does reach a steady state, under what
conditions can the steady state be one of balance between selfishness and
empathy, rather than one of them dominating the other over time?
Figures 19. land 19.2 show examples of the behavior of our network. In all
neural networks, there are variables called node activities. These activities are
abstract but if the nodes represent brain areas they correspond roughly to
electrical activity in the area. If the nodes represent psychological entities such
as concepts, percepts, or emotions, the activities correspond roughly to the
amount that the concept is actively thought about, the percept is perceived, or
the emotion is felt. The graphs represent activities of the "selfishness" and
"empathy" nodes in our network.
Both figures represent cases where the mathematical parameters representing
attentional biases toward selfishness and toward empathy are time-varying. In
Figure 19.1, there are two sets of biases, one in favor of selfishness and one in
favor of empathy. The biases between the two regimes reverse when either
variable (selfishness or empathy) gets below a fixed threshold. Periodic
oscillations are obtained between the two variables. We have also simulated the
case, not shown here, whereby the biases are changed at fixed time intervals. In
that case while there is an overall dominance of selfishness (due to the way other
network parameters were set), the activity of the empathy node becomes larger
than that of the selfishness node whenever the biases are shifted. The waves in
the two variables do not, however, repeat themselves; hence the changes
between the two variables could be described as chaotic rather than periodic. In
either case, an effective and lasting balance between selfishness and empathy
has not been achieved.
Neural Network Theory 389

Figure 19.1. Oscillatory Interaction between "Selfishness" and "Empathy" Node Activ-
ities when Biases in Network Shift at Regular Time Intervals

This type of balance between the selfishness and empathy systems was
obtained in Figure 19.2 by adding to the network a third node representing an
idealized "frontal lobe executive." As Cory suggested, the frontal lobes exert a
kind of higher-order mediating function that makes sure that neither the self-
33
interest nor the empathic claims are neglected. The influence of the frontal
mediation parameter causes biases in favor of empathy or selfishness to shift
when either variable is too low, but to shift in a gradual rather than a sudden
manner.
We add the caveat that this network is primitive compared with both the
anatomical interconnections of the brain and the interacting behaviors it seeks to
represent. None of the actual connectivity between the prefrontal cortex and
either the basal ganglia, midbrain transmitter systems, or limbic system has yet
been incorporated here.
390 The Evolutionary Neuroethology of Paul MacLean

Figure 19.2. Graph of "Selfishness" and "Empathy" Activities with Addition of Frontal
Executive" Node

Yet these simulations show that an abstract system of reciprocity between

conflicting claims might have some of the basic properties of a socioeconomic
system based on interactions of the triune brain. Our model also mimics some
properties of the prefrontal executive in mediating between claims of different
parts of the triune brain. The oscillations obtained in the network with an absent
35
or weak frontal executive reinforces the suggestion made elsewhere that the
perseverative behaviors of prefrontally damaged patients are exaggerations of
perseverative, "stuck" behavior common in humans whose frontal lobes are
physically intact (but may at times be stuck in "Park"!). Indeed, this is what
MacLean suggested much earlier with his powerful metaphor of our
disassociated three brains as "a man, a horse, and a crocodile in the same
5
room."
Neural Network Theory 391

CONCLUSIONS

One of the authors (D.S.L.) got his start in behavioral neuroscience in the late
1960s when he arrived with a mathematics background at the National Institutes
of Health. Paul MacLean, one of his mentors, challenged him to develop a
mathematics of emotions, where "positives" and "negatives" prevailed but no
"zero." On the abstract level, this has already been accomplished by the
dynamical systems approach to neural networks. What has not been done yet is
the development of a good model for specific emotions (anger, fear, joy, and so
forth) and their interrelationship. Models have not yet captured the intricate
connections between the limbic system, hypothalamus, and what Pribram called
36
the "four Fs": feeding, fleeing, fighting, and sex.
Yet as computational modeling becomes more and more a part of neuro-
physiology and neuropsychology, the current methods and architectures are
likely to reach that point in the next several years. In this process of theoretical
understanding, the triune brain, as a source both of functional constructs and of
metaphors, will remain useful.
Some of the details of MacLean's earlier formulation of triune concepts have
been modified by the development of science. MacLean incorporates much of
this modification in his updated and encyclopedic The Triune Brain in Evolution
published in 1990. For example, the mapping between specific brain areas and
roles is fully acknowledged to be more complex than the rather neat panellation
3 7
of his earlier articles (e.g., see Pribram for other ideas about the limbic
38
system, and Houk, Davis & Beiser for newer hypothesis about the basal
ganglia). Also, the idea from these earlier articles about three separate biological
computers with different information processing styles has gradually yielded to
a more integrated dynamical systems approach in which all three brains play
constructive roles. The paranoid streak that MacLean discussed and related to
39,40
limbic system and R-complex information-processing actually has a
neocortical component as well, because paranoia directed at a particular group
requires the neocortical facility of categorization. Similarly, information pro-
cessing of a caring and cooperative nature requires parts of all three brains.
Yet it is not in the minutiae but in the overarching concepts that triunity
remains scientifically useful. MacLean was one of several scientists promoting
the ideas that emotion is coequal with reason in decision-making and that
instinct or habit is dissociable from emotion. Both of these are seminal ideas in
behavioral neuroscience, and modern computational theories increasingly
assume them as basic truths.
The triune brain can also be a source of valuable metaphors for explaining
processes in a number of disciplines. Sam Leven reviews the literature about
different processes in a wide range of social science areas including organiza-
tional management, decision theory, developmental psychology and many
41
others. He finds analogues of the instinctive/emotional/rational "triunity" in all
42
of them. For example, he cites work in managerial psychology describing three
styles of people at work: implementing (an "instinctive" process); pathfinding
(an "emotional" process); and problem solving (a "rational" process). Leven
392 The Evolutionary Neuroethology of Paul MacLean

applied this same set of distinctions to different theories of learned helplessness,

one relying mainly on physiological responses, one on feelings, and one on
cognitions, and integrated all three theories into a qualitative neurochemical
43
network model. Are all these processes subcases of a broad principle of brain
organization? It has been suggested elsewhere that the three styles Leven
discusses might all be attracting states of the same mathematical dynamical
44
system in our brains. Years of exciting work lie ahead. But it is clear that theo-
retical neuropsychology as a partner with experiment is here to stay, and that the
triune brain remains one of the key concepts in the elaboration of this
partnership.

NOTES

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Associates, 1994.
3. Maslow AH: Toward a Psychology of Being. NY: Van Nostrand, 1968.
4. MacLean PD: The Triune Brain in Evolution: Role in Paleocerebral Functions.
NY: Plenum, 1990.
5. MacLean PD: New findings relevant to the evolution of psychosexual functions of
the brain. Journal of Nervous and Mental Disease, 1962; 135, 289-301. (Quotation is on
p. 289.)
6. Damasio A: Descartes' Error: Emotion, Reason, and the Human Brain. NY:
Grosset/Putnam, 1994.
7. Levine DS, Leven SJ (Eds.): Motivation, Emotion, and Goal Direction in Neural
Networks. Hillsdale, NJ: Lawrence Erlbaum Associates, 1992, p. vii.
8. Nauta WJH: Personal communication, March 1971.
9. Pribram KH, McGuinness D: Arousal, activation, and effort in the control of
attention. Psychological Review, 1975; 82, 116-149.
10. Levine DS: Introduction to Neural and Cognitive Modeling. Mahwah, NJ: Law-
rence Erlbaum Associates, 2000.
11. Werbos PJ: Beyond regression: New tools for prediction and analysis in the
behavioral sciences. Unpublished doctoral dissertation, Harvard University, 1974.
Reprinted as The Roots of Backpropagation: From Ordered Derivatives to Neural
Networks and Political Forecasting. NY: Wiley, 1993.
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rations in the Microstructure of Cognition. Vol 1 and 2, Cambridge, MA: MIT Press,
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14. Gaudiano P, Grossberg S: Vector associative maps: Unsupervised real time error-
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16. Grossberg S, Schmajuk NA: Neural dynamics of attentionally-modulated Pavlov-

ian conditioning: conditioned reinforcement, inhibition, and opponent processing.
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Cambridge Research Laboratories Research Report AFCRL-72-0164, Bedford, MA,
1972.
18. Klopf AH: A neuronal model of classical conditioning. Psychobiology, 1988; 16,
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25. Levine DS, Prueitt PS: Modeling some effects of frontal lobe damage: novelty
and perseveration. Neural Networks, 1989; 2, 103-116.
26. Mishkin M, Malamut B, Bachevalier, J: Memories and habits: two interacting
systems. In G Lynch, JL McGaugh, & NM Weinberger (Eds.): Neurobiology of Learning
and Memory, (pp. 65-77). New York, London: Guilford, 1984.
27. Parks RW, Levine DS: Neural network modeling of Wisconsin Card Sorting and
verbal fluency tests: Applications with frontal lobe-damaged and Alzheimer's disease
patients. In RW Parks, DS Levine & DL Long (Eds.): Fundamentals of Neural Network
Modeling: Neuropsychology and Cognitive Neuroscience (pp. 357-380). Cambridge,
MA: MIT Press, 1998.
28. Bapi RS, Levine DS: Modeling the role of the frontal lobes in performing
sequential tasks. I. Basic structure and primacy effects. Neural Networks, 1994; 7, 1167-
1180.
29. Bapi RS, Levine, DS: Modeling the role of the frontal lobes in sequential task
performance. II. Classification of sequences. Neural Network World, 1997; 1/97, 3-28.
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for various tasks. Information Sciences Journal, 1998; 113, 221-243.
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segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience,
1986; 9 , 3 5 7 - 3 8 1 .
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33. Cory GA Jr: The Reciprocal Modular Brain in Economics and Politics: Shaping
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34. Grossberg S, Levine DS: Some developmental and attentional biases in the
contrast enhancement and short-term memory of recurrent neural networks. Journal of
Theoretical Biology, 1975; 53, 341-380.
35. Levine DS: Don't just stand there, optimize something! In DS Levine & W
Elsberry (Eds.): Optimality in Biological and Artificial Networks? (pp. 3-18). Mahwah,
NJ: Lawrence Erlbaum Associates, 1997.
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ton, DC: American Physiological Society, 1960.
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(Eds.), Approaches to Emotion (pp. 13-38). Hillsdale, NJ: Lawrence Erlbaum Associates,
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38. Houk J C , Davis JL, Beiser DG (Eds.): Models of Information Processing in the
Basal Ganglia. Cambridge, MA: MIT Press, 1995.
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sity of Texas at Arlington, 1987.
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 20

CONCLUSION:
CONVERGENCES A N D FRONTIERS

Gerald A. Cory, Jr. and Russell Gardner\ Jr.

As shown in the varied articles that comprise this volume, MacLean's influence
spans many disciplines. Although this single volume cannot capture the full
range of MacLean's influence, it does delineate some major thrusts that draw
substantially upon his contributions. In this chapter we attempt to sum up the
main features of the various chapters and identify some convergences and
frontiers deriving from the emerging literature, which spans multiple disciplines
and perspectives.

CONVERGENCES

Pribram's chapter assisted us in identifying some of the divergent aspects of

neuroscience that have shaped directions in research for the decades since the
1950s. As Pribram also noted some of these divergent paths have now tended to
move toward convergence. Three major thrusts of divergence can be identified.
They are the issues or perspectives of (1) reduction vs. integration; (2) evolu-
tionary phylogenetic vs. comparative structural functional; and (3) cognitive and
objective vs. emotions and subjectivity. The third chapter by Cory illustrated
how legitimate differences in scientific perspective can become distorted by
academic isolation, partisanship, and careless scholarship. Although the pursuit
of these divergent paths in specific research programs is legitimate, even neces-
sary, for sharp focus in many research programs, the emerging convergences are
equally necessary and productive.
Our leading sociobiologist, Edward O. Wilson of Harvard, catches the
essence of the reductive/integrative process when he writes that much of the
history of biological science may be seen dynamically as a tension between unit
and aggregate, reduction and holism. Considering an equilibrium in this tension
as neither desirable nor possible, he concludes that: "As large patterns emerge,
396 The Evolutionary Neuroethology of Paul MacLean

ambitious hard-science reductionists set out to dissolve them with noncon-

forming new data. Conversely, whenever empirical researchers discover enough
new nonconforming phenomena to create chaos, synthesizers move in to restore
order. In tandem the two kinds of endeavors nudge the discipline forward"
(Wilson 1993: 243).
Reduction and phylogenetic perspectives are not mutually exclusive. The
chapter by Smith on the implications of the relatively new discipline of
molecular biology for understanding the evolution of brains and social
communication made this clear. Nothing could be more reductionist from the
larger organism or human perspective than the study of molecules that make up
the trillions of cells of our bodies. The very process of moving up the scale of
integration from molecules to the human organism as a whole illustrates
dramatically the interdependence of the reductionist/integrationist perspectives
in science. Nowhere is the convergence of the two perspectives more conspi-
cuous or more necessary to the understanding of science. The discovery of HOX
genes common to species from worms to the highest vertebrates graphically
makes the case for homology, defined as phylogenetic relatedness or similarity
based on informational continuity. And homology only makes sense in an
evolutionary perspective. The remarkable conservation of homologous structure
and function from the molecules and body plans of early life certainly converges
with the evolutionary perspective of MacLean, whose triune brain concept
emphasizes the conservation of ancient mechanisms from which subsequent
variation and development proceed. A standard comparative approach to
anatomical structure and function must converge to a fully evolutionary
perspective for an adequate explanation of such research-revealed phenomena.
As Smith notes, "the hallmark of Paul MacLean's neuroscience is its evolu-
tionary perspective" as well as its emphasis on conservation of ancient
protocols.
In the chapter by Greenberg we saw the validation of the position by
MacLean (1990) that research should be continued to clear up the question of
whether the basal ganglia are limited to motor circuitry as traditionally held or
whether they also contribute to species-typical behavior patterns and have a role
in higher cognitive processes. This was listed as a point of questionable specul-
ation on MacLean's part in the Science review of October 1990. Greenberg
reported on the extensive new findings that show these basic forebrain nuclei to
be involved not only in many species-typical behaviors, but also in the
sequencing of complex cognitive responses up to and including language.
Cognitive neuroscientist and linguist Philip Lieberman, in his recent Human
Language and Our Reptilian Brain (2000), explores in detail the extensive role
of these early forebrain nuclei in the evolution and production of language as
well as the sequencing of higher level cognitive behavioral repertoires.
The chapters in Part III illustrated the well-documented influence of
MacLean's evolutionary thought on what has in recent years come to be called
evolutionary psychiatry. Gardner discussed how MacLean's focus on social
behaviors stemming from adaptations originating in deep time, supported by
data from the genome project as well as other genetic and brain research,
Convergences and Frontiers 397

combined to respond to psychiatry's need to connect brain actions with normal

human communicative behavior. Gardner reported that, based on these new
findings and data, during its Spring 2000 meeting, the research committee of the
Group for the Advancement of Psychiatry (GAP), a specialty think-tank, issued
a written recommendation that psychiatry's basic science should be designated
sociophysiology or the social brain. The utility of the social brain concept was
further supported by Price, Sloman, and Wilson, who related the pathological
syndromes of depression and mania to phylogenetic roots in the triune brain
structure. The convergences from the various perspectives are notable and the
symptomatology becomes explicable when viewed from the evolutionary
perspective. Price commented on the clarifying effect of triune brain theory
upon ideas of depression and mania. From the phylogenetic perspective,
depression can be seen as neocortical malfunction or interference with de-
escalation and escalation adaptive social strategies wired into our earlier
reptilian and mammalian brain structures. Sloman described an involuntary
defeat strategy (IDS) as an adaptive de-escalation of agonistic behavior of
probable reptilian origin which made possible social hierarchies the attachment
aspects of which find themselves in the later evolved mechanisms of the early
mammalian accretions. An ineffective IDS is described as leading to psycho-
pathological symptoms. In his discussion of primarily manic pathology, Wilson
perceived that the converging evidence on brain research confirms that the brain
evolved quite in keeping with MacLean's synthesis. Brain evolution was seen to
be characterized by phylogenetic accretion of successively higher and more
pluralistic mechanisms for executive action, without, however, obviating the
capacity of the earlier reptilian and mammalian mechanisms to override
executive control in times of urgency and/or pathology.
The varied chapters in Part IV illustrated further the converging insights
from MacLean's evolutionary formulations. Harris argued that the all-important
human highly generalized capacity for empathy relies on integration of
phylogenetically older and newer structures of the brain. He saw the deficits of
the perplexing syndrome of autism as resulting from the failure of this
integration in the ontogenetic developmental processes. Empathy, the capacity
to enter into the emotional states of others, depends upon cognitive represent-
ation and integration of our earlier self-maintaining reptilian mechanisms and
the later emerging kinship-bonding mechanism of our paleomammalian
structures. Harris cited the new observations of empathic behavior in primate
species, especially in macaque monkeys and bonobo chimpanzees. The chapter
by Pontius, on the other hand, focused on a very specific syndrome which she
has identified as the Limbic Psychotic Trigger Reaction (LPTR). In a very
detailed and thorough analysis, Pontius described LPTR as a disconnect reaction
between the higher control centers of the brain and the emotional limbic centers,
which results in the otherwise inexplicable cases of motiveless homicide. As a
longtime forensic psychiatrist troubled by the etiology of this unusual syndrome,
Pontius found that MacLean's triune brain concept provided a convergent
explanatory framework and perspective for this otherwise baffling syndrome.
398 The Evolutionary Neuroethology of Paul MacLean

Weisfeld returned to a higher level of integration in his examination of the

neural and functional aspects of pride and shame. At the outset he reminded us
that the study of comparative neuroanatomy makes clear that motivated
behaviors evolved earlier than complex cognitive capacities. As MacLean
emphasized repeatedly in his writings: The brain stem, basal ganglia, and limbic
system antedated the expansion of the neocortex. Weisfeld followed MacLean's
lead in his emphasis upon the primacy of emotions and the conservation of
primitive brain structures, reminding us in phylogenetic terms that even
primitive organisms needed to fulfill all the functions necessary for survival so
that any capacities that evolved later had to be elaborations of the earlier
mechanisms. Although care must be taken in overgeneralizing this principle,
especially in passing across the various phyla, converging evidence from
evolutionary genetics in the form of ancient neuropeptides, proteins, and HOX
genes supports this principle of conservation.
The chapter by Mirsky and Duncan proceeded from an evolutionary
perspective, drawing upon the concept of the triune brain to build a model of the
organization and development of attentional functions in the human brain. The
basic neural foundation for attention is the brain stem system that has existed for
millions of years and is still present and functioning in the brains of modern
reptiles and in earlier vertebrates. Mirsky and Duncan pointed out convergence
of MacLean's reptilian brain with the centrencephalon concept of neuroanato-
mists Penfield and Jasper, and also with Lindsley's concept of the ascending
reticular activation system. Added to these significant convergences from
varying research perspectives of the foundational vertebrate attentional system,
are the subsequent limbic and neocortical components of the paleo- and
neomammalian brain structures. The capacity to shift focus from one aspect of
the environment to another in a flexible, adaptive manner is dependent upon the
integrity of the prefrontal cortex, including the anterior cingulate gyrus, and may
be a unique function of the neomammalian brain. Mirsky and Duncan concluded
that while ordinarily the three brain regions operate together harmoniously,
damage or dysfunction in any one of these brain regions, brain stem, limbic, and
neocortical, can lead to circumscribed or specific deficits in a particular attention
function.
The chapters in Part V represented a change in focus. Brody presented a
provocative attempt to argue for convergences in physics and triune theory.
Drawing principally upon the work of physicist Stuart Kaufftnan, Brody saw
evolution as constrained by the fluctuations of the triarchic pattern of stasis,
chaos, and the integrative, phase transition. Brody argued that these concepts
from statistical physics suggested a platform in biology for Darwinian natural
selection as well as a basis in neural architecture for the pursuit of binary and
tertiary models such as MacLean's triune brain concept. He presented the
implications for theory as well as diagnosis and therapy of such a convergent
perspective.
The chapter by Itzkoff, proceeding from an evolutionary perspective, argued
for a reversal of the usual emphasis on the precedence of primitive mechanisms
in discussions of evolved brain structure. Building upon the work of Jerison and
Convergences and Frontiers 399

others, Itzkoff saw the neo- or isocortex as leading the Darwinian evolutionary
selection path from early vertebrate neural architecture to the brain of Homo
sapiens. Although we end up with a largely chicken-or-egg question in our
current state of knowledge, Itzkoff s chapter reminds us that in evolution, like
adaptive behavior, feedback and general recursiveness in interaction among the
many variables prohibits a simplistic linear account of brain evolution. For
example, Gilsofi and Mora (2000) recently argued uniquely for the previously
neglected role of temperature regulation in the progressive encephalization that
characterized mammalian evolution. Once again we are reminded that science
progresses in a seemingly dialectical manner by successive divergences and
convergences, by successive reductions and integrations.
The chapter by Masters proceeded from the perspective of evolutionary
neuroscience to examine the effects of environmental pollution upon abnormal
social behavior. Masters presented provocative and disturbing evidence that the
introduction of heavy metals (e.g., lead, cadmium, aluminum, and others) into
the environment through industry and technology has produced defects in the
functioning of our evolved neural architecture contributing to violent behavior
and learning deficits. These heavy elements were not present at modern levels in
our environment of evolutionary adaptation and therefore our nervous system
did not evolve adequate protection against them. When uptaken into the brain
and nervous system, these elements interfere with the normal neurological
functioning and information processing. Social science has previously attempted
to explain the resulting deviancy by purely social factors. Masters argued that a
complete understanding—even prevention and mitigation—of such deviant
behaviors must include a full grasp of the new findings proceeding from
evolutionary neuroscience. Based upon a clearly demonstrated need for such
cross-disciplinary exchange, Masters concluded with an appeal for an end to
academic insularity and convergence to a unified scientific approach to confront
the challenges of our industrial and technological civilization.
The chapters in Part VI carried forward the challenge by Masters for a
convergence with the social sciences necessitated by the advances in
evolutionary biology and neuroscience. Proceeding from a different level of
integration toward the same objective of convergence, they comprised a
bridging effort between the concepts of evolutionary neuroethology and those of
social psychology and socio-economic theory. Peterson drew upon MacLean's
thought to discuss the human tendency to give created beliefs superordinate
status. This tendency to reification becomes understandable when seen as rooted
in the species-typical ritualizing behaviors of the neostriatum, MacLean's
protoreptilian brain. Peterson argued that although reification and the related
concept of hegemony have stabilizing effects on society, they also contributed to
the sanctifying of domination and social inequality.
Bailey presented his model of paleopsychology, which builds upon and
extends MacLean's research and concepts, to develop new clinical insights as
well as a bridge from individual into social psychology. Bailey saw the human
brain as capable of upshifting to control by the higher and more recently evolved
neocortical centers as well as downshifting to control by the more primitive
400 The Evolutionary Neuroethology of Paul MacLean

paleomammalian and reptilian centers. From his research among students,

Bailey concluded that the rewards of primal functioning (i.e., eating, drinking,
sex, etc.); were (with some notable exceptions) inherently more pleasurable and
satisfying than the higher cortical ones of planning and studying. Under
conditions of stress (or damage, dysfunction) and given the right environmental
cues, individual behavior might downshift to more ancient reptilian patterns of
behavior that are inappropriate, undesirable, and even destructive in modern
social situations. In illustration of this downshifting capacity Bailey analyzed
insightfully the behaviors of serial killer Ted Bundy, and two normal youths
who precipitated the Columbine school massacres.
Cory's chapter was complementary to Bailey's in certain aspects. Whereas
Bailey emphasized the downshifting (as well as upshifting) between neocortical
control and evolutionarily older brain systems, Cory—remaining essentially at
the neocortical level—saw the dynamic of social life based in the largely
conflictual dynamic between the older self-preservational programming of the
reptilian or early vertebrate brain tissues and the later evolved affectional
mechanisms of the early mammalian brain regions as they were represented in
the neocortex as ego and empathy, respectively. In Bailey's terms, then, Cory
emphasized the upshifted neocortical spectrum of representation.
Moving further into socio-economic theory and drawing upon a wide range
of multidisciplinary research, Cory derived reciprocal algorithms of behavior
from this neocortically represented ego/empathy conflictual dynamic to account
for the ubiquitous reciprocity of behavior found in all human societies. These
algorithms were offered as the evolved functional complement in neural
architecture to Hamilton's cost/benefit equation of inclusive fitness and can be
expressed in essentially the same cost/benefit terms. This linkage of Hamilton's
rule with the evolved algorithms of neural architecture establishes a needed
bridging linkage between the disciplines of evolutionary psychology and
evolutionary neuroscience. The reciprocal algorithms were further expressed as
mathematical operations comparable to the dynamics of social stratification as
well as the laws of supply and demand of economic theory. The tying of
reciprocal algorithms of evolved neural architecture to the fundamental shaping
dynamics of human social and economic exchange activities indicates a possible
path for theoretical unification of evolutionary neuroscience and evolutionary
psychology with the social sciences. Additionally, the perspectives of Bailey and
Cory may well converge to provide a useful multidimensional model of indivi-
dual and social behavior applicable to numerous areas of social psychology and
social theory.
Further supporting this thrust into social psychology and social theory, the
chapter by Levine and Jani reported their ongoing efforts to model a neural
network architecture representing the triune dynamic. Preliminary results
showed that the model developed had features that could match the socio-
economic exchange dynamic postulated by Cory.
Convergences and Frontiers 401

FRONTIERS

The foregoing paragraphs have shown the various convergences from several
disciplinary perspectives, some of which also indicate frontiers for future
research. In this remaining section we will point out further the frontiers of
research and integration that challenge us from the evolutionary perspective.
The frontiers of research extend in both directions from evolutionary
neuroscience—up the scale of integration and down—in both reductive and
holistic directions. The emergent disciplines of biophysics and molecular bio-
logy are moving us in a reductive direction that is throwing almost dazzling new
light on the nature of life itself and the evolutionary process. New detail and
new concepts will emerge as the linkages between ancient DNA, RNA,
neuropeptide and protein configurations, and body plans merge with our still-
developing grasp of brain evolution.
In the opposite direction, moving up the scale of integration, new research
and developments are taking us up the standard hierarchy of academic
disciplines, giving us new insights into our psychological, even social and
economic functioning. For instance, the pleasure-pain principle has been a
mainstay of psychoanalytical as well as behavioral psychology since Freud's
popularization of it in his writings. This was complemented more recently by the
agonic/hedonic systems structure so effectively presented and developed by
Michael R. A. Chance and others (see Chance, 1988, 1984; also Montagner et al.
1970; Hold 1976; Pearce and Newton 1969). Both perspectives have led to
useful insights and interpretations. MacLean's formulation further provides the
foundation in neuroscience for the emergence of another perspective on the
structure of behavior—the dynamic interplay of self-preservation and affectional
circuitry, neocortically represented in the concepts of ego and empathy as set out
by Cory (1999; also this volume). Neither perspective is exclusive of the others
but each allows insightful and useful discriminations and interpretations that
vary from their particular viewpoints. The evolutionary perspective based on
MacLean's triarchic concept presents a frontier for research that has yet to be
fully explored in its implications for social theory.
Also at the immediate frontier of research is the necessity to integrate with
evolutionary neuroscience the findings of the research programs progressing
under the general academic rubric of evolutionary psychology. In their article
"The Seven Sins of Evolutionary Psychology" Panksepp and Pankepp (2000)
have detailed convincingly the case for integration. As noted in the introductory
chapter, current mainstream evolutionary psychology fails to even acknowledge
the seminal early work of evolutionary neuroscience. Cory's proposed linkage
of Hamilton's rule and the reciprocal algorithms of our evolved neural architec-
ture may represent a helpful step in that direction. We should correct this
isolation first in such closely related fields so that we are avoiding needless
duplication of effort—reinvention of the wheel. In our departmented university
system of disciplines, such isolation persists in many areas of modern science.
A full integration of evolutionary neuroscience with evolutionary psychology is
in the interest of good science and will avoid the repetition of awkward
402 The Evolutionary Neuroethology of Paul MacLean

omissions and interpretations such as noted above and as seen so conspicuously

in Pinker's unfortunate, and likely inadvertent, misrepresentation of MacLean's
position (Pinker 1997: 370, 580).
We are not the first to make this call for the breakdown of isolation and the
improvement of communication among the scientific disciplines. Numerous
scholars have made this appeal. Among them, biologist Lynn Margulis made an
eloquent appeal some years ago (1997, 1998). And E. O. Wilson has issued his
call for consilience—the unification of the natural with the social sciences
(1998). Wilson, primarily an entomologist and population biologist, neverthe-
less recognizes that neuroscience is the key to consilience. Responding to the
call for consilience, Paul Lawrence and Nitin Nohria (2002) of the Harvard
Business School, proceeding from a business management perspective, have
presented a welcome and thought-provoking effort at linking evolved brain
structure with the dynamics of management.
The evolutionary perspective promoted by MacLean in neuroscience, and as
argued for in this volume, is increasingly being recognized as a necessary
perspective (Panksepp 1998; Damasio 1999; Lieberman 2000; Cory 1999, 2000;
Gilsofi & Mora 2000). We hope that the convergences indicated in the varied
chapters of this volume will contribute to the achievement of this worthy
challenge that confronts the scientific community in this new millennium.

REFERENCES

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Chance, Michael R. A. (Ed.). 1988. Social Fabrics of the Mind. Hillsdale, NJ: Lawrence
Erlbaum Associates.
Cory, Gerald A., Jr. 1999. The Reciprocal Modular Brain in Economics and Politics.
NY: Kluwer Academic/Plenum Publishers.
Cory, Gerald A., Jr. 2000. Toward Consilience: The Bioneurological Basis of Behavior,
Thought, Experience, and Language. NY: Kluwer Academic/Plenum Publishers.
Damasio, A. R. 1999. The Feeling of What Happens. NY: Harcourt Brace.
Gilsofi, Carl V. and Francisco Mora. 2000. The Hot Brain: Survival, Temperature, and
the Human Body. Cambridge, MA: The MIT Press.
Hold, B.C.L. 1976. "Attention structure and rank specific behaviour in pre-school
children." In M.R.A. Chance and R.R. Larsen (eds.) The Social Structure of Atten-
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Lawrence, Paul R. and Nohria, Nitin. 2002. Driven: How Human Nature Shapes Our
Choices. San Francisco: Jossey-Bass.
Lieberman, Philip. 2000. Human Language and Our Reptilian Brain. Cambridge, MA:
Harvard University Press.
Margulis, Lynn. 1998. Symbiotic Planet: A New Look at Evolution. NY: Basic Books.
Margulis, Lynn and Sagan, Dorion. 1997. Slanted Truths: Essays on Gaia, Symbiosis and
Evolution. NY: Copernicus Books.
Convergences and Frontiers 403

Montagner. H.; Henry, J.; Lombardst, ML; Restoin, A.; Benedini, M.; Godard, F.; Boillot,
F., Pretot, M.; Bolzoni, D.; Burnod, J.; & Nicolas, R. 1970. "Behavioral: Profile and
Corticosteriod Excretion Rhythms in Young Children from 1-6 years." In V.
Reynolds and N.G. Burton-Jones (eds.). Human Behavior and Adaptation. London:
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Panksepp, Jaak. 1998. Affective Neuroscience. NY: Oxford University Press.
Panksepp, Jaak and Jules B. Panksepp. 2000. "The Seven Sins of Evolutionary
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Pearce. J. and S. Newton. 1969 The Conditions of Human Growth. NY: Citadel.
Pinker, Steven. 1997. How the Mind Works. NY: Norton.
Wilson, Edward O. 1998 Consilience: The Unity of Knowledge. NY: Alfred A. Knopf.
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 NAME INDEX

Abbott, D., 144, 148 Anthony, B., 227

Abbott, J., 81 Antonides, G., 378
Abell, F., 164 Aosaki, T., 77
Abrador, S., 191 Aparicio, M, 379, 381
Adamec, R., 185, 188 Apicella, P., 80
Ackerman, R., 20, 68, 75-76 Arbib, M., 301-302, 312
Ackermann, H., 25 Ariens Kappers, C, 35, 44
Adelman, G., 394 Arieti, S., 314, 342
Adolphs, R., 162, 164-165 Aristotle, 135
Aerts, J., 80 Arnold, M. B., 8
Aggleton, J., 207, 211-212, 376 Arnold, S., 188, 228
Ahearn, M., 227 Arnold, U., 76, 168, 171, 187, 188
Ahern, S., 331,340 Arthur, W., 17-18,24
Ahlberg, P., 274 Aschengau, A., 281, 293
Akert, K., 214 Aschner, M., 276-277, 283, 293
Alberts, S., 125, 132 Ashbumer, J., 164
Aldridge, J., 13,24 Assheuer, J., 302, 314
Alexander, G., 393 Atkinson, L., 122, 132
Alexander, M., 76 Austin, J., 74
Alexander, R., 293, 309, 312, 360, 376 Avoli, N., 228
Allan, S., 124-125, 131 Awouters, F., 149
Allen, C , 377 Axelrod, R., 328, 343, 360, 376
Allen, D., 164 Aynesworth, H., 342
Allman, J., 254, 256
Altman, J., 20, 24 Baars, B., 351-352, 374, 376, 380
Altmann, J., 125, 132 Bachevalier, J., 166, 352, 376, 393
Alway, D., 15, 25 Bachus, S., 75
Andermann, F., 188 Bacon, A., 161, 164
Anderson, C., 56, 74 Bagshaw, M., 4-5, 7-8
Anderson, G., 74 Bailey, A., 280, 293,
Anderson, P., 256 Bailey, K., xxxv, 100, 104, 148, 173,
Anderson, S., 206, 211 317, 340,399
Andreasen, N., 80 Bailey, P., 4
Andrews, C, 213 Bakay Pragay, E., 226, 228
Anisman, H., 75 Baker, R., 190
Antelman, S., 54, 74, 313 Baker, S., 165
406 Name Index

Bakker, C , 104 Bernhard, J., 332, 340

Ball, P., 237, 255 Berridge, K., 14, 24-25, 332, 343
Baltimore, D., 88, 92, 103 Bianchi, L., 200, 207,211
Bandler, R., 80 Bihrle, S., 190
Bandura, A., 337, 340 Birtchnell, J., 115-117
Bapi, R., 393 Blanc, G., 78, 81
Barash, D., 144, 148 Blanchard, D., 73, 75
Barbeau, A., 72, 74 Blaxter, J., 274
Bard, P., 4 Blessing, W., 18-19, 24
Bargmann, C , 44 Bloom, K , 234, 255
Barkley, R., 256 Boag, T., 314
Barkow, J., 143, 148, 196, 211, 256, Boden, M , 75
361, 376 Boehm, C., 294
Barlow, R. 403 Bohannan, P., 293-294
Baron-Cohen, S. 100, 105 Bohm, D., 103
Barrett, P., 44 Boillot, F., 403
Barrette, J., 148 Bolwig, T., 188, 191
Bartelmez, G., 104 Bolzoni, D., 403
Barto, A., 393 Bonadonna, F., 26
Bass, E., 25 Bone, Q , 274
Bateman, A., 256 Bonin, G., 4
Bateson, G., 122, 127, 131 Bonner, H., 26
Bateson, P., 75, 379 Booth, A, 150, 198, 213
Batson, C., 375-376 Borner, H., 79
Bauman, M., 161-162, 164 Bosch, A., 75
Baxter, L., 64, 70-71, 74-75 Boslough, J., 328-329, 340
Bayandurovi, V., 313 Bottjer, D., 63, 69, 78
Bayer, S., 20, 24 Bouchard, T., 256-257
Bazan, L., 323, 328, 335, 340 Boucher, J., 377
Beasley, L., 26 Bowers, W., 49, 69, 75
Beatty, J., 302-303, 305, 312, Bowlby, J., 373, 376
Beavin, J., 116 Bowles, S., 360, 376
Bechara, A., 162, 164, 206,211 Bownds, D., 95, 104
Beck, A., 116, 143, 148 Bozarth, M , 49, 81
Beck, L., 228 Bradshaw, J., 56, 75, 81
Beeman, M., 376 Brady, J., 135, 148
Beijer, A., 78 Brammer, G., 132, 150-151
Beiser, D., 48, 75, 391, 394 Bransome, E., 228
Belew, R., 257 Brauth, S., 63, 75
Bellairs, A., 64, 75 Bridges, R., 26
Belluzzi, J., 307, 314 Brizendine, E., 294
Benecke, R., 14, 24 Broca, P., 4, 9, 88, 133, 135-136, 148,
Benedini, M., 403 168, 188
Bennett, J., 116 Brody, E., 200, 211
B e n n e t t J . , 304, 312 Brody, J., xxxiv, 231, 256, 398
Benson, D., 200, 204, 210, 214 Broekkamp, C., 307, 312
Benton, A., 210, 213 Bronowski, J., 256
Berg, J., 276-277, 295 Brooks, D., 79
Berger, P., 300, 311-312 Brooks, V., 149
Berger, T., 53, 63, 81 Brothers, L., 197-198, 212, 352,
Bergson, H., 309 376
Name Index 407

Brown, J., 18, 24 Chance, M., 44, 149, 212, 401-402

Brown, L., 52-53, 58, 75 Charney, D., 138, 149
Brown, M., 293 Chen, T., 77
Brown, P., 75 Chiarello, C , 376
Brown, R., 380 Chio, C , 141, 149
Brown, S., 133, 148 Chomsky, N., 92
Brownell, FL, 350, 376 Chrzanowski, G., 314, 342
Bruhn, P., 79 Churchland, P., 373, 376
Brunswick, N., 165 Cierpial, M., 80
Bryce-Smith, D., 277, 279, 294 Clark, E., 50, 64, 70, 75-76
Buchwald, N., 303, 312 Clark, J., 300, 312
Buck, R., 328, 337, 339, 340 Clark, R., 304,312
Bucy, P., 5, 7, 133, 148, 150 Cleckley, H., 335, 340, 391
Bull, N., 5, 7 Cleeremans, A., 80
Bundy, Ted, 328 Cleland, C , 335, 341
Bunney, B., 149 Clinton, Bill, 127
Burghardt, G., 15, 25, 78 Clivelli, O., 44
Burnod, J., 402 Clutton-Brock, T., 16, 25
Burns, D., 323, 328, 335, 340 Coburn, T., 277, 294
Burr, D., 257 Coe, K., 330, 340
Burton-Jones, N., 403 Cohadon, F, 210, 213
Bushnell, W., 132 Cohadon, S., 210, 213
Buss, A., 127, 131, 256-257, 367, 376 Cohen, A., 293
Butler, A., 12, 16, 20, 25, 46, 75, 116 Cohen, D., 249, 257, 281
Butter, C., 199,211 Cole, S., 131
Buu, N., 74 Collins, P., 306,313
Connolly, C , 78
Cabib, S., 75 Contreras-Vidal, J., 387, 393
Caggiula, A., 54, 74 Cook, E., 283, 294
Cajal, Ramon y, 88, 97, 135, 148-149, Cools, A., 59, 75, 303,312
275 Cooper, J., 76
Callaerts, P., 44 Cooper, W., 55, 76
Callahan, P., 317 Coopersmith, R., 26
Calvin, W., 96, 104 Coplan, M., 279, 283-284, 295
Cameron, ML, 294 Corbin, M , 75
Campbell, C , 20, 25, 372, 376 Cork, L., 79
Campbell, D., 73, 294, 314 Cornford, F., 116
Canales, J., 55, 75 Corning, P., 360, 376
Canfield, D., 313 Corrado, R., 190
Cannon, W., 4, 211 Cortez, D., 257
Cardinaud, B., 151 Cory, G., xxxii, 9, 22, 25, 102, 105,
Carpenter, M , 135, 149, 303, 312 337 340, 345, 377, 387, 389, 393,
Carr, G., 378 395, 400-402
Capranica, R., 77 Cosmides, L., 256, 317, 341, 318, 332,
Carruthers, P., 377 338, 3 4 0 , 3 4 3 , 3 6 1 , 3 7 3 , 3 7 6
Carter, C , 16,25, 2 5 1 , 3 5 3 , 3 7 6 Cote, L., 302, 312
Cassirer, E., 274 Cotterill, R., 52, 62-63, 76
Casti, J., 255 Courtlandt, C , 296
Castro, S., 228 Cowan, W., 303, 312, 353, 377
Chachko, R., 56, 75 Cox, N., 294
Chan, T., 131 Coyle, J., 81
408 Name Index

Coyne, J., 116 Degueldre, C , 80

Crawford, S., 255, 320, 322, 331-332, Delgado-Escueta, A., 191
341,361,377 Delfiore, G., 80
Crews, D., 69, 76-78, 277, 294, 373, DeLong, M , 393
377 DelRosso, M , 283, 294
Crick, F., 352, 377, 374 Demski, L., 67, 81
Critchley, M., 205,212 Dennett, D., 350, 353, 377
Cromwell, H., 14, 25 Denno, D., 280-281, 294
Crosby, E., 199, 203,212 Denny-Brown, D., 302, 313
Crosson, B., 303, 312 De Olmos, J. S., 72, 76
Crutcher, M , 302, 312 Depue, R., 306, 313
Cruz, I., 228 De Robertis, E., 44
Cruz, M., 228 D'Esposito, M., 76
Cummings, J., 14, 25, 55, 76, 171, 180, Destrebecqz, A., 80
186, 1 8 8 - 1 9 1 , 3 7 5 , 3 7 8 , 3 8 0 Devinsky, O., 352, 378
Cummins, D., 373, 377, 394 DeVore, I., 373, 381
Cuppernoll, C. 25 DeWaal, F., 155-158, 165, 360, 373,
Cuvier, 96 377, 381
Dewey, W., 283, 294
Dabbs, J., 150 Diamond, A., 203, 212
Dabrowski, K., 328, 341 Diamond, J., 256, 332, 341
Dahmer, Jeffrey, 328 Dicalzi, G., 278, 294
Dalenoort, G., 301, 312 Dick, J., 24
Dallaire, L., 74 Dimitrov, M., 20, 25
Dam, M., 174, 180, 188, Dingwall, J., 373, 378
Damasio, A., xxxi, 22, 25, 155, 158, Distel, H., 67, 76
162 164-165, 199, 205-206, 211, Divac, I., 14, 26-27, 58, 76, 303, 314
348, 350, 353, 373-374, 377, 384, Doane, B., 188
392, 402 Dobzhansky, T., 31-32
Damasio, H., 125, 164, 206, 211 Dodd, J., 304, 313
Danieli, J., 306-307, 312 Dolan, R., 158, 164-166
Dantzer, R., 53, 76 Dorothy (case), 128
Darlington, C , 241, 256 Doshi, A., 278-280, 295
Darwin, C , 35, 44, 96-97, 104, 155, Douglas, R., 185, 188
157-158, 196,212 Douglass, J., 44
Daum, I., 20, 25 Dover, M , 74
Davidson, J., 74 Dowling, J., 403
Davidson, M., 78, 104, 149 Dreisbach, C , 294
Davidson, R., 74, 200, 213, 350, 377 Dreyer, B., 296
Davies, J., 313, 394 Dumanoski, D., 277, 294
Davies, N., 134, 141, 144, 150, 259 Dunbar, R., 146, 149, 256
Davis, K., 149, 391 Duncan, C , xxxiv, 215, 227-228, 398
Davison, K., 116 Dunipace, A., 277, 294-295
Dawkins, R., 156, 165, 325, 341 Dunsmore, R., 3, 7
Dawson, K., 313 Durant, J., 345
Dawson, R., 313 Dure, L., 75
Day, B., 24 Durfee, E., 352, 378
Dayan, P., 58, 76, 80 Dykes, J., 287, 295
Deaner, R., 166
De Duve, C , 273 Eaton, S., 332, 341
De laRiva, C , 81 Ebbesson, S., 76
Name Index 409

Eckel, C , 375, 378 Finger, S., 255

Edelman, G., 22, 25, 48, 76, 96, 104, Fischer, R., 61, 76
249, 257, 350, 353, 378 Fisher, A., 313
Edey, M., 320, 341, 378 Fisher, C., 40, 44, 60
Edgerton, R., 335, 342 Flaherty, A., 77
Ehlers, S., 165 Flannery, K., 25
Eibl-Eibesfeldt, I., 133, 149, 238, 256, Fleming, A., 15, 25, 352, 373-374, 378
320, 322, 326 341, Fleischer, S., 15, 25
Eidelberg, E., 79 Fletcher, J., 74
Eimas, P., 217, 227 Fletcher, P., 163, 165
Einstein, A., 329, 374, 378 Flourens, M , 133, 149
Eisenberg, H., 210, 213 Foley, FL, 317, 342
Eisenberg, N., 375, 378 Font, E., 72-73, 76, 78
Eiserer, L., 185, 188 Fortey, R., 104
Ekman, P., 213, 394 Fossey, D., 261
Ellenberger, H., 116 Fox, M., 207,212
Ellenwood, E., 142, 149 Fox, R., 338,341
Ellis, L., 196,212 Frackowiak, R., 79
Elsberry, W., 394 Franck, G., 80
Engel, J., 191 Frankel, M., 55, 76
English, J., 27 Freedman, D., 95, 116, 196, 212
Epstein, J., 3-4, 7 Freeman, J., 15,25,293
Erdal, D., 373-374, 378 French, L., 228
Erdi, P., 301, 312 Freud, S., 54, 135, 255, 351, 401
Ernandes, M., 267-268, 274 Fried, I., 168, 174, 178, 180-181, 187-
Ervin, F., 185, 189 188
Eslinger, P., 375, 378 Friston, K., 164
Etcoff,N., 166 Frith, C., 79, 165
Etzioni, A., 364, 378 Frith, U., 16, 26, 165
Evans, A., 294 Fryxell, K., 44, 139, 149
Ewert, J., 77 Fudge, J., 56, 78
Eysenck, H., 272, 274 Fukuyama, F., 294
Fuller, R., 130-131
Fagen, R., 16,25 Fullerton, B., 228
Fahrbach, S., 318, 341 Fulton, J., 3^1, 7-8, 200,212
Fairbanks, L., 51, 79 Fuster, J., 16, 18, 26, 61, 76, 198, 2 0 0 -
Fantie, B., 228 204,212,304,313,351,378
Farkas, I., 255
Farmelo, G., 380 Gabbard, G., 104
Farmer, J., 255 Gabriel, M , 25, 378
Faulkes, C., 148 Gabrieli, J., 50, 60, 76
Fawzy, F., 132,210,213 Gachter, S., 378
Fehr, E„ 360, 378 Gadjusek, D., 273
Fein, D., 164 Gadow, PL, 274
Fellner, M., 335, 341 Gagliardo, A., 18, 20, 26
Fentress, J., 14, 24, 255 Galanter, E., 257
Fenwick, J., 188 Galen, 134
Ferguson, L., 77 Gallagher, FL, 164-165
Fernald, A., 206, 212, 333, 341 Gambarian, L., 313
Field, J., 227, 394 Gans, C., 16-17, 26, 76
Fierman, A., 296 Gardner, E., 313
410 Name Index

Gardner, R., xxxiii, 40, 44, 85, 1 0 2 - Gouldner, A., 360, 378
103 116, 131-132, 149-150, 341 Grafman, J., 25
395-396 Graham, R., 149
Garey, L., 165 Gram, L., 174, 179,189
Garrison, F., 134, 149 Gramski, A., 299, 308-310, 313
Gaudiano, P., 392 Graybiel, A., 48-56, 58, 61, 75-77, 79,
Gauthier, J., 80 81
Gawin, F., 142, 149 Greenberg, N., xxxiii, 45, 165, 396
Gazzaniga, M., 91-92, 103, 257, 2 7 5 - Gromminger, O., 76
276, 294, 378 Groenewegen, H., 48, 78
Gee, H., 103 Grossberg, S., 384-385, 388, 392, 3 9 3 -
Gehring, W., 18, 26, 44, 96, 103 394
Geist, V., 317, 322-326, 330, 332-333, Grossman, J., 375, 378
341 Grossman, P., 378
Gemar, M., 122, 132 Gruenewald, T., 381
George, A., 148 Gruter, M , 184, 189, 293-294
George, K., 295 Guillemin, R., 303, 313
George, M , 74 Guillery, R., 352, 381
Gergel, I., 132 Gulson, B., 282, 294
German, D., 78 Gurdjieff, 113, 115
Geschwind, N., 168, 188 Gurung, R., 381
Ghiglieri, M., 339, 341 Gutbrod, K., 353, 381
Giammanco, S., 267-268, 274 Gutnick, M , 353, 378
Gibson, K., 378
Gilbert, P., 100, 104, 125-126, 1 3 1 - Haber, S., 56, 78
132, 138, 143-144, 149-150, 213, Hadley, M., 63, 78
317,321-323,341 Haeckel, E., 10, 17
Gillberg, C., 161, 165 Haig, D., 255, 257
Gilsofi, C., 399, 402 Hailman, J., 54, 78
Gintis, H., 360, 376 Haider, G., 44
Girgis, M , 203,212 Haley, J., 131
Glantz, K., 143, 149, 332, 340-341 Halgren, E., 200, 210, 212
Glausiusz, J., 255 Hall, B., 17-18, 26
Glod, C . 74 Hall, L., 74
Gloor, P., 24, 26, 103, 185, 187-189, Hall, V., 227, 394
196, 198, 200, 202,212, 228 Hallett, M., 25
Glowinski, J., 78, 81 Hamburg, D., 338, 343
Godard, F., 403 Hameroff, S., 375, 379
Goddard, C., 174, 179, 185-186, 188- Hamilton, S., 163, 166, 304, 314
189 Hamilton, W., 149, 255, 360, 367, 376,
Goldberg, E., 351, 378 379
Goldenberg, G., 60, 76 Hanson, N., 169, 179, 189
Goldstein, D., 63, 76 Happe, F„ 163, 165
Goldstein, K., 228 Harley, J., 12, 27
Gonzalez, A., 46, 50, 64, 79 Harlow, H., 8, 133, 148-149, 373, 379
Goodall, J., 261,373, 378 Harlow, M., 149, 379
Goodman, D., 293 Harper, R., 75
Goodwin, B., 257 Harrington, A., 10, 26, 345, 379
Goos, L., 256 Harris, Eric, 317, 324, 336-340
Gould, S., 18, 32, 36, 165, 333, 341, Harris, J., xxxiv, 155, 165, 249, 257,
343 377, 397
Name Index 411

Harris, S., 228 Hodos, W., 12, 16, 21-23, 25, 46, 75,
Hart, L., 321-322, 341-342 116
Harm, E., 352, 376, 379 Hoebel, B., 294
Hartmann, L., 145, 149 Hoffman, A., 78, 185, 188
Hasey, G., 125, 131 Hoffman, M., 63, 375, 379
Hashimoto, R., 60, 78 Hofstader, D., 374, 379
Hauser, M., 157, 255 Hogness, D., 44
Hawking, S., 328-329 Holahan, J., 74
Hayek, F., 169-170, 189, Hold, B., 401^102
Hayes, A., 52, 59, 78, Hollandsworth, J., 313
Hayes, B., 236, 255 Holloway, R., 212, 321-322, 341
Hazrati, L., 46-47, 59, 63, 80 Holstege, G., 80
Heath, R., 185, 189 Holt, D., 56, 78
Heckers, S., 56, 78 Holthoff-Detto, V., 14, 26
Heidegger, M., 310, 313 Hone, B., 277-280, 283, 289, 295
Heidnik, Gary, 328 Hornak, I , 213
Heilman, K., 303, 313 Hornykiewicz, O., 191, 303, 313
Heimer, L., 52, 76, 78 Horowitz, S., 188
Heiss, W., 26 Houk, J., 48, 52, 75, 391, 394
Helbing, D., 255 Hovde, K., 78
Heller, W., 350, 379 Howell, T., 139
Hen, R., 140, 149 Hrdy, S., 234, 256
Henderson, L., 273 Huether, G., 63, 78
Henderson, R., 44 Hugdahl, K., 377
Hendrickson, C., 26 Hull, C., 312
Henriksen, L., 79 Hume, D., 375
Henry, J., 145, 149, 402 Humphrey, N., 373-374, 379
Herbert, E., 43 Humphrey, T., 199, 203,212
Hercus, M., 63, 78 Hunt, M., 301, 313
Hereford, S., 341 Huntingford, F., 116, 196, 212
Herholz, K., 26 Huntington, A., 295
Herman, M., 24, 78 Hussein, Saddam, 117
Hernandez, A., 79 Huttenlocher, P., 138, 149
Herrero Hernandez, E., 294 Huxley, J., 53, 78
Herrick, C., 6, 97, 104, 275 Huxley, T., 157, 165
Herrnstein, R., 325, 330, 341 Hyde, T., 78
Hersh, L., 78 Hyman, S., 150
Herve, D., 49, 78-79
Hess, E., 257 Ingle, D., 77
Hess, G., 149 Ingrao, B., 366, 379
Hesse, H., 160 Insel, T., 55, 74, 78
Heymer, A., 54, 78 Iqbal, M., 75
Hickman, C., 12, 26 Irwin, I., 72-73, 79
Hickman, F., 26 Isaac, G., 360, 373, 379
Higgins, J., 25 Isaacson, R., 265, 274 305, 313
Hilburn-Cobb, C., 121, 131 Israel, G., 366, 379
Hill, D., 143, 149 Itzkoff, S., xxxiv, 259, 398
Hillegaart, V., 78 Ivry, R., 294
Hinde, R., 326, 341, 379, 389
Hirosaka, O., 79 Jablonski, D., 63, 69, 78
Hitri, A., 151 Jackson, D., 116, 131
412 Name Index

Jackson, J., 31, 40, 43, 133, 149, 218, Kawagoe, R., 79
227, 275 Keck, P., 141, 149
Jackson, R., 277, 295 Keefe, R., 217, 341
James, W., 4 Keele, S., 78
Jamison, K., 256 Keenleyside, M., 144, 150
Jani, N., xxxv, 383, 400 Keff, A., 116
Janssen, P., 141-142, 149 Keil, F., 79
Janvier, P., 273 Kellam, S., 227
Jasper, H., 6, 218-220. 226-227, Kellerman, H., 8
398 Kelly, J., 295, 304, 313
Jencks, C , 353, 375, 379 Kelly, P., 314
Jenike, M , 166 Kelly, S., 295
Jenner, P., 71-72, 79 Kemp, G., 75
Jennett, B, 205, 211 Kemp, J., 303, 313
Jenssen, T., 54, 78 Kemper, T., 146, 150, 161-162, 164
Jerison, H., 263, 265, 273-274, 398 Kendler, K., 228
Jessell, T., 6, 26, 198, 212, 312, 373, Kendrick, D., 317, 341
377, 379 Kerbeshian, J., 104
Jog, M., 52, 55, 78 Kerr, M , 255
Johanson, D., 320, 322, 341 Kessler, J., 26
Johanson, Z., 274 Kevles, D., 104
Johansson, M., 165 Keverne, E., 81
Johnson, D., 80 Keyes, D., 303, 311, 313
Johnson, R., 131 Khuder, S., 296
Joiner, T., 116 Kieffer, J., 294
Jones, B., 228 Kilts, C., 80
Jones, D., 79 Kim, C., 79
Jones, R., 77 Kimble, D., 5, 7, 15, 26
Jouvet, M., 159, 165 Kimelberg, M., 276-277, 283, 293
Juberg, D., 295 Kimura, D., 256
Jueptner, M , 52, 79 Kimura, M , 33, 43, 77
Jung, C , 183, 189 Kinkle, Kip, 280
Kinsey, W., 381
Kaada, B., 3, 7, 185, 189 Kirkpatrick, B., 25, 376
Kaas, J., 103 Kirkpatrick, S, 255
Kaftawy, A., 244, 294 Kitt, C., 63, 75, 79
Kagan, J., 95, 104 Klebold, D., 317, 324, 336-340
Kahn, R., 149 Klein, D., 131
Kakade, S., 76 Klein, L., 381
Kalin, N., 26 Kleinman, J., 78
Kandel, E., 16, 26, 93, 104, 198, 212, Kleinow, K., 77
352, 373, 379 Kling, A., 184, 189, 197-199, 202, 206,
Kandler, O., 273 212,
Kanner, L., 165 Klopf A., 384-385, 392-393
Kant, I., 182, 189 Klopfer, P., 75
Kaplan, H., 116 Kluver, FL, 133, 148, 150,
Karoum, F., 151 Knecht, J., 160
Kaszniak, A., 378-379 Knobil, E., 380
Katz, B., 294-295 Knowlton, B., 52, 79
Kauffman, S., xxxiv, 232, 234, 236, Knutson, B., 130-131
238, 244, 250, 255, 398 Ko, G., 149
Name Index 413

Koch, C , 353, 379 Lauer, J., 283, 295

Kocheudoerfer, G., 44 Laurent, J., 43
Kockelmans, J., 314 Laureys, S., 80
Koerselman, F., 91, 103 Lawrence, P. 402
Koestler, A., 394 Leavitt, FL, 394
Kohlberg, L., 358, 379 LeBar, K., 305, 313
Kohut, FL, 131 Lederhendler, I., 25, 376
Kokmen, E., 23, 26 LeDoux, J., 16, 19, 26-27, 92, 103,
Kolb, B., 203, 212, 303, 313 194, 196, 2 0 5 , 2 1 3 , 3 0 5 , 3 1 3 , 3 1 8 ,
Koliatsos, V., 104 325, 328, 339, 373, 379, 342
Kollar, E., 40, 44 Lee, M., 166
Konner, M , 332, 341 Legano, L., 296
Koob, G., 169, 189 Leila (case), 129
Kopin, L, 73, 79 Lejoyeux, M., 295
Korsch, M., 294 LeMay, M., 190
Kos, L., 44 Lennox, M., 1, 7
Kosseff, P., 25 Leon, ML, 27
Kosten, T., 142, 150 Lettvin, J., 257, 318, 342
Kostopoulos, G., 228 Leubke, C., 25
Kourakis, M , 96, 104 Levav, M., 228
Kozak, M , 80 Leven, S., 379, 391-394
Kramer, D., 165 Leventhal, B., 294
Kramer, P., 156, 257 Levesque, M., 80
Krams, M., 164 Levin, FL, 203, 207, 210, 213
Krasnegor, N. 26, 228, 378 Levine, D., xxxv, 375, 379, 381, 383,
Krasowski, M , 294 392, 400
Krebs, J., 134, 144, 150, 254-256, 361, Levine, M., 312
377 Levitan, R., 125, 131
Kringelbach, M., 213 Levitt, M., 281, 295
Kropotkin, P., 155, 157, 166 Lewin, R., 325, 342
Kruger, FL, 296 Lewis, A., 143, 150
Kruger, L., 4, 6, 8 Lewis, B., 381
Krulish, L., 77 Lezak, M., 304, 313
Kubota, Y., 78 Li, Y., 294, 295
Kuhn, T., 169, 189, 238,256 Lidsky, T., 52, 75, 80,314
Kwok, E., 81 Lieberman, P., xxxiii, 88, 103,
374, 380, 396, 402
LaBerge, D., 352, 379 Liebowitz, M., 132
Lake, J., 43 Limb, S., 296
Lamendella, J., 373, 379 Lindsley, D., 5, 220, 221, 226-227, 398
Landsburg, S., 371, 379 Linkey, FL, 210, 214
Langston, J., 72-73, 79 Liotti, G., 121, 132
Langton, C., 236, 255 Lippa, A., 307, 313
Laplane, D., 79 Lippard, S., 276-277, 295
Lappe, PL, 79, 332, 341 Lipsett, L., 217, 227
Lappe, M., 332, 342 Lipursky, S., 377
Lars, T., 314 Litvan, I. 25
Larsen, R., 402 Lively, C., 103
Larson, E., 82 Livingston, K., 188, 191
Lashley, K., 3-5 Ljungberg, T., 80
Lauer, E., 199, 203, 212 Loewi, O., 136
 Name Index

Loiseau, P., 210, 213 Martino, G., 350, 376

Lombardst, M., 403 Martin-Rodriguez, J., 191
Lombroso, 311, 320 Maslow, A., 392
Long, D., 393 Mason, G., 55, 79
Long, J., 273-274 Mass, R., 197, 200, 202, 206, 212-213
Looney, J., 104 Masters, R., xxxv, 184, 189, 198-199,
Lorenz, K., 256, 373, 380 213, 275, 295, 374-375, 380, 399
Losco, J., 380 Matlin, M., 317, 342
Lou, H., 56, 79 Matter, J., 71, 79
Lubart, T., 81 Maturana, H., 257, 318, 342
Luciano, D., 352, 378 Mayberg, H., 168, 189
Luckmann, T., 300, 312 Mayes, A., 60, 79
Luria, A., 5, 381 Maynard Smith, J., 43, 123, 132, 135,
Lutz, M., 364, 380 150, 257,358, 360, 380
Luu, P., 350, 381 Mayr, E., 86, 97, 104
Luxen, A., 80 Mazur, A., 196, 198, 213
Lydiard, R., 132 Mazure, A., 146, 150
Lykken, D, 257 McClelland, J., 384, 392
Lynch, G., 393 McConnel, E., 295
Lynne, G., 364, 380 McCulloch, W., 4, 257, 342
Lyon, G., 228, 378 McDonald, J., 199,211
McEwen, B., 57, 75, 79
Maas, L., 74 McGaugh, J., 393
MacAndrew, C, 335, 342, McGue, M., 257
Macmillan, M., 85, 102 McGuinness, D., 392
Magoun, H., 5, 227, 394 McGuire, M., 51, 79, 125, 132, 137,
Mahaffey, K., 294 150-151, 198-199,210,213,238,
Mai, J., 302, 314 256, 275, 295-296
Malamut, B., 393 Mclnerney, S., 166
Malkova, L., 163, 166 Mclntyre, D., 174, 179, 185-186, 188
Malloy, P., 188-191,204,213 McKinney, W., 89, 103
Maloney, A., 257 McNeil, M., 5, 8
Malthus, T., 157 Mead, G., 359, 380
Mangels, J., 79 Mealey, L., 335, 339, 342
Mangun, G., 275-276, 294 Meaney, M., 380
Mansbridge, J., 329 Mechler, F., 190
Manuzza, S., 278-279, 295 Medina, L., 27
Maquet, P., 80 Meerlo, J., 321, 342, 337
Marchione, K., 74 Mega, M., 168, 189
Margulis, L., 273, 401-402 Meldrum, B., 174, 189
Marin, O., 46, 50, 64, 79 Meliga, F., 294
Mark, V., 185, 189 Mellars, P., 378
Markey, S., 73, 79 Mellen, S., 321-322, 342
Markowitz, J., 116 Meloy, J., 190, 335-336, 338, 342
Marks, I., 95, 104 Meltzer, PL, 141-142, 150
Marsden, C, 14, 24, 27, 52-53, 58, 71- Mendelsohn, A., 281,296
72, 75, 80 Mendez, M., 186, 191
Marshall, N., 274 Merchant, H„ 52, 79
Martin, R., 326, 342 Merrill, M., 166
Martin, W., 295 Meulemans, T., 80
Martindale, M., 96, 104 Meyer, A., 155, 159, 166
Name Index 415

Meyerowitz, E., 44 Nadvornik, P., 191

Michaud, S., 342 Nakano, I., 78
Mickle, W., 189 Naquet, R., 228
Miczek, K., 190 Nathans, J., 44
Middleton, F., 52, 59, 69, 79, 303, 314 Nauta, W., 170, 184, 189, 205,
Middleton, W., 295 213, 392
Mielke, H., 280-281, 296 Nava, G., 329, 340, 391
Miller, B., 375, 378, 380, 388 Needleman, FL, 277, 279-281, 292,
Miller, E., 294 296
Miller, G., 255-257, 379 Neil, J., 380
Miller, L., 294, 338, 342 Neisser, U., 314
Miller, S., 12, 27 Neri, P., 257
Miller, T., 375, 380, 393 Nesse, R., 144, 150, 205, 209, 213,
Milligan, K., 121, 132 332, 342
Milson, M., 295 Nestler, E., 149-150, 168, 189
Mink, J., 50, 52-53, 62, 79 Nevin, R., 282-283, 296,
Minsky, M., 380 Newcomb, T., 256
Mirsky, A., xxxiv, 215, 224-228, 352, Newman, J., 165-166, 352, 380
380, 398 Newton, S., 401,403
Mirsky, C., 228 Ng, L., 166, 273
Mishkin, M., 163, 166, 387, 393, Nicholson, C., 44
Mitchell, M., 257 Nicol, C., 55, 76
Mithen, S., 146, 150, 342 Nicolas, R., 403
Mizon, K., 294 Nielsen, J., 79
Moberg, G., 57, 79 Niemegeers, C., 149
Mody, I., 353, 378 Nieuwenhhuys, R., 44, 61, 80, 224, 274
Mogenson, G., 48, 79 Nilsson, G., 82
Monchi, O., 387, 393 Nisbet, E., 273
Monassin, R., 255 Nitecki, M., 78
Monroe, R., 189, 338, 342 Nitschke, J., 379
Montagner, H., 401, 403 Noblin, T., 295
Montague, P., 58, 76, 80 Noblitt, T., 294
Moore, E., 131 Nohria, N. 402
Moore, J., 43 Norris, D., 77
Moore, P., 206, 207,213 Numaguchi, Y., 81
Mora, F., 399, 402 Numan, M., 15, 27, 352, 373-374, 380,
Morata, G., 44
Morgan, FL, 25, 378 Oberg, R., 14, 27, 58, 76, 303, 314
Morris, D., 53-54, 79, 268, 274 O'Doherty, J., 213
Morris, J., 43, 166 Ohman, A., 164, 166
Morris, L., 32, 38, 44 Olkon, D., 294
Morris, R., 164 O'Leary, D., 80
Morris, S. C., 32, 38, 44 O'Leary, J., 205, 212
Morrone, C., 257 Olivier, A., 188
Moyer, K., 318, 338, 342 Olsen, K., 81
Mullis, K., 257 Oshima, FL, 227-228
Murchison, C., 132 Otto, R., 76
Murphy, M., 162, 166, 303, 314 Ouspensky, P., 116
Murray, E., 163, 166 Owens, M., 140-141, 150
Myers, J., 277, 294
416 Name Index

Paglia, C , 143, 150 Plutchnik, R., 8

Palmini, A., 185, 187, 189 Poirier, J., 74
Panksepp, Jaak, xxxi, 16, 27, 89, 91, Polcari; A., 74
98, 103, 194,213, 196, 199, 204, Pollack, D„ 132
207, 211, 353, 373-374, 379, 380, Pontius, A., xxxiv, 167, 188-190, 204,
401-403 213, 397
Panksepp, Jules, xxxi, 91, 401, 403 Pooley, A., 17, 27
Pantelis, C , 81 Popper, K., 92, 170, 256
Papageorgiou, M., 228 Porges, S., 321, 342
Papez, J., 4 - 5 , 89, 133, 136, 150, 168, Post, R., 122, 131
189 Powell, T., 303, 312-313
Paradiso, S., 49, 80 Powles, W., 150
Parent, A., 46-47, 52, 59, 62-63, 71, Powers, A., 68, 80
80, 135, 150 Pratt, J., 103
Parks, R., 393 Premack, D., 157
Partridge, M., 201, 213 Pretot, M., 403
Pascal, B., 108 Prewitt, K., 313
Pascualvaca, D., 228 Pribram, K., xxxii, 2, 52, 80 133, 150,
Passingham, R., 15, 27, 79, 164, 198, 185, 1 8 8 , 2 5 4 , 2 5 7 , 2 7 5 , 3 5 1 , 3 7 5 ,
213 381,384,392,395
Paul, D., 104 Price, D., 79
Pavlov, 248, 385 Price, J., xxxiii, 89, 97, 100, 103-104,
Paxinos, G., 302, 314 107, 119-120, 126, 132, 139, 143,
Pearce. J., 143, 149, 332, 341, 401, 403 150, 2 3 4 , 2 5 5 , 3 9 7
Peele, T., 303, 305, 309, 314, Proust, M., 184
Peigneux, P., 52, 80 Prueitt, P., 393
Penfield, W., 6, 218-221, 226-227, Pryadarshi, A., 296, 278
398 Pugh, G., 205, 213
Pennington, B., 257 Purcell, R., 81
Pennisi, E., 156, 166 Puglisi-Allegra, S., 75
Penrose, R., 375, 379 Purves, D., 275-276, 278, 296
Peroutka, S., 139
Pert, A., 306, 314 Quesney, L., 188
Petersilia, J., 276, 282, 296 Quiroga, J., 265, 274
Peterson D., 343, 358
Peterson, S., xxxv, 299, 314, 399 Radinsky, L., 273-274
Petrie, A., 203, 213 Raine, A., 190, 276, 296
Pfaff, D., 318, 341 Rafal, R., 78
Philippe, H., 43, 151,257 Raleigh, M., 130, 132, 145, 150
Phinney, J., 294 Ramachandran, V. 378
Piaget, J., 358, 381 Rapoport, J., 211, 214, 274, 327, 342:
Pianka, E., 148, 150 Rasmussen, S., 255
Pietrzyk, U., 26 Rauch, I., 378
Pinker, S., xxxii, 103, 318, 342, 353, Rauch, S., 166
374,381,402^03 Ray, C , 228
Pira, E., 294 Ray, J., 145, 151
Pitts, C., 132, 342 Reich, D., 171, 190
Pitts, W., 257 Reiner, A., 10-11, 14, 1 6 - 1 9 , 2 1 , 2 7 -
Platigorsky, J., 44 28, 68, 80, 103,372,381
Plomin, R., 257 Reitz, S., 5, 8
Ploog, D. 27 Renner, K., 81
Name Index 417

Renshaw, P., 74, 319 Sargent, J., 293

Res, V., 131 Sarkisyan, Z., 313
Restak, R., 19, 27, 319, 342 Sasai, Y., 44
Restoin, A., 403 Sato, F., 80
Reynolds, V., 311,314, 403 Savin-Williams, R., 196,214
Rhode, P., 150 Scarnati, E., 80
Richard II, 123 Schaeffer, D., 77
Richards, R., 151 Schafer, E., 133, 148
Ridley, M., 257 Schantz, P., 228
Ridley, R., 190 Schaub, E., 296
Risch, S., 140-141, 150 Scheerer, M., 228
Rizendine, E., 295 Scheller, R., 328, 343
Roberts, L., 26 Scherer, K., 394
Rockland, C , 164 Schick, K., 343
Roe, A., 8 Schiller, F., 103
Roesch, R., 190 Schjelderupp-Ebbe, T„ 126, 132
Rogers, L., 26 Schlesinger, L., 343
Roffler-Tarlov, S., 50, 80 Schlozman, K., 308, 315
Rohde, P., 105, 132 Schmajuk, N., 393
Rolls, E., 198, 213-214, 302, 307, 314 Schmidt, R., 305, 314
Romo, R., 79 Schneider, J., 52, 75, 80,314
Ronan, P., 79 Schnider, A., 353, 381
Rosack, J., 104 Schore, A., 204, 214
Rose, J., 4 Schrag, C., 310, 314
Rosellini, R., 80 Schrier, A., 1, 149, 379
Rosen, C , 296 Schubert, G., 306, 314
Rosen, D., 116 Schultz, W., 52, 58, 80, 387, 393
Rosenblatt, J., 16, 25-26, 378 Schuri, U., 76
Rosenstein, G., 384, 386, 393 Schwartz, J., 16, 26, 198, 212, 312,
Rosvold, H., 200, 211,228 373, 379
Roth, V., 18 Schwerdtfeger, W., 77
Rothwell, J., 24 Scott, A., 378
Rucinska. E., 74 Scott, J., 89, 103, 378
Rudomin, P., 378 Scott, M., 77
Rumelhart, D., 384, 392 Scott, P., 80
Ruse, M., 151 Searle, J., 22, 27,350, 381
Russell, K., 295 Sedlak, P., 191
Segal, N., 214, 256-257
Sadalla, E., 317, 341 Segal, Z., 122, 132
Sadik, A., 296 Segerstrale, U., 92, 103
Sagan, C., 9-10, 17, 27, 321-322, 342 Sejnowski, T., 373, 376
Sagan, D., 402 Seligman, M , 57, 80, 132
Sainsbury, R., 15, 27 Selman, B., 255
Sakai, R., 75 Senault, B., 314
Salamone, J., 49, 80 Sengel, R., 306, 314
Salinas, E., 79 Shafer, E., 133, 148
Salloway, S., 188-191 Shakespeare, 123
Sanchez-Herrero, E., 44 Shaw, S., 314
Saper, C., 78, 80-81 Shaywitz, B., 74
Sapolsky, R., 125, 132, 145, 151 Shaywitz, E., 74
Sarason, I., 228 Sheehan, T., 352, 373-374, 380
418 Name Index

Sheer, D., 8 Stein, J., 53, 81

Sheppard, D., 56, 75, 81 Stein, L„ 307, 314
Sherman, S., 352, 381 Stein, M., 130, 132, 294
Sherrington, C , 133, 151, 257 Stephens, P., 145, 149
Shibata, D., 49, 81 Stern, C., 15, 27
Shick, K., 332, 343 Sternberg, R., 62, 81, 274
Shipman, P., 333, 343 Stevens, A., 234, 255
Shostak, M., 332, 341 Stevenson, J., 3, 7
Shreeve, J., 333, 343 St. Hilaire, G., 96
Shrier, D., 81 Stollnitz, F., 149, 379
Shrivastava, S., 296 Stookey, G., 294-295
Sicherman, J., 300, 311, 314 Strick, P., 52, 59, 63, 69, 79, 303-304,
Sickler, C , 257 314, 393
Sidow, A., 44 Strickberger, M., 12, 27
Sigmund, K., 235, 255 Strieker, E., 53, 81
Sigmund, M., 161, 166 Striedter, G., 14, 18, 27
Silverman, C , 282, 296 Stuss, D., 200, 204, 210, 214
Silverman, I., 256 Suddath, R., 151
Simpson, G., 8 Sugerman, R., 67, 81
Sinton, D., 78 Sullivan, K., 17
Skipper, J., 294 Sullivan, R., 26
Skoyles, J., 256 Summers, C., 67, 70-71, 79, 81
Sloman, L., xxxiii, 104, 112, 119, 131, Sung-Bae Cho, 380.
143, 1 5 1 , 2 1 3 , 3 8 7 , 3 9 7 Suomi, S., 166
Slotnik, B., 15, 25, 27 Sutton, B., 104
Smeets, W., 46, 50, 64, 77-79 Sutton, R., 295, 393
Smith, C.U.M., xxxii, 18, 22, 27, 31, Svare, B., 77
241,255-256,350,381,396 Swallow, S., 128, 132
Smith, H., 274 Swann, A., 104
Smith, P., 25 Sweet, W., 191
Smith, R., 318-319, 343 Switzer, R., 72-73, 76, 78
Smuts, B., 255 Symonds, D., 328, 343
Smythies, J., 177, 191, 394 Szathmary, E., 43
Snowden, C., 16, 2 5 - 2 6 , 3 7 8 Szentagothai, J., 301, 312
Snyder, D., 199, 2 0 0 , 2 1 1 , 2 1 4
Snyder, S., 307, 314 Takahata, N., 43
Sober, E., 158, 166 Takakawa, Y., 79
Sokolov, E., 5 Tanaka, Y., 78
Sonnenborn, A., 282, 296 Tangi, R., 82
Spar, J., 132,210,213 Tarr, R., 67, 81
Spencer, H., 31, 43, 135, 151, 157 Tassin, J., 78, 81
Sperry, R., 91 Tatman, J., 228
Spevack, A., 5, 8 Taylor, C, 255
Spitz, R., 373, 381 Taylor, J., 149, 319, 323, 335, 343,
Sporns, O., 256 381,393
Squire, L., 79, 93, 103-104 Taylor, P., 340
Sramka, M., 185, 191 Taylor, S. 374, 381
St. Augustine, 134 Teasdale, J., 122, 132
Stamm, J., 15, 17, 27 Tecce, J., 226-227
Stapp, H., 375, 381 Teicher, M., 74
Steadman, L., 332, 341 Tellegen, A., 257
Name Index 419

Ten Donkelar, J., 44 Van Raaij, W., 378

Terlecki, L., 15, 27 Van Ree, J., 314
Terpstra, A., 131 Van Schaik, C., 56, 156, 166
Teske,N„ 375, 381 Van Valen, L., 18, 27
Vaughan, G., 77
Teuber, H., 57, 81, 20-23, 206, 213, Veenman, C., 14, 27
303,314 Verba, S., 308, 315
Thierry, A., 49, 81 Verhulst, J., 104
Thomas, D., 44 Vernier, P., 136, 139, 151
Thomas, E., 103 Vicsek, T., 255
Thomson, K., 17, 27 Victor, J., 190
Tillier, B., 317, 335, 343 Villablanca, J., 312
Tinbergen, N., 34, 65, 81 Vimpani, G., 294
Tipton, R., 323, 335, 340, 343 Vincent, J., 151
Toates, F., 381 Vogel, G., 156, 166
Todes, D., 157, 166 Vogt, B., 378
Tomarev, S., 44 Volkmar, F„ 378
Tong, E., 79 Von Baer, 17
Tononi, G., 22, 25, 48, 76, 249, 2 5 6 - Von Hoist, D., 126, 132
257, 350, 353, 378 Voogd, J., 274
Tooby, J., 256, 318, 332, 338, 340-343, Vrba, E., 333, 341,343
373, 376, 381
Toth, N., 332, 343 Wachs, J., 25
Tranel. D., 164 Wada, J., 174, 180, 185, 191
Trevarrow, B., 18, 27 Wagner, K., 26, 104
Trimble, M., 176, 177, 186, 188, 191 Waldrop, M., 255
Trivers, R., 144, 151, 158, 166, 2 0 6 - Walker, A., 333, 343
207,214,360,381 Walker, M., 104
Troisi, A., 132, 209, 213, 238, 256, Walker, S., 279, 296
275, 296 Wall, P., 3, 5, 7-8
Troyansky, L., 255 Walsh, C., 252, 378
Tucker, D., 350, 381 Walsh, D., 228
Tucker, G., 89, 103 Wamboldt, F., 104
Turbiglio, M., 294 Wang, H., 81
Turner, A., 116, 196, 212 Warren, J., 214, 296
Turner, D., 228 Warrick, J., 294
Tuthill, R. 292, 296 Washburn, S., 212, 338, 343
Waterhouse, L., 164
Updegraff, J., 381 Watson, R., 303, 313
Uttal, W., 300, 315 Watzlawick, P., 113, 116
Weakland, J., 131
Vaccarino, F., 25 Weinberger, D., 170, 184, 191
Valdenaire, O., 151 Weinberger, N., 393
Valenstein, E., 303, 313 Weiner, J., 104
Valentini, C., 294 Weiser, H., 185, 191
Valzelli, L., 321, 322, 339, 343 Weisfeld, C., 201
Van Baal, J., 360, 376 Weisfeld, G., xxxiv, 193, 214, 353, 398
Van den Bercken, J., 57, 75, 312, 322, Weiss, B., 296
339, 343 Weiss, J., 80, 104
Van der Linden, M., 80 Weiss, S., 75, 104, 122, 131
Van Hoesen, G. 78, 187, 191 Weissman, N., 116
 Name Index

Weissmann, G., 403

Wendorf, C., 210, 219 Yahr, P., 81
Werbos, P., 384, 386, 392, 393 Yakovlev, P., 168, 191
Whalen, P., 164, 166 Yang, B., 74
Wheelis, M., 273 Yardley, S., 228
Whishaw, I., 14, 24, 203, 212, 303, 313 Yodyingyuad, U., 81
Whitaker, H„ 379 Yokoyama, S., 44
White, E., 51,380-381 Yuwiler, A., 132, 150-151
White, N., 81
Whiten, A., 373-374, 378, Zacharko, R., 75
Wickelgren, I., 59, 81 Zainos, A., 79
Wienhard, K., 26 Zajonc, R., 208, 214
Wieser, H., 185, 191 Zecchina, R., 255
Wilford, J., 273 Zhang, W., 294-295
Willhoite, F., 361 381 Zhong, J., 81
Williams, G., 209, 213, 302, 308, 314, Ziegler, S., 281, 293
315, 332, 343 Zigmond, M , 53, 63, 81
Williams, J., 122, 132 Zimmer, L., 24
Williamson, P., 180, 191 Zinovieva, R., 44
Willingham, E., 294 Zuckermann, S., 119, 132
Willis, T., 135
Wilson, C., 135,294
Wilson, D. R., xxxiv, 104, 133, 1 4 3 -
144, 151, 319, 343, 397
Wilson, D.S., 158, 166
Wilson, E., 92, 103, 240, 309, 315, 330,
343, 349, 395-396, 402-403
Wilson, H.E., 294
Wilson, J.Q., 276, 282, 296
Wilson, M , 294
Wilson, R„ 79
Wilson, S.A.K., 151
Winberg, S., 71, 81
Wingfield, J., 77
Winston, P., 380
Wise, R., 49, 81
Wise, S., 211, 214
Wispe, L., 375, 381
Woese, C., 273
Wolfe, E., 131
Wolkowitz, 0., 131
Wolpe, J., 257
Wood, H., 328, 340
Woodhead, A, 78.
Woolsey, C., 8, 148
Wrangham, R., 343, 338
Wright, C., 78
Wright, R., 240, 255, 256, 332, 344
Wu, Y., 80
Wurker, PL, 26
Wyatt, R., 142, 151
 SUBJECT I N D E X

Abductive reasoning, 169 as emotional and triggering devi<

Acetylcholine, 38, 139, 267 304,318,
Across-Species Comparisons and 322, 347, 352
Psychopathology (ASCAP) Anapsid reptiles, 346
Society, 100, 332 Angelman syndrome, 99
ACTH (adrenocorticotropic Anions, 277
hormone), 34 Anolis carolensis, 54, 64-69
Activity level, 355-356 Anthropology, 360
Affect, 45, 270, 304 Anti-depressant medications, 145
Affectional program, 337, 346-354 Aplysia, 93-94
Affective, motivational, cognitive, Approach-avoidance behavior, 15
interface, 48 archaebacteria, 33, 37, 262
Agnatha, 34, 263 Archeopteryx, 41
Agonic-hedonic, 143 Archetype, 183
Agonism, 110-114, 124, 321, 396 Arginine vasopressin, 353
Algorithms of reciprocal behavior, Artificial intelligence, 347, 352,
356-359 383
Alliances and hierarchies, 239-240 ASCAP, 100,332
Allocortex, 162 Ascending reticular activating
Altruism, 155, 158, 234, 267, 272, system (ARAS), 220-221, 226,
339, 364, 367, 375 398
Alzheimer's disease, 60 Asperger syndrome, 163
American Scientist, 19, 20, 23 Attachment, 121, 159, 247, 321,
Amino acids, 34 373, 397
Amnesia, 171-172, 177, 181 Attachment theory, 121
Amniotes, 12, 22, 346-347 Attention, 57-58, 352;
Amphetamines, 145 functional analysis, 215
Amphibians, 12, 347 Attention deficit disorder, 204, 225
Amygdala, 5, 10, 46, 48, 50, Attention deficit hyperactivity
60; role in fear and startle, 156; disorder (ADHD), 56, 96, 276,
abnormalities in autism, 162, 278, 292
163-164; in seizure kindling, 172, Attitude theory of emotions, 5
180, 185-186; as part of fear Australopithecus africanus, 157
pathway, 194-200, 2 0 3 - Aura, 172, 174,
207; as part of dominance pathway, Autism, 55, 155, 161, 163,225,
210; as part of limbic system, 264; 397
422 Subject Index

Baboon, 201 Cartesian mind/brain split, 93, 350

Bacteriorhodopsin, 37 Catecholamines, 139
"Barrel of Staves" conformation, Categorical imperative, 182
36-37 Cations, 276
Basal cortex, 4 Caudate nucleus, 6, 226, 302, 304
Basal ganglia, 6, 10, 13; array of C-elegans, 39-40, 43
structures included, 45-47; Centrencephalon, 6, 217-221, 223,
motor, sensor, & cognitive 226, 398
functions 51-53,; role in Cerebellum, 19-20, 50, 53, 59, 6 1 -
attention 57-59; memory 62, 162, 263,265
disorders, 61-62; effects of Cerebrum, 216
lesions, 68-72, 87; Chaos, 231, 236, 240, 245, 250,
extrapyramidal motor system, 253-254, 398
135; in reification, 302-303; Chaotic networks, 233-235
self-survival circuitry, 352; in Chimpanzees, 156-158, 203
neural network theory, 387, Cilia, 263
389, in cognitive process, 396, Cingulate cortex (gyrus), 4, 10, 1 4 -
Basal nucleus of Meynert, 46 16; in autism, 155, 162-163; in
Behavioral conflict, 348 parenting and affection, 206; as
Behavioral tension: as internal part of limbic system, 216; role
emotional compass, 349; in attention, 224-225; included
algorithmic dynamic, 356-357; in limbic system, 347; in mam-
in economic exchange 362, malian nurturing, 352-353
367-368, 371-372, 376 Circadian cyclicity, 97
Behavior-experience-mental Claustrum, 46
(BME), 93-95, 99 CLIP (Corticotropin-like
Binding problem, 180-181 intermediate lobe protein, 34
Biogenic amines, 139 Cnidaria, 34, 40
Biological psychiatry, 95 Cognition, 4 5 , 6 1 - 6 2 , 193
Biophysics, 401 Cognitive/objective vs
Blood-brain barrier, 276 emotional/subjective, 395
BME-MCO, 93-95, 99 Columbine killings, 317, 336-338,
Body plan, 86, 96-97, 396, 401 400
Bonobo chimpanzees, 397 Comparative structural functional
Boolian net, 235 vs evolutionary phylogenetic,
Bradykinesis, 53 395
Brain/body ratio, 265-266 Compassion, 156
Brain chemistry, effect of heavy Competition by attraction, 122
metals, 275-293 Competition by intimidation, 122
Brain stem, 13, 15, 18, 59; Complex partial seizures, 174, 177,
neurotransmitters, 70, 188
135, 162, 193, 196-197; Conflict-resolution, 110
attentional functions, 216, Conflict systems neurobehavioral
218-227; as part of R-complex, (CSN) model 3 4 5 , 3 5 1 , 3 5 3 ,
248-249; self-preservation 364, 367, 369
program, 347-348, 352 Consciousness, 7; moral, 22-23;
Burgess shales, 32-33, 35 alteration of in LPTR, 173, 182;
as attention, 218, 221; dynamic
+
C a channels, 39-40 core, 350; self-awareness, 351,
Calculus, in price theory, 371-372 360
Care-taking, 85, 339 Consilience, 402
Subject Index 423

Continuous Performance Test (CPT), Dove, 134, 144, 146-147

221-222, 226 Drosophila, 35, 4 1 , 9 6 - 9 7
Corpus callosum, 68, 226 DSM III, 98
Corpus striatum, 45, 107, 135, Duality of the Market, 369-370
224-225 Dynamic balance range, 354-355,
Correspondence, 17-18 357, 363, 366, 368, 372
Corticosterone, 69 Dynamic core of consciousness,
Cost/benefit equation, 367 350
Cotylosaurs, 12-13 Dynorphin, 34
Creativity, 62-63
Crocodiles, 10, 23 Ear, 194-195
Cro-magnon, 157, 271 Echolalia, 87
Crotaphytus collaris, 67 Echopraxia, 87
Crysemys, 68 E-coli, 38
Ctenopthora, 34 Economics, 345, 360, 369
Cyclostomes, 139 Economic theory, 345, 400
Cynodonts, 264-266 Ediacaran outcrops, 32-33, 35
EEG, 219, 226
De-escalation, 107, 112, 122, 134 Effective IDS, 121
Deep time chronology of life, 33 Ego, 135,225, 345;
Demand and supply, 362-363, 3 6 9 - neocortical representation of
371,400 self-survival in CSN model, 347,
Demand curve, 369 350,353-358,360,365,369-
Demander performs egoistic role, 370, 376, 401
364 Ego-empathy reciprocal algorithm,
"Demonic" males, 338 400
Depression: as adaptive Egoistic range, 354-355, 363
behavior 108-112, 114-115; Egyptians, 134
neurobiology of, 119, 125, 127- Elasmobranch fishes, 6
128, 133; evolutionary Electro-convulsive therapy, 130
epidemiologic analyses, 143— Emotion, 91-92, primacy of, 193—
144, 146; as expression of 194,397
chaos, 246-247 Emotional brain, 107-108
Deuterocerebrum, 137 Emotional/subjective vs
Diencephalon, 6, 260 cognitive/objective, 395
Dinosaurs, 10, 12, 14 Empathetic range, 354-355, 363
DNA, 86 Empathy, 15, 87; failure to develop
Dominance behavior, 198 in autism, 155-164; selective
Dominance hierarchies, 119, 126, lack in psychopaths, 178; in
239, 374 complex social behavior 206,
Dominance pathway, 197, 199 234, 267, 337, 345; neocortical
Dominance/submission, 196 representation of affectional
Donnen Equilibrium, 277 circuitry in CSN model, 347,
Dopamine, 49-50, 56-57, 64, 7 0 - 350, 352-357, 360-365, 3 6 9 -
71, 139, 140-142, 146, 370, 375-376; in neural network
261,279, 283,288 modeling, 387-390
Dorsolateral prefrontal cortex (DL), Empathy as economic preference,
202-206 taste, problems with, 371
Dorsal raphe, 46 Encephalization, 137
Dorsal ventricular ridge (DVR), Endorphins, 4 9 , 3 0 6 , 3 5 3
63-64, 67, 69 Endothermy, 21
424 Subject Index

Energy level, 355-356 Frontal cortex, 6, 18, 60, 87, 99,

Enkaphalins, 353, 386 134, 141, 184,302,399
Entorhinal cortex, 162, 264 Frustration-aggression, 99
Entropy, 231
Environment of evolutionary Gage, Phineas, 201
adaptation (EEA), 330 Galen ofPergamum, 134-135
Environmental pollution, 275-296 Game theoretic Darwinism, 134
Epilepsy, 217, 226 Game theoretic models, 133-134
Epinephrine, 139 Game theory, 123, 133, 147
Epistemics, 38, 161, 181 Gamma-amino butyric acid
Epithimetikon, 134 (GABA), 38, 40, 48, 50, 139,
Equilibrium price, 368-369, 371 — 278
372 Gene deletion, 34
Equation of neural architecture, Gene duplication, 34
366-368 Genetic specificity, 138
Escalation, 107 Gift, 361-362
Escalation de-escalation theory, Globus pallidus, 13, 45-47, 54,
110 135,302
Ethogram, 194 Glycine, 38
Eubacteria, 33 Gnathostomata, 34
Eugenics, 92 G-Proteins, 37, 139
Eukaryocytes, 32-33, 262-263 Grand lobe limbique, 4, 135, 155,
Eusocial affiliation, 133 168
Evolutionary epidemiology, Grand mal epilepsy, 321
98, 133 Greek brain science, 134
Evolutionary neuromentalities, 147 Group bond, 361
Evolutionary neuroscience, 2, Group for the Advancement of
231, 345, 361, 368 Psychiatry(GAP), 100-102, 397
Evolutionary perspective Group selection, 158
neglect of, 1-2 GTP (guanine triphosphate), 37
Evolutionary phylogeny vs
comparative structural Habenula, 59
functional, 395 Halobacteria, 37
Evolutionary psychiatry, 142, 368 Hamilton's rule, 345, 366-367, 401
Evolutionary psychology, 345, 361, Hamlet, 236
368, 401 Hawk, 134, 144, 146-147
Executive functions, 241 Heavy metals and brain chemistry,
Executive programming, 337, 3 5 0 - 275-293, 399
351,354 Hedonic, 143,321,352
Exons, 34 Hegemony, 2 9 9 , 3 1 2 , 3 9 9
Extrapyramidal motor system, 135 Hegemony of regression, 330
Helminths, 136
Family related behavior, 15, 23, Hemispheric lateralization, 350—
87-90, 158,339,361,373 351
Fear pathway, 194-195 Hierarchical behavior, 200
Fibrinopeptides, 33 Hierarchical encounters, 119
Fixed action patterns, 53-54, 183, Hindbrain, 347-348
196, 327 Hippocampus, 4, 6; role in
Flat affect, 172, 184 learning, memory 10, 12, 15;
Foraging society, 347 interaction with striatum
Fragile X syndrome, 99 48, 60; neurotransmitters, 7 0 -
Subject Index 425

71; abnormalities in autism, Involuntary subordinate strategy,

162-163; imbalance with 120
amygdala in limbic seizures, Ion channels, 35
185-187, 2 0 3 , 2 0 5 , 2 1 6 , 2 1 9 ; Isocortex, 13; reptilian contrasted
encoding of stimuli, 225; with mammalian, 64; as
vulnerability to neurotoxins, alternative term for neocortex,
278; CSN model, 347, 352 235, 259-260, 262, 350; as
Histones, 33 decisive selection element in
Horn genes, 97 human evolution, 269-270, 350
Homeobox gene, 96, 136-138, ISS, 120
248-249
Homeostasis, 1, 329 James-Lange theory, 4
Homeostatic control of social behavior, Jellyfish, 40, 136
49, 364, 368
+
Homo erectus, 157 K channels, 39-40
Homology, 10, 17-19, 2 3 , 3 5 , 5 1 , Kin altruism, 206
97, 139,346-347,396 Kindling, 113, 122, 174, 185
Homoplasy, 19 Kindness, 156
Homo sapiens, 32, 43, 108, 157, Kin selection, 133, 360
273, 328, 332 Kinship-based foraging society,
Homo sapiens sapiens (Hss), 262, 347
269, 271 Kluver Bucy sybdrome, 207
Hormones, 348, 353 Komodo dragon, 217
HOX complex, 35, 86, 96,396 Koresh, David, 312
HP A axis, 125,130
Huntington's syndrome, 14, 48, 50, Laboratory of Brain Evolution and
60, 101 behavior, 9, 345
Hypostatizing, 300, 306-307 Lactation, 269
Hypothalamic-pituitary-adrenal Language module, 374
axis, 125, 130 Lateral thalamic nuclei, 59
Hypothalamus, 46, 49, 99, 141, 162; Leaded gas, toxic effects, 281-283
as part of fear & dominance Learning deficits, heavy metals
pathways, 194, 196-197, 199, and, 292
210; in reticular formation, 226; Lenticular nucleus, 46
302, Ligand gated ion channels, 35, 3 8 -
40
Id, 235 Limbic-motor interface, 48
IDS (involuntary defeat strategy), Limbic psychotic trigger reaction
119,397 (LPTR), 167,397
Impulse control disorders, 177 Limbic seizure, 167
Inclusive fitness, 345, 361, 3 6 6 - Limbic system, 10;
367 elaboration in mammals, 12-16;
Individual range of response, 331 interaction with striatum,
Informational macromolecules, 32 46-48; emotion and
Inhibition and release, 319, 338 communication, 90, 107, 111;
Integration, 395 as component in IDS, 125;
"Interpersonal stickiness," 86 neurotransmitters, 141;
Invisible hand, 345, 365-366, 3 6 8 - abnormalities in autism,
369 161-163; seizure activity and
Involuntary defeat strategy (IDS), motiveless homicide, 167-188;
119 neural mediation of emotions of
426 Subject Index

fear, dominance, pride, 193— 13

200; functions in attention, Mismatch theory, 331-332
224-227, 235; phase transitions, Modal range of response, 329-330
245, 247; as selective element in Molecular biology, 396, 401
human brain evolution, 259-273; in Molecular-cellular-organic MCO,
reification circuitry, 302-304; in 98-99
phylogenetic regression, 339; in Molecular embryology, 41
CSN model 347-348; memory of Molecular neurobiology, 18
rewards, 387 Monoamine behavior modulation,
Logistikon, 134 71
Long term potentiation (LPT), 278 Monotreme, 265
LPH (lipotropic hormone), 34 Montreal Neurological Institute, 24
Mood and thought disorders, 133
Macaque brain, 222, 226 Mood disorders, 107, 133, 142
Macaque monkeys, 119, 156, 373 Moral choice, 351, 365
397 Moral consciousness, 22-23
Major ranges of reciprocal behavior, Moral stages of development, 3 5 8 -
353-356 359
Male bonding and the lethal raid, Morganucodon, 264
338 Morphospaces, 38
Mammalary bodies, 162 Motivation, 45
Mammalian brain, 215-216, 235, Motiveless homocide, 168-188
252 Motor stereotypies, 55
Mammals, 12, 14, 57, 88 Mozu, 156
Mania, 133, 143-144, 146,210 MPTP, 72-73
Manic-depression, 134 mRNA, 141
Manic illness, 126, 128, 171, 177, MSH (melanocyte stimulating
397 hormone), 34
Manic patients, 126 Multiple utility, 364
Market, 365; duality of, 369-371; Mummification, 134
evolution of, 361-363, Mus, 42
Market equilibrium, 370 Mutual aid, 158, 240
Maternal behavior, 15-16, 19, 21,
158-159, 347, 353 +
N a channel, 40
Medial preoptic area, 15, 352, 373 Nature, 231
Medial septal nucleus, 162 NAZI regime, 92
Medieval scholasticism, 135 Neanderthal, 271
Mediobasal cortex, 4-5 Neocortex, 4, 13, 16; limbic &
Medulla oblongata, 226 striatal connections, 59; as
Medusa, 136 isocortex, 91; as rational, 111;
Memory disorders, 60-61 as executive, 137-138, 147; in
Mesencephalic reticular formation, fear, dominance, pride
222 pathways, 193-195,203; in
Mesopontine reticular formation, attention, 216-217, 224; phase
224-225 transitions, 235, 245, 247,
Metabolism, 348 249-250; in evolutionary
Metaeconomics, 264 selection, 262, 264, 268; in
Metazoa, 33, 139 reification, 302, 305-306;
Midbrain, 194-199,347 inhibition, 324; executive
Miocene, 271 programming, 346-348, 350; in
Mirror display of squirrel monkey, neural modeling 389
Subject Index 427

Neomammalian, 107, 1 4 7 , 2 1 5 - CSN model, 245, 247, 352-353

216, 224-225, 235, 346-347, Osteolepiforms, 266
352 Other-interest, 22, 247, 350, 354,
Neopallium, 260 375
Neostriatum, 4, 46, 58-59, 156, 302 Oxcytocin, 355
Neural architecture, 235,
345, 348, 363, 366, 398, 4 0 0 - Pair-bonding, 133
401; and duality of the market, Paleomammalian (brain) complex,
369-370, 372 107, 147,217, 224-225,249,
Neural Darwinism, 96 347, 387
Neural global workspace model, Paleomentation, 40
352 Paleopsychology, 32, 319, 399
Neural modeling, 383 Papez circuit, 168
Neural network architecture, 351, Paradoxical kinesia, 53, 58
368, 400 Parallel evolution, 19
Neural network theory of brain, Parallel processing, 234
383 Parental behavior, 14-17, 162
Neural tube, 137 Parietal cortex (lobe), 224
Neuroactive peptides, 34 Parkinson's syndrome, 14, 48, 50,
Neurobiotaxis, 35 53,58-60,71,278
Neuroembryology, 35 Pars compacta, 46, 61, 71
Neuroimaging, 163 Pars reticulata, 46, 62
Neuromental phylogeny, 136 Paternal caring behavior, 353
Neuronal algorithms, 102 Pathogenesis, 95
Neuronal pruning, 138 Pattern detection, 169
Neurotoxins, effects of, 276-278 PAX-6, 40-41
Neurotransmitters, 136, 138, 348, Pecking order, 126
353 Pedunculopontine tegmental
Nonconvulsive seizures, 177 nucleus, 59
Norepinephhrine, 57, 139 "Per" gene, 97
Norm of reciprocity, 360-361 Perirhinal cortex, 4, 6
Nucleic acids, 32 Permian-Triassic, 12, 264, 346
Nucleus accumbens, 45-46, 48-49, Perseveration, 87
56, 60, 63 Petit mal seizure, 218, 226
Nucleus basalis, 46, 59 Phase boundary, 232-233
Phase transition, 231, 233-234,
Objective reduction (OR), 375 236-237, 242, 245, 253-254,
Obsessive-compulsive disorder 398
(OCD), 55, 204,211 Phrenology, 135
Octopamine, 139 Phylogenetic regression-
Olfactory striatum, 46 progression theory, 133,
Ontogeny, 136 317
Ontogeny recapitulates phylogeny, Physics, 231-232, 236, 364, 375
10, 17 Piriform allocortex, 91
Opioids, 353 Pituitary, 195
Optic chiasm, 226 Platonic neuroscience, 134
Optic tectum, 64 Platyhelminth-like worms, 32
Orbitofrontal cortex (OFC), 4; in Play, 15, 133, 159, 162, 269
modulation of behavior, 99, Political economy, 368
162, 179; in dominance Pollution, 275-293
behavior, 198-202, 205-207; in POMC (pro-opiomelanocortin) 34,
428 Subject Index

Pons, 222 Raphe-hippocampal-limbic circuit,

Pontine reticular formation, 222, 142
226 Raphe nucleus (dorsal) 268
Positron emission tomography Raphe obscurus, 268
(PET), 48-49, 163,252 Rational choice, 351
Prader-Willi syndrome, 99 R(reptilian)-complex (brain);
Precursor proteins, 34 controversy in definition, 6; 10,
Prefrontal (cortex) lobes, 18; 12-13; as striatum, basal
in unity of thought & behavior, ganglia, 45, 51; in frustration-
48-49; higher order cognitive aggression, 99; as instinctive,
functions, 125; empathy 107-108, 133; in attention, 2 1 5 -
emerging from linkage with 2 1 7 , 2 1 9 - 2 2 3 , 2 2 5 ; in phase
cingulate cortex, 155; in LPTR transition, chaos, stasis, 245,
170, 174, 179, 180; mediates 248, 250; as perfected in seas,
complex social behavior, 93, 262-264; as source of magical
200, 202-207; role in thought, 268, 270; in CSN
shifting focus of attention; 2 2 4 - model, 346
225; modulates quick acting Receptors, 241
amydala, 318 Reciprocal modular brain, 387
Prefrontal leucotomy, 201 Reciprocal algorithms of behavior,
Premotor cortex, 210, 225 345, 356-357, 400
Price, as endogenous, exogenous Reciprocal altruism, 158, 206, 209
variable, 371-372 Reciprocity through conflict, 357—
Price equilibrium, 364, 371 358
Pride, 193 Reduction, 395
Primitive-advanced response Reduction vs integration, 395
continuum, 335-336 Reflex arcs, 233
Prokaryocytes, 38 Reflex epilepsy, 173
Prolactin, 353 Reframing the situation, 113
Protein brain structures, 87 "Region of moral insanity," 135
Proteins, 32-34 Regression-progression,
Protocerebrum, 136 continuum, 325-326
Protoreptilian complex, 19, Reification, 299-312,399
248, 346, 348, 352 Relationship psychiatry, 94
Protozoan, 193, 262 Releaser, 54, 318-319, 327
"Psalics," 40, 97-98 Reptile neuroethology, 63-73
Pseudodominance, 26 Resource holding potential (RHP),
Psychoanalysis, 93 147
Psychomotor epilepsy, 197-198, Reticular activating system, 6
260, 270 Reticular formation, 6
Prozac, 247 Retroductive reasoning, 169
Putamen, 6, 4 5 , 2 1 6 , 3 0 2 Rhesus monkey, 373
Pythagoras, 235 Rhinencephalon, 267
Rhodopsins, 37
Quantitative neuroscience, 7 RHP (resource holding potential),
Quantum gravity, 376 147
Quantum mechanics, 376 Ritalin, 279
Quantum physics, 358-359 Ritual agonistic behavior (RAB),
120, 147
RAB (ritual agonistic behavior), Ritualistic displays, 239
120, 147 RNA, 401
Subject Index 429

Russian evolutionists, 157 111, 121, 128, 142-148

Social competition and attachment,
SAD (seasonal affective disorder), 121
109 Social Darwinism, 157
SAHP (social attention holding Social exchange, 345
potential), 127, 147 Social psychology, 369
Schema theory, 301 Social theory, 369
Schizophrenia, 55-56, 59, 62, Sociobiology, 92, 26, 309
171-172, 174, 177-179, 183, Sociology, 360, 369
187, 2 2 5 , 2 7 2 , 3 1 9 , 3 3 6 Sociopathy, 202, 204
Schizophysiology, 4 Sociophysiology, 85, 89, 95,
Schragstellung gait, 261 97,110,397
Science, 20, 23, 90, Somatic intellect, 136
156,396 Somatic marker, 374, 384
Science, physical vs social, 358— Species-typical behavior, 13-14,
359 45, 66-67
Sclepoporous occidentalism 65 Stasis, 231,235, 240, 245,398
Seasonal affective disorder (SAD), Statistical physics, 231-232,
109 398
Self-esteem, 133,206 Stem reptiles, 12-13, 346-247, 372
Self-interest, 21; as expression of Stress, 57, 323, 349
ego in CSN model, 347, 350, Striatal complex, 13-14, 46,
352, 354, 356-358; confused 48, 63-72, 2 3 5 , 2 4 7 , 2 6 6
with self reference in economic Striatopallidal complex, 46
theory, 364-365 Striosomes, 46
Selfish genes, 156 Subjective experience, 22
Self-preservation, 21, 345, 347, 353 Submissive behavior, 124
Self-preservational programmining, Substantia innominata, 46
337,346,348-351,354 Substantia nigra, 46, 48, 56, 61-62,
Self-reference, fallacy of, 364, 371 71-72, 135, 226, 302
Sensorium communale, 135 Subthalamic nucleus, 135
Septum, 10, 45, 50, 267, 352, 373 Suicide, 238
Serotonergic drugs, 130 Superego, 135, 235
Serotonin, 70-71, 73, 139-142, Supply as mammalian nurturing,
145-146, 198, 241,247, 2 6 7 - 365
268, 283 Supply and demand, 345, 362-363,
Serotonin spectrum disorders, 247, 371,400
353 Supply curve, 370
Serpentine 7TM proteins, 35-37 Synapsid reptile, 22, 266
Sexual abuse, 124 Syndrome "E," 178-180
Sham rage, 185
Shame, 193 Tabula rasa, 276
Signature display (Anolis), 65 Tectum, 224
Silicofluorides, toxic effects, 2 8 4 - Telencephalon, 46, 70, 135, 216,
292 260
Social attention holding potential Temporal lobe epilepsy (TLE),
(SAHP), 127, 147 171-172, 181
Social bonding, 184 Temporal (cortex) lobes, 180-181,
Social brain concept, 100— 185, 187,210, 224-225
102,366-368,397 Temporal lobe seizures, 205
Social competition, 100, 109, Testosterone, 69, 196, 198, 353
430 Subject Index

TE striatal loop, 59, 62 Vervet monkey, 200

Thalamic sensory relay, 299 VGIC (voltage gated ion channels),
Thalamocingulate division, 15, 51, 35, 38-40, 43
206, 267, 339 Viceral brain, 4-5, 90
Thalamocortical system, 48 Violent crime; heavy metals and
Thalamus, 15; as relay between brain chemistry, 275-293, 399
limbic system and cortex, 47, Von Baerian recapitulation, 17
61-62, 182; in fear and
dominance pathways, 194-197, Warmbloodness, 21, 347
203; as relay to the neocortex in Wave function, 359, 375
reification, 302, 304; gateway to "Will to power," 148
cortex, 352 Wisconsin card sorting test, 386
Theories of addition, 20 Witzelsucht, 210
Theoretical neuropsychology, 392 Working memory, 352
Theory of mind, 157, 163 World Psychiatric Association, 100
Therapsids, 12, 261, 264, 266, 269
Thermodynamics, 359 Xenopus, 35
Thermoregulation, 133
Thimoeides, 134 Zebrafish, 43
Toxic metals, 277
Transaction, 362-363
Transposons, 34
Triarchic theory, 259
Tritocerebrum, 136
Triune brain, 5;
reappraisal of concept, 10-11;
as soundly grounded in
evolutionary neuroscience, 2 1 -
22; most useful bridging link
between neuroscience and the
social sciences, 23; clarifying
effects in social competition
theory, 110-112, 115; as
representing a long tradition; 134-
136, accurate of brain evolution,
137; utility in conceptualizing
autism, 155, 160-161, 164; utility in
grasping limbic psychotic trigger
reaction, 168-170, 184, 186; in
analysis of attention, 215-227,
2 3 1 , 2 3 5 , 2 4 5 , 272,317; as
neural substrate for CSN model,
345-347; utility in neural modeling,
390-392, 397
Tourette's syndrome, 14
Tuning, 252

Urbilateralia, 34, 42

Vagus nerve, 4, 182, 186, 188

Vagusstoff, 136
 A B O U T THE CONTRIBUTORS
A N D EDITORS

Kent Bailey, Professor Emeritus of Psychology, Virginia Commonwealth

University, Richmond, VA

James Brody, Clinical Psychologist, 1262 West Bridge St., Spring City, PA

Gerald A. Cory, Jr., Director, The Center for Behavioral Ecology and San Jose
State University, San Jose, CA

Connie C. Duncan, Research Associate Professor of Psychiatry, Uniformed

Services University of the Health Sciences, Bethesda, MD

Russell Gardner, Jr., Clinical Professor of Psychiatry, Medical College of

Wisconsin, Madison, WI

Neil Greenberg, Professor, Department of Ecology and Evolutionary Biology,

University of Tennessee, Knoxville, TN

James C. Harris, Professor of Psychiatry and Behavioral Sciences and

Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD

Seymour W. Itzkoff, Professor, Smith College, Northhampton, MA

Nilendu G. Jani, Iconoci, Inc. Bedford, TX

Daniel S. Levine, Professor of Psychology, University of Texas at Arlington,

Arlington, TX

Roger D. Masters, Professor, Department of Government, Dartmouth College

and Foundation for Neuroscience and Society, Hanover, NH
432 About the Contributors and Editors

Allan F. Mirsky, Chief, Section on Clinical and Experimental Neuropsycho-

logy, National Institute of Mental Health, Bethesda, MD

Jaak Panksepp, Chicago Institute for Neurosurgery and Neuroresearch,

Chicago, IL

Steven A. Peterson, Professor, School of Public Affairs, Perm State Harrisburg

Middletown, PA

Anneliese A. Pontius, Associate Clinical Professor of Psychiatry (retired),

Harvard Medical School, Boston, MA

Karl H. Pribram, Professor Emeritus, Stanford University, Distinguished

Professor and Eminent Scholar, Radford University, Distinguished Research
Professor, Georgetown University

John S. Price, Retired: Former Consultant Psychiatrist, UK National Health

Service, Odintune Place, Plumpton, E. Sussex, UK

Leon Sloman, Associate Professor, Department of Psychiatry, Honorary

Consultant in Psychiatry, Center for Addiction and Mental Health,
University of Toronto, Ontario, Canada

C.U.M. (Chris) Smith, Honorary Visiting Fellow, Vision Sciences, Aston

University, Birmingham, UK

Glenn E. Weisfeld, Professor of Psychology, Wayne State University, Detroit,

MI

Daniel R. Wilson, Professor & Chairman of Psychiatry, School of Medicine,

Creighton University, Omaha, NE