Action (Verb Naming) Uency As An Executive Function Measure: Convergent and Divergent Evidence of Validity
Action (Verb Naming) Uency As An Executive Function Measure: Convergent and Divergent Evidence of Validity
Action (Verb Naming) Uency As An Executive Function Measure: Convergent and Divergent Evidence of Validity
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Abstract
Numerous studies have demonstrated dissociable neuroanatomic underpinnings for the retrieval of grammatical classes of
words such as nouns and verbs. Whereas retrieval of common and proper nouns is primarily mediated by posterior and anterior
temporal regions, respectively, verb retrieval is primarily mediated by frontal regions. The majority of studies evaluating verb
production have utilized tasks requiring subjects to name a graphically depicted action (i.e. action naming), leaving tests of verb
generation in the absence of prompting stimuli (i.e. action ¯uency) largely unexamined. In a recent study, Piatt, Fields, Paolo,
Koller and TroÈster (in press) found that an action ¯uency task discriminated demented Parkinson's disease (PD) patients from
non-demented PD patients and healthy control subjects, whereas lexical and categorical ¯uency tasks did not. These authors
suggested that action ¯uency was sensitive to the fronto±striatal pathophysiology associated with PD dementia, and thus, that
action ¯uency might serve as an indicator of executive functioning. This study was undertaken to evaluate the construct validity
of action ¯uency as an executive function measure in a group of healthy elderly control subjects. Findings revealed modest to
moderate relationships between action ¯uency and several putative executive measures. Action ¯uency was unrelated to indices
of semantic and episodic memory. Results support the construct validity of action ¯uency as an executive function measure and
suggest that this task may provide some unique information not tapped by traditional executive function tasks. # 1999 Elsevier
Science Ltd. All rights reserved.
Numerous studies have demonstrated dissociable frontal and posterior lesions. For example, in a study
neuroanatomic underpinnings for the retrieval of involving patients with aphasia syndromes suggestive
grammatical classes of words such as nouns and verbs. of neuroanatomical dysfunction in frontal (agrammatic
An accumulation of evidence supports the contention aphasics) and temporal (anomic aphasics) regions,
that common and proper nouns are represented in pos- Miceli et al. [15] found that agrammatic aphasics
terior and anterior temporal regions, respectively, demonstrated notable de®cits in verb production,
whereas verb retrieval is strongly mediated by frontal despite preservation of noun retrieval. In contrast, the
neural circuits [1,3,5±9,11,14,15,19]. Evidence for the anomic aphasic subjects demonstrated greater diculty
prominent role of the frontal lobes in verb retrieval with noun retrieval in comparison to verb production.
comes predominantly from studies comparing noun Similar ®ndings were reported by Damasio and Tranel
and verb retrieval in patients with known or suspected [7] who found that patients with frontal lobe injury
demonstrated notable diculty with verb but not noun
retrieval. In contrast, patients with posterior lesions
* Corresponding author. Tel.: +1-913-588-7187; fax: 1-913-588- demonstrated the opposite pattern of preserved verb
6965.
E-mail address: atroster@kumc.edu (A.I. TroÈster)
retrieval in the presence of poor noun generation.
1
Present address Department of Psychiatry and Human Behavior, Based on this double-dissociation, Damasio and
Brown University School of Medicine Tranel asserted that verb naming is mediated by the
0028-3932/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 8 - 3 9 3 2 ( 9 9 ) 0 0 0 6 6 - 4
1500 A.L. Piatt et al. / Neuropsychologia 37 (1999) 1499±1503
frontal regions, whereas noun retrieval is mediated by dysfunction that undermines the ability to mentally
the dominant, anterior temporal lobe. In a recent coordinate and manipulate the diverse range of infor-
study by Cappa et al. [2], similar dissociations were mation that may be associated with a verb. Although
observed among patients with Alzheimer's disease there is ample evidence to support the contention that
(AD) and fronto±temporal dementia (FTD). the retrieval of verbs re¯ects executive functioning, and
Speci®cally, Cappa et al. reported that both the AD possibly a unique aspect of executive functioning, these
and the FTD subjects exhibited inferior object and hypotheses have not been directly evaluated in non-
action naming relative to normal controls. However, clinical populations. Moreover, investigations of verb
the patients with FTD, relative to patients with AD, retrieval employing a ¯uency-based task are extremely
performed signi®cantly better on the object naming rare. The absence of both ¯uency-based methods of
test. Cappa et al. interpreted these ®ndings as assessing verb retrieval and the use of such measures
suggesting that the retrieval de®ciencies noted in the as indicators of frontal lobe and/or executive function-
AD subjects re¯ect more general loss of semantic in- ing is surprising given the notably wide use of lexical
formation, whereas the dissociation between object ¯uency as an executive function test.
and action naming observed in patients with FTD This study was undertaken to evaluate the construct
underscores the importance of the frontal lobes in the validity of an action ¯uency task as a measure of
retrieval of verbs. In a similar vein, Williamson et al. executive functioning in a sample of healthy elderly
[18] reported that patients with AD performed signi®- subjects. Given the prominent role ascribed to the
cantly more poorly on object than action naming, even frontal lobes in verb retrieval, it was hypothesized that
once word-frequency eects were controlled for. action ¯uency would be signi®cantly related to puta-
Although these and other studies [1,3,5,6,8,11,14,19] tive measures of executive functioning (convergent val-
support the hypothesized dierential neuroanatomic idity), but not signi®cantly related to measures tapping
substrates of noun and verb retrieval, functional ima- semantic and episodic memory (divergent validity).
ging (PET) studies have suggested a more widely dis- However, based on evidence that verb retrieval
tributed representation of verb retrieval including involves neural circuits distinct from those involved in
heavy reliance on the dominant temporal and parietal traditional executive function tasks, we anticipated
regions [17]. only modest relationships between action ¯uency and
To date, the assessment of verb retrieval abilities has the executive function measures.
been generally limited to action naming tasks that
require subjects to identify the verb associated with a
graphically depicted image, similar to the action nam- 1. Method
ing subtest of the Boston Diagnostic Aphasia
Examination (BDAE) [10], see also Refs. 1.1. Participants
[1,3,11,14,15,19]. In contrast, the ability to generate
verbs in the absence of prompting stimuli (i.e. action Participants consisted of 67 healthy elderly control
verbal ¯uency) had been virtually unexamined until subjects recruited as caregivers of patients enrolled in
recently. In a study assessing the utility of an action studies at the Neurodegenerative Disease Research
¯uency task (rather than action naming) as an indi- Center at the University of Kansas Medical Center.
cator of frontal±subcortical pathophysiology, Piatt et Forty-two (63%) of the participants were female.
al. [16] found that action ¯uency, but not lexical or Sixty-four (96%) of the subjects were right-handed.
semantic ¯uency scores, discriminated patients with Additional sample characteristics are presented in
Parkinson's disease (PD) and dementia from non- Table 1. All subjects were free of histories of neuro-
demented PD and healthy elderly control groups. logic disease or injury, psychiatric illness including
Based on their ®ndings, Piatt et al. concluded that substance abuse or dependence, or self-reported
action ¯uency was particularly sensitive to the fronto± speci®c developmental disorders. All subjects under-
striatal pathophysiology of PD with dementia, went comprehensive interviews, neuropsychological
suggesting that action ¯uency may have utility as an testing, and neurologic examinations.
indicator of frontal lobe functioning in clinical popu-
lations. 1.2. Materials and procedures
Findings across clinical populations and assessment
methods (i.e. task) suggest that verb retrieval abilities As part of a larger test battery, subjects were admi-
re¯ect the underlying integrity of frontal lobe neural nistered the Dementia Rating Scale (DRS), Wisconsin
circuitry, and can be considered to re¯ect the cognitive Card Sorting Test (WCST), Trail Making Tests
construct of executive function. In a recent report, (Trails), Boston Naming Test (BNT), California
Grossman [12] discussed the hypothesis that verb Verbal Learning Test (CVLT), and the Wechsler
retrieval de®cits re¯ect underlying executive system Memory ScaleÐRevised (WMS-R), all in standard
A.L. Piatt et al. / Neuropsychologia 37 (1999) 1499±1503 1501
Age 71.39 (6.45) 57±84 The following measures of episodic memory were
Education 14.96 (2.31) 12±20 included: The number of words recalled on CVLT
Dementia Rating Scale total (/144) 139.37 (4.05) 128±144
Action ¯uency (words/min) 16.75 (4.73) 8±30 trials one through ®ve and the WMS-R Logical
Dementia Rating Scale I/P (/37) 36.49 (1.30) 31±37 Memory (WMS-R LM) immediate recall raw score.
Dementia Rating Scale CNC (/39) 37.45 (2.36) 30±39 The BNT total correct score was used as a measure of
Trails B (total time) 83.00 (33.32) 37±218 semantic memory.
WCST-Categories (/6) 4.77 (2.13) 0±6
WCST-Conceptual Responses (%) 66.15 (24.34) 5±91
WCST-Perseverative Responses 15.98 (14.56) 3±65
WCST-Perseverative Errors 14.26 (11.94) 3±51
Boston Naming Test (/60) 57.09 (3.34) 36±60
CVLT total (/80) 50.91 (10.45) 24±70 2. Results
WMS-R Logical Memory Immediate (/50) 27.15 (5.53) 10±36
3. Discussion
Education DRS±I/P DRS±CNC Trails B WCST±PR WCST±PE WCST±CR WCST±Categories CVLT total WMS-R LM BNT total
1.0
As hypothesized, action ¯uency was signi®cantly,
but moderately, related to several putative executive
function measures. Although no signi®cant relation-
ship was observed between action ¯uency and DRS±I/
0.18
P scores, this may have re¯ected a marked restriction
1.0
of range in DRS±I/P scores (60 of the 67 subjects
obtained scores of 36 or 37/37). However, the signi®-
cant relationships between DRS±I/P scores and Trails
0.37b
0.25a
B and WCST±PE argue against this explanation.
1.0
Another possibility is that the low correlation between
DRS±I/P and action ¯uency stems from the fact that
the DRS±I/P score is heavily in¯uenced by category
(semantic) verbal ¯uency (up to 20 of 37 points), and
action and semantic ¯uency tasks tap somewhat dier-
0.42b
0.30a
0.01
ent retrieval processes (see [16]). Of the executive
1.0
ÿ0.40b
ÿ0.35a
ÿ0.22
ÿ0.31a
0.23
ÿ0.12
ÿ0.21
0.18
0.11
0.09
ÿ0.25a
ÿ0.24
0.22
0.20
0.13
0.03
0.15
1.0
0.29a
ÿ0.01
0.03
0.04
ÿ0.15
ÿ0.16
0.14
ÿ0.02
0.03
ÿ0.22
1.0
Action ¯uency Age
ÿ0.37b
ÿ0.38b
0.39b
0.40b
0.26a
ÿ0.28a
0.24
0.04
0.18
0.19
1.0
P < 0.05,.
P < 0.01.
WCST±PR
WCST±PE
Education
Trails B
Table 2
a
b
known frontal±subcortical involvement from those Trabucci M. Object and action naming in Alzheimer's disease
with only suspected or no frontal±subcortical involve- and frontotemporal dementia. Neurology 1998;50:351±5.
[3] Caramazza A, Hillis AE. Lexical organization of nouns and
ment [16], suggest that action ¯uency may have clinical verbs in the brain. Nature 1991;349:788±90.
utility as a measure of executive functioning. It is also [4] Corcoran R, Upton D. A role for the hippocampus in card
of note that while action ¯uency was not related to in- sorting? Cortex 1993;29:293±304.
dices of semantic or episodic memory, Trails B and [5] Damasio AR. Aphasia. New England Journal of Medicine
WCST±CR were signi®cantly related to BNT scores, 1992;326:531±9.
[6] Damasio AR, Damasio H. Brain and language. Scienti®c
and all four WCST scores were signi®cantly related to American 1992;267:63±71.
both the CVLT Total Learning score and the WMS-R [7] Damasio AR, Tranel D. Nouns and verbs are retrieved with dif-
Logical Memory I scores. These ®ndings could parallel ferentially distributed neural systems. Proceedings of the
earlier accounts of hippocampal involvement in per- National Academy of Science, USA 1993;90:4957±60.
formance on executive functioning tasks (e.g. card [8] Damasio AR, Tranel D, Damasio H. Verbs but not nouns:
Damage to left temporal cortices impairs access to nouns but
sorting) [4], and, to the extent that this is the case, one not verbs. Society for Neuroscience Abstracts 1992;18:387.
could argue that action ¯uency is a frontally mediated [9] Daniele A, Giustolisi L, Silveri MC, Colosimo C, Gainotti G.
task that is less susceptible to hippocampal in¯uence. Evidence for a possible neuroanatomical basis for lexical proces-
Moreover, it appears that action ¯uency may tap sing of nouns and verbs. Neuropsychologia 1994;32:1325±41.
aspects of executive functioning not measured by tra- [10] Goodglass H, Kaplan E. Boston diagnostic aphasia examin-
ation, 2nd ed. Philadelphia: Lea and Febinger, 1987.
ditional executive instruments, thus perhaps adding to [11] Goodglass H, Klein B, Carey P, Jones K. Speci®c semantic
what is considered by many to be a very limited pool word categories in aphasia. Cortex 1966;2:74±89.
of sensitive and speci®c executive function tests [13]. [12] Grossman M. Not all words are created equal: category-speci®c
Although these initial ®ndings are promising, the lit- de®cits in central nervous system disease. Neurology
erature examining verb retrieval generally, and action 1998;50:324±5.
[13] Lezak M. Neuropsychological assessment, 3rd ed. Oxford:
¯uency speci®cally, remains sparse. Additional research
Oxford University Press, 1995.
examining the construct validity and clinical utility of [14] McCarthy RA, Warrington EK. Category-speci®city in an
action ¯uency with a range of clinical populations will agrammatic patient: the relative impairment of verb retrieval
be needed in order to establish action ¯uency as an and comprehension. Neuropsychologia 1985;23:709±27.
executive functioning measure in its own right. [15] Miceli G, Silveri MC, Villa G, Caramazza A. On the basis of
the agrammatic's diculty in producing verbs. Cortex
Nonetheless, should research continue to support the
1984;20:207±20.
ability of action ¯uency to assess unique aspects of [16] Piatt AL, Fields JA, Paolo A, Koller WC, TroÈster AI. (in
executive functioning, action ¯uency may prove to be press). Lexical, semantic, and action ¯uency in Parkinson's dis-
a useful and easily administered instrument in the ease with and without dementia. Journal of Clinical and
daily practice of clinical neuropsychology. Experimental Neuropsychology.
[17] Warburton E, Wise RJS, Price CJ, Weiller C, Hadar U,
Ramsay S, Frackowiak RSJ. Noun and verb retrieval by normal
subjects: Studies with PET. Brain 1996;119:159±79.
References [18] Williamson DJG, Adair JC, Raymer AM, Heilman KM. Object
and action naming in Alzheimer's disease. Cortex 1998;34:601±
[1] Baxter DM, Warrington EK. Category-speci®c phonologic dys- 10.
graphia. Neuropsychologia 1985;23:653±66. [19] Zingeser LB, Berndt RS. Retrieval of nouns and verbs in
[2] Cappa SF, Binetti G, Pezzini A, Padovani A, Ruzzini L, agrammatism and anomia. Brain and Language 1990;39:14±32.