contributed articles

Do I :1 0.1 1 4 5 /1 9 4 1 4 8 7 .1 9 4 1 5 06
It has been known since the pio-
The brain’s electrical signals enable people neering work of Hans Berger more
than 80 years ago that the brain’s
without muscle control to physically interact electrical activity can be recorded
with the world. noninvasively through electrodes on
the surface of the scalp.23 Berger ob-
BY DennIs J. mCfaRLanD anD Jonathan R. WoLPaW served that a rhythm of about 10Hz
was prominent on the posterior scalp
and reactive to light. He called it the

Brain-Computer
alpha rhythm. This and other obser-
vations showed the electroencepha-
logram (EEG) could serve as an index
of the gross state of the brain. Despite

Interfaces for Berger’s careful work many scientists

were initially skeptical, with some
suggesting that the EEG might repre-
sent some sort of artifact. However,

Communication subsequent work demonstrated con-

clusively that the EEG is indeed pro-
duced by brain activity.23

and Control
Electrodes on the surface of the
scalp are at some distance from brain
tissue, separated from it by the cover-
ings of the brain, skull, subcutaneous
tissue, and scalp. As a result, the signal
is considerably degraded, and only the
synchronized activity of large numbers
of neural elements can be detected,
limiting the resolution with which
brain activity can be monitored. More-
over, scalp electrodes pick up activ-
BraIn aCtIVIty ProDUCEs electrical signals detectable ity from sources other than the brain,
on the scalp, on the cortical surface, or within the including environmental noise (such
as 50Hz or 60Hz activity from power
brain. Brain-computer interfaces (BCIs) translate lines) and biological noise (such as ac-
these signals into outputs that allow users to tivity from the heart, skeletal muscles,
communicate without participation of peripheral and eyes). Nevertheless, since the time
of Berger, many studies have used the
nerves and muscles36 (see Figure 1). Because they do EEG to gain insight into brain function,
not depend on neuromuscular control, BCIs provide with many of them using averaging to
separate EEG from superimposed elec-
options for communication and control for people trical noise.
with devastating neuromuscular disorders (such as
amyotrophic lateral sclerosis, or ALS, brainstem stroke, key insights
cerebral palsy, and spinal cord injury). The central Brain-computer interfaces provide a
new communication-and-control option
purpose of BCI research and development is to enable for individuals for whom conventional
methods are ineffective.
these users to convey their wishes to caregivers, use
Current BCI technology is slow,
word-processing programs and other software, and even benefiting only those with the most
control a robotic arm or neuroprosthesis. Speculation severe disabilities.

has suggested that BCIs could be useful even to people Research may greatly expand the
number of people who would benefit
with lesser, or no, motor impairment. from the technology.

60 Commu n ICat Ion s of t h e aCm | MAY 2 0 1 1 | VOL . 5 4 | N O. 5

 BCIs are a direct communication pathway between the brain and external devices. eeG measurements at the Danish master’s program in
medicine & technology; http://www.medicin-ing.dk/kandidat/en.

EEG research reflects two major 1970s based on visual evoked-poten- negative and positive peaks, and the
paradigms: evoked potentials and tials.34 His users viewed a diamond- numbers indicating the approximate
oscillatory features. Evoked poten- shape red checkerboard illuminated latency in msec.
tials are transient waveforms, or brief with a xenon flash. By attending to dif- Vidal’s achievement was an in-
perturbations in the ongoing activ- ferent corners of the flashing checker- teresting demonstration of proof of
ity, that are phase-locked to an event board, they could generate right, up, principle. In the early 1970s, it was far
(such as a visual stimulus). They are left, and down commands, enabling from practical, given that it depended
typically analyzed by averaging many them to move through a maze present- on a time-shared system with limited
similar events in the time-domain. ed on a graphics terminal. An IBM360 processing capacity. Vidal34 also in-
Although oscillatory features in an mainframe digitized the data, and cluded in his system online removal
EEG may occur in response to specific an XDS Sigma 7 computer controlled of ocular artifacts to prevent them
events, they are usually not phase- the experimental events. Users first from being used for control. A decade
locked and typically studied through provided data to train a stepwise lin- earlier, Edmond Dewan6 of the Air
spectral analysis. Historically, most ear discriminant function, then navi- Force Cambridge Research Lab, Bed-
EEG studies have examined phase- gated the maze online in real time. ford MA, instructed users to explicitly
locked evoked potentials. Both these Thus, Vidal34 used signal-processing use eye movements to modulate their
major paradigms have been applied techniques to realize real-time analy- brain waves, showing that subjects
PHOTOG R APH BY L AR S BAH L

in BCIs.36 sis of the EEG with minimal averag- could learn to transmit Morse code
The term “brain-computer inter- ing. The waveforms showed by Vidal34 messages using EEG activity associ-
face” can be traced to Jacques Vidal of suggested his BCI used EEG activity in ated with eye movement.
the University of California, Los An- the timeframe of the N100-P200 com- The fact that both Vidal’s and De-
geles who devised a BCI system in the ponents, with the N and P indicating wan’s BCIs depended on eye move-

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contributed articles

ment made them somewhat less in- use of a P300-based spelling device bet and several other symbols, focus-
teresting from a scientific or clinical (see Figure 2b) in which a positive po- ing attention on the desired selection,
point of view, since they required ac- tential around 300msec after an event as the rows and columns of the ma-
tual muscle control or eye movement, significant to the subject is consid- trix were repeatedly flashed to elicit
simply using EEG to reflect the result- ered a “cognitive” potential since it is visual evoked potentials. Farwell and
ing gaze direction. generated in tasks where the subject Donchin7 found their users were able
discriminates among stimuli. Far- to spell the word “brain” through the
Varieties of BCI signals well’s and Donchin’s7 users viewed a P300 spelling device; in addition, they
Farwell and Donchin7 reported the first 6×6 matrix of the letters of the alpha- did an offline comparison of detection
algorithms, finding the stepwise linear
figure 1. Basic design and operation of a BCI system.
discriminant analysis was generally
best. The fact that the P300 potential
Signal Acquisition Translation
reflects attention rather than simply
and Processing Signal Features Algorithm Device Commands gaze-direction implied this BCI did not
depend on muscle, or eye-movement,
control, thus representing a significant
advance. Several groups have since fur-
ther developed this BCI method.13
Wolpaw et al.38 reported the first use
of sensorimotor rhythms (SMRs) for
cursor control (see Figure 2a), or EEG
rhythms that change with movement
or imagination of movement and are
spontaneous in the sense they do not
require specific stimuli to occur. Peo-
ple learned to vary their SMRs to move
a cursor to hit one of two targets on the
top or bottom edge of a video screen.
Signals from the brain are acquired by electrodes on
the scalp or head and processed to extract specific Cursor movement was controlled by
signal features reflecting the user’s intent. These SMR amplitude (measured by spectral
features are translated into commands to operate analysis). A distinctive feature of this
a device. Users must develop and maintain good
task is that it required users to rapidly
correlation between their intent and the BCI’s signal
features. The BCI must select and extract features switch between two states to select a
the user can control, translating them into device particular target. The rapid bidirec-
commands (adapted from Wolpaw et al.36). tional nature of the Wolpaw et al.38
paradigm made it distinct from prior
studies that produced long-term uni-

figure 2. Current human BCI systems.

A and B are noninvasive, and C is invasive. A. In a sensorimotor rhythm BCI, scalp EEG is
recorded over sensorimotor cortex; users control the amplitude of rhythms to move a cursor
to a target on the screen. B. In a P300 BCI, a matrix of choices is presented on screen, and
scalp EEG is recorded as these choices flash in succession. C. In a cortical neuronal BCI,
electrodes implanted in the cortex detect action potentials of single neurons; users learn to
control the neuronal firing rate to move a cursor on screen (adapted from Wolpaw et al.36).

(a) sensorimotor Rhythms (b) P300 evoked Potential (c) Cortical neuronal activity
Power
Pz Induction Transmitter
4 –50
Cement
other choices Skull Bone Gold wire

3 0
amplitude (μV)

Top Target
Voltage (a/d u)

desired choice
Cortex

2 50 Glass
Neurites cone
100 μV

1 100 Row of Neurons

0.5 s

Bottom Target 100 μV

0 150
20 s
0 5 10 15 20 25 30 –100 0 100 200 300 400 500
frequency (hz) time (ms) On
Top Target 10 μV
On Off On Off Off

1 sec
Bottom Target

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 contributed articles

directional changes in brain rhythms; encephalography (MEG),20 functional by the algorithm the BCI is using. It
for example, users were required to magnetic resonance imaging (fMRI),28 is thus not possible to predict results
maintain an increase in the size of an and near-infrared systems (fNIR).4 precisely from offline analyses that
EEG rhythm for minutes at a time. In Current technology for recording cannot account for these effects.
a series of subsequent studies, this MEG and fMRI is both expensive and Blankertz et al.3 identified several
group showed that the signals control- bulky, making it unlikely for practical trends in the results of a BCI data-
ling the cursor were actual EEG activity applications in the near term; fNIR is classification competition. Most win-
and that covert muscle activity did not potentially cheaper and more com- ning entries used linear classifiers,
mediate this EEG control.18,31 pact. However, both fMRI and fNIR are the most popular being Fisher’s dis-
These initial SMR results were sub- based on changes in cerebral blood criminant and linear support vector
sequently replicated by others21,24 and flow, an inherently slow response.11 machines (SVMs). The winning entries
extended to multidimensional con- Electrophysiological features repre- for data sets with multichannel oscil-
trol.37 These P300 and SMR BCI stud- sent the most practical signals for BCI latory features often used common
ies together showed that noninvasive applications today. spatial patterns. In their review of the
EEG recording of brain signals can literature on BCI classifiers, Lotte et
serve as the basis for communication- system Design al.16 concluded that SVMs are particu-
and-control devices. Communication-and-control applica- larly efficient, attributing the efficien-
A number of laboratories have ex- tions are interactive processes requir- cy to their regularization property and
plored the possibility of developing ing users observe the results of their immunity to the curse of dimensional-
BCIs using single-neuron activity de- effort to maintain good performance ity. They also concluded that combina-
tected by microelectrodes implanted and correct mistakes. For this reason, tions of classifiers seem efficient, not-
in the cortex12,30 (see Figure 2c). Much BCIs must run in real time and provide ing a lack of comparison of classifiers
of the related research has been done real-time feedback to users. While within the same study using otherwise
in non-human primates, though trials many early BCI studies satisfied this identical parameters.
have also been done with humans.12 requirement,24,38 later studies were Muller and Blankertz21 advocated a
Other studies have shown that record- often based on offline analyses of pre- machine-learning approach to BCIs in
ings of electrocorticographic (ECoG) recorded data1; for example, the Lotte which a statistical analysis of a calibra-
activity from the surface of the brain et al.16 review of studies evaluating BCI tion measurement is used to train the
can also provide signals for a BCI15; signal-classification algorithms found system. The goal is to develop a “zero-
to date they indicate that invasive re- most used offline analyses. Indeed, training” method providing effective
cording methods can also serve as the the current popularity of BCI research performance from the first session,
basis for BCIs. Meanwhile, important is probably due in part to the ease of- contrasting it with one based on train-
issues concerning their suitability for fline analyses are performed on pub- ing users to control specific features
long-term human use have yet to be licly available data sets. While such of brain signals.38 A system that can
resolved. offline studies may help guide actual be used without extensive training is
Earlier studies demonstrating oper- online BCI investigations, there is no appealing since it requires less initial
ant conditioning of single units in the guarantee that offline results will gen- effort on the part of both the BCI user
motor cortex of primates,9 hippocam- eralize to online performance. Users’ and the system operator. Operation
pal theta rhythm of dogs,2 and senso- brain signals are often affected by BCI of such a system is based on the as-
rimotor rhythm in humans29 showed outputs that are in turn determined yet uncertain premise that users can
brain activity could be trained with
operant techniques. However, these figure 3. three approaches to BCI design.
studies were not demonstrations of
BCI systems for communication and
Let the Machines Run Operant Conditioning Optimized Co-Adaptation
control since they required subjects
to increase brain activity for periods
of many minutes, showing that brain User User User
activity could be tonically altered in
a single direction through training.
However, communication-and-control
devices require that users be able to
select from at least two distinct alter-
natives; that is, there must be at least BCI System BCI System BCI System
one bit of information per selection.
Effective communication-and-control
devices require users to rapidly switch
between multiple alternatives. Arrows indicate the element that adapts; the BCI, the user, or both adapt
to optimize and maintain BCI performance (adapted from McFarland et al.17).
In addition to electrophysiological
measures, researchers have also dem-
onstrated the feasibility of magneto-

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contributed articles

repeatedly and reliably maintain the suggested that cognitive tasks (such ger necessary to operate a sensorimo-
specified correlations between brain as navigation and auditory imagery) tor rhythm-based BCI. As is typical
signals and intent. Figure 3 outlines might be more useful in driving a BCI of many simple motor tasks, perfor-
three different conceptualizations of than motor imagery. However, senso- mance becomes automatized through
where adaptation might take place to rimotor rhythm-based BCIs may pro- extended practice. Automatized per-
establish and maintain good BCI per- vide several advantages over systems formance may be less likely to inter-
formance: In the first, the BCI adapts that depend on complex cognitive op- fere with mental operations users
to the user; in the second, the user erations; for example, the structures might wish to engage in concurrent
adapts to the BCI; and, in the third, involved in auditory imagery are also with their BCI use; for example, com-
user and system adapt to each other. likely to be driven by auditory sen- posing a manuscript is much easier
A number of BCI systems are de- sory input. Wolpaw and McFarland37 if the writer does not need to think
signed to detect user performance of reported that with extended practice extensively about each individual key-
specific cognitive tasks. Curran et al.3 users report motor imagery is no lon- stroke.
As noted, EEG recording may be
figure 4. BCI2000 design consists of four modules: operator, source, signal processing,
contaminated by non-brain activity
and application.
(such as line noise and muscle activ-
ity); see Fatourechi et al.8 for a review.
operator
Activity recorded from the scalp rep-
resents the superposition of many
System Configuration Visualization
signals, some originating in the brain,
some elsewhere. These signals include
potentials generated by retinal dipoles,
or eye movement and blinks, and facial
muscles. It is noteworthy that mental
Source effort is often associated with changes
Brain Signals Signal Control Signals User in eye-blink rate and muscle activity.35
Processing Application BCI users might generate these arti-
Event Markers Event Markers
Storage facts without being aware of what they
are doing simply by making facial ex-
pressions associated with effort.
Event Markers Facial muscles can generate sig-
Operator deals with system configuration and online presentation of results to the
nals with energy in the spectral bands
investigator; during operation, information is communicated from source to signal processing used as features in an SMR-based
to user application and back to source (adapted from Schalk et al.25). BCI18 Muscle activity can also modu-
late SMR activity; for example, users
can move their right hands in order
to desynchronize the mu rhythm over
the left hemisphere. This sort of me-
diation of the EEG through peripheral
muscle movements was a concern in
the early days of BCI development.
As noted earlier, Dewan6 trained us-
ers to send Morse code messages us-
ing occipital alpha rhythms modu-
lated by voluntary movements of eye
muscles. For this reason, Vaughan
et al.33 recorded EMG from 10 distal
limb muscles, while BCI users used
central mu or beta rhythms to move
a cursor to targets on a video screen.
EMG activity was very low in these
well-trained users. Most important,
the correlations between target po-
sition and EEG activity could not be
accounted for through EMG activity.
Similar studies have been done with
BCI users moving a cursor in two di-
mensions,37 showing that SMR modu-
figure 5. hardware in the Wadsworth Center’s home BCI system, including 16-channel
electrode cap for signal recording, solid-state amplifier, laptop, and additional monitor
lation does not require actual move-
as user display. ments or muscle activity.

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 contributed articles

applications options of practical value mainly for

Several recent BCI spelling systems people severely limited in their motor
are based on different EEG signals, skills and thus have few other options.
including the mu rhythm22,26 and the Widespread use of BCI technology by
P300.31 The Mu rhythm systems made individuals with little or no disability
use of machine-learning paradigms sensorimotor is unlikely in the short-term and would
that minimized training, with users
of both mu-based systems reportedly
rhythm-based require much greater speed and accu-
racy than has so far been demonstrat-
averaging between 2.3–7 characters/ BCIs may provide ed in the scientific literature.
minute22 and 2.85–3.38 characters/
minute.26 The P300 system averaged
several advantages Noninvasive and invasive methods
would both benefit from improved
3.66 selections/minute.31 Townsend et over systems recording methods. Current invasive
al.24 noted the reported rate depends
on how the figure is computed, but
that depend on methods do not deal adequately with
the need for long-term performance
study authors do not always provide complex cognitive stability. The brain’s complex reac-
details. Omitting time between trials tion to an implant is still imperfectly
increased Townsend et al.31 results operations. understood and might impair long-
from 3.66 to 5.92 characters/second. term performance. Noninvasive EEG
In any case, these systems perform electrodes require some level of skill
within a similar general range. At cur- in the person placing them, as well as
rent BCI character rates, only users in periodic maintenance to ensure suf-
with limited options could benefi. ficiently good contact with the skin;
BCI systems have also been de- more convenient and stable electrodes
veloped for control applications; for are under development. Improved
example, several groups have shown methods for extracting key EEG fea-
that human subjects can use their EEG tures and translating them into device
activity to drive a simulated wheel- control, as well as user training, would
chair.10,14 Bell et al.1 showed the P300 also help improve BCI performance.
could be used to select among complex Recent developments in computer
commands to a partially autonomous hardware provide compact portable
humanoid robot; for a review of the systems that are extremely powerful.
use of BCI for robotic and prosthetic Use of digital electronics has also led
devices see McFarland and Wolpaw.19 to improved size and performance of
Several commercial concerns re- EEG amplifiers. Thus it is no longer
cently produced inexpensive devices necessary to use a large time-shared
purported to measure EEG. Both Emo- mainframe, as it was with Vidal34; stan-
tiv and Neurosky developed products dard laptops easily handle the vast ma-
with a limited number of electrodes jority of real-time BCI protocols. Sig-
that do not use conventional gel-based nal-processing and machine-learning
recording technology27 and are intend- algorithms have also been improved.
ed to provide input for video games. Coupled with discovery of new EEG
Not clear is the extent to which they use features for BCI use and development
actual EEG activity, as opposed to scalp- of new paradigms for user training,
muscle activity or other non-brain such improvements are gradually in-
signals. Given the well-established creasing the speed and reliability of
prominence of EMG activity in activity BCI communication and control, de-
recorded from the head, it seems likely velopments facilitated by the BCI2000
that such signals account for much of software platform.25
the control these devices provide.27 BCI2000 is a general-purpose re-
search-and-development system in-
Conclusion corporating any brain signal, signal-
In a review of the use of BCI technology processing method, output device,
for robotic and prosthetic devices, Mc- and operating protocol. BCI2000
Farland and Wolpaw19 concluded that consists of a general standard for cre-
the major problem facing BCI applica- ating interchangeable modules de-
tions is how to provide fast, accurate, signed according to object-oriented
reliable control signals, as well as other principles (see Figure 4), including a
uses of BCIs. Current BCI systems that source module for signal acquisition,
operate using actual brain activity can signal-processing module, and user-
provide communication-and-control application module. Configuration

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contributed articles

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James S. McDonnell Foundation. We 19. McFarland, D.J. and Wolpaw, J.R. Brain-computer Department of Health, Albany, NY.
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script. based brain-computer interface (BCI). Neuroimage Repair in the Wadsworth Center of the New York State
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