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Motor Systems NeuroReport

NeuroReport 10, 1767±1771 (1999)

THE feasibility of using the EEG signal to operate a


hand grasp neuroprosthesis was investigated. Two able- EEG-based control of a
bodied subjects and one neuroprosthesis user were
trained to control the amplitude of the beta rhythm hand grasp
recorded over the frontal areas. After 6 months, all
subjects exhibited a high level of control, being able to neuroprosthesis
use this signal to move a cursor to targets on a
computer screen with a high (. 90%) accuracy rate.
Control over the EEG signal was unaffected by upper
Richard T. Lauer,CA P. Hunter Peckham
extremity movement or electrical activation of the and Kevin L. Kilgore
muscles, indicating that this signal would be adequate
for neuroprosthetic use. To test this concept, the
neuroprosthesis user operated his system with the
Case Western Reserve University, FES Center of
cortical signal, and was able to effectively manipulate Excellence, Cleveland VA Medical Center,
several objects. NeuroReport 10:1767±1771 # 1999 Lip- Hamann 601, MetroHealth Medical Center, 2500
pincott Williams & Wilkins. MetroHealth Drive, Cleveland, OH 44109, USA

Key words: Command±control; Electroencephalogram;


Neuroprosthesis CA
Corresponding Author

Introduction the motor cortex. They observed that a neuron in


the motor cortex will ®re in response to a given
Functional neuromuscular stimulation (FNS) has direction or muscle action, and by recording from
restored functional hand grasp in individuals who these neurons, it is possible to reconstruct the
have sustained a spinal cord injury at the ®fth or desired movement. One goal of this research, still in
sixth cervical level. The current hand grasp neuro- the early fundamental research stage, would be to
prosthesis developed at Case Western Reserve Uni- use this complex signal to operate a neuroprosthesis.
versity and the Cleveland VA Medical Center [1±5] The use of intracortical signals to operate the
electrically excites the muscles of the forearm and neuroprosthesis is attractive since it would allow for
hand to provide the user with two possible grasp a more natural operation of the hand by restoring
patterns. The control over the degree of hand open- the link between the brain and hand movements.
ing and closing is provided by either an external [5] Another possible method of using the brain signals
or implanted [6] transducer mounted at the shoulder to operate the neuroprosthesis is the EEG recorded
or wrist. However, as the neuroprosthesis continues from the scalp using surface mounted electrodes.
to develop to allow its implementation in both arms This has several advantages over the use of the
or implantation in persons with a higher cervical intracortical recordings. First, it is non-invasive and
level injury, the need for other methods of control- second, it would allow for a more rapid implementa-
ling the system becomes greater. tion into the current neuroprosthesis. Wolpaw et al.
There are currently several options for the control [15,16] and Pfurtscheller et al. [17] have demon-
of the neuroprosthesis besides the use of shoulder or strated that subjects can be trained to voluntarily
wrist motion. These include muscle activation [1], control the amplitude of a speci®c frequency com-
head movement [7], respiration control [8] and voice ponent of the EEG. This signal has been used to
control [9]. Another method which has been pro- move a cursor on a computer screen, which is the
posed is the use of signals recorded through the use basis of an assistive communication device for those
of intracortical electrodes. Kennedy et al. [10,11] persons with severe physical disabilities (i.e. ALS
have successfully developed and implanted an elec- and stroke).
trode into the cortex of an individual with amyo- Birbaumer et al. [18,19] have also investigated the
trophic lateral sclerosis (ALS) to allow him to use of cortical signals recorded from surface
operate a computer cursor. These signals might have mounted electrodes. However, their studies differ
future applications in controlling electrically stimu- from those of Wolpaw and Pfurtscheller in that the
lated muscles. focus is on the self-regulation of slow cortical
Other investigators [12±14] have also studied the potentials instead of a speci®c frequency component
signals which can be acquired from the neurons of of the EEG. Birbaumer and his group have success-

0959-4965 # Lippincott Williams & Wilkins Vol 10 No 8 3 June 1999 1767


NeuroReport R. T. Lauer, P. H. Peckham and K. L. Kilgore

fully developed a thought translation device (TDD) 10) was used to generate cursor movement. One (or
which allows individuals in a locked-in state to two) of the electrodes constituted the recording sites
communicate by selecting letters with the slow used to drive cursor movement, while the remaining
cortical potential to form words. four (or eight) electrodes were used to provide
The objective of this study was to develop an spatial ®ltering. The recording sites used for each of
EEG-based controller for use with the neuroprosth- the subjects are presented in Table 1.
esis based upon the system developed by Wolpaw. Subjects were trained to control the amplitude of
To investigate the feasibility of this approach, three the beta rhythm. The beta is the 18±40 Hz compo-
studies were conducted: training of both able-bodied nent of the EEG signal recorded primarily from the
subjects and neuroprosthesis users to control the frontal and somatomotor cortices. For the subjects
beta rhythm recorded from the frontal cortex; in this study, the beta band was restricted to be-
evaluating interference with the EEG control signal tween 25 and 28 Hz. Training for each subject
introduced by factors such as extremity movement involved 1±3 sessions per week. Each session con-
and artifacts of electrical stimulation; and developing sisted of eight runs which were 3 min in duration
an interface between the EEG signal and the neuro- with a 1 min break between runs. During the course
prosthesis. of a given run the subject was presented with 30±35
targets generated randomly, depending upon the
skill and speed of the subject. The initial sessions
Materials and Methods were used to determine what mental states caused
Subjects: Three subjects (two able-bodied and one movement of the cursor up and down. These usually
neuroprosthesis user) ranging in age from 27 to 40 involved the subject focusing upon the cursor or
participated in these studies. The neuroprosthesis target to make the cursor move up, and relaxing to
user was male, while in the able-bodied group, one make the cursor move down. As training progressed,
was male and one was female. All subjects were subjects were able to move the cursor by thinking of
asked to read and sign an informed consent form the appropriate direction.
which was approved by the Institutional Review
Board of MetroHealth Medical Center before parti- Neuroprosthetic issues: The second stage of the
cipation in the study. study involved addressing issues relevant to using
the EEG to operate the neuroprosthesis: can the
Beta rhythm control: The instrumentation and pro- subject control the EEG signal while generating
tocols used for the training of the subjects to control limited movements of the upper extremity; and will
the amplitude of the beta rhythm were similar to the stimulation of the muscles provided by the
those used by Wolpaw et al. to control the mu neuroprosthesis interfere with the operation of cur-
rhythm [12]. Only a preliminary description of the sor movement?
methods and of the brain±computer interface (BCI) To address the ®rst question, each able-bodied
are provided since these have been covered exten- subject was asked to perform the following experi-
sively in previous publications [20,21]. ment. The subject was seated in front of the
The subject was seated in an upright position computer monitor, as before. However, on the table
facing a computer monitor upon which appeared were also placed a white line which corresponded
targets at the top and bottom of the screen and a with the midline of the subject and a 0.5 kg weight.
cursor which they could control. Sixty-four electro- The session began with the subject moving the
des mounted in a cloth cap (Electro-Cap Interna- cursor to targets appearing on the computer screen.
tional, Inc.) were placed on the scalp, the spacing However, the length of the run was decreased to
and location based on a modi®ed 10-20 system. The 2 min and the targets appeared in a ®xed pattern.
output from each of the electrodes was referenced to After completing two runs, the subject was then
the right ear, and the ground was located behind the instructed to reach out for the weight and grasp it
ear on the mastoid process. Referential recordings with the right hand, move the weight across the line,
are used in this case to maximize the amplitude of
the EEG signals being recorded. The signal recorded Table 1. Location of the recording sites for the frontal beta
from each of the electrodes was ampli®ed (320 000) rhythm. The designations are based on the modi®ed 10-20
system. The beta rhythm was recorded from two sites in subject
and bandpass ®ltered (1±35 Hz). The output from AB-1. In the other subjects, only one site was used
the ampli®er was sent to two computers. One
Subject Recording site
computer stored the raw EEG signal for later off-
line analysis. The second computer was responsible AB-1 F3 and F4
for the conversion of the EEG signal into cursor AB-2 FP1
NP-1 F3
movement. From the 64 electrodes, a subset of 5 (or

1768 Vol 10 No 8 3 June 1999


EEG-based control of a hand grasp neuroprosthesis NeuroReport

release the weight and return their hand to their lap. neuroprosthesis. When the signal was maintained
They were to continue to do this at a self pace that above a preset threshold, this generated the com-
was comfortable while moving the cursor to targets mand to go from hand opening to hand closing. The
on the screen. This continued for the entire 2 min rate at which the hand closed was ®xed (,2±3 s to
run. In the next run, the subject was instructed to full closure), and was only generated when the
repeat the same movement with the left hand. The amplitude of the input signal was maintained above
series of non-movement, right side movement, and the threshold. When the signal fell below the thresh-
left side movement was then repeated twice more, old, the hand stopped closing. To go from the hand
for a total of nine runs. For the neuroprosthesis closed to the hand open position, the signal must be
user, this protocol was modi®ed slightly since he below a preset low threshold, which generated the
was unable to grasp the weight and move it when command to go from hand closed to hand open at a
his system was off, but could move the proximal much faster rate than hand opening (,1 s to full
joints (i.e. shoulder and elbow). Therefore, move- opening).
ment was restricted to reaching out and touching The use of the gated ramp only allowed for
the weight. All other aspects of the study were the dynamic hand operation. Therefore, the subject was
same. only asked to perform simple activities of daily
To address the second issue, the neuroprosthesis living with the system. These tasks included picking
user was asked to turn his system on and lock his up and moving a weight, grasping and releasing a
hand in an open or closed position, and then fork, and grasping and releasing a cup. The subject
proceeded with a normal training session. The was also asked to open and close his hand using the
system was turned off between runs in order to EEG signal as quickly as possible, and at the verbal
prevent fatigue of the muscles. command of the investigator. Finally, the subject
was also asked to open and close his hand in the
Neuroprosthetic control: Neuroprosthetic operation absence of visual feedback (i.e. not looking at the
with the EEG signal was implemented to demon- hand to determine whether it was open or closed).
strate the feasibility of this control method. The
BCI system was modi®ed to allow the signal which
is used to drive the cursor movement to be sent out
Results
of the computer through the serial port into a Beta rhythm control: The ability of the subjects to
second computer. The second computer, running a control the amplitude of the beta rhythm, as meas-
routine written using the LabVIEW programming ured in accuracy rate, is shown in Fig. 2. The
language, provided additional signal processing and subjects accuracy rate is plotted as a function of time
conversion of the EEG signal into a command for (training session). The neuroprosthesis user is given
the neuroprosthesis. The experimental setup for the the designation NP-1, while the two able bodied
hybrid system in shown in Fig. 1. subjects are given the designations AB-1 and AB-2.
The EEG signal was converted into a command During the 6-month period the subjects participated
signal using the gated ramp method. This method in 10±20 training sessions. By the end of this time,
has been used previously [7] for the conversion of all three subjects were able to achieve excellent
the myoelectric signal into a command for the control over the beta rhythm, achieving on a con-
sistent basis an accuracy rate . 90%. Subject NP-1

PC EEG
signal amplifier 100
processing Electrode 95
matrix 90
Accuracy (%)

85
80 AB-1
PC
75 AB-2
signal Display 70
Implanted NP-1
conversion stimulator 65
60
External 55
control 50
0 5 10 15 20
unit Session

FIG. 1. Schematic showing the components of the EEG-based control- FIG. 2. Plot of subject accuracy over time. Accuracy rate in hitting the
ler for the FNS hand grasp system. This system allowed for the targets on the computer screen with the cursor is a measure of the
conversion of the raw EEG signal into a command-control signal for the degree of control each subject has over the beta rhythm. Subject
neuroprosthesis to provide the subject with hand opening and closing by accuracy rates reached a plateau of . 90% after just six training
thinking about it. sessions.

Vol 10 No 8 3 June 1999 1769


NeuroReport R. T. Lauer, P. H. Peckham and K. L. Kilgore

achieved an average accuracy rate of 94.2  4.2% of the wrong direction, and thus generate the
(s.d.), subject AB-1 achieved an accuracy rate of opposite command to the neuroprosthesis. Another
95.0  4.3% and subject AB-2 achieved an accuracy dif®culty encountered was the fact that the algo-
rate of 90.9  4.1%. Figure 2 shows that there was a rithm used did not provide a means by which the
learning period involved for all subjects. This period subject could lock his hand in the closed position
of time is restricted to the ®rst six sessions (,2±3 once the object was acquired. Therefore, the subject
weeks). Control over the beta rhythm was main- had to continually think `hand closed' while manip-
tained at a consistent accuracy rate for as long as 17 ulating the object, which the subject stated was
weeks in subject NP-1 and for at least 8 weeks in all increasingly dif®cult as the session went on (,1.5±
subjects. 2 h testing).

Neuroprosthetic issues: Table 2 shows the effect of


movement upon the subjects' ability to control the
Discussion
beta rhythm as measured in the accuracy rate. The The results from this study demonstrate that the
values given are the average accuracy rate from the EEG signal can be used to operate a neuroprosthesis
three runs in which that condition (non-movement, for the restoration of hand function. The fact that
right side movement, or left side movement) was the electrical stimulation of the muscles and remain-
maintained. From these data it can be concluded ing voluntary arm movement did not interfere with
that extremity movement had little effect upon the the quality of the control signal was important to
subjects' ability to control the EEG signal. For ascertain to validate further investigation in this area.
subject AB-1, there was no effect of movement upon If either of these factors had interfered with the
accuracy rate. For the other subjects, there was a quality of the EEG signal, then the feasibility of this
change in the accuracy rate; however, the difference as an alternative control signal would be greatly
between the averages was not statistically signi®cant limited.
(Student's t-test, á ˆ 0.005). There are several questions which need to be
The effects of neuroprosthesis operation upon addressed if frontal beta is to be used to operate the
beta rhythm control were also limited. The overall neuroprosthesis. First, since the signal is being
accuracy rate for subject NP-1 when the neuro- recorded from the frontal areas, there is the concern
prosthesis was active was 93.5  4.1%, which was that this is not `true' EEG control, but that the
only 0.7% lower than the subject's average accuracy subjects are using the electromyographic (EMG)
rate without the neuroprosthesis (94.2  4.2%). signal which can be generated by the frontalis
However, given the large standard deviations which muscles to generate cursor control. This possibility
exist under both conditions, the effect of the neuro- has been ruled out with these subjects since topo-
prosthesis upon beta rhythm control was not statis- graphic and spectral analyses of the EEG signal did
tically signi®cant (Student's t-test, á ˆ 0.005). not indicate the presence of muscle activity. Future
investigations will address this more fully. Second,
Neuroprosthetic operation: The neuroprosthesis the command±control algorithm used to convert the
user was able to manipulate all three objects using EEG signal into hand opening and closing only
the EEG-based controller with his neuroprosthesis. provided dynamic hand function, i.e. the hand was
To achieve hand opening, the subject was instructed either open or closed. To achieve full bene®ts from
to think of moving the computer cursor up, and to the neuroprosthesis, the user must be able to achieve
think of moving the cursor down to make his hand hand positions between either hand open or hand
close. The transition between thinking cursor move- closed, as well as have the ability to lock the hand in
ment and generating hand opening and closing place once a desired hand posture is achieved. These
required ,10 min of training. However, the subject issues will be addressed as the software and hard-
did state that there were times where he would think ware interfaces continue to evolve.
Finally, it is not known whether the EEG signal
will be able to provide multiple control signals to
Table 2. The effects of upper extremity movement upon beta allow for the operation of a bilateral neuroprosthesis
rhythm control. As before, the degree of beta rhythm control is (i.e. a hand grasp system implemented in both
measured by accuracy rate. For all subjects, there was little to
no effect of extremity movement upon beta rhythm control. hands). Studies by Wolpaw [16] indicate that sub-
jects can learn to independently control the EEG
Subject Non-movement Right Left
generated by each hemisphere. This would mean
AB-1 100% 100% 100% that one hemisphere could control the operation of
AB-2 91.5% 94.8% 96.1% one hand, independent of the other hemisphere.
NP-1 96.3% 92.1% 96.3%
However, these studies were conducted with the mu

1770 Vol 10 No 8 3 June 1999


EEG-based control of a hand grasp neuroprosthesis NeuroReport

rhythm recorded from the somatomotor cortex. neuroprosthesis. Subjects demonstrated that they
Whether this level of control can be achieved with could achieve a high degree of accuracy with the
the frontal beta rhythms has yet to be investigated. signal, and could maintain this level of accuracy
However, if this bilateral activation cannot be while generating voluntary movements or while the
achieved, there are still control algorithms which can neuroprosthesis is in operation. The answers to these
be implemented once the characteristics of the beta questions were critical in determining whether the
rhythm are better de®ned which would allow the EEG signal was feasible as a control source for the
subject to switch between the right and left hand neuroprosthesis. The results from the ®nal study
and use the same site to control hand function. demonstrate that the EEG signal is a feasible option
The results from this study provide information for controlling the neuroprosthesis. Further work is
that is not only useful for the ®eld of neuropros- underway to develop algorithms to convert the EEG
thetics, but also for assistive communication devices. signal into a neuroprosthetic control signal which
This study focused on training subjects to control the would allow subjects to maintain their hold upon an
beta rhythm component of the EEG recorded from object for a long period of time, as well as to
the frontal cortex to operate an external device (ini- provide ®ner control over the amount of hand
tially cursor movement, but later hand function via a opening and closing (i.e. to achieve positions be-
neuroprosthesis). The frontal beta rhythm was se- tween fully open and fully closed).
lected because there should be little effect of extre-
mity movement upon the subjects control of the
signal. The previous work in this area by Wolpaw References
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ment such a recording array with surgically placed ACKNOWLEDGEMENTS: This study was funded by the NIH Neural Prosthesis
subdermal electrodes and an external telemeter. Program, the Ron Shapiro Charitable Foundation, and the Movement Disorder
Foundation. This work was conducted in the FES Center, a consortium of CWRU, the
Cleveland VAMC, and MetroHealth Medical Center. The authors acknowledge Dr
Jonathan Wolpaw and Dr Dennis McFarland for their assistance in the start-up of
Conclusions these studies.

The analysis of the data indicates that the use of the Received 17 February 1999;
frontal beta rhythm is viable for operation of the accepted 13 April 1999

Vol 10 No 8 3 June 1999 1771

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