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Cortical potentials related to voluntary and passive finger movements recorded from subdural electrodes in humans.

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Cortical Potentials Related to Voluntary
and Passive Finger Movements Recorded
from Subdural Electrodes in Humans
B. 1. Lee, MD," H . Liiders, MD,? R. P. Lesser, MD,? D. S. Dinner, MD,i and H. H. Morris, 111, MD'F
Movement-related potentials were recorded from subdural electrodes placed on the precentral and postcentral cortex
in 3 patients undergoing operation for intractable epilepsy. With self-initiated index finger movement, a negative
potential of 25 to 50 microvolts in amplitude, preceding onset of the electromyographic activity by 60 to 95 ms (or
onset of movement by 150 to 230 ms), was recorded from the hand somatosensory postrolandic area in all 3 patients. A
similar potential preceding the movement was recorded from the precentral hand motor area in one subject who was
the only patient in whom the precentral electrodes were placed on the hand motor area. Following active and passive
movements, a clearly defined positivity (18 to 32 ms after a photometer trigger) that reversed phase across the central
fissure was recorded. The premovement potentials are most probably generated by pyramidal tract neurons and motorfunction-related neurons located in the post- and prerolandic areas. The postmovement positivity is most probably due
to short-latency kinesthetic reafferent activation of the posterior bank of the central fissure (equivalent to Pz of the
somatosensory evoked potentials).
Lee BI, Luders H, Lesser RP, Dinner DS, Morris HH: Cortical potentials related to voluntary and passive
finger movements recorded from subdural electrodes in humans. Ann Neurol 20:32-37, 1986
Since Kornhuber and Deecke {12} demonstrated cerebral potentials preceding voluntary movement by using opisthochronic averaging techniques in 1965 (that
is, averages of activity prior to and after a trigger), it
has been recognized that movement-related potentials
(MRPs) consist of various distinct components 14, 5,
10, 21, 223. Three potentials preceding voluntary
movements have been distinguished when recording
from the human scalp: Bereitschaft's potential, premovement positivity, and motor potential E4, 53. The
motor potential has been defined as a negativity
superimposed on the Bereitschaft's potential which
starts approximately 60 ms prior to the first muscle
action potential. This has been thought, on the basis of
scalp recordings, to be of highest amplitude in the
contralateral rolandic area { S ] , and it has been
speculated that the motor potential reflects activation
of the prerolandic motor cortex during its generation
of the pyramidal tract volley C4, 21, 22).
However, recordings from scalp do not permit accurate localization of neural generators and there are
only a few reports of MRPs recorded from human
cortex [ 11, 19, 20). In this manuscript, we report on
MRPs recorded from long-term implanted subdural
electrodes covering precentral and postcentral cortex
in patients who were candidates for surgical treatment
of epilepsy.
From the "Department of Neurology, Indiana University Medical
Center, Indianapolis, IN, and ?Department of Neurology, Cleveland Clinic Foundation, Cleveland, OH 44 106.
Address reprint requests to Dr Lee, Department of Neurology, I. U.
Riley Hospital, Room A599N, 702 Barnhill Dr, Indianapolis, IN
Received June 11, 1985, and in revised form Oct 11. Accepted for
publication Oct 28, 1985.
Three patients were included in this study. Patients 1 and 3
were suffering from chronic complex partial seizures that
were intractable to medical treatment. Results of neurological examination and the computed tomographic (CT) scan of
the head were normal in both patients. Patient 2 had experienced recent onset of focal motor seizures involving the right
face, with occasional secondarily generalized tonic-clonic sei-.
zures. Results of neurological examination were normal. C'I'
scan of the head revealed a small radiolucent lesion in the left
central area, which subsequently proved to be a grade I1
astrocytoma. In all 3 patients, subdural electrode plates were
implanted to establish with precision the spatial distribution
of the epileptogenic focus and of adjacent functional areas
(Fig 1).The study was explained to the patients, with consent
obtained by procedures approved by our Institutional Review Board.
Materials and Methods
The subdural electrode plates consisted of 8 x 8 arrays of
stainless steel electrodes, 3 mm in diameter, and with a center-to-center interelectrode distance of 1 cm. These electrodes were embedded in 1.5-mm-thickness Silastic rubber.
The electrodes were identified by a common terminology
@ Aphasia
0 Upper extremity
f) Hand
@ Face
Fig 1. Diagram of electrode nomenclature i n Patient I . Columns
of e1ectrode.r are labeled A through H from front t o back. In each
column, electrodes are labeled 1 through 8 from top to bottom.
The diagram was copied from lateral skull x-ray films. Filled
circles represent motor responses, dotted circles represent somatosensory responses, diagonally lined circles represent speech arrest, and
cross-hatched circles represent negative motor responses (cessation
of ongoing voluntary moziements during electrical stimulation
{14, 16). obtained by electrical stimulations of each electroh).
Circle1 indicate the anatomical representation ofthe cortex cwered by electrodes,e.g., electrical stimulation of electrode DS
elicited negative motor responses in the contralateral hand and
face areas. Moflement-relatedpotentials shown in Figure 2 were
recorded from the electrodes shown inside the squares.
that lettered the vertical columns alphabetically from anterior
to posterior and numbered the horizontal rows consecutively
from superior to inferior (Fig 1). The method of placement
of the subdural electrode plates and the methods of electrical
stimulation for the functional localization of the underlying
cortex have been described previously C13, 151. In all subjects, at least one electrode was located over the postcentral
somatosensory area of the hand. However, the precentral
hand motor area was covered in onIy 1 patient (Patient 2).
Voluntary and passive finger movements were produced
according to the technique described previously by Shibasaki
et a1 [21,22], with minor modifications. For voluntary extension of the index finger, the subjects sat in a comfortable
chair with the contralateral forearm placed on an arm rest
and were asked to make a brisk extension of the index finger
at the metacarpophalangeal joint followed by a slow return
movement to the resting position by relaxing the extended
finger. The extent of the movement was approximately 10 to
20 degrees. The movement was repeated at a self-paced variable rate with at least 5 sec between movements. Movements
repeated at intervals shorter than 5 sec were automatically
excluded from averaging. Each session was composed of 200
trials. Voluntary extension of the contralateral index finger
was performed in all 3 subjects, but extension of the ipsilateral index finger was performed only in Patient 3.
Passive extension of the contralateral index finger at the
metacarpophalangeal joint was performed by the examiner
pulling up a string bound around the distal portion of the
subject’s index finger. The string was approximately 10 cm
long and kept slightly stretched between movements in order to avoid a shock effect in the finger. The movements
were repeated at intervals exceeding 5 sec at an irregular rate
paced by the examiner, again with shorter intervals automatically excluded. Each session was composed of 200 trials in
Patient 1 and 100 trials in Patient 2. Passive movement was
not performed in Patient 3.
A trigger pulse was obtained by using a photometer. A
narrow beam of light was projected onto a photocell and the
index finger was placed so that raising the finger tip interrupted the photobeam and triggered the averager. An electromyogram (EMG) was recorded from a pair of silver-silver
chloride-cup electrodes fixed with collodion that were placed
about 3 cm apart on the skin overlying the contracting extensor indicis muscle in the forearm. In addition, in Patient 3
the movement of the index finger was recorded by an accelerometer attached to the moving finger. Seven channels of
electrocorticogram and one channel of EMG or finger movement (accelerometer) were averaged with an opisthochronic
averaging program employing the photometer pulse as a
trigger, using a Nicolet Pathfinder 11. Trials in which artifact exceeded a threshold voltage preset by the computer
operator were automatically rejected by the computer. The
reference electrode used in the electrocorticogram was the
scalp vertex electrode (CJ. The band width of filters used in
both voluntary and passive finger movements was from DC
to 250 Hz in Patients 1 and 2, and 1 to 250 Hz in Patient 3.
For voluntary movement, the period averaged was 600 ms,
from 300 ms before to 300 ms after the trigger pulse. For
passive movement in Patient 1, the period averaged was 200
ms, from 50 ms before to 150 ms after the trigger pulse, and
in Patient 2, it was 300 ms, from 150 ms before to 150 ms
after the trigger pulse. The resultant waveforms were plotted
on an X - Y plotter. The latency of each component was
measured by a cursoring program, and the amplitude of each
component was measured from the baseline or from the
preceding peak of opposite polarity. The somatosensory cortical potentials, evoked by electrical stimulation of the contralateral median nerve at the wrist, were recorded from the
same subdural electrodes used in the recording of MRPs.
These procedures have been described in detail previously
A clearly defined, extremely localized negative potential preceding the onset of the EMG activity was recorded from electrodes placed in the postcentral
somatosensory area for the hand in all subjects (Figs
2-4). In Patient 2, who was the only patient with precentral electrodes over the hand motor area, the negative potential was also recorded from the electrodes on
the precentral hand motor area (Fig 3). In contrast, no
potentials preceding the EMG onset were recorded
from other electrodes placed on the precentral motor
and postcentral somatosensory areas for the face, eyes,
and upper arm.
In Patients 1 and 2, the onset of this negative potential occurred 60 to 95 ms prior to the onset of EMG
Lee et al: Cortical Motor Potentials in Humans
, -<
- 300
F i g 2. Corticalpotentials associated with voluntary, selj-paced,
contralateral index finger extension recorded from subdural electrodes placed in front o f and behind the central fissure in Patient
1. In this and the following figures. the centralfissure was
defined by the results of electrical stimulation of the cortex. The
upward dejection of potentials indicates negativity ( - ) and
downujard deflection indicates positizity ( f ). (EMG = electromyogram.)
activity or 150 to 170 ms before the photic trigger.
The peak latency of the initial negativity was close to
the peak latency of the EMG activity and was 33 to 44
ms before the photic trigger. The initial negative wave
recorded from the postcentral hand somatosensory
area consisted of an upgoing slope that became more
rapid at the time of EMG onset (Figs 2, 3). The negative potential recorded from Patient 3 showed somewhat earlier onset (230 ms before the photic trigger)
and a bell-shaped waveform, with the peak occurring
91 ms before the photic trigger.
In the postcentral cortex, the initial negativity was
followed by a large positive wave, with the highest
amplitude in the same electrode that showed the highest initial negativity. The peak latencies for postrolandic positivity were 30 ms in Patient 1 and 18 ms in
Patient 2. Over the precentral motor cortex in Patients
1 and 2, a surface negative potential occurred at a peak
latency identical with the postrolandic positivity. In
other words, this initial postmovement potential reversed polarity across the central sulcus. Patient 3
showed essentially no postmovement potentials in the
prerolandic area.
Potentials to voluntary movement of the ipsilateral
index finger were obtained only in Patient 3 and
34 Annals of Neurology
Vol 20
No 1 July 1986
- 300
+ 300
0 rnsec
Fig 3. Corticalpotentials associated with voluntary, selj-paced,
contralateral index finger extension recorded from subdural electrodes placed across the central fissure in Patient 2 (see legend for
Figure 2). This was the only patient in whom subdural electrodes roveredprecentral hand motor cortex (D, and E l ) . (EMG
= electromyogram.)
- 300
i I 2 5 ~
Fig 4. Corticalpotentials associated with voluntary, self-pared,
contralateral index finger extension recorded from subdural electrodes placed across the central fissure in Patient 3 (see legend for
Figure 2J.
12 47
t L1
Fig 5 . Cortical responses associated with passioe, contralateral
index finger extension in Patient 1 . The electrodes are the same
as in Fzgure 2 (see Figure 2 legend).
showed no negative porential preceding the movement. After the movement, low-amplitude but reproducible potentials occurred at the hand somatosensory
Potentials to passive movement of the contralateral
index finger were obtained in Patients 1 and 2. No
potentials preceding the finger movement were recorded in either subject. The first potential recorded
from the postcentral somatosensory cortex was a positive wave whose onset and peak latencies were 4 to
34.8 ms before and 12 to 3.6 ms after the photometer
trigger, respectively (Fig 5). The distribution of the
positive wave was similar to the first positive wave
recorded during voluntary movement, and in Patient 1
there was evidence of phase reversal across the central
fissure (Fig 5). In the postcentral cortex, the initial
positivity was followed by a large negative potential
whose amplitude was 100 to 125 microvolts and which
had a peak latency of 38.4 to 47 ms after the photometer trigger.
Somatosensory evoked potentials to contralateral
median nerve stimulation were recorded from the
postcentral hand somatosensory cortex. In Patients 1
and 3, the typical initial negativity (N1) was followed
by a positivity (Pz) [15]. The peak latencies of the
components were approximately 20 ms and 23 ms,
respectively, after electrical stimulation of the contralateral median nerve. In Patient 1 both N1 and Pz
showed phase reversal across the central fissure (Fig 6).
In Patient 3, however, these potentials were not phase
reversed across the central fissure (similar to the postmovement potentials elicited by voluntary finger
movement in this patient).
MRPs recorded directly from subdural electrodes
demonstrated a negative potential preceding the onset
Fig 6. Cortical somatosensory potentials evoked by electrical
stimulation of the contralateral median newe at the wrist in
Patient 1 . The recording electrodes are similar t o those in Figure
2 (see Figure 2 legend).
of the self-initiated contralateral index finger movement. This potential was localized in the rolandic hand
area and started 60 to 95 ms prior to the EMG onset
(in Patients 1 and 2) or 150 to 230 ms befo;e the
photic trigger. Based on latency and distribution criteria we conclude that this premovement negative potential most probably corresponds to what has been described as motor potential in recordings from scalp
From the results obtained by recording MRPs with
scalp electrodes, it was previously concluded that the
motor potential is generated in the hand motor area [4,
5, 21, 221 and most probably is a reflection of the
firing of pyramidal tract neurons. This conclusion was
based on the approximate localization of the scalp recorded motor potential to the rolandic hand area and
on results published by Evarts [G, 7) that pyramidal
firing preceding movement occurs exclusively in the
precentral motor cortex. It was further supported by
previous reports of cortical recordings of MRPs in humans [l 1, 20) and trained monkeys [ 1-31. In contrast,
the results obtained in our study suggest a prominent
postrolandic contribution to the motor potential, a
conclusion supported by a number of recent reports.
Murray and Coulter [ 171 demonstrated that about
half of the pyramidal tract neurons in the primate brain
were located in the postcentral somatosensory cortex,
comprising Brodmann’s area 3, 1, 2, and in the adjacent area 5. The size and termination of the pyramidal
tract neurons in area 4,in the subdivisions of primary
sensory cortex, and in area 5 were different, suggesting
specialization of the neurons depending on their origin
and destination. Recently, Soso and Fetz [23] showed
that during active limb movements, about one-third of
the somatosensory neurons located in the postcentral
Lee et al: Cortical Motor Potentials in Humans
primary somatosensory Cortex, mainly areas 1 and 2,
change their activity 100 ms or more before the EMG
discharge of the agonist muscle. Fromm and Evarts [8,
91 also demonstrated by microelectrode recordings in
monkeys that pyramidal tract neurons in the postcentral somatosensory cortex discharged before the onset
of voluntary movement, and they suggested that the
postcentral somatosensory cortex is directly involved
with the initiation as well as control of movement.
Therefore, if the MP reflects the neuronal discharges
generating the corticospinal outflow, we would expect
to record it from both precentral motor and postcentral somatosensory cortex.
Only a few cortical recordings of MRPs from human
beings have been reported Ell, 19, 201. The cortical
recordings of MRPs by Papakostopoulos et al 1191
covered only three electrodes each on the prefrontal,
precentral, and postcentral cortex, and failed to demonstrate any localized electrical activity preceding the
movement consistent with motor potentials. Goldring
and Ratcheson { 1I} recorded premovement neuronal
activation from the contralateral hand motor area;
however, no recordings were performed from the
postcentral somatosensory cortex. The study by Pieper
et al[203 was also mainly concerned with recordings of
MRPs from the precentral motor cortex and area 6,
and only selected recordings were performed from the
postcentral somatosensory cortex. In addition, they
used a very long averaging period (3 to 8 seconds) and
a filter setting adequate for slow-frequency potentials
but which might obscure relatively higher-frequency
neuronal events occurring close to EMG onset. We
have no good explanation for the absence of postrolandic motor potentials during cortical recordings by
Arezzo and Vaughan { 1-31, However, although these
previous studies were not in good agreement with
ours, our results were consistent in all 3 patients
studied and were supported by other more recent
neurophysiological findings 18, 9, 17, 231.
In our study, the premovement motor potential was
followed by a prominent positive potential that phase
reversed across the central fissure and showed a peak
postrolandic positivity 18 to 32 ms after the photometer trigger. The potentials evoked by passive movement and by electrical stimulation showed an initial
postrolandic positivity that also phase reversed across
the central fissure. In the one case (Patient 3) in which
this initial postmovement potential showed no phase
reversal (probably due to oblique placement of the
plate which did not cover the hand prerolandic area),
the somatosensory evoked potential to median nerve
stimulation was also absent. All these results are consistent with the conclusion that this early postmovement positive potentid represents short-latency reactivation of the rolandic area, similar to the P2 wave of
36 Annals of Neurology
Vol 20
No 1 July 1986
the somatosensory evoked potential obtained by electrical stimulation, which was previously interpreted by
Liiders et al [lS} as the reflection of kinesthetic sensory projections to areas 4,3a, 1, and 2.
As mentioned previously, during passive index
finger movement, the initial potential recorded from
the postcentral cortex was a positive wave that phase
reversed across the central fissure. This initial positive
potential over the postcentral cortex during passive
finger displacement was also a very consistent feature
in the study by Papakostopoulos et al[18}. In addition,
direct cortical recordings of evoked potentials elicited
by mechanical stimulation of the fingertip demonstrate
a positive potential as the initial component [24}.
Thus, the initial component of short-latency somatosensory potentials evoked by mechanical stirnulation
seems to be a surface positivity equivalent to P2 of
the electrically evoked somatosensory evoked potentials. The absence of a preceding negative potential
(similar to wave N1 of the somatosensory evoked PO-.
tential) during passive finger movement could be due
to relatively poor synchronization of the finger movements compared with the precise synchronization of
the electrical stimulation of median nerve. However, it
is also possible that the absence of N1 is related to
different modalities of nerve stimulation: N1 and P2
are apparently generated by afferent fibers of different
sizes reaching different cortical areas (area 3b and areas
1, 2, and 4,respectively) {lS].
Originally presented at the International Symposium on Somatosensory Evoked Potentials, Kansas City, MO, Sept 22, 1984.
We thank B. Rossa, N. Kane, and G. Klem for their assistance.
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Lee et al: Cortical Motor Potentials in Humans
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