Summated human EEG potentials with voluntary movement

ELECTROENCEPHALOGRAPHY AND CLINICAL NEUROPHYSIOLOGY

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S U M M A T E D H U M A N EEG P O T E N T I A L S W I T H V O L U N T A R Y M O V E M E N T 1, 2 L. GILDEN, H. G. VAUGHANJR. AND L. D. COSTA Saul R. Korey Department of Neurology, Albert Einstein College of Medicine, New York, N.Y. (U.S.A.) (Accepted for publication: November 17, 1965)

Bates (1951) studied EEG correlates of movement in human subjects by superimposing EEG tracings in relation to the onset of EMG activity. With this technique he was able to discern a cortical potential beginning 20-40 msec after the onset of, but none antecedent to contraction. Since Bates' work was reported, electronic summation of EEG activity time-locked to peripheral stimulation has been developed and proven to be a powerful technique for studying neurophysiological correlates of sensory and perceptual processes. It was reasonable therefore to study brain activity related to voluntary movement by summating EEG in the period prior to and during discrete muscular contractions. This method makes it possible to observe electrical signs of cerebral processes associated with the initiation and execution of movement. The present report describes an experiment designed to investigate this phenomenon. METHOD

Ten normal adults, eight males and two females, served as subjects. In addition, a patient with cortical and deep electrodes implanted prior to surgery for intractable epileptic seizures was studied. The subjects lay on a cot in a dark, sound-damped room, where they performed quick, repetitive voluntary contractions with the left or right fist or dorsiflexions of either foot. The contractions were self-paced at a frequency of about one every 2 sec. Recordings were made from scalp electrodes over both hemispheres, including the region 1 Research supported by United States Public Health Service Grants NB-03356, MH-06723, and MH-6418. ~' Presented in part at the Eastern Psychological Association, Atlantic City, April, 1965.

presumably overlying motor area. In the experiments involving foot dorsifiexion, electrodes were placed according to international convention at Cz, Oz, C3, and C4. For the fist contraction experiments, exploratory recordings were made within an area of 1 sq in. around C3 and C4 to determine the placements providing the largest potentials associated with hand movement. In the case of the patient, recordings were made from several points estimated to be on pre-motor cortex, as determined by radiographic localization of the cortical electrodes. Control recordings were obtained from electrodes under the eye and on the chin. Linked ear electrodes served as a reference throughout the experiment. EEG was amplified with Tektronix 122 preamplifiers cascaded with Philbrick K2-W operational amplifiers, providing a gain of 2 x 105 and a frequency response down 3 db at 0.2 and 50 c/see.

EMG was recorded with surface electrodes placed over the flexor musculature of the forearms and the anterior tibial region of the legs. The E M G signals triggered the sweep of a Tektronix type 532 oscilloscope when 60 #V of muscle potential was generated. The oscilloscope produced a pulse delayed for a specified period; e.g., 1 sec or 250 msec, with respect to the onset of the muscle bursts. Amplified EEG, EMG, and the delayed pulses were recorded on magnetic tape. Analysis of the data was accomplished by playing the tape backwards, thereby reversing the temporal order of the delayed pulses and the E M G and EEG events. The pulses triggered a modified Mnemotron Computer of Average Transients, model 400, and the E M G and EEG activity were summated by the computer. It was thus possible to record the summated potentials Eleetroeneeph. clin. Neurophysiol., 1966, 20:433--438

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occurring before and during the motor contraction. In order to obtain aaa accurate representation of the onset and development of motor contraction, the amplified E M G potentials were passed through a fuU-wave rectifier circuit, thus inverting the negative going portions of the waves to positive polarity before summation. When summated, rectified E M G activity represents the total electrical activity derived from the recording electrodes and indicates precisely the earliest contraction, as well as the period of peak contraction. RESULTS

by a larger negative wave. This wave developed peak amplitude of 10-15 #V during the rising phase of the summated EMG. Immediately following the negative deflection, and 50-150 msec after onset of contraction, a larger positive wave, 20-30 /zV in amplitude, was seen. This wave persisted or slowly decayed with sustained contraction, but with brief, brisk contractions its duration was similar to that of the E M G event. The general form of the MP was reliably reproducible for each subject. Fig. 2 presents four additional summated potentials obtained from the subject whose MP is presented in Fig. 1. Again, foot dorsiflexion was being performed.

A characteristic wave which we have designated the " m o t o r potential" (MP) was identified in all eleven subjects as a cerebral correlate of voluntary motor activity. A typical form of the potential that developed with dorsiflexion of the foot is presented in Fig. 1. The MP was comprised of 3 components. A slow negative shift of the baseline developed approximately 1 see prior to onset of E M G evidence of muscular contraction. Beginning 50-150 msec prior to contraction, the slow negative variation terminated in a small positive deflection followed

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Fig. 2 Additional motor potentials obtained from subject L.C. under same conditions as in Fig. I. The traces indicate the degree of intra-subject variability with foot dorsiflexion. White arrow indicates time of onset of the abrupt negative deflection. The dark arrow indicates time of initiation of muscle contraction.

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Summated EEG and EMG potentials associated with dorsiflexion of the left foot by subject L.C. Onset of the contraction is preceded by a slow negative shift beginning at point indicated by first arrow, and a positive-negative deflection indicated by second arrow. In this and subsequent figures the traces are based upon 100 samples and negativity is downward. EMG: electromyogram from anterior tibial muscle; O.S. : activity from electrode below left eye.

The greatest intra-subject variability of the MP was associated with the behavior of the ongoing rhythmic activity. In those subjects displaying prominent central 8-12/sec activity (mu rhythm), such activity was seen in the summated records prior to the MP. Two alternative forms of mu rhythm behavior were associated with motor behavior. As indicated in Fig. 1, central rhythmic activity might block during the period of gradual negative deflection. This occurred in 25-30% of the series of 100 trials. In other instances (Fig. 2) mu rhythm persisted during the early negative Electroenceph. clin. Neurophysiol., 1966, 20:433-438

SUMMATEDEEG WITH VOLUNTARYMOVEMENT phase of the MP and, occasionally, throughout the MP. Systematic variations in the form of the MP were observed as a function of the limb moved and the placement of the electrode. With dorsiflexion of the foot, the amplitude was maximal near the vertex, and small in the region thought to overlie hand area of the motor cortex. Contraction of the fist was also associated with a large vertex potential. With this movement, however, electrodes 3 in. lateral to the vertex (C3 and C4) showed clear MPs, especially in the contralateral hemisphere (see below). The potentials time-locked to movement and recorded from Oz were substantially smaller than those derived from central regions (Fig. 1). A control electrode just below the eye on occasion showed activity apparer~tly associated with eye or lid movement. However, dissociation of the ocular and motor potentials was readily accomplished since MPs were frequently present in the absence of activity recorded near the eyes. The MPs obtained with contraction of the fist closely resembled those associated with foot dorsiflexion. Five summated MPs of another subject who performed contraction of the right fist are presented in Fig. 3. The recording was ca

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obtained with an electrode at C3. Observations were also made in eight subjects with respect to variations in form and amplitude of the MP over both hemispheres with unimanual contractions. A typical set of recordings is presented in Fig. 4. LEFT HAND

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Fig. 4 Motor potentials recorded simultaneously over ipsilateral and contralateral hemispheres with unimanual fist contraction. Arrows indicate onset of forearm muscle activity. Contraction of the left fist was associated with a negative-positive deflection at C4 more than twice the amplitude of the MP recorded simultaneously at C3. This amplitude difference was due to the smaller amplitude of both the negative and the positive components of the MP of the left hemisphere. Conversely, with the same electrode placements, contraction of the right fist was associated with an MP at C3 which was more prominent than the MP at C4. The summated E M G records showed differences consistent with the cerebral activity. As indicated in Fig. 2 and 3, intra-subject variability was small when the same movement was performed. The forms of the MP with dorsiflexion of the foot were also similar across subjects, but inter-subject variability of MPs associated with fist contraction was considerable. Summated potentials obtained from five subElectroenceph. din. Neurophysiol., 1966, 20:433-438

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jects performing fist contractions with the right hand are presented in Fig. 5. The recording in Fig. 5, a was made from the subject with implanted electrodes. In the other cases, with normal subjects, the electrode was positioned at

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Fig. 5 Motor potentials obtained from five subjects performing contractions of the right fist. Trace a was obtained from a patient with implanted electrode estimated to be over pre-motor cortex; traces b, c, d and e from normal subjects with electrodes at C3. Arrow indicates onset of muscle contraction.

or within 0.5 in. of C3. In general, the individual differences in MP involved variations in the relative amplitudes and duration of the positive and negative deflections. It has not been determined to what degree such variability in MPs is due to variations in position of the recording electrode relative to underlying motor cortex and to variations in pattern of muscular contraction. The similarity of the cortical recording to the scalp recordings makes it unlikely that the MP represents extracranial artifact. DISCUSSION

It appears that the MP reflects at least three distinct sets of events related to the discrete voluntary movements performed in this experiment: (1) preparatory events associated with

facilitation of motor cortex, (2) processes reflecting activation of the corticospinal pathways, and (3) activity resulting from kinesthetic feedback produced by the movement. Several investigators have described changes in EEG activity in motor cortex with voluntary movements in human subjects. Jasper and Penfield (1949), recording from the pre-central gyrus in patients under local anesthesia, reported that beta activity tended to block with the onset of motor behavior but returned while contraction was maintained. With relaxation beta rhythm again blocked for a brief period. The Rolandic mu rhythm (wicket rhythm or rythme en arceau), which Gastaut (1952) considers to be the beta rhythm halved and amplified, also undergoes changes during movement. Chatrian et al. (1959) reported that voluntary, passive and reflex movements were associated with blocking of mu activity, particularly in the hemisphere contralateral to the limb being moved. Those investigators also observed that blockade occurred, on the average, 1.5 sec before EMG discharges were recorded in the contracting muscle. The data of the present experiment in part support these observations, but indicate that there is considerable variability in the behavior of rhythmic cortical activity antecedent to movement. Assessment of background rhythm must take into consideration the statistical features of the summation procedure. The activity prior to the MP tended to sum in proportion to the square root of the number of samples. It was concluded therefore that the mu rhythm was not time-locked to the onset of muscular contraction, but present as background activity. Frequently apparent blockade of the mu rhythm was observed 500-750 msec before movement, as in Fig. 1. In approximately 75% of the series, however, blockade occurred either immediately prior to onset of contraction or not at all. Since direct experimental manipulation of attention was not possible without introducing external stimulation, the factors determining the behavior of the background rhythm antecedent to and during spontaneous voluntary movements have not been adequately defined. The protocols of the subjective state of subjects during tht: experimental sessions suggest, however, that Electroenceph. clin. Neurophysiol., 1966, 20:433-438

SUMMATED EEG WITH VOLUNTARY MOVEMENT

heightened awareness and attention were correlated with the occurrence of early blocking of the central rhythm. The development of a slow negative potential with movement has been reported previously. Walter et al. (1964, 1965) described the occurrence of a slow negative potential or "contingent negative variation" (CNV) during a 1-2 sec interval between two sensory stimuli, when subjects were required to perform a response to the second signal. This slow potential is interpreted by Walter and his associates as a sign of cortical events which facilitate the response to the second signal. Attention, expectancy, and response contingencies are seen as variables contributing to the amplitude of the CNV. Since, however, in the present experiment, the early negative shift associated with the MP occurred in the absence of a warning signal, the CNV might represent processes occurring in preparation for movement, which are not necessarily dependent upon anticipation of an external stimulus. Caspers (1963) described slow surface negative cortical deviations in freely moving rats with chronically implanted electrodes. Distinct negative shifts occurred synchronous with movement. Furthermore, irregular negative waves superimposed on the slow deviation were often associated with individual motor acts. Casper's EEG recordings resembled the summated motor potentials in that both slow negative deflections and abrupt negative waves were present. The averaging technique appears, however, to offer the possibility of detailed analysis of central events time-locked to movement. Summated recordings make it possible, for example, to estimate conduction time from motor cortex to limb. The data of Fig. 1 and 2 indicate that foot dorsiflexion was initiated 110-160 msec after onset of the abrupt negative deflection. Determination of brain-hand conduction time is, however, more difficult, for the time of onset of the abrupt negative wave is more variable than that associated with foot dorsiflexion. This may be due to the greater inter-trial variability of hand movements, as well as the greater difficulty of locating the region of cortex controlling hand movement. The estimate of brain to foot transmission

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time is appreciably higher than that which might be inferred from studies of Betz cell conduction velocity. It is, however, consonant with smaller pyramidal fiber conduction velocities (Evarts 1965; Takahashi 1965). Further analysis of the temporal relationships of the MP to voluntary motor contractions in a reaction time experiment has been made by Vaughan et al. (1965). Other studies support the inference that the abrupt negative or positive-negative deflection occurring just prior to and during muscle contraction may reflect activation of pyramidal tract neurons. Li and Chou (1962) found that with weak direct cortical stimulation 95% of the cells investigated in somatosensory cortex discharged during the initial surface negative potential. These investigators attributed the development of the surface negative wave to excitatory post-synaptic potentials. Following peripheral stimulation, Betz cell activity in somatosensory area of cats under chloralose anesthesia is greatest in the period of the surface evoked potential between peak positivity and peak negativity (Patton and Amassian 1960). Recently, Jasper and Stefanis (1965) reported that spontaneous spindle bursts recorded from the cortical surface tended to correspond to the discharge of pyramidal tract neurons in anesthetized or cerveau isold cats. Spike discharges were usually, although not invariably, associated with surface negative spindle waves. It may be postulated on the basis of these data that the abrupt negative or positive-negative wave of the summated potential developing with voluntary movement represents synaptic potentials associated with pyramidal cell discharge. This does not exclude the possibility that inhibitory events, which also appear to be associated with surface negativity (Sugaya et al. 1964), are taking place simultaneously. The late positive component of the MP seems to correspond to the wave identified by Bates (1951). This component might be attributed, at least in part, to afferent feedback generated by movement. Since the positive deflection developed more than 50 msec after onset of contraction, sufficient time elapsed to permit somatosensory and proprioceptive impulses to reach the cortex. The possibility cannot be excluded, however, that the positive component is an Electroenceph. clin. Neurophysiol., 1966, 20:433-438

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after-positive event related to efferent activity. Further research is needed to differentiate contributions o f efferent and feedback processes to the late c o m p o n e n t o f the MP. The M P m a y be viewed as an analog o f the sensory evoked potential. Just as the evoked potential serves as an index o f central events associated with afferent impulses, components o f the M P m a y represent central correlates o f efferent discharge. I f this is the case, the M P could provide information about the patterns o f brain activity associated with the control o f various m o t o r functions.

REFERENCES

SUMMARY

BATES,J. A. V. Electrical activity of the cortex accompanying movement. J. Physiol. (Lond.), 1951, 113: 240257. CASPERS, H. Relations of steady potential shifts in the cortex to the wakefulness-slecp spectrum. In M. A. B. BRAZIER (Ed.), Studies in brain function. Univ. of California Press, New York, 1963, 1: 177-213. CHATRIAN,G. E., PETERSEN,M. C. and LAZARTE,J. A. The blocking of the rolandic wicket rhythm and some central changes related to movement. Electroenceph. clin. Neurophysiol., 1959, 11: 497-510. EVARTS,E. V. Relation of discharge frequency to conduction velocity in pyramidal tract neurons. J. Neurophysiol., 1965, 28: 216--228. GASTAUT,H. ]~tude 61ectrocorticographique de la r6activit6 des rythmes rolandiques. Rev. nearol., 1952, 87:

Electroencephalographic recordings obtained prior to and during voluntary muscular contractions o f h u m a n subjects were analyzed by the summation method. A characteristic wave form called the " m o t o r potential" (MP) was found to be associated with foot dorsiflexion and fist contraction. It consisted o f 3 major components. Beginning as m u c h as 1 sec prior to contraction, a slow negative shift developed. Frequently, central r h y t h m blockade occurred at this time. The slow potential culminated in an abrupt negative wave having an amplitude o f 10-15/~V. The onset o f the abrupt negative c o m p o n e n t occurred 50-150 msec before the first signs of contraction and reached a peak with maximal muscle contraction. This was followed by a late positive deflection that tended to persist for the duration o f the contraction. MPs developed concurrently in the two hemispheres with unimanual contraction but differed significantly. Both the abrupt negative wave and the subsequent positive deflection were larger in the hemisphere contralateral to the activated limb. The possibility that the slow negative shift reflected facilitatory events associated with preparation for movement is suggested. The abrupt negative wave is interpreted as a sign o f synaptic potentials associated with corticospinal discharge, and the positive deflection m a y represent afferent, movement-produced feedback.

JASPER,H. and PENFIELD,W. Electrocorticograms in man : effect of voluntary movement upon the electrical activity of the precentral gyrus. Arch. Psychiat. Nervenkr., 1949, 183: 163-174. JASPER, H. and S~FANIS, C. Intracellular oscillatory rhythms in pyramidal tract neurones in the cat. Electroenceph. clin. Neurophysiol., 1965, 18: 541553. LI, C. L. and CHOU, S. N. Cortical intracellular synaptic potentials and direct cortical stimulation. J. cell. comp. Physiol., 1962, 60: 1-16. PATRON,H. D. and AMASSlAN,V. E. The pyramidal tract: its excitation and functions. In J. FIELDet al. (Eds.), Handbook of physiology, Sect. 1. Amer. Physiol. Soc., Washington, 1960, 2: 837-861. SUGAYA,E., GOLORING,S. and O'LEARV,J. L. Intracellular potentials associated with direct cortical response and seizure discharge in cat. Electroenceph. clin. Neurophysiol., 1964, 17. 661-669. TAKAHASHI,K. Slow and fast groups of pyramidal tract cells and their respective membrane properties. J. Neurophysiol., 1965, 28: 908-924. VAUGHANJR., H. G., COSTA, L. D., GILDEN, L. and SCHIMMEL, H. Identification of sensory and motor components of cerebral activity in simple reactiontime tasks. Proc. 73rd Conf. Arner. Psychol. Ass., 1965, 1: 179. WALTER, W. G., COOPER, R., ALDRIDGE, V. J., MCCALLUM,W. C. and WINTER,A. L. Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature (Lond.), 1964, 203: 380-384. WALTER,W. G., COOPER,R., MCCALLUM,C. and COHEN,J. The origin and significance of the contingent negative variation or "expectancy wave". Electroenceph, clin. Neurophysiol., 1965, 18: 720.

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Reference: GILDEN,L., VAUGHANJR., H. G. and COSTA, L. D. Summated human EEG potentials with voluntary movement. Electroenceph. clin. Neurophysiol., 1966, 20: 433-438.