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Cortical potentials associated with voluntary foot movement in man
Electroencephalography and Clinical Neurophysiology, 1981, 52:507--516
507
Elsevier/North-Holland Scientific Publishers, Ltd.
C O R T I C A L P O T E N T I A L S A S S O C I A T E D W I T H V O L U N T A R Y F O O T M O V E M E N T IN MAN H. SHIBASAKI l , G. BARRETT2 , ELISE HALLIDAY and A.M. HALLIDAY 2 Institute o f Neurology, The National Hospital, Queen Square, London WC I N 3BG (England)
(Accepted for publication: September 1, 1981)
Previous a u t h o r s have r e p o r t e d differing t o p o g r a p h i c a l d i s t r i b u t i o n s for scalp-recorded p o t e n t i a l s o c c u r r i n g in close association with h a n d m o v e m e n t s c o m p a r e d with t h o s e for f o o t m o v e m e n t s ( K o r n h u b e r and D e e c k e 1 9 6 5 ; Gilden et al. 1 9 6 6 ; Vaughan et al. 1968). This result is n o t surprising given the somatotopic organization of the human m o t o r c o r t e x ( F o e r s t e r 1 9 3 6 ; Penfield and B o l d r e y 1 9 3 7 ; Penfield and Rasmussen 1 9 5 0 ) . In a previous s t u d y , the present a u t h o r s identified 2 small negative waves o c c u r r i n g in very close association with the o n s e t o f finger m o v e m e n t : a p r e - m o t i o n negativity in the c o n t r a l a t e r a l m o t o r area (N -- 10) and a postm o t i o n negativity over t h e contralateral f r o n t a l r e g i o n (N + 50) (Shibasaki et al. 1 9 8 0 a , b). T h e f o r m e r wave is m o s t likely to r e p r e s e n t t h e activity o f cortico-spinal t r a c t cells, c o r r e s p o n d i n g to t h e m o t o r p o t e n t i a l o f D e e c k e et al. ( 1 9 6 9 , 1 9 7 3 , 1 9 7 6 ) ; the latter c o u l d be g e n e r a t e d within the central sulcus and m i g h t reflect the kinesthetic f e e d b a c k f r o m muscle a f f e r e n t s (Shibasaki et al. 1 9 8 0 b ) . If this h y p o t h e s i s is c o r r e c t , t h e d i s t i n c t i o n b e t w e e n these 2 negative c o m p o nents should be m o r e obvious in f o o t movem e n t , as the length o f the p a t h w a y and the resulting c o n d u c t i o n t i m e is greater. T h e
1 On leave from the Department of Neurology, Neurological Institute, Kyushu University, Fukuoka, Japan, being supported by the Japan Society for the Promotion of Science and the Royal Society. 2 Members of the External Staff of the Medical Research Council.
p r e s e n t s t u d y was designed to test this h y p o t h esis and t o c o n f i r m the previous studies comparing the scalp t o p o g r a p h y o f p o t e n t i a l s associated with f o o t m o v e m e n t s with t h a t for finger m o v e m e n t s .
Methods Subjects were 8 h e a l t h y volunteers, 5 m e n and 3 w o m e n . Their age ranged f r o m 19 to 39 years, t h e m e a n age being 27. All subjects were r i g h t - h a n d e d a c c o r d i n g t o t h e E d i n b u r g h h a n d e d n e s s i n v e n t o r y (Oldfield 1 9 7 1 ) . T h e p u r p o s e o f the e x p e r i m e n t was e x p l a i n e d to t h e subject b e f o r e each r e c o r d i n g session. T h e subject sat in a c o m f o r t a b l e chair and was i n s t r u c t e d t o fix his gaze at a target in f r o n t o f him b e f o r e and a f t e r each i n t e n d e d movem e n t o f an e x t r e m i t y . T h e m o v e m e n t s emp l o y e d were brisk e x t e n s i o n o f a middle finger and brisk d o r s i f l e x i o n o f a f o o t . Middle finger e x t e n s i o n was p e r f o r m e d using the same m e t h o d as in the previous e x p e r i m e n t (Shibasaki et al. 1980a). F o r f o o t dorsiflexion, b o t h heels were placed on a soft pad slightly lower t h a n the chair, with hip and knee joints semi-flexed and ankle joints held in a natural position. M o v e m e n t s were r e p e a t e d voluntarily at a self-paced interval e x c e e d i n g 3 sec. F i f t y m o v e m e n t s o f the same kind f o r m e d o n e session, and 4 sessions were given for each m o v e m e n t . B o t h hands and b o t h feet were t e s t e d separately. The electroencephalogram (EEG) was r e c o r d e d b y the same m e t h o d as used for the
0013-4649/81/0000--0000/$02.75 © 1981 Elsevier/North-Holland Scientific Publishers, Ltd.
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H. SHIBASAKI ET AL.
previous study (Shibasaki et al. 1980a, b). In 7 of the 8 subjects 14 silver-silver chloride electrodes fixed on the scalp as shown in Fig. 1 were referred to the c o m m o n linked ear reference electrodes. In one subject, the EEG was recorded from only 6 electrodes (Fz', LHM, C I ' , Cz, C2' and RHM). The electrooculogram (EOG) was also recorded from periorbital skin electrodes as shown in Fig. 1. Electrode resistance for all electrodes was reduced to below 5 k~2. The amplifiers for EEG and EOG had a time cons t a nt of 3.0 sec and a high f r e q u e n c y c ut - of f of less than 3 dB at 5000 Hz. T he electr o my o gr a m (EMG) was recorded
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with a pair of surface electrodes fixed approximately 3 c m apart over the contracting muscle in the forearm for middle finger extension and on the shin for f o o t dorsiflexion. The EMG amplifier had a time constant of 0.03 sec. Its o u t p u t was rectified and integrated, and a trigger pulse was obtained by matching the amplifier gain to the threshold level of the integrator. The 14 channel EEGs (6 channel in one subject), EOG and the rectified EMG were simultaneously input to a PDP-12 c o m p u t e r and averaged with an opisthochronic averaging program, using the trigger pulse. Using an ordinate period of 7.5 msec, the window time covered a period from 1500 msec before, to 420 msec after, the trigger pulse. Fifty samples were averaged in each session, and all the samples for each m o v e m e n t (200) were later added together. The results were stored digitally on magnetic tape and subsequently written o u t on an X-Y plotter. Measurements were made on the individual records using a cursoring program. The amplit ude of the initial slow negativity (BP) was measured from the baseline to the point at which its slope changed. The baseline was determined by averaging the initial 16 o u t of 256 ordinates per channel. In middle finger extension the following negative slope was measured from the change of slope of the BP to the culminating negative peak ( N - - 9 0 ) (Shibasaki et al. 1980a). In f o o t dorsiflexion the peak of this negative slope was defined as the culmination of its abrupt negative rise in close association with m o v e m e n t onset. The amplitude of o t h e r c o m p o n e n t s was measured from the preceding peak of opposite polarity, but when the latter was not clearly recognizable, t he amplitude was measured from the preceding abrupt change of slope. Components in middle finger extension were named according to the terminology used in our previous report (Shibasaki et al. 1980a). In f o o t dorsifiexion, c o m p o n e n t s ot her than the 2 pre-motion slow negativities were named according to the polarity and the r o u n d e d - o f f mean time interval in msec between the peak
M O T O R P O T E N T I A L S A S S O C I A T E D WITH M O V E M E N T
of each c o m p o n e n t and the initial peak of the averaged, rectified EMG (using combined data from both left and right foot movements). This terminology is illustrated in Fig. 2.
Results
(I) Cortical potentials associated with voluntary foot dorsiflexion Records of one subject were excluded due to their contamination by eye movement artifacts. As seen in Figs. 2 and 3, voluntary foot extension was preceded by a diffuse, sym-
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509
metric slow negativity beginning 750--1350 msec before the EMG peak (Bereitschaftspotential, BP). At 250--550 msec before the EMG peak, a marked increase of its gradient was seen, maximal at the vertex electrode (NS' (--400 to --100)). This negative slope was followed by another abrupt negative deflection culminating in a sharp negative peak at the vertex in very close association with the EMG peak. Immediately after the EMG peak, a negative component occurred over the frontal region, forming a composite or double peaked negativity with the preceding negativity. With the present method of analysis using the post-trigger window time of 420 msec, the last c o m p o n e n t was a widely distributed large positivity. The general waveform was fairly similar among subjects, and constant within an individual subject. In 3 out of 7 subjects, a small positivity was seen bilaterally immediately before the EMG peak over the precentral and parietal region. (1) Bereitschaftspotential (BP). This is a slowly rising negativity beginning 750 to 1350 msec before the EMG peak, being maximal at the midline precentral and parietal electrodes and diffusely and symmetrically distributed (Fig. 3). Its mean amplitude measured at the vertex (Cz) ranged from 2 to 9 pV. The BP was seen in all records (right and left foot dorsiflexion) of all 7 subjects. (2 ) NS' (--400 to --100). The gradient of the BP abruptly increased at 2 5 0 - 5 5 0 msec before the EMG peak (Figs. 2 and 3). This negative slope was very prominent at the vertex electrode (Cz), extending widely with diminishing amplitude both anteriorly and posteriorly in a symmetric fashion (Fig. 3). At 40--190 msec before the EMG peak, this negative slope usually showed another abrupt negative deflection or culminated in a negative sharp peak ( N - 100). The amplitude of this slope measured at the vertex (Cz) was 6-13 pV. It was seen in all records of all subjects. (3) NO. Following the NS' (--400 to --100), a sharp negative c o m p o n e n t was identified in 6 of the 7 subjects or in 11 of
510
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t h e 14 records. This was m a x i m a l at the vertex, e x t e n d i n g at smaller a m p l i t u d e to t h e f r o n t a l as well as to the parietal region, and laterally even to the h a n d m o t o r area in a s y m m e t r i c fashion (Fig. 3). T h e peak o c c u r r e d at f r o m 45 msec b e f o r e , t o 60 msec after, the EMG peak, the m e a n interval being 1 msec a f t e r the EMG peak (n = 10, S.D. = 37 msec). T h e a m p l i t u d e m e a s u r e d at the v e r t e x (Cz) ranged f r o m 2 t o 5 pV, the m e a n being 3.9 pV (n = 8, S.D. = 1.0 ~V). (4) P +8 0 . F o l l o w i n g the peak o f NO, a small positive slope was seen over the midline p r e c e n t r a l a n d / o r parietal region, e x t e n d i n g at diminishing a m p l i t u d e bilaterally (Figs. 2 and 3). It appears to be slightly m o r e a c c e n t u a t e d in t h e c o n t r a l a t e r a l parietal channels (Fig. 3). This c o m p o n e n t was r e c o g n i z e d in all r e c o r d s in 6 o f the 7 subjects. T h e p e a k o c c u r r e d at
1 0 - - 1 5 0 msec a f t e r t h e EMG peak, and was usually f o l l o w e d b y a small negative i n f l e x i o n d u e to the b a c k w a r d e x t e n s i o n o f t h e following negativity ( N + 1 1 0 , see below). The a m p l i t u d e m e a s u r e d either at the v e r t e x (Cz) or the midline parietal e l e c t r o d e (Pz) ranged f r o m 1 to 10 pV. (5) N + 110. At a p p r o x i m a t e l y 110 msec a f t e r the EMG p e a k , a c o m p o s i t e negativity consisting o f 2 or 3 peaks a p p e a r e d over the frontal and f r o n t o p o l a r region (Figs. 2 and 3). This c o m p o s i t e was seen in b o t h right and left f o o t d o r s i f l e x i o n s in 5 subjects and in o n l y o n e m o v e m e n t in 2 subjects. In m o s t individual r e c o r d s and in t h e grand average records with left f o o t m o v e m e n t (Fig. 3), t h e initial peak o f this c o m p o s i t e a p p e a r e d to be the forward e x t e n s i o n o f NO. This initial negative peak was i m m e d i a t e l y f o l l o w e d b y a m o r e p r o m i n e n t negative peak, which was m a x i m a l at t h e midline f r o n t a l e l e c t r o d e and s y m m e t r i cally d i s t r i b u t e d . This c o m p o n e n t e x t e n d e d b a c k w a r d s with m u c h smaller a m p l i t u d e to t h e p r e c e n t r a l region, and even to the parietal region in some records. T h e peak o c c u r r e d 5 0 - - 1 6 0 msec a f t e r the EMG peak, t h e m e a n time interval being 111 msec a f t e r t h e EMG peak (n = 12, S.D. = 38 msec). T h e a m p l i t u d e o f this main peak could n o t be m e a s u r e d in m o s t records, because o f its o c c u r r e n c e t o o soon a f t e r the p r e c e d i n g negative peak. ( 6 ) P + 280. This is a large, widespread positivity seen following the p r e c e d i n g negative c o m p o n e n t (N + 110) (Figs. 2 and 3). This was seen in all subjects e x c e p t for o n e r e c o r d of o n e subject. T h e peak, d e f i n e d b y the t e r m i n a t i o n of this steep positive slope, o c c u r r e d 2 2 0 - - 3 3 0 msec after t h e EMG peak. This c o m p o n e n t was m a x i m a l over the v e r t e x and distributed very diffusely and s y m m e t r i cally. T h e a m p l i t u d e m e a s u r e d at t h e v e r t e x f r o m the preceding negative peak (N + 110) ranged f r o m 5 to 18 #V. (H) Cortical potentials associated with voluntary middle finger extension T h e wave f o r m and c o m p o n e n t s o f the averaged cortical p o t e n t i a l s in association
511
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512 with middle finger extension were essentially the same as those previously reported by the authors (Shibasaki et al. 1980a). In particular, the majority of the components were predominantly recorded over the scalp contralateral to the movement, as shown in Fig. 3. The amplitude and time interval for each of these components are compared with those for foot movement in Table I.
(III) Comparison of foot dorsiflexion and middle finger extension The averaged cortical potentials associated with f o o t dorsiflexion and middle finger extension, as a whole, were composed of a series of similar components: the two slow premotion negativities, several short~luration, small potentials occurring in close association with the movement onset, and the postmotion large positivity. But a remarkable difference was noted in the scalp topbgraphy of the components associated with the two kinds of movement. With the foot movement all recognizable components were maximal over the midline electrodes and symmetrically distributed, whereas with the finger movement most components were asymmetric. Firstly, the maximal location of the negatire slope (NS') occurring within approximately 400 msec of the EMG peak was completely different in the two movements. The NS' (--400 t o - - 1 0 0 ) for foot movement was clearly maximal at the vertex electrode (Cz) whereas the NS' ( - - 5 0 0 t o - - 9 0 ) for finger movement was maximal over the contralateral precentral region, usually halfway between the vertex and the contralateral hand m o t o r area (C1' or C2'). In contrast, the earlier slow negativity (BP) was symmetric for both kinds of movement. Secondly, the small negative c o m p o n e n t occurring almost concomitantly with the movement onset (NO) was seen maximally at the vertex electrode (Cz) in foot dorsiflexion, whereas the corresponding c o m p o n e n t in middle finger extension ( N - 10) was fairly well localized to the hand m o t o r area contralateral to the movement (Fig. 3). Moreover,
H. SHIBASAKI ET AL. the NO for foot movement showed wider extension both antero-posteriorly and laterally in comparison with the N - 10 for finger movement which showed little extension (Fig. 3). Likewise, the positive slope occurring shortly after the EMG peak over the parietal and precentral region was maximal over the midline in foot movement (P + 80), whereas it was predominant over the contralateral hemisphere in finger movement (P + 90) (Fig. 3). Thirdly, a negative component occurring over the frontal region shortly after the EMG peak appeared approximately 50 msec later with respect to the EMG peak in foot movement (N + 110) than in middle finger movemerit (N + 50) (Table I). The mean time interval from the peak of the preceding negativity to that of this negativity ('NO to N + 110' in foot movement and ' N - - 1 0 t o N + 5 0 ' in middle finger movement) was 99 msec (n = 8, S.D. = 24 msec) for foot movement and 51 msec (n = 7, S.D. = 29 msec) for middle finger movement. Moreover, this post-motion frontal negativity in foot movement (N + 110) appeared broader in its duration than that in finger movement (N + 50) probably due to the forward extension of the preceding negativity (NO), forming a double-peaked composite, in the former movement (Fig. 3). Lastly, components for the foot movemerit corresponding to the pre-motion positive component ( P - - 5 0 ) and the post-motion, contralateral parietal negativity (N + 160) seen in finger movements were observed only in a few subjects.
Discussion
The averaged cortical potentials associated with brisk voluntary self-paced foot dorsiflexion and middle finger extension showed a markedly different scalp topography for most of their components, although the potentials comprised similar components for both kinds of movement. Most components associated with foot dorsiflexion (NS' (--400 to --100),
MOTOR POTENTIALS ASSOCIATED WITH MOVEMENT NO, N + 110, and P + 280) were maximal over the midline and symmetrically distributed, whereas the corresponding c o m p o n e n t s in middle finger extension (NS' (--500 t o - - 9 0 ) , N - - 1 0 , N + 5 0 , and P + 3 0 0 ) were asymmetric and p r e d o m i n a n t over the contralateral hemisphere. These findings are in c o n f o r m i t y with the s o m a t o t o p i c organization of the h u m an sensorimotor cortex (Foerster 1936; Penfield and Boldrey 1937; Penfield and Rasmussen 1950). The different behaviour of the two prem o t i o n slow negativities (BP and NS') is notew o r t h y . The earlier, slow negative shift (BP) was maximal over the midline precentral and parietal region, being widely and symmetrically distributed, for bot h f o o t and finger movements. In strong contrast with this, the later negative slope (NS') appeared to be localized to a specific part of the precentral area corresponding to the movement" over the midline precentral area in f o o t m o v e m e n t and over the contralateral precentral area in finger m o v e men t. This finding can be interpreted to support the two c o m p o n e n t hypothesis proposed by Hillyard (1973) for the contingent negative variation (CNV) and by Kutas and Donchin (1977) for the readiness potential, and later substantiated by the authors (Shibasaki et al. 1980a). The finding by Neafsey et al. (1978) of two different kinds of neurones in the cat m o t o r cor t e x is of especial interest in this regard. T h e y showed t hat neurones changing their firing rate within 500 msec before the onset of voluntary forelimb m o v e m e n t were pyramidal tract neurones located in the lateral as well as medial cortex, whereas those doing so earlier were n o t necessarily pyramidal tract neurones and were exclusively located in the medial c or t ex. Although they have n o t studied hind limb m o v e m e n t , this late activity might correspond to the late slow negativity (NS') d e m o n s t r a t e d in the previous (Shibasaki et al. 1980a) as well as the present study. It is reasonable to conclude that the late negative slope (NS') is specifically related to the m o v e m e n t and the earlier negative shift (BP) is related to a non-
513
specific preparation of the cerebral c o r t e x for voluntary m ovem ent . Vaughan et al. (1968) studied the scalp distribution of averaged cortical potentials associated with voluntary f o o t m o v e m e n t , and found t hat the total negative shift; occurring before m o v e m e n t onset (N) was maximal close to the midline central region, whereas it was lateralized to the contralateral hemisphere in hand m ovem ent . From the results of our present study, the 'N' of Vaughan et al. (1968) appears to have included the BP and NS', and possibly the small, sharp negative c o m p o n e n t fairly well localized t o the precentral area corresponding to the m o v e m e n t (NO in f o o t m o v e m e n t and N -- 10 in finger movement) as well. It can be concluded that it is the NS' and possibly the N-O or N -- 10, but not the BP, that cont ri but ed to the somatotopic localization of their 'N'. The small negative c o m p o n e n t occurring in very close association with the EMG peak over the precentral area corresponding to the m o v e m e n t (NO in f o o t m o v e m e n t and N -- 10 in finger m o v e m e n t ) showed an extension of varying degree in the two kinds of m ovem ent . It appears to extend rather widely, especially frontally, in f o o t m o v e m e n t , whereas it is fairly well localized to the contralateral hand m o t o r area in finger m ovem ent . This finding could be attributed to the different organization of the m o t o r cortex in hand and f o o t areas, with the location of the foot area mainly over the anterior bank of the central sulcus while that of the hand area lies mainly buried within the central sulcus (Foerster 1936). But this conclusion awaits a further correlative study in the animal using intracortical recording. With regard to the time relationship with m o v e m e n t onset., the peak of this negative c o m p o n e n t occurred nearly simultaneously with the peak of the averaged, rectified EMG in bot h f o o t and finger move-. ments. If this c o m p o n e n t represents an activity of t he corticospinal tract cells in the m o t o r cortex, corresponding to the m o t o r potential of Deecke et al. (1969, 1973, 1976) and the N2a c o m p o n e n t observed in the mon-
514 key by Arezzo and Vaughan (1980), as suggested in our preceding paper (Shibasaki et al. 1980a), this would be e xpe c t e d to occur earlier in f o o t m o v e m e n t than in hand m o v e m e n t with respect to m o v e m e n t onset. But this was n o t the case in the present study, which was based on the time interval between the peak of each c o m p o n e n t and the EMG peak. In this c o n t e x t , the time relationship between the o n s e t o f each c o m p o n e n t and the EMG onset obviously becomes i m por t ant . With the present technique, however, the precise onset of the averaged, rectified EMG is of t e n difficult to determine. Likewise, the onset of NO or N - - 10 is n o t always distinct, due t o an uninterrupted occurrence of this negative comp o n e n t at the culmination of the preceding negative slope (NS') in the same channel. A clear difference in the time relationship of the post-motion frontal negativity with the EMG peak was f o u nd in f o o t and finger movements (N + 110 versus N + 50). In the previous e x p e r i m e n t with passive extension of the middle finger, the authors recorded a similar potential over the frontal region and proposed that this activity might be related to the kinaesthetic feedback from muscle afferents (Shibasaki et al. 1980b). In view of the current hypothesis concerning the kinaesthetic input to the sensorimotor c o r t e x (Phillips et al. 1971; Zarzecki et al. 1978; L e m o n 1979) and of the similarity of this c o m p o n e n t to the N2b observed in the m o n k e y cor t e x by Arezzo and Vaughan (1980), t he authors further proposed t hat this frontal negativity might be a potential field projected from a dipole source within the central sulcus (area 3a) (Shibasaki et al. 1980a, b). Occurrence of this c o m p o n e n t in f oot m o v e m e n t approximately 50 msec later than t ha t in finger movement, either with respect to the EMG peak or with respect to the peak of the preceding negative c o m p o n e n t (NO or N - 10), appears to be in c o n f o r m i t y with the above h y p o t h esis. The cause o f the failure to record, in f o o t m o v e m e n t , the c o m p o n e n t corresponding to
H. SHIBASAKI ET AL. the pre-motion positivity ( P - - 5 0 ) recorded in finger m o v e m e n t remains unsettled.
Summary In order to clarify the functional significance of some c o m p o n e n t s of the movementrelated cortical potential, averaged cortical potentials associated with brisk voluntary, self-paced f o o t dorsiflexion and middle finger extension were compared in 8 healthy subjects. Simultaneous recording and averaging, by an opisthochronic averaging program, of 14 channel EEGs, EOG and EMG revealed a different topographical distribution for the various c o m p o n e n t s in the two kinds of movement. A negative slope occurring within 400 to 500 msec of the EMG peak (NS') was maximal over the midline precentral region and symmetrically distributed in f o o t m o v e m e n t , but was localized to the contralateral precentral region in finger m ovem ent . In contrast, an earlier negative shift (Bereitschaftspotential, BP) showed a similar distribution for both f o o t and finger movements. It is concluded t hat the NS' is specifically related to the m o v e m e n t , whereas the BP is related to a nonspecific preparation of the cerebral cortex for voluntary movement. A small negative comp o n e n t occurring in close association with the EMG peak, a post-motion frontal negativity, a post-motion positivity over the parietal and precentral region and a large,widespread postm o t i o n positivity also showed a midline predominance with symmetric distribution in f o o t m o v e m e n t versus a contralateral predominance in finger m o v e m e n t . T he post-motion frontal negativity for f o o t m o v e m e n t (N + 110) occurred a p p r o x i m a t e l y 50 msec later than that for finger m o v e m e n t (N + 50) with respect to the EMG peak, suggesting that this c o m p o n e n t represents the kinaesthetic feedback from muscle afferents.
MOTOR POTENTIALS ASSOCIATED WITH MOVEMENT
R~sum~
515
sant p o u r r a i t r e p r e s e n t e r le ' f e e d - b a c k ' k i n ~ s t h ~ s i q u e des p o t e n t i e l s a f f ~ r e n t s musculaires.
P o t e n t i e l s c o r t i c a u x associds a u x m o u v e m e n t s volontaires du p i e d c h e z l ~ o m m e References A f i n de m i e u x d~finir l ' i m p o r t a n c e f o n c t i o n n e l l e de q u e l q u e s c o m p o s a n t s du p o t e n tiel c o r t i c a l li~ au m o u v e m e n t , les p o t e n t i e l s c o r t i c a u x m o y e n n ~ s li~s a u x m o u v e m e n t s rapides v o l o n t a i r e s de la f l e x i o n dorsale d u p i e d et ~ l ' e x t e n s i o n d u d o i g t m~dius de 8 sujets o n t ~t~ c o m p a r e s . Un p r o g r a m m e opisthochronique r~glait l'enregistrement s i m u l t a n ~ et l ' ~ t a b l i s s e m e n t de la m o y e n n e p o u r 14 voies d ' E E G , d ' E O G et d ' E M G ; o n a c o n s t a t ~ q u e la d i s t r i b u t i o n t o p o g r a p h i q u e des divers c o m p o s a n t s est d i f f ~ r e n t e p o u r les d e u x sortes de m o u v e m e n t . U n e p e n t e n~gative (PN) se p r ~ s e n t a n t d a n s les 4 0 0 ~ 500 m s e c de la p o i n t e E M G associ~e au m o u v e m e n t avait u n m a x i m u m d ' a m p l i t u d e d a n s la r~gion p r ~ c e n t r a l e p r o c h e de la ligne m ~ d i a n e . Elle avait u n e d i s t r i b u t i o n s y m ~ t r i q u e d a n s les m o u v e m e n t s du p i e d , mais a s y m ~ t r i q u e dans c e u x des doigts, corresp o n d a n t ~ la r~gion m o t r i c e c o n t r a l a t ~ r a l e de la m a i n . Par c o n t r e , u n e n~gativit~ p r ~ c o c e s y m ~ t r i q u e ( B e r e i t s c h a f t s p o t e n t i a l , BP) se p r ~ s e n t a i t avec u n e d i s t r i b u t i o n similaire d a n s les m o u v e m e n t s du p i e d et des doigts. O n en c o n c l u que la PN est s p ~ c i f i q u e m e n t li~e a u x m o u v e m e n t s , tandis q u e le BP est li~ ~ la p r e p a r a t i o n n o n - s p ~ c i f i q u e du c o r t e x c~r~bral un mouvement volontaire quelconque. U n p e t i t c o m p o s a n t n~gatif ~ t r o i t e m e n t li~ a u x p o i n t e s E M G , u n e o n d e n~gative f r o n tale, u n e positivit~ pari~tale et p r ~ c e n t r a l e et u n e positivit~ ~ t e n d u e , t o u t e s arrivant apr~s le m o u v e m e n t , avaient aussi u n m a x i m u m d ' a m p l i t u d e t o u t pros de la ligne m ~ d i a n e . Les p o t e n t i e l s associ~s a u x m o u v e m e n t s du p i e d ~taient s y m ~ t r i q u e m e n t distribu~s, m a i s c e u x li~s a u x m o u v e m e n t s des doigts l ' ~ t a i e n t d ' u n e m a n i ~ r e a s y m ~ t r i q u e et c o n t r a l a t ~ r a l e . L a n~gativit~ f r o n t a l e associ~e a u x m o u v e m e n t s du p i e d arrivait, p a r r a p p o r t a u x p o i n t e s E M G 5 p e u pros 50 m s e c plus t a r d q u e celle li~e attx m o u v e m e n t s des doigts. Ce c o m p o -
Arezzo, J. and Vaughan, Jr., H.G. lntracortical sources and surface topography of the motor potential and somatosensory evoked potential in the monkey. In: H.H. Kornhuber and L. Deecke (Eds.), Motivation, Motor and Sensory Processes of the Brain: Electrical Potentials, Behaviour and Clinical Use, Prog. Brain Res., Vol. 154. Elsevier, Amsterdam, 1980: 77--83. Deecke, L., Scheid, P. and Kornhuber, H.H. Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements. Exp. Brain Res., 1969, 7: 158--168. Deecke, L., Becker, W., Gr6zinger, B., Scheid, P. and Kornhuber, H.H. Human brain potentials preceding voluntary limb movements. Electroenceph. clin. Neurophysiol., 1973, Suppl. 33: 87--94. Deecke, L., Gr6zinger, B. and Kornhuber, H.H. Voluntary finger movement in man: cerebral potentials and theory. Biol. Cybernet., 1976, 23: 99--119. Foerster, O. The motor cortex in man in the light of Hughlings Jackson's doctrines. Brain, 1936, 59: 135--159. Gilden, L., Vaughan, Jr., H.G. and Costa, L.D. Summated human EEG potentials with voluntary movement. Electroenceph. clin. Neurophysiol., 1966, 20: 433--438. Hillyard, S.A. The CNV and human behaviour. A review. Electroenceph. clin. N europhysiol., 1973, Suppl. 33: 161--171. Kornhuber, H.H. und Deecke, L. Hirnpotential//nderungen bei Willkfirbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflfgers Arch. ges. Physiol., 1965, 284: 1--17. Kutas, M. and Donchin, E. The effect of handedness, of responding hand, and of response force on the contralateral dominance of the readiness potential. In: J.E. Desmedt (Ed.), Prog. clin. Neurophysiol., Vol. 1, Attention, Voluntary Contraction and Event-related Cerebral Potentials. Karger, Basel, 1977: 189--210. Lemon, R.N. Short-latency peripheral inputs to the motor cortex in conscious monkeys. Brain Res., 1979, 161: 150--155. Neafsey, E.J., Hull, C.D. and Buchwald, N.A. Preparation for movement in the cat. I. Unit activity in the cerebral cortex. Electroenceph. clin. Neurophysiol., 1978, 44: 706--713.
516 Oldfield, R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 1971, 9: 97--113. Penfield, W. and Boldrey, E. Somatic m o to r and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 1937, 60: 389--443. Penfield, W. and Rasmussen, T. The Cerebral Cortex of Man. A Clinical Study of Localization of Function. MacMillan, New York, 1950 : 11--65. Phillips, C.G., Powell, T.P.S. and Wiesendanger, M. Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. J. Physiol. (Lond.), 1971, 217: 419--446. Shibasaki, H., Barrett, G., Halliday, E. and Halliday,
H. SHIBASAKI ET AL. A.M. Components of the movement-related cortical potential and their scalp topography. Electroenceph, clin. Neurophysiol., 1980a, 49: 213-226. Shibasaki, H., Barrett, G., Halliday, E. and Halliday, A.M. Cortical potentials following voluntary and passive finger movements. Electroenceph. clin. Neurophysiol., 1980b, 50: 201--213. Vaughan, Jr., H.G., Costa, L.D. and Ritter, W. Topography of the human motor potential. Electroenceph, clin. Neurophysiol., 1968, 25: 1--10. Zarzecki, P., Shinoda, Y. and Asanuma, H. Projection from area 3a to the m o t o r cortex by neurons activated from group I muscle afferents. Exp. Brain Res., 1978, 33: 269--282.
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C O R T I C A L P O T E N T I A L S A S S O C I A T E D W I T H V O L U N T A R Y F O O T M O V E M E N T IN MAN H. SHIBASAKI l , G. BARRETT2 , ELISE HALLIDAY and A.M. HALLIDAY 2 Institute o f Neurology, The National Hospital, Queen Square, London WC I N 3BG (England)
(Accepted for publication: September 1, 1981)
Previous a u t h o r s have r e p o r t e d differing t o p o g r a p h i c a l d i s t r i b u t i o n s for scalp-recorded p o t e n t i a l s o c c u r r i n g in close association with h a n d m o v e m e n t s c o m p a r e d with t h o s e for f o o t m o v e m e n t s ( K o r n h u b e r and D e e c k e 1 9 6 5 ; Gilden et al. 1 9 6 6 ; Vaughan et al. 1968). This result is n o t surprising given the somatotopic organization of the human m o t o r c o r t e x ( F o e r s t e r 1 9 3 6 ; Penfield and B o l d r e y 1 9 3 7 ; Penfield and Rasmussen 1 9 5 0 ) . In a previous s t u d y , the present a u t h o r s identified 2 small negative waves o c c u r r i n g in very close association with the o n s e t o f finger m o v e m e n t : a p r e - m o t i o n negativity in the c o n t r a l a t e r a l m o t o r area (N -- 10) and a postm o t i o n negativity over t h e contralateral f r o n t a l r e g i o n (N + 50) (Shibasaki et al. 1 9 8 0 a , b). T h e f o r m e r wave is m o s t likely to r e p r e s e n t t h e activity o f cortico-spinal t r a c t cells, c o r r e s p o n d i n g to t h e m o t o r p o t e n t i a l o f D e e c k e et al. ( 1 9 6 9 , 1 9 7 3 , 1 9 7 6 ) ; the latter c o u l d be g e n e r a t e d within the central sulcus and m i g h t reflect the kinesthetic f e e d b a c k f r o m muscle a f f e r e n t s (Shibasaki et al. 1 9 8 0 b ) . If this h y p o t h e s i s is c o r r e c t , t h e d i s t i n c t i o n b e t w e e n these 2 negative c o m p o nents should be m o r e obvious in f o o t movem e n t , as the length o f the p a t h w a y and the resulting c o n d u c t i o n t i m e is greater. T h e
1 On leave from the Department of Neurology, Neurological Institute, Kyushu University, Fukuoka, Japan, being supported by the Japan Society for the Promotion of Science and the Royal Society. 2 Members of the External Staff of the Medical Research Council.
p r e s e n t s t u d y was designed to test this h y p o t h esis and t o c o n f i r m the previous studies comparing the scalp t o p o g r a p h y o f p o t e n t i a l s associated with f o o t m o v e m e n t s with t h a t for finger m o v e m e n t s .
Methods Subjects were 8 h e a l t h y volunteers, 5 m e n and 3 w o m e n . Their age ranged f r o m 19 to 39 years, t h e m e a n age being 27. All subjects were r i g h t - h a n d e d a c c o r d i n g t o t h e E d i n b u r g h h a n d e d n e s s i n v e n t o r y (Oldfield 1 9 7 1 ) . T h e p u r p o s e o f the e x p e r i m e n t was e x p l a i n e d to t h e subject b e f o r e each r e c o r d i n g session. T h e subject sat in a c o m f o r t a b l e chair and was i n s t r u c t e d t o fix his gaze at a target in f r o n t o f him b e f o r e and a f t e r each i n t e n d e d movem e n t o f an e x t r e m i t y . T h e m o v e m e n t s emp l o y e d were brisk e x t e n s i o n o f a middle finger and brisk d o r s i f l e x i o n o f a f o o t . Middle finger e x t e n s i o n was p e r f o r m e d using the same m e t h o d as in the previous e x p e r i m e n t (Shibasaki et al. 1980a). F o r f o o t dorsiflexion, b o t h heels were placed on a soft pad slightly lower t h a n the chair, with hip and knee joints semi-flexed and ankle joints held in a natural position. M o v e m e n t s were r e p e a t e d voluntarily at a self-paced interval e x c e e d i n g 3 sec. F i f t y m o v e m e n t s o f the same kind f o r m e d o n e session, and 4 sessions were given for each m o v e m e n t . B o t h hands and b o t h feet were t e s t e d separately. The electroencephalogram (EEG) was r e c o r d e d b y the same m e t h o d as used for the
0013-4649/81/0000--0000/$02.75 © 1981 Elsevier/North-Holland Scientific Publishers, Ltd.
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previous study (Shibasaki et al. 1980a, b). In 7 of the 8 subjects 14 silver-silver chloride electrodes fixed on the scalp as shown in Fig. 1 were referred to the c o m m o n linked ear reference electrodes. In one subject, the EEG was recorded from only 6 electrodes (Fz', LHM, C I ' , Cz, C2' and RHM). The electrooculogram (EOG) was also recorded from periorbital skin electrodes as shown in Fig. 1. Electrode resistance for all electrodes was reduced to below 5 k~2. The amplifiers for EEG and EOG had a time cons t a nt of 3.0 sec and a high f r e q u e n c y c ut - of f of less than 3 dB at 5000 Hz. T he electr o my o gr a m (EMG) was recorded
E O G --.........
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Fig. 1. Electrode placement for the EEG and EOG used in the present study. The same montage was used in the previous studies on movement-related cortical potentials (Shibasaki et al. 1980a, b).
with a pair of surface electrodes fixed approximately 3 c m apart over the contracting muscle in the forearm for middle finger extension and on the shin for f o o t dorsiflexion. The EMG amplifier had a time constant of 0.03 sec. Its o u t p u t was rectified and integrated, and a trigger pulse was obtained by matching the amplifier gain to the threshold level of the integrator. The 14 channel EEGs (6 channel in one subject), EOG and the rectified EMG were simultaneously input to a PDP-12 c o m p u t e r and averaged with an opisthochronic averaging program, using the trigger pulse. Using an ordinate period of 7.5 msec, the window time covered a period from 1500 msec before, to 420 msec after, the trigger pulse. Fifty samples were averaged in each session, and all the samples for each m o v e m e n t (200) were later added together. The results were stored digitally on magnetic tape and subsequently written o u t on an X-Y plotter. Measurements were made on the individual records using a cursoring program. The amplit ude of the initial slow negativity (BP) was measured from the baseline to the point at which its slope changed. The baseline was determined by averaging the initial 16 o u t of 256 ordinates per channel. In middle finger extension the following negative slope was measured from the change of slope of the BP to the culminating negative peak ( N - - 9 0 ) (Shibasaki et al. 1980a). In f o o t dorsiflexion the peak of this negative slope was defined as the culmination of its abrupt negative rise in close association with m o v e m e n t onset. The amplitude of o t h e r c o m p o n e n t s was measured from the preceding peak of opposite polarity, but when the latter was not clearly recognizable, t he amplitude was measured from the preceding abrupt change of slope. Components in middle finger extension were named according to the terminology used in our previous report (Shibasaki et al. 1980a). In f o o t dorsifiexion, c o m p o n e n t s ot her than the 2 pre-motion slow negativities were named according to the polarity and the r o u n d e d - o f f mean time interval in msec between the peak
M O T O R P O T E N T I A L S A S S O C I A T E D WITH M O V E M E N T
of each c o m p o n e n t and the initial peak of the averaged, rectified EMG (using combined data from both left and right foot movements). This terminology is illustrated in Fig. 2.
Results
(I) Cortical potentials associated with voluntary foot dorsiflexion Records of one subject were excluded due to their contamination by eye movement artifacts. As seen in Figs. 2 and 3, voluntary foot extension was preceded by a diffuse, sym-
4 subjects Lt Vol. Foot Dorsiflex. I'""'T-'"-T'"'"'T"'""T"'"'T-" T N*IlO
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Fig. 2. T e r m i n o l o g y used in t h e p r e s e n t s t u d y t o ident i f y e a c h c o m p o n e n t o f t h e cortical p o t e n t i a l s associated w i t h v o l u n t a r y self-paced brisk f o o t dorsiflexion. S e l e c t e d c h a n n e l s f r o m t h e g r a n d average o f left f o o t m o v e m e n t (Fig. 3). E a c h c o m p o n e n t , e x c e p t for t h e slow negativities BP a n d N S ' , was n a m e d according t o t h e p o l a r i t y a n d t h e r o u n d e d - o f f m e a n t i m e interval in m s e e b e t w e e n its peak and t h e p e a k of t h e averaged, rectified EMG. T h e negative p r e f i x indicates t h a t t h e p e a k o c c u r s b e f o r e t h e E M G peak, t h e positive prefix t h a t t h e p e a k o c c u r s a f t e r t h e E M G peak.
509
metric slow negativity beginning 750--1350 msec before the EMG peak (Bereitschaftspotential, BP). At 250--550 msec before the EMG peak, a marked increase of its gradient was seen, maximal at the vertex electrode (NS' (--400 to --100)). This negative slope was followed by another abrupt negative deflection culminating in a sharp negative peak at the vertex in very close association with the EMG peak. Immediately after the EMG peak, a negative component occurred over the frontal region, forming a composite or double peaked negativity with the preceding negativity. With the present method of analysis using the post-trigger window time of 420 msec, the last c o m p o n e n t was a widely distributed large positivity. The general waveform was fairly similar among subjects, and constant within an individual subject. In 3 out of 7 subjects, a small positivity was seen bilaterally immediately before the EMG peak over the precentral and parietal region. (1) Bereitschaftspotential (BP). This is a slowly rising negativity beginning 750 to 1350 msec before the EMG peak, being maximal at the midline precentral and parietal electrodes and diffusely and symmetrically distributed (Fig. 3). Its mean amplitude measured at the vertex (Cz) ranged from 2 to 9 pV. The BP was seen in all records (right and left foot dorsiflexion) of all 7 subjects. (2 ) NS' (--400 to --100). The gradient of the BP abruptly increased at 2 5 0 - 5 5 0 msec before the EMG peak (Figs. 2 and 3). This negative slope was very prominent at the vertex electrode (Cz), extending widely with diminishing amplitude both anteriorly and posteriorly in a symmetric fashion (Fig. 3). At 40--190 msec before the EMG peak, this negative slope usually showed another abrupt negative deflection or culminated in a negative sharp peak ( N - 100). The amplitude of this slope measured at the vertex (Cz) was 6-13 pV. It was seen in all records of all subjects. (3) NO. Following the NS' (--400 to --100), a sharp negative c o m p o n e n t was identified in 6 of the 7 subjects or in 11 of
510
H. SHIBASAKI ET AL. 4
subjects
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i ,
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Fig. 3. Grand averaged records of cortical potentials associated with voluntary self-paced brisk dorsiflexion of left foot (Lt. Vol. Foot Dorsiflex.) and extension of left middle finger (Lt. Vol. MF Ext.) from 4 subjects. 200 trials of each movement for each subject.
t h e 14 records. This was m a x i m a l at the vertex, e x t e n d i n g at smaller a m p l i t u d e to t h e f r o n t a l as well as to the parietal region, and laterally even to the h a n d m o t o r area in a s y m m e t r i c fashion (Fig. 3). T h e peak o c c u r r e d at f r o m 45 msec b e f o r e , t o 60 msec after, the EMG peak, the m e a n interval being 1 msec a f t e r the EMG peak (n = 10, S.D. = 37 msec). T h e a m p l i t u d e m e a s u r e d at the v e r t e x (Cz) ranged f r o m 2 t o 5 pV, the m e a n being 3.9 pV (n = 8, S.D. = 1.0 ~V). (4) P +8 0 . F o l l o w i n g the peak o f NO, a small positive slope was seen over the midline p r e c e n t r a l a n d / o r parietal region, e x t e n d i n g at diminishing a m p l i t u d e bilaterally (Figs. 2 and 3). It appears to be slightly m o r e a c c e n t u a t e d in t h e c o n t r a l a t e r a l parietal channels (Fig. 3). This c o m p o n e n t was r e c o g n i z e d in all r e c o r d s in 6 o f the 7 subjects. T h e p e a k o c c u r r e d at
1 0 - - 1 5 0 msec a f t e r t h e EMG peak, and was usually f o l l o w e d b y a small negative i n f l e x i o n d u e to the b a c k w a r d e x t e n s i o n o f t h e following negativity ( N + 1 1 0 , see below). The a m p l i t u d e m e a s u r e d either at the v e r t e x (Cz) or the midline parietal e l e c t r o d e (Pz) ranged f r o m 1 to 10 pV. (5) N + 110. At a p p r o x i m a t e l y 110 msec a f t e r the EMG p e a k , a c o m p o s i t e negativity consisting o f 2 or 3 peaks a p p e a r e d over the frontal and f r o n t o p o l a r region (Figs. 2 and 3). This c o m p o s i t e was seen in b o t h right and left f o o t d o r s i f l e x i o n s in 5 subjects and in o n l y o n e m o v e m e n t in 2 subjects. In m o s t individual r e c o r d s and in t h e grand average records with left f o o t m o v e m e n t (Fig. 3), t h e initial peak o f this c o m p o s i t e a p p e a r e d to be the forward e x t e n s i o n o f NO. This initial negative peak was i m m e d i a t e l y f o l l o w e d b y a m o r e p r o m i n e n t negative peak, which was m a x i m a l at t h e midline f r o n t a l e l e c t r o d e and s y m m e t r i cally d i s t r i b u t e d . This c o m p o n e n t e x t e n d e d b a c k w a r d s with m u c h smaller a m p l i t u d e to t h e p r e c e n t r a l region, and even to the parietal region in some records. T h e peak o c c u r r e d 5 0 - - 1 6 0 msec a f t e r the EMG peak, t h e m e a n time interval being 111 msec a f t e r t h e EMG peak (n = 12, S.D. = 38 msec). T h e a m p l i t u d e o f this main peak could n o t be m e a s u r e d in m o s t records, because o f its o c c u r r e n c e t o o soon a f t e r the p r e c e d i n g negative peak. ( 6 ) P + 280. This is a large, widespread positivity seen following the p r e c e d i n g negative c o m p o n e n t (N + 110) (Figs. 2 and 3). This was seen in all subjects e x c e p t for o n e r e c o r d of o n e subject. T h e peak, d e f i n e d b y the t e r m i n a t i o n of this steep positive slope, o c c u r r e d 2 2 0 - - 3 3 0 msec after t h e EMG peak. This c o m p o n e n t was m a x i m a l over the v e r t e x and distributed very diffusely and s y m m e t r i cally. T h e a m p l i t u d e m e a s u r e d at t h e v e r t e x f r o m the preceding negative peak (N + 110) ranged f r o m 5 to 18 #V. (H) Cortical potentials associated with voluntary middle finger extension T h e wave f o r m and c o m p o n e n t s o f the averaged cortical p o t e n t i a l s in association
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512 with middle finger extension were essentially the same as those previously reported by the authors (Shibasaki et al. 1980a). In particular, the majority of the components were predominantly recorded over the scalp contralateral to the movement, as shown in Fig. 3. The amplitude and time interval for each of these components are compared with those for foot movement in Table I.
(III) Comparison of foot dorsiflexion and middle finger extension The averaged cortical potentials associated with f o o t dorsiflexion and middle finger extension, as a whole, were composed of a series of similar components: the two slow premotion negativities, several short~luration, small potentials occurring in close association with the movement onset, and the postmotion large positivity. But a remarkable difference was noted in the scalp topbgraphy of the components associated with the two kinds of movement. With the foot movement all recognizable components were maximal over the midline electrodes and symmetrically distributed, whereas with the finger movement most components were asymmetric. Firstly, the maximal location of the negatire slope (NS') occurring within approximately 400 msec of the EMG peak was completely different in the two movements. The NS' (--400 t o - - 1 0 0 ) for foot movement was clearly maximal at the vertex electrode (Cz) whereas the NS' ( - - 5 0 0 t o - - 9 0 ) for finger movement was maximal over the contralateral precentral region, usually halfway between the vertex and the contralateral hand m o t o r area (C1' or C2'). In contrast, the earlier slow negativity (BP) was symmetric for both kinds of movement. Secondly, the small negative c o m p o n e n t occurring almost concomitantly with the movement onset (NO) was seen maximally at the vertex electrode (Cz) in foot dorsiflexion, whereas the corresponding c o m p o n e n t in middle finger extension ( N - 10) was fairly well localized to the hand m o t o r area contralateral to the movement (Fig. 3). Moreover,
H. SHIBASAKI ET AL. the NO for foot movement showed wider extension both antero-posteriorly and laterally in comparison with the N - 10 for finger movement which showed little extension (Fig. 3). Likewise, the positive slope occurring shortly after the EMG peak over the parietal and precentral region was maximal over the midline in foot movement (P + 80), whereas it was predominant over the contralateral hemisphere in finger movement (P + 90) (Fig. 3). Thirdly, a negative component occurring over the frontal region shortly after the EMG peak appeared approximately 50 msec later with respect to the EMG peak in foot movement (N + 110) than in middle finger movemerit (N + 50) (Table I). The mean time interval from the peak of the preceding negativity to that of this negativity ('NO to N + 110' in foot movement and ' N - - 1 0 t o N + 5 0 ' in middle finger movement) was 99 msec (n = 8, S.D. = 24 msec) for foot movement and 51 msec (n = 7, S.D. = 29 msec) for middle finger movement. Moreover, this post-motion frontal negativity in foot movement (N + 110) appeared broader in its duration than that in finger movement (N + 50) probably due to the forward extension of the preceding negativity (NO), forming a double-peaked composite, in the former movement (Fig. 3). Lastly, components for the foot movemerit corresponding to the pre-motion positive component ( P - - 5 0 ) and the post-motion, contralateral parietal negativity (N + 160) seen in finger movements were observed only in a few subjects.
Discussion
The averaged cortical potentials associated with brisk voluntary self-paced foot dorsiflexion and middle finger extension showed a markedly different scalp topography for most of their components, although the potentials comprised similar components for both kinds of movement. Most components associated with foot dorsiflexion (NS' (--400 to --100),
MOTOR POTENTIALS ASSOCIATED WITH MOVEMENT NO, N + 110, and P + 280) were maximal over the midline and symmetrically distributed, whereas the corresponding c o m p o n e n t s in middle finger extension (NS' (--500 t o - - 9 0 ) , N - - 1 0 , N + 5 0 , and P + 3 0 0 ) were asymmetric and p r e d o m i n a n t over the contralateral hemisphere. These findings are in c o n f o r m i t y with the s o m a t o t o p i c organization of the h u m an sensorimotor cortex (Foerster 1936; Penfield and Boldrey 1937; Penfield and Rasmussen 1950). The different behaviour of the two prem o t i o n slow negativities (BP and NS') is notew o r t h y . The earlier, slow negative shift (BP) was maximal over the midline precentral and parietal region, being widely and symmetrically distributed, for bot h f o o t and finger movements. In strong contrast with this, the later negative slope (NS') appeared to be localized to a specific part of the precentral area corresponding to the movement" over the midline precentral area in f o o t m o v e m e n t and over the contralateral precentral area in finger m o v e men t. This finding can be interpreted to support the two c o m p o n e n t hypothesis proposed by Hillyard (1973) for the contingent negative variation (CNV) and by Kutas and Donchin (1977) for the readiness potential, and later substantiated by the authors (Shibasaki et al. 1980a). The finding by Neafsey et al. (1978) of two different kinds of neurones in the cat m o t o r cor t e x is of especial interest in this regard. T h e y showed t hat neurones changing their firing rate within 500 msec before the onset of voluntary forelimb m o v e m e n t were pyramidal tract neurones located in the lateral as well as medial cortex, whereas those doing so earlier were n o t necessarily pyramidal tract neurones and were exclusively located in the medial c or t ex. Although they have n o t studied hind limb m o v e m e n t , this late activity might correspond to the late slow negativity (NS') d e m o n s t r a t e d in the previous (Shibasaki et al. 1980a) as well as the present study. It is reasonable to conclude that the late negative slope (NS') is specifically related to the m o v e m e n t and the earlier negative shift (BP) is related to a non-
513
specific preparation of the cerebral c o r t e x for voluntary m ovem ent . Vaughan et al. (1968) studied the scalp distribution of averaged cortical potentials associated with voluntary f o o t m o v e m e n t , and found t hat the total negative shift; occurring before m o v e m e n t onset (N) was maximal close to the midline central region, whereas it was lateralized to the contralateral hemisphere in hand m ovem ent . From the results of our present study, the 'N' of Vaughan et al. (1968) appears to have included the BP and NS', and possibly the small, sharp negative c o m p o n e n t fairly well localized t o the precentral area corresponding to the m o v e m e n t (NO in f o o t m o v e m e n t and N -- 10 in finger movement) as well. It can be concluded that it is the NS' and possibly the N-O or N -- 10, but not the BP, that cont ri but ed to the somatotopic localization of their 'N'. The small negative c o m p o n e n t occurring in very close association with the EMG peak over the precentral area corresponding to the m o v e m e n t (NO in f o o t m o v e m e n t and N -- 10 in finger m o v e m e n t ) showed an extension of varying degree in the two kinds of m ovem ent . It appears to extend rather widely, especially frontally, in f o o t m o v e m e n t , whereas it is fairly well localized to the contralateral hand m o t o r area in finger m ovem ent . This finding could be attributed to the different organization of the m o t o r cortex in hand and f o o t areas, with the location of the foot area mainly over the anterior bank of the central sulcus while that of the hand area lies mainly buried within the central sulcus (Foerster 1936). But this conclusion awaits a further correlative study in the animal using intracortical recording. With regard to the time relationship with m o v e m e n t onset., the peak of this negative c o m p o n e n t occurred nearly simultaneously with the peak of the averaged, rectified EMG in bot h f o o t and finger move-. ments. If this c o m p o n e n t represents an activity of t he corticospinal tract cells in the m o t o r cortex, corresponding to the m o t o r potential of Deecke et al. (1969, 1973, 1976) and the N2a c o m p o n e n t observed in the mon-
514 key by Arezzo and Vaughan (1980), as suggested in our preceding paper (Shibasaki et al. 1980a), this would be e xpe c t e d to occur earlier in f o o t m o v e m e n t than in hand m o v e m e n t with respect to m o v e m e n t onset. But this was n o t the case in the present study, which was based on the time interval between the peak of each c o m p o n e n t and the EMG peak. In this c o n t e x t , the time relationship between the o n s e t o f each c o m p o n e n t and the EMG onset obviously becomes i m por t ant . With the present technique, however, the precise onset of the averaged, rectified EMG is of t e n difficult to determine. Likewise, the onset of NO or N - - 10 is n o t always distinct, due t o an uninterrupted occurrence of this negative comp o n e n t at the culmination of the preceding negative slope (NS') in the same channel. A clear difference in the time relationship of the post-motion frontal negativity with the EMG peak was f o u nd in f o o t and finger movements (N + 110 versus N + 50). In the previous e x p e r i m e n t with passive extension of the middle finger, the authors recorded a similar potential over the frontal region and proposed that this activity might be related to the kinaesthetic feedback from muscle afferents (Shibasaki et al. 1980b). In view of the current hypothesis concerning the kinaesthetic input to the sensorimotor c o r t e x (Phillips et al. 1971; Zarzecki et al. 1978; L e m o n 1979) and of the similarity of this c o m p o n e n t to the N2b observed in the m o n k e y cor t e x by Arezzo and Vaughan (1980), t he authors further proposed t hat this frontal negativity might be a potential field projected from a dipole source within the central sulcus (area 3a) (Shibasaki et al. 1980a, b). Occurrence of this c o m p o n e n t in f oot m o v e m e n t approximately 50 msec later than t ha t in finger movement, either with respect to the EMG peak or with respect to the peak of the preceding negative c o m p o n e n t (NO or N - 10), appears to be in c o n f o r m i t y with the above h y p o t h esis. The cause o f the failure to record, in f o o t m o v e m e n t , the c o m p o n e n t corresponding to
H. SHIBASAKI ET AL. the pre-motion positivity ( P - - 5 0 ) recorded in finger m o v e m e n t remains unsettled.
Summary In order to clarify the functional significance of some c o m p o n e n t s of the movementrelated cortical potential, averaged cortical potentials associated with brisk voluntary, self-paced f o o t dorsiflexion and middle finger extension were compared in 8 healthy subjects. Simultaneous recording and averaging, by an opisthochronic averaging program, of 14 channel EEGs, EOG and EMG revealed a different topographical distribution for the various c o m p o n e n t s in the two kinds of movement. A negative slope occurring within 400 to 500 msec of the EMG peak (NS') was maximal over the midline precentral region and symmetrically distributed in f o o t m o v e m e n t , but was localized to the contralateral precentral region in finger m ovem ent . In contrast, an earlier negative shift (Bereitschaftspotential, BP) showed a similar distribution for both f o o t and finger movements. It is concluded t hat the NS' is specifically related to the m o v e m e n t , whereas the BP is related to a nonspecific preparation of the cerebral cortex for voluntary movement. A small negative comp o n e n t occurring in close association with the EMG peak, a post-motion frontal negativity, a post-motion positivity over the parietal and precentral region and a large,widespread postm o t i o n positivity also showed a midline predominance with symmetric distribution in f o o t m o v e m e n t versus a contralateral predominance in finger m o v e m e n t . T he post-motion frontal negativity for f o o t m o v e m e n t (N + 110) occurred a p p r o x i m a t e l y 50 msec later than that for finger m o v e m e n t (N + 50) with respect to the EMG peak, suggesting that this c o m p o n e n t represents the kinaesthetic feedback from muscle afferents.
MOTOR POTENTIALS ASSOCIATED WITH MOVEMENT
R~sum~
515
sant p o u r r a i t r e p r e s e n t e r le ' f e e d - b a c k ' k i n ~ s t h ~ s i q u e des p o t e n t i e l s a f f ~ r e n t s musculaires.
P o t e n t i e l s c o r t i c a u x associds a u x m o u v e m e n t s volontaires du p i e d c h e z l ~ o m m e References A f i n de m i e u x d~finir l ' i m p o r t a n c e f o n c t i o n n e l l e de q u e l q u e s c o m p o s a n t s du p o t e n tiel c o r t i c a l li~ au m o u v e m e n t , les p o t e n t i e l s c o r t i c a u x m o y e n n ~ s li~s a u x m o u v e m e n t s rapides v o l o n t a i r e s de la f l e x i o n dorsale d u p i e d et ~ l ' e x t e n s i o n d u d o i g t m~dius de 8 sujets o n t ~t~ c o m p a r e s . Un p r o g r a m m e opisthochronique r~glait l'enregistrement s i m u l t a n ~ et l ' ~ t a b l i s s e m e n t de la m o y e n n e p o u r 14 voies d ' E E G , d ' E O G et d ' E M G ; o n a c o n s t a t ~ q u e la d i s t r i b u t i o n t o p o g r a p h i q u e des divers c o m p o s a n t s est d i f f ~ r e n t e p o u r les d e u x sortes de m o u v e m e n t . U n e p e n t e n~gative (PN) se p r ~ s e n t a n t d a n s les 4 0 0 ~ 500 m s e c de la p o i n t e E M G associ~e au m o u v e m e n t avait u n m a x i m u m d ' a m p l i t u d e d a n s la r~gion p r ~ c e n t r a l e p r o c h e de la ligne m ~ d i a n e . Elle avait u n e d i s t r i b u t i o n s y m ~ t r i q u e d a n s les m o u v e m e n t s du p i e d , mais a s y m ~ t r i q u e dans c e u x des doigts, corresp o n d a n t ~ la r~gion m o t r i c e c o n t r a l a t ~ r a l e de la m a i n . Par c o n t r e , u n e n~gativit~ p r ~ c o c e s y m ~ t r i q u e ( B e r e i t s c h a f t s p o t e n t i a l , BP) se p r ~ s e n t a i t avec u n e d i s t r i b u t i o n similaire d a n s les m o u v e m e n t s du p i e d et des doigts. O n en c o n c l u que la PN est s p ~ c i f i q u e m e n t li~e a u x m o u v e m e n t s , tandis q u e le BP est li~ ~ la p r e p a r a t i o n n o n - s p ~ c i f i q u e du c o r t e x c~r~bral un mouvement volontaire quelconque. U n p e t i t c o m p o s a n t n~gatif ~ t r o i t e m e n t li~ a u x p o i n t e s E M G , u n e o n d e n~gative f r o n tale, u n e positivit~ pari~tale et p r ~ c e n t r a l e et u n e positivit~ ~ t e n d u e , t o u t e s arrivant apr~s le m o u v e m e n t , avaient aussi u n m a x i m u m d ' a m p l i t u d e t o u t pros de la ligne m ~ d i a n e . Les p o t e n t i e l s associ~s a u x m o u v e m e n t s du p i e d ~taient s y m ~ t r i q u e m e n t distribu~s, m a i s c e u x li~s a u x m o u v e m e n t s des doigts l ' ~ t a i e n t d ' u n e m a n i ~ r e a s y m ~ t r i q u e et c o n t r a l a t ~ r a l e . L a n~gativit~ f r o n t a l e associ~e a u x m o u v e m e n t s du p i e d arrivait, p a r r a p p o r t a u x p o i n t e s E M G 5 p e u pros 50 m s e c plus t a r d q u e celle li~e attx m o u v e m e n t s des doigts. Ce c o m p o -
Arezzo, J. and Vaughan, Jr., H.G. lntracortical sources and surface topography of the motor potential and somatosensory evoked potential in the monkey. In: H.H. Kornhuber and L. Deecke (Eds.), Motivation, Motor and Sensory Processes of the Brain: Electrical Potentials, Behaviour and Clinical Use, Prog. Brain Res., Vol. 154. Elsevier, Amsterdam, 1980: 77--83. Deecke, L., Scheid, P. and Kornhuber, H.H. Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements. Exp. Brain Res., 1969, 7: 158--168. Deecke, L., Becker, W., Gr6zinger, B., Scheid, P. and Kornhuber, H.H. Human brain potentials preceding voluntary limb movements. Electroenceph. clin. Neurophysiol., 1973, Suppl. 33: 87--94. Deecke, L., Gr6zinger, B. and Kornhuber, H.H. Voluntary finger movement in man: cerebral potentials and theory. Biol. Cybernet., 1976, 23: 99--119. Foerster, O. The motor cortex in man in the light of Hughlings Jackson's doctrines. Brain, 1936, 59: 135--159. Gilden, L., Vaughan, Jr., H.G. and Costa, L.D. Summated human EEG potentials with voluntary movement. Electroenceph. clin. Neurophysiol., 1966, 20: 433--438. Hillyard, S.A. The CNV and human behaviour. A review. Electroenceph. clin. N europhysiol., 1973, Suppl. 33: 161--171. Kornhuber, H.H. und Deecke, L. Hirnpotential//nderungen bei Willkfirbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflfgers Arch. ges. Physiol., 1965, 284: 1--17. Kutas, M. and Donchin, E. The effect of handedness, of responding hand, and of response force on the contralateral dominance of the readiness potential. In: J.E. Desmedt (Ed.), Prog. clin. Neurophysiol., Vol. 1, Attention, Voluntary Contraction and Event-related Cerebral Potentials. Karger, Basel, 1977: 189--210. Lemon, R.N. Short-latency peripheral inputs to the motor cortex in conscious monkeys. Brain Res., 1979, 161: 150--155. Neafsey, E.J., Hull, C.D. and Buchwald, N.A. Preparation for movement in the cat. I. Unit activity in the cerebral cortex. Electroenceph. clin. Neurophysiol., 1978, 44: 706--713.
516 Oldfield, R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 1971, 9: 97--113. Penfield, W. and Boldrey, E. Somatic m o to r and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 1937, 60: 389--443. Penfield, W. and Rasmussen, T. The Cerebral Cortex of Man. A Clinical Study of Localization of Function. MacMillan, New York, 1950 : 11--65. Phillips, C.G., Powell, T.P.S. and Wiesendanger, M. Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. J. Physiol. (Lond.), 1971, 217: 419--446. Shibasaki, H., Barrett, G., Halliday, E. and Halliday,
H. SHIBASAKI ET AL. A.M. Components of the movement-related cortical potential and their scalp topography. Electroenceph, clin. Neurophysiol., 1980a, 49: 213-226. Shibasaki, H., Barrett, G., Halliday, E. and Halliday, A.M. Cortical potentials following voluntary and passive finger movements. Electroenceph. clin. Neurophysiol., 1980b, 50: 201--213. Vaughan, Jr., H.G., Costa, L.D. and Ritter, W. Topography of the human motor potential. Electroenceph, clin. Neurophysiol., 1968, 25: 1--10. Zarzecki, P., Shinoda, Y. and Asanuma, H. Projection from area 3a to the m o t o r cortex by neurons activated from group I muscle afferents. Exp. Brain Res., 1978, 33: 269--282.