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Topographical arrangement between thalamic ventro-lateral nucleus and precentral motor cortex in man
437
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
T O P O G R A P H I C A L A R R A N G E M E N T BETWEEN T H A L A M I C VENTRO-LATERAL NUCLEUS AND PRECENTRAL MOTOR CORTEX IN M A N MASATAKE UNO, M.D., KISOU KUBOTA, M.D., CHIHIRO OHYE, M.D., TOMONORI NAGAO, M . D . AND HIROTARO NARABAYASHI, M . D .
Neurological Clinic, 3-1001, Naka-meguro, Meguro-ku, Tokyo (Japan) (Accepted for publication: November 21, 1966)
INTRODUCTION
The topographical differentiation or somatotopical organization within the ventro-lateral nucleus of the thalamus (VL) was demonstrated anatomically by the retrograde degeneration method in the macaque monkey (Walker 1938), after removing parts of the precentral motor cortex. It is said that the face, arm and leg areas of the cerebral motor cortex are projected in this sequence from the medial, intermediate and lateral part of VL, respectively. In the human being, a similar topical representation of VL has been reported (Walker 1949). Furthermore, in the course of VL thalamotomy it has been found that destruction of its upper or medial part is more effective in the case of upper limb muscle disorders, whereas destruction of its lower or lateral part affects preferentially the lower limb muscles (Hassler and Riechert 1961 ; Mundinger and Zinsser 1966). The stimulation of VL in humans has produced on the ipsilateral motor area characteristic rhythmic potentials (Housepian and Purpura 1963; Ohye et al. 1964; Yoshida et al. 1964), which may be considered similar to the augmenting responses of the cat, though there are minor differences of the potential shape. The purpose of the present study was to determine the possible existence of a spatial relationship between portions of VL and of the precentral motor cortex; i.e., to find evidence of topical arrangement within the human VL. The results to be reported would suggest that small circumscribed lesions may relieve extrapyramidal motor
symptoms of a local nature such as those affecting only the arm or the leg. METHODS
Detailed data were obtained from seven patients (aged from 15 to 49 years) affected by Parkinsonism or cerebral palsy, in the course of stereotaxic thalamotomy. Most operations were performed under general anesthesia (i.v. amobarbital) in order to facilitate the detection of cortical potentials evoked by VL stimulation. The technical aspects of the stereotaxic VL thalamotomy have been described previously (Narabayashi 1964; Ohye et al. 1964; Yoshida et al. 1964). A thin concentric bipolar needle electrode was inserted through the fronto-central area, so that it would reach the assumed standard point (S.P.) under radiological measurements. The S.P. was usually settled at 1-2 mm behind and 1-2 mm above the mid-point of the intercommissural line in the lateral view and 10-13 mm lateral from the mid-line in the anteroposterior view. This point is used as a reference to indicate the spatial position of the electrode tip during surgery. A silver ball electrode was placed on the dura mater under the same small burr hole used for needle insertion. In three cases, additional small holes were trephined on its more lateral part and one or two other silver ball electrodes were placed epidurally. Scalp EEGs were recorded from the frontal and from the medial, middle and lateral central regions of the ipsilateral side. The nose was selected as the reference point, and the potentials were recorded both on the ink-writer and the cathode ray oscilloscope Electroenceph. clin. Neurophysiol., 1967, 22:437-443
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M. UNO et al.
(negativity is s h o w n as u p w a r d deflection). D u r i n g insertion of the s t i m u l a t i n g depth electrode, the tip p o s i t i o n was repeatedly checked radiologically (there has been n o o p p o r t u n i t y , up to now, to confirm a n y of the positions histologically).
A
RESULT
As already reported, s t i m u l a t i o n of VL at low frequency repetition produces, m a i n l y o n the ipsilateral precentral m o t o r cortex, r h y t h m i c evoked potentials, consisting of a n initial small
b
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cm Fig. 1 A : Three sets of cortical activities recorded through the scalp from the medial (med), middle (mid) and lateral Oat) part of the ipsilateral precentral area in a cerebral palsy patient. Columns a, b and c represent potentials evoked from the respective thalamic points, illustrated in B (stimulation parameters: 6/see, 30V, 1 msec). Calibrations: 1 sec and 100/~V. B: A pair of the X-ray photographs (left: lateral view; right: frontal view)showing recording and stimulating sites. Small letters a, b and c indicate stimulating points along one needle track, respectively 16, 10 and 4 mm above the S.P. (a plane between anterior and posterior commissures). Recording electrodes: medial (reed) placed 2 cm lateral from the mid-line, middle (mid) at 2 cm lateral part from the burr hole and lateral Oat) at 4 cm lateral part from the middle electrode. Electroenceph. din. Neurophysiol., 1967, 22:437~43
ORGANIZATION IN HUMAN THALAMIC VL
positive deflection and a large negative-positive component with the latency of 20-30 msec for the negative phase (Yoshida et al. 1964). These rhythmic potentials could appear over the medial as well as the lateral central region. The size of the negative portion of the diphasic component, probably representing local activity (Spencer and Brookhart 1961), was compared at different cortical points. Spatial relations between sites of stimulation in the thalamic nucleus and the points where the evoked potentials appeared at the cortical level, were studied in detail in four cases by scalp records and in three eases by epidural records. Selected cases will be described respectively. In the ease ofa 15-year-old cerebral palsy patient, scalp EEGs were recorded from 3 points approximately along the line between the two ears; 2 cm lateral from the mid-line (med), from the middle point; 6 cm lateral from the mid-line and 2 cm lateral from the edge of the burr hole for the needle insertion (mid) and from the lateral point; 4 cm lateral from the middle point and 10 cm lateral from the mid-line Oat) (see Fig. 1, B). In Fig. 1, A, EEG traces from these 3 points are shown during stimulation of 3 different sites within the thalamus. The stimulating electrode was inserted through the burr hole to the standard point (S.P.) in ventro-caudal and slightly medial direction (Fig. 1,B). Tracings a, b and c show the responses obtained, respectively, by stimulation of points 16 mm, 10 mm and 4 mm above the S.P., as indicated by the corresponding letters in Fig. l, B. In a, the negative-positive complexes were most prominent on the medial central region and practically absent on the lateral region. The potential complex was smallest for the first shock and developed gradually with repetitive stimulation, reaching the maximum after 4 or 5 shocks. When the repetitive shocks were applied to point b (6 mm deeper than a), the responses were observed in all 3 cortical points, the peak to peak amplitude and that of the negative phase tending to be larger in the middle central region (Fig. 1, Ab). With stimulation at c (4 mm above the S.P. and, presumably, within the ventral or ventromedial portion of VL), the evoked responses were predominant on the lateral lead (Fig. I, Ae). Thus, in this case, stimulation of the dorsal part of the nucleus would activate predominantly the
439
medial region, while that of the ventral part activated the lateral region of the motor cortex. In three other patients, in which two or three epidural silver electrodes had been placed on the precentral motor area, a similar spatial relation between intrathalamic points stimulated and the sites of cortical evoked potentials could be demonstrated. Fig. 2, A illustrates an example of epidural evoked responses in a 25-year-old cerebral palsy patient. The recording electrodes were introduced through two small burr holes and placed in proximity to the medial (med) and lateral Oat) motor region (see Fig. 2, B). The stimulating electrode inserted through the medial hole was placed at different depth levels. A pair of X-ray films of Fig. 2, B was taken when the electrode tip was at 1 mm below the S.P. Superimposed traces (Fig. 2, A) were recorded at medial and lateral cortical regions by stimulations at 14 mm (a), 9 mm (b) and 4 mm (c) above the S.P., respectively. From point a, the response was maximal at the medial cortical lead with a latency of 20-30 msec to the first negative deflection and with a peak latency of 50-60 msec to the late negativity of undetermined origin. Stimulation at point b resulted in a predominantly negative response (latency of about 30 msec) with initial positivity; the response was better developed on the lateral lead. Stimulation at point c elicited a similar potential mainly on the lateral lead. One example of a Parkinsonian patient is shown in Fig. 3 and 4. In this case too, the recording was epidural and stimulation was applied to the thalamus. Three small holes were made on the skull approximately along the line several centimeters rostral to a plane between both ears. EEG was recorded from the 3 points, shown in Fig. 4, A, B and designated as medial (med), middle (mid) and lateral (lat) lead, respectively. The stimulating electrode was inserted through the medial hole. Fig. 3, A shows cortical responses during stimulations of 3 thalamic points. From a (12 mm above the S.P.), repetitive shocks produced the VL responses which was present on the 3 areas, but maximal on the medial portion (Fig. 3, Aa). From b and c (8 and 4 mm above the S.P., respectively) responses of the same nature were obtained, but these were mainly on the lateral precentral motor area, being hardly apElectroenceph. clin. Neurophysiol., 1967, 22:437~43
440
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c~ Fig. 2 A : Epidural EEG records from the medial (med) and lateral Oat) precentral motor areas in another cerebral palsy patient, during stimulation (at 6/sec, 30 V, 1 msec) of 3 thalamic points 14 mm (a), 9 mm (b) and 4 mm (c) above the S.P. Each oscilloscopic record consists of more than 8 superposed responses during the repetitive stimulation. Stimulating points are illustrated in B. Calibrations: 50 c/sec and 100 t~V. B: X-ray photographs showing recording points on the dura and stimulating sites within the thalamus. Medial (reed) electrode ~s placed under the burr hole for insertion of stimulating electrode, lateral one Oat) is placed under another hole. made 6 cm lateral from the medial hole.
preciable f r o m the m e d i a l lead. The series o f responses in Fig. 3, B was o b t a i n e d d u r i n g s t i m u l a t i o n a l o n g a n o t h e r t r a c k in a m o r e m e d i a l direction t h a n the first one, as seen in the f r o n t a l view o f Fig. 4, C. S t i m u l a t i o n at b' (7 m m a b o v e the S.P.) - - v e n t r o - m e d i a l p o r t i o n o f VL a c c o r d ing to r a d i o l o g i c a l criteria - - p r o d u c e d r h y t h m i c responses a l m o s t exclusively on the lateral a n d the m i d d l e areas (Fig. 3, Bb'). I n this case, it w o u l d a p p e a r t h a t s t i m u l a t i o n to the d o r s o lateral p a r t o f the V L nucleus p r o d u c e d p r o m i -
nent responses on the medial p a r t of m o t o r cortex and shocks to the v e n t r o - m e d i a l p a r t affected mainly the lateral p a r t o f m o t o r cortex. Similar spatial relationships in the t h a l a m o cortical p r o j e c t i o n s f r o m the VL nucleus were confirmed in four cases with scalp a n d in three cases with e p i d u r a l recordings. I n Fig. 5, A,B t h e t h a l a m i c p o i n t s which u p o n s t i m u l a t i o n were f o u n d c a p a b l e o f inducing cortical responses were collected a n d p l o t t e d schematically to indicate the regions from which m o t o r cortex effects
Electroenceph. clin. Neurophysiol., 196"/, 22:437-443
441
ORGANIZATION IN HUMAN THALAMIC VL
B
A
a'
a lat
mid
b
were primarily medial or lateral. Thalamic areas indicated with open and solid circles seem to coincide to the radiologically determined VL as in the previous investigations (Ohye et al. 1964; Yoshida et al. 1964). It may be seen further that the open circles ("medial" effects) occupy the dorsal or dorso-lateral part and the solid ones ("lateral" effects) the ventral or ventro-medial half of VL with a distribution suggesting two separate populations within the nucleus. DISCUSSION
c'
-C
Fig. 3 The rhythmic evoked potentials (epidural recording) in a 49-year-old Parkinsonian patient from the lateral Oat), middle (mid) and medial (med) precentral motor areas. A and B represent responses during two different insertion trackings. Directions of the inserting electrode are shown in Fig. 4. Responses a, b, c and a', b', c' were induced from thalamic points along the track shown in Fig. 4, B and C. Calibrations: 1 sec and 200/~V.
A
The present investigation by epidural and scalp recordings has suggested that there is a relative difference of localization of the cortical potentials evoked by stimulation of different points within VL ; i.e., the response was maximal on the medial part of the motor cortex for stimulation of the dorso-lateral part of VL and would predominate on the lateral side with stimuli applied to the ventro-medial part of VL. The topographical arrangement of the motor cortical representation is well known (Penfield and 13oldrey 1937; Woolsey 1958). It would thus appear possible, in view of the demonstrated thalamic projection to the motor cortex, that contralateral leg, arm and face would be represented
B
C
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Fig. 4 Lateral (A) and antero-posterior (B) X-ray view, showing recording and stimulating points for EEG traces of Fig. 3, A. Small letters a, b and c indicate thalamic points at 12, 8 and 4 mm above the S.P. along the first needle track. The tip of the electrode is located at 14 mm lateral from the midline and 1 mm above the intercomm~ssural line. C: Antero-posterior view showing stimulating points for EEG traces of Fig. 3, B along the second track in the same patient. Small letters (a', b' and e') represent thalamic points of 11, 7 and 3 mm above the S.P. The electrode tip is located 10 mm lateral from the mid-line and 3 mm above intercommissural line.
Electroenceph. clin. Neurophysiol., 1967, 22:437-443
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I Fig. 5 Summary of the distributions (in 7 patients) of the thalamic stimulating points capable of evoking the rhythmic potentials most predominantly on the medial (open circle) and on the lateral (solid circles) precentral motor areas. Thalamic points are projected on the schematic picture of radiological findings of the third ventricle in its lateral (.4) and antero-posterior (B) view. A : The horizontal X-axis indicates the intercommissural line (CA-CP). Thus, each point is represented by a distance from CA on this line and by a vertical distance from this line on the Y-axis. Eight straight lines interconnecting the circles show series of stimulations along each track in seven cases (two tracks were tried in one case). CA: anterior commissure, CP: posterior commissure. B: The mid-line is used as horizontal Y-axis. The horizontal coordinate is drawn on the same level as intercommissural line and each point is represented by a distance from this line and by a distance
from the mid-line.
within VL in an orderly sequence along an axis from dorso-lateral to ventro-medial, as is shown on the specific sensory projection of the sensory cortex from the ventro-basal nucleus (Walker 1938; Rose and Mountcastle 1959). In the macaque monkeys, following lesions of the motor cortex in the leg, arm and face fields, the retrograde cell degenerations were found in the lateral, intermediate and medial portions of VL, respectively (Walker 1938). In contrast, Chow and Pribram (1956) showed in the same species that the medio-lateral axis of VL corresponds to a medio-lateral dimension of the precentral gyrus. In human beings it has been shown that after removal of the face and arm portions of area 4 and area 6, the thalamo-cortical projections originate from VL and mainly from its medial half (Walker 1949). The present observations are in line with the findings by Walker in the human being and monkeys.
From clinical observations after VL lesions in humans, Hassler and Riechert (1961) came to conclusions that are similar to ours, having shown the somatotopical sequence of face-armleg from medial to lateral within this nucleus. This somatotopical arrangement should be confirmed in the experimental animal by electrophysiological methods. SUMMARY
1. Rhythmic responses of the precentral motor cortex during repetitive stimulations of various points within the ventro-lateral (VL) nucleus of the human thalamus were recorded with scalp and epidural electrodes in anesthetized Parkinsonian and cerebral palsy patients, and the topical relation between intrathalamic stimulating points and the cortical areas showing dominant potentials was analyzed. 2. Stimulation of the dorsal or dorso-lateral Electroenceph. clin. Neurophysiol., 1967, 22:437443
443
ORGANIZATION IN HUMAN THALAMIC VL
part of VL produced the evoked potentials (negative-positive c o m p l e x with a latency o f 20-30 msec) p r e d o m i n a n t l y on the m e d i a l p o r t i o n o f the p r e c e n t r a l m o t o r area, whereas its l a t e r a l p o r t i o n was a c t i v a t e d preferentially when t h e v e n t r o - m e d i a l p a r t o f V L was s t i m u l a t e d . 3. I t a p p e a r s t h a t the d o r s o - l a t e r a l p a r t o f the V L nucleus has close c o n n e c t i o n with the m e d i a l m o t o r a r e a (leg area), a n d the r e m a i n i n g v e n t r o m e d i a l a r e a with t h e lateral p r e c e n t r a l a r e a (face area). RI~SUMI~ ORGANISATION TOPOGRAPHIQUE ENTRE LE NOYAU VENTRO-LATtf/RAL DU THALAMUS ET LE CORTEX MOTEURPRI~CENTRALCHEZ L'HOMME
1. Les r6ponses r y t h m i q u e s d u cortex pr6cent r a l m o t e u r p e n d a n t des s t i m u l a t i o n s r6p6titives de plusieurs p o i n t s / t l'int6rieur d u n o y a u ventrolat6ral (VL) d u t h a l a m u s de l ' h o m m e sont enregistr6es p a r des 61ectrodes sur le scalp et des 61ectrodes 6pidurales chez des P a r k i n s o n i e n s et des m a l a d e s h6mipl6giques sous anesth6sie. Ceci p e r m e t l ' a n a l y s e des relations t o p i q u e s entre les p o i n t s de s t i m u l a t i o n i n t r a t h a l a m i q u e s et les aires corticales m o n t r a n t des potentiels d o m i nants. 2. L a s t i m u l a t i o n de la p a r t i e dorsale ou d o r s o - l a t 6 r a l e d u V L e n t r a l n e des potentiels 6voqu6s ( c o m p l e x e n6gatif-positif avec une latence de 20-30 msec) qui p r 6 d o m i n e n t sur la p o r t i o n m6diale de l ' a i r e m o t r i c e pr6centrale, t a n d i s que sa p o r t i o n lat~rale est activ6e de fa~on pr6f6rentielle q u a n d la p a r t i e v e n t r o - m f d i a l e du V L est stimul6e. 3. I1 a p p a r a i t que la p a r t i e dorso-lat6rale d u n o y a u V L a des c o n n e c t i o n s 6troites avec l ' a i r e m o t r i c e m6diale (aire du pied) et la partie v e n t r o m6diale avec l ' a i r e pr6centrale lat6rale (aire de la face).
REFERENCES Chow, K. L. and P~aR~M, K. H. Cortical projection of the thalamic ventrolateral nuclear group in monkeys. J. comp. NeuroL, 1956, 104: 57-75. HASSLER,R. und RIECHERT,T. Wirkungen der Reizungen und Koagulationen in den Stammganglien bci stereotaktischen Hirnoperationen. Nervenarzt, 1961, 32: 97-109. HOUSEPIAN,E. M. and PURPURA,D. P. Electrophysiological studies of subcortical relations in man. Electroenceph, olin. NeurophysioL, 1963, 15: 20-28. MUNDINGER, F. und ZINSSER,O. Klinisch-experimentelle Untersuchungen zur stereotaktischen Thalamotomie der oralcn Ventralkerne bei extrapyramidalen Bewegungsst6rungen. Neurochirurgia, 1966, 9: 41-61. NARABAYASHI,H. Neurophysiological and clinical observations and analysis of the ventrolateral thalamotomy on various extrapyramidal disorders. 14th biennal int. Congr. int. Coll. Surg., Vienna, May 1964. OHYE, C., KUBOTA, K., HO~qGO, T., NAGAO, T. and NARABAYASHI,H. Ventrolateral and subventrolateral thalamic stimulation. Arch. Neurol. ( Ch&. ) , 1964, 11: 427-434. PENFIELO, W. and BOLDREV,E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 1937, 60: 389-443. ROSE, J. E. and MOtrNTCASTLE,V. B. Touch and kinesthesis. In J. FIELD, H. W. MOGOUNand V. E. HALL ('Eds.), Handbook of physiology, sect. 1. Amer. Physiol. Soc., Washington, 1959, 1 : 387-430. SPENCER,W. A. and BROOKHART,J. M. Electrical patterns of augmenting and recruiting waves in depths of sensorimotor cortex of cat. J. Neurophysiol., 1961, 24: 26-49. WALKER,A. E. The primate thalamus. University of Chicago Press, Chicago, I11., 1938: 182-187. WALKER, A. E. Afferent connections. In P. C. Bucv (Ed.), The precentral motor cortex. University of Illinois Press, Urbana, I11., 1949:113-132. WOOLSEY, C. N. Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. HARLOW and C. N. WOOLSEY(Eds.), Biological and biochemical bases oj behavior. University of Wisconsin Press, Madison, Wisc., 1958: 63-82. YOSHIDA, M., YANAGISAWA,H., SHIMAZU,H., GIVRE, A. and NARABAYASHI,H. Physiological identification of the thalamic nucleus. Arch. Neurol. (Chic.), 1964, 11:
435~43.
Reference: UNO, M., KUBOTA,K., OHYE, C., NAGAO,T. and NARABAYASHI,H. Topographical arrangement between thalamic ventro-lateral nucleus and precentral motor cortex in man. Electroenceph. din. Neurophysiol., 1967, 22:
437-443.
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
T O P O G R A P H I C A L A R R A N G E M E N T BETWEEN T H A L A M I C VENTRO-LATERAL NUCLEUS AND PRECENTRAL MOTOR CORTEX IN M A N MASATAKE UNO, M.D., KISOU KUBOTA, M.D., CHIHIRO OHYE, M.D., TOMONORI NAGAO, M . D . AND HIROTARO NARABAYASHI, M . D .
Neurological Clinic, 3-1001, Naka-meguro, Meguro-ku, Tokyo (Japan) (Accepted for publication: November 21, 1966)
INTRODUCTION
The topographical differentiation or somatotopical organization within the ventro-lateral nucleus of the thalamus (VL) was demonstrated anatomically by the retrograde degeneration method in the macaque monkey (Walker 1938), after removing parts of the precentral motor cortex. It is said that the face, arm and leg areas of the cerebral motor cortex are projected in this sequence from the medial, intermediate and lateral part of VL, respectively. In the human being, a similar topical representation of VL has been reported (Walker 1949). Furthermore, in the course of VL thalamotomy it has been found that destruction of its upper or medial part is more effective in the case of upper limb muscle disorders, whereas destruction of its lower or lateral part affects preferentially the lower limb muscles (Hassler and Riechert 1961 ; Mundinger and Zinsser 1966). The stimulation of VL in humans has produced on the ipsilateral motor area characteristic rhythmic potentials (Housepian and Purpura 1963; Ohye et al. 1964; Yoshida et al. 1964), which may be considered similar to the augmenting responses of the cat, though there are minor differences of the potential shape. The purpose of the present study was to determine the possible existence of a spatial relationship between portions of VL and of the precentral motor cortex; i.e., to find evidence of topical arrangement within the human VL. The results to be reported would suggest that small circumscribed lesions may relieve extrapyramidal motor
symptoms of a local nature such as those affecting only the arm or the leg. METHODS
Detailed data were obtained from seven patients (aged from 15 to 49 years) affected by Parkinsonism or cerebral palsy, in the course of stereotaxic thalamotomy. Most operations were performed under general anesthesia (i.v. amobarbital) in order to facilitate the detection of cortical potentials evoked by VL stimulation. The technical aspects of the stereotaxic VL thalamotomy have been described previously (Narabayashi 1964; Ohye et al. 1964; Yoshida et al. 1964). A thin concentric bipolar needle electrode was inserted through the fronto-central area, so that it would reach the assumed standard point (S.P.) under radiological measurements. The S.P. was usually settled at 1-2 mm behind and 1-2 mm above the mid-point of the intercommissural line in the lateral view and 10-13 mm lateral from the mid-line in the anteroposterior view. This point is used as a reference to indicate the spatial position of the electrode tip during surgery. A silver ball electrode was placed on the dura mater under the same small burr hole used for needle insertion. In three cases, additional small holes were trephined on its more lateral part and one or two other silver ball electrodes were placed epidurally. Scalp EEGs were recorded from the frontal and from the medial, middle and lateral central regions of the ipsilateral side. The nose was selected as the reference point, and the potentials were recorded both on the ink-writer and the cathode ray oscilloscope Electroenceph. clin. Neurophysiol., 1967, 22:437-443
438
M. UNO et al.
(negativity is s h o w n as u p w a r d deflection). D u r i n g insertion of the s t i m u l a t i n g depth electrode, the tip p o s i t i o n was repeatedly checked radiologically (there has been n o o p p o r t u n i t y , up to now, to confirm a n y of the positions histologically).
A
RESULT
As already reported, s t i m u l a t i o n of VL at low frequency repetition produces, m a i n l y o n the ipsilateral precentral m o t o r cortex, r h y t h m i c evoked potentials, consisting of a n initial small
b
a .,
I
C IAI
I
I
'
reed
sid Izt I
cm Fig. 1 A : Three sets of cortical activities recorded through the scalp from the medial (med), middle (mid) and lateral Oat) part of the ipsilateral precentral area in a cerebral palsy patient. Columns a, b and c represent potentials evoked from the respective thalamic points, illustrated in B (stimulation parameters: 6/see, 30V, 1 msec). Calibrations: 1 sec and 100/~V. B: A pair of the X-ray photographs (left: lateral view; right: frontal view)showing recording and stimulating sites. Small letters a, b and c indicate stimulating points along one needle track, respectively 16, 10 and 4 mm above the S.P. (a plane between anterior and posterior commissures). Recording electrodes: medial (reed) placed 2 cm lateral from the mid-line, middle (mid) at 2 cm lateral part from the burr hole and lateral Oat) at 4 cm lateral part from the middle electrode. Electroenceph. din. Neurophysiol., 1967, 22:437~43
ORGANIZATION IN HUMAN THALAMIC VL
positive deflection and a large negative-positive component with the latency of 20-30 msec for the negative phase (Yoshida et al. 1964). These rhythmic potentials could appear over the medial as well as the lateral central region. The size of the negative portion of the diphasic component, probably representing local activity (Spencer and Brookhart 1961), was compared at different cortical points. Spatial relations between sites of stimulation in the thalamic nucleus and the points where the evoked potentials appeared at the cortical level, were studied in detail in four cases by scalp records and in three eases by epidural records. Selected cases will be described respectively. In the ease ofa 15-year-old cerebral palsy patient, scalp EEGs were recorded from 3 points approximately along the line between the two ears; 2 cm lateral from the mid-line (med), from the middle point; 6 cm lateral from the mid-line and 2 cm lateral from the edge of the burr hole for the needle insertion (mid) and from the lateral point; 4 cm lateral from the middle point and 10 cm lateral from the mid-line Oat) (see Fig. 1, B). In Fig. 1, A, EEG traces from these 3 points are shown during stimulation of 3 different sites within the thalamus. The stimulating electrode was inserted through the burr hole to the standard point (S.P.) in ventro-caudal and slightly medial direction (Fig. 1,B). Tracings a, b and c show the responses obtained, respectively, by stimulation of points 16 mm, 10 mm and 4 mm above the S.P., as indicated by the corresponding letters in Fig. l, B. In a, the negative-positive complexes were most prominent on the medial central region and practically absent on the lateral region. The potential complex was smallest for the first shock and developed gradually with repetitive stimulation, reaching the maximum after 4 or 5 shocks. When the repetitive shocks were applied to point b (6 mm deeper than a), the responses were observed in all 3 cortical points, the peak to peak amplitude and that of the negative phase tending to be larger in the middle central region (Fig. 1, Ab). With stimulation at c (4 mm above the S.P. and, presumably, within the ventral or ventromedial portion of VL), the evoked responses were predominant on the lateral lead (Fig. I, Ae). Thus, in this case, stimulation of the dorsal part of the nucleus would activate predominantly the
439
medial region, while that of the ventral part activated the lateral region of the motor cortex. In three other patients, in which two or three epidural silver electrodes had been placed on the precentral motor area, a similar spatial relation between intrathalamic points stimulated and the sites of cortical evoked potentials could be demonstrated. Fig. 2, A illustrates an example of epidural evoked responses in a 25-year-old cerebral palsy patient. The recording electrodes were introduced through two small burr holes and placed in proximity to the medial (med) and lateral Oat) motor region (see Fig. 2, B). The stimulating electrode inserted through the medial hole was placed at different depth levels. A pair of X-ray films of Fig. 2, B was taken when the electrode tip was at 1 mm below the S.P. Superimposed traces (Fig. 2, A) were recorded at medial and lateral cortical regions by stimulations at 14 mm (a), 9 mm (b) and 4 mm (c) above the S.P., respectively. From point a, the response was maximal at the medial cortical lead with a latency of 20-30 msec to the first negative deflection and with a peak latency of 50-60 msec to the late negativity of undetermined origin. Stimulation at point b resulted in a predominantly negative response (latency of about 30 msec) with initial positivity; the response was better developed on the lateral lead. Stimulation at point c elicited a similar potential mainly on the lateral lead. One example of a Parkinsonian patient is shown in Fig. 3 and 4. In this case too, the recording was epidural and stimulation was applied to the thalamus. Three small holes were made on the skull approximately along the line several centimeters rostral to a plane between both ears. EEG was recorded from the 3 points, shown in Fig. 4, A, B and designated as medial (med), middle (mid) and lateral (lat) lead, respectively. The stimulating electrode was inserted through the medial hole. Fig. 3, A shows cortical responses during stimulations of 3 thalamic points. From a (12 mm above the S.P.), repetitive shocks produced the VL responses which was present on the 3 areas, but maximal on the medial portion (Fig. 3, Aa). From b and c (8 and 4 mm above the S.P., respectively) responses of the same nature were obtained, but these were mainly on the lateral precentral motor area, being hardly apElectroenceph. clin. Neurophysiol., 1967, 22:437~43
440
M.
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c~ Fig. 2 A : Epidural EEG records from the medial (med) and lateral Oat) precentral motor areas in another cerebral palsy patient, during stimulation (at 6/sec, 30 V, 1 msec) of 3 thalamic points 14 mm (a), 9 mm (b) and 4 mm (c) above the S.P. Each oscilloscopic record consists of more than 8 superposed responses during the repetitive stimulation. Stimulating points are illustrated in B. Calibrations: 50 c/sec and 100 t~V. B: X-ray photographs showing recording points on the dura and stimulating sites within the thalamus. Medial (reed) electrode ~s placed under the burr hole for insertion of stimulating electrode, lateral one Oat) is placed under another hole. made 6 cm lateral from the medial hole.
preciable f r o m the m e d i a l lead. The series o f responses in Fig. 3, B was o b t a i n e d d u r i n g s t i m u l a t i o n a l o n g a n o t h e r t r a c k in a m o r e m e d i a l direction t h a n the first one, as seen in the f r o n t a l view o f Fig. 4, C. S t i m u l a t i o n at b' (7 m m a b o v e the S.P.) - - v e n t r o - m e d i a l p o r t i o n o f VL a c c o r d ing to r a d i o l o g i c a l criteria - - p r o d u c e d r h y t h m i c responses a l m o s t exclusively on the lateral a n d the m i d d l e areas (Fig. 3, Bb'). I n this case, it w o u l d a p p e a r t h a t s t i m u l a t i o n to the d o r s o lateral p a r t o f the V L nucleus p r o d u c e d p r o m i -
nent responses on the medial p a r t of m o t o r cortex and shocks to the v e n t r o - m e d i a l p a r t affected mainly the lateral p a r t o f m o t o r cortex. Similar spatial relationships in the t h a l a m o cortical p r o j e c t i o n s f r o m the VL nucleus were confirmed in four cases with scalp a n d in three cases with e p i d u r a l recordings. I n Fig. 5, A,B t h e t h a l a m i c p o i n t s which u p o n s t i m u l a t i o n were f o u n d c a p a b l e o f inducing cortical responses were collected a n d p l o t t e d schematically to indicate the regions from which m o t o r cortex effects
Electroenceph. clin. Neurophysiol., 196"/, 22:437-443
441
ORGANIZATION IN HUMAN THALAMIC VL
B
A
a'
a lat
mid
b
were primarily medial or lateral. Thalamic areas indicated with open and solid circles seem to coincide to the radiologically determined VL as in the previous investigations (Ohye et al. 1964; Yoshida et al. 1964). It may be seen further that the open circles ("medial" effects) occupy the dorsal or dorso-lateral part and the solid ones ("lateral" effects) the ventral or ventro-medial half of VL with a distribution suggesting two separate populations within the nucleus. DISCUSSION
c'
-C
Fig. 3 The rhythmic evoked potentials (epidural recording) in a 49-year-old Parkinsonian patient from the lateral Oat), middle (mid) and medial (med) precentral motor areas. A and B represent responses during two different insertion trackings. Directions of the inserting electrode are shown in Fig. 4. Responses a, b, c and a', b', c' were induced from thalamic points along the track shown in Fig. 4, B and C. Calibrations: 1 sec and 200/~V.
A
The present investigation by epidural and scalp recordings has suggested that there is a relative difference of localization of the cortical potentials evoked by stimulation of different points within VL ; i.e., the response was maximal on the medial part of the motor cortex for stimulation of the dorso-lateral part of VL and would predominate on the lateral side with stimuli applied to the ventro-medial part of VL. The topographical arrangement of the motor cortical representation is well known (Penfield and 13oldrey 1937; Woolsey 1958). It would thus appear possible, in view of the demonstrated thalamic projection to the motor cortex, that contralateral leg, arm and face would be represented
B
C
lit
Cm
Fig. 4 Lateral (A) and antero-posterior (B) X-ray view, showing recording and stimulating points for EEG traces of Fig. 3, A. Small letters a, b and c indicate thalamic points at 12, 8 and 4 mm above the S.P. along the first needle track. The tip of the electrode is located at 14 mm lateral from the midline and 1 mm above the intercomm~ssural line. C: Antero-posterior view showing stimulating points for EEG traces of Fig. 3, B along the second track in the same patient. Small letters (a', b' and e') represent thalamic points of 11, 7 and 3 mm above the S.P. The electrode tip is located 10 mm lateral from the mid-line and 3 mm above intercommissural line.
Electroenceph. clin. Neurophysiol., 1967, 22:437-443
442
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: CA
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I Fig. 5 Summary of the distributions (in 7 patients) of the thalamic stimulating points capable of evoking the rhythmic potentials most predominantly on the medial (open circle) and on the lateral (solid circles) precentral motor areas. Thalamic points are projected on the schematic picture of radiological findings of the third ventricle in its lateral (.4) and antero-posterior (B) view. A : The horizontal X-axis indicates the intercommissural line (CA-CP). Thus, each point is represented by a distance from CA on this line and by a vertical distance from this line on the Y-axis. Eight straight lines interconnecting the circles show series of stimulations along each track in seven cases (two tracks were tried in one case). CA: anterior commissure, CP: posterior commissure. B: The mid-line is used as horizontal Y-axis. The horizontal coordinate is drawn on the same level as intercommissural line and each point is represented by a distance from this line and by a distance
from the mid-line.
within VL in an orderly sequence along an axis from dorso-lateral to ventro-medial, as is shown on the specific sensory projection of the sensory cortex from the ventro-basal nucleus (Walker 1938; Rose and Mountcastle 1959). In the macaque monkeys, following lesions of the motor cortex in the leg, arm and face fields, the retrograde cell degenerations were found in the lateral, intermediate and medial portions of VL, respectively (Walker 1938). In contrast, Chow and Pribram (1956) showed in the same species that the medio-lateral axis of VL corresponds to a medio-lateral dimension of the precentral gyrus. In human beings it has been shown that after removal of the face and arm portions of area 4 and area 6, the thalamo-cortical projections originate from VL and mainly from its medial half (Walker 1949). The present observations are in line with the findings by Walker in the human being and monkeys.
From clinical observations after VL lesions in humans, Hassler and Riechert (1961) came to conclusions that are similar to ours, having shown the somatotopical sequence of face-armleg from medial to lateral within this nucleus. This somatotopical arrangement should be confirmed in the experimental animal by electrophysiological methods. SUMMARY
1. Rhythmic responses of the precentral motor cortex during repetitive stimulations of various points within the ventro-lateral (VL) nucleus of the human thalamus were recorded with scalp and epidural electrodes in anesthetized Parkinsonian and cerebral palsy patients, and the topical relation between intrathalamic stimulating points and the cortical areas showing dominant potentials was analyzed. 2. Stimulation of the dorsal or dorso-lateral Electroenceph. clin. Neurophysiol., 1967, 22:437443
443
ORGANIZATION IN HUMAN THALAMIC VL
part of VL produced the evoked potentials (negative-positive c o m p l e x with a latency o f 20-30 msec) p r e d o m i n a n t l y on the m e d i a l p o r t i o n o f the p r e c e n t r a l m o t o r area, whereas its l a t e r a l p o r t i o n was a c t i v a t e d preferentially when t h e v e n t r o - m e d i a l p a r t o f V L was s t i m u l a t e d . 3. I t a p p e a r s t h a t the d o r s o - l a t e r a l p a r t o f the V L nucleus has close c o n n e c t i o n with the m e d i a l m o t o r a r e a (leg area), a n d the r e m a i n i n g v e n t r o m e d i a l a r e a with t h e lateral p r e c e n t r a l a r e a (face area). RI~SUMI~ ORGANISATION TOPOGRAPHIQUE ENTRE LE NOYAU VENTRO-LATtf/RAL DU THALAMUS ET LE CORTEX MOTEURPRI~CENTRALCHEZ L'HOMME
1. Les r6ponses r y t h m i q u e s d u cortex pr6cent r a l m o t e u r p e n d a n t des s t i m u l a t i o n s r6p6titives de plusieurs p o i n t s / t l'int6rieur d u n o y a u ventrolat6ral (VL) d u t h a l a m u s de l ' h o m m e sont enregistr6es p a r des 61ectrodes sur le scalp et des 61ectrodes 6pidurales chez des P a r k i n s o n i e n s et des m a l a d e s h6mipl6giques sous anesth6sie. Ceci p e r m e t l ' a n a l y s e des relations t o p i q u e s entre les p o i n t s de s t i m u l a t i o n i n t r a t h a l a m i q u e s et les aires corticales m o n t r a n t des potentiels d o m i nants. 2. L a s t i m u l a t i o n de la p a r t i e dorsale ou d o r s o - l a t 6 r a l e d u V L e n t r a l n e des potentiels 6voqu6s ( c o m p l e x e n6gatif-positif avec une latence de 20-30 msec) qui p r 6 d o m i n e n t sur la p o r t i o n m6diale de l ' a i r e m o t r i c e pr6centrale, t a n d i s que sa p o r t i o n lat~rale est activ6e de fa~on pr6f6rentielle q u a n d la p a r t i e v e n t r o - m f d i a l e du V L est stimul6e. 3. I1 a p p a r a i t que la p a r t i e dorso-lat6rale d u n o y a u V L a des c o n n e c t i o n s 6troites avec l ' a i r e m o t r i c e m6diale (aire du pied) et la partie v e n t r o m6diale avec l ' a i r e pr6centrale lat6rale (aire de la face).
REFERENCES Chow, K. L. and P~aR~M, K. H. Cortical projection of the thalamic ventrolateral nuclear group in monkeys. J. comp. NeuroL, 1956, 104: 57-75. HASSLER,R. und RIECHERT,T. Wirkungen der Reizungen und Koagulationen in den Stammganglien bci stereotaktischen Hirnoperationen. Nervenarzt, 1961, 32: 97-109. HOUSEPIAN,E. M. and PURPURA,D. P. Electrophysiological studies of subcortical relations in man. Electroenceph, olin. NeurophysioL, 1963, 15: 20-28. MUNDINGER, F. und ZINSSER,O. Klinisch-experimentelle Untersuchungen zur stereotaktischen Thalamotomie der oralcn Ventralkerne bei extrapyramidalen Bewegungsst6rungen. Neurochirurgia, 1966, 9: 41-61. NARABAYASHI,H. Neurophysiological and clinical observations and analysis of the ventrolateral thalamotomy on various extrapyramidal disorders. 14th biennal int. Congr. int. Coll. Surg., Vienna, May 1964. OHYE, C., KUBOTA, K., HO~qGO, T., NAGAO, T. and NARABAYASHI,H. Ventrolateral and subventrolateral thalamic stimulation. Arch. Neurol. ( Ch&. ) , 1964, 11: 427-434. PENFIELO, W. and BOLDREV,E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 1937, 60: 389-443. ROSE, J. E. and MOtrNTCASTLE,V. B. Touch and kinesthesis. In J. FIELD, H. W. MOGOUNand V. E. HALL ('Eds.), Handbook of physiology, sect. 1. Amer. Physiol. Soc., Washington, 1959, 1 : 387-430. SPENCER,W. A. and BROOKHART,J. M. Electrical patterns of augmenting and recruiting waves in depths of sensorimotor cortex of cat. J. Neurophysiol., 1961, 24: 26-49. WALKER,A. E. The primate thalamus. University of Chicago Press, Chicago, I11., 1938: 182-187. WALKER, A. E. Afferent connections. In P. C. Bucv (Ed.), The precentral motor cortex. University of Illinois Press, Urbana, I11., 1949:113-132. WOOLSEY, C. N. Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. HARLOW and C. N. WOOLSEY(Eds.), Biological and biochemical bases oj behavior. University of Wisconsin Press, Madison, Wisc., 1958: 63-82. YOSHIDA, M., YANAGISAWA,H., SHIMAZU,H., GIVRE, A. and NARABAYASHI,H. Physiological identification of the thalamic nucleus. Arch. Neurol. (Chic.), 1964, 11:
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Reference: UNO, M., KUBOTA,K., OHYE, C., NAGAO,T. and NARABAYASHI,H. Topographical arrangement between thalamic ventro-lateral nucleus and precentral motor cortex in man. Electroenceph. din. Neurophysiol., 1967, 22:
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