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Characteristics of driving of units in the sensorimotor cortex by center median nucleus and its inhibition by entopeduncular nucleus
1389-1396, 1870. Pinted~n~reatoBritâin~ l' PP'
Pergamon Press
CHARACTERISTICS OF DRIVING OF UNITS IN THE SENSORIM(YTOR CORTE% HY CENTER MEDIAN NUCLEUS AND ITS INHIBITION BY ENTOPEDUNCUIJIR NUCLEUS* B. Blum ** Mount Zion Neurological Institute, San Francisco, California,U .S .A .
(Received 10 July 1970; in final form 20 October 1970) Interactions between the sensorimotor cortex (SM),thalamic nuclei, the striatum and the pallidum (1,2,3,4) may be assumed to depend on connectivitiea such as those schematized in Fiq . 1.
earoa erRUe t ~RE~ ~ s e) /ROREUD AllE1.e
erRw e-e)
Fig .
1
Proposed network emphaslzinq closed-circuit cornectivities of the cat SM . One circuit includes as a descending limb the cortico-putaminal projections (3) and as an ascending limb, projections from putamen (PUT) to entopeduncular nucleus (ENT),
the assumed cat homologue of primates' medial globus .pallidus (5), hence
to ventrolateral thalamus center median (CM)
(VL)
and then to SM .Another hypothetic circuit is from
to PUT and back to CM (5) . Projections from and to CM and VL
to and from SM are also shown (5,6,7,8,9 ,1p iHlum et al ., in preparation) . *This paper is dedicated to the memory of my friend and fellow scientist Warren S .Mc:Culloch . The results were presented in part to the lat Meeting of the European Brain and Behaviour Society, Marseilles, Oct . 1969 . Present address : Department of Physiology and Pharmacology, Tel Aviv University Medical School, Tel Aviv, Israel .
1389
139 0
iJNITS IN SENSORIMOTOR CORTEX
Vol. 9, No. 24
Accumulated information on CM-SM interactions are suggestive of the importance of CM for integration of movement at the sensorimotor cortex as well as at other levels
(2, and Blum et al . in preparation) . An intimate relationship has
been claimed for this nucleus also to the extrapyramidal system
(11,
12,13,14,15,
16,17) . Functionally, CM seems to be part of the thalamic reticular formation (11) and in fact it has been shown to play a role in gating excitability at cortical (1,2) and at subcortical levels
(4) .
An attempt was made to investigate some of the meanings of these relationships by a study of unitary responses in SM
to CM
stimulation, including the
effects upon these responses of preconditioning stimuli to ENT, VL, or to PUT . Since the location of CM in the cat is shown differently by different authors because of use of different criteria
(2,5) selection of CM targets in the
present work was based on microphysiological and electrophysiological consider ations, as guideline was used the often proposed division of that nucleus into medio-roatral and ventro-lateral portions
(5) . A preliminary report of our re-
sups will be presented here . METHODS Ten adult cats were prepared surgically under ether anesthesia and were studied electrographically under local procaine anesthesia, Gallamine HC1 paralysis and artificial respiration . Stimulation electrodes and microelectrodes were applied, using methods already reported in our previous studies (19,20), Bipolar stimuli were delivered to targets in CM,VL,PUT,ENT and pyramids which were selected according to Nissl and silver impregnation histological sections . Test stimuli delivered to CM consisted of single pulses 0 .1 to 0 .2 msec . in duration and close to threshold in intensity which amounted to about 0 .06-1 mAmp . currents . Preconditioning stimuli delivered to ENT,PUT, or VL consisted of trains of stimuli . Each such train was 40 cosec . in duration, consisting of pulses at 125200 c/sec .,
each pulse 0 .1-0 .2 cosec . in duration and of threshold intensity for
evoking cortical field potentials . Curreht spread to neighbouring structures was
Vol. 9, No. 24
UNITS IN SENSORIMOTOR CORTEX
1391
minimized by use of short pulse durations and of threshold voltages . it was monitored by placing electrodes at critical sites . Current spread to the capsule interns was checked by having electrodes on the pyramids . Inter-stimuli intervals of 0 to BO cosec . were tested . Neurones were identified whether they were of pyramidal tract neurone (p .t .n .)
type or not (n .p .t .n .) before being studied
further . This was done by testing whether they gave antidromic responses following stimulation of the pyramd.d . Criteria used in this and also in defining unit responses to CM
whether they were antidromic or post-synaptic discharges
were those mentioned in our previous studies (20) " In some recent confirmatory experiments* safer answers to these questions were obtained by use of the col lision teat as follows : the spontaneous diechargea of the unit tested were made to trigger the oscilloscope and after a selected interval also to trigger the stimulator . Thus, the test atimulua could be given at a selected delay from the spontaneous unit discharge or, in same cases, from a spike triggered by stimulation through the microelectrode . This interval was then adjusted so that any antidromlc impulse generated by the test atimulua would meet, en route,
the
orthodromic impulse of the spontaneous discharge, and mutual annulment
would
occur . Therefore, observations of such annulment
or of lack of annulment of
unit responses under such conditions following the test Stimulus would provide supportive evidence whether the unit evoked otherwise by this stimulus is antidromic or orthodramic .** At the end of each experiment the actual locations of stimulation and of recording electrodes were confirmed hiatologically (21) .
* These experiments were done at the author's present address with aid of Mr . Deli whose technical assistantship was enabled by generous support from L.E .Phillipa Fund for psychobiological research . ** In extracellular recordings such a test can be carried out only with units which show spontaneous discharges, or that can be excited through the microelectrode . Other limitations of the test are that a spontaneous or evoked discharge of the soma may produce an impulse that may not travel under the conditions of the experiment into the fiber tested
(Slum et al . unpublished) .
1392
iJNITS IN 3EN30RIMOTOR CORTEX
Vol. 9, No . 24
RESULTS SM units were driven by CM stimulation with latencies which range from 2,8 to 15 msec, or more . A large number of these, which satisfied criteria for postsynaptic discharges, including lack of collision of the impulse generated by the CM stimulation with that of the spontaneous discharges showed the following characteristics : they lacked in individual variability among successive responses, they showed sharp thresholds, they were intensely stimulus-bound, they were widely scattered in SM in all its various parts as delimited by Hassler and Muhs-Clement (22), they were p .t .n . and n .p .t .n, and some were shown to be inhibited by high frequency train stimuli delivered as pre-conditioning to ENT (Fig . 2 and 3) .
Fig. 2 Extracellular SM unit responses following CM stimulation showing the characteristics enumerated in the text . In these tracings and in the following ones the time of stimulation is marked with dots at bottom . A,B,E taken from cat and C,D,F from squirrel monkey . In(A~are depicted stimulus-bound waves (f) recorded in area 4 which presumably are synaptic potentials . They simanate on intensifying tlhe stimulus until a spike (#) is triggered, the latter identified as p .t .n . In fib)
reversal of stimulus polarity evoked similar synaptic potentials and a spike
nt twice the latency (~) identified as n .p .t .n . In (C) a unit
(~) within phase
Vol. 9, No. 24
UNITS IN SENSORIMOTOR CORTEX
relationship to the EEG slow waves (upper channel)
1393
is driven by a stimulus deli-
vered to CM a short time after a spontaneous discharge of the unit
(lower chan-
nel) . Note lack of collision suggesting the orthodromic nature of the unit response . in (D) a unit ( ""
) is evoked at a latency of as much as 15 cosec . and
which was also confirmed as orthodromic response . In
(E) a unit is evoked phase-
locked to the recruiting wave . A notable low variability of latency value,
high
reliability and sharp threshold for one discharge at weak stimulus and with double discharge at stronger stimulus level were observed . In (F) three successiv® unit responses are shown which were each obtained with 2.5 cosec . delay after their spontaneous discharge, which is about half the latency of the unit response . Note lack of collision, high reliability for the double discharge and the practically constant latent value .
Fiq. 3 An illustration of the inhibition of CM-evoked area 6 unit by ENT preconditioning. In
(A) are shown successive control unit responses to CM stimulation at
1001 response rate and in
(B) the full inhibition by the preconditioning stimu-
1394
iJNITS IN SENSORIMOTOR CORTEX
Vol . 9, No. 24
lus obtained with inter-stimuli intervals not longer than 30 meet . In (C) only part of the responses (338) are inhibited when inter-stimulus interval is 36 msec ., and in
(D) the inhibition ie at nil when the interval is 50 meet . The
insert diagram shows the e-fold decline of the inhibition with increase in inter-stimulus interval . Sane of these units were evoked by ENT single pulse stimulation as well and evidence was obtained in some of these cases of ENT-driven units that they were post-synaptically discharged . DISCUSSION The characteristics of most SM unit responses to stimulation of CM, including those shown to be post-synaptically discharged, were found to be low variability of latency among successive responses of a unit, a sharp threshold,
and
reliability of response which approached unity . All of these characteristics are not claimed to be unique to CM . Low variability in successive units was shown also with unit responses in other regions (23) . They are in accord with an hypothetic gating function ascribed to this nucleus
(1,2,4) . They are shown all at
the same time with the CM-driven units . One may assume that, if appropriately synchronised, a CM input with such characteristics may provide a ramp of exitation for effective occurrence of hetero-synaptic summation with a dependable timing . It is noteworthy that these properties satisfy also the requirement of cybernetic theory that a gate should not display threshold jitter . It is rather significant that CM signals possessing all of these characteristics at the same time can also be inhibited by preconditioning stimuli to ENT, logue of globus pallidus medium . However,
the presumed homo-
it must be emphasized that the mechan-
ism of this latter inhibition is not yet clear and the possibility that it may be a result of action through axon collaterals of fibers en passage activated antidromically was not eliminated .
Vol . 9, No . 24
UNITS IN SENSORIMOTOR CORTEX
1395
SUMMARY Responses of neurones of the cat aenaorimotor cortes
(SM) are synoptically
evoked by single pulse stimulation of center median nucleus (CM) with latencies ranging from 2 .8 to 15 meet . or more . These were shown to be characteristically lacking in individual variability, to have great reliability of response, a very sharp threshold, to be widely distributed among each neuronal type of SM, and some to be inhibited by ENT preconditioning with high frequency 40 meet . train of stimuli, an inhibition which may last as long as 50 meet . or more . It has been proposed that the above mentioned characteristics are consistent with a function of gating of excitability which has been ascribed to the CM nucleus . Acknowledgement - The author is grateful to Professor B . Libet for his encouragement, advice and commenta, to Dre. W.W .Alberta, E.W .Wright,Jr ., and W .Mehler for their suggestions and discussions, and to Arthur Johnston and Ruth Blum for their assistance throughout this work . This investigation was supported , in part, by USPHS Grant NS-05061 from the National Institutes of Health, Bethesda, Md ., U .S .A . REFERENCES 1.
H .H . JASPER, Electroenceph . and Clin . Neurophysiol . 1, 405 (1949) . s
2.
H .H . JASPER, in : Handbook of Physiology, Neurophyaiology iI , S . Field, H .W . Maqoun, and V .E . Hall (Eds .) Amer . Physiol . Soc., Washington D .C . p 1307 (1960) .
3.
B . BLUM, M. MANOACH, S . GITTER and H. ASKENASY, Proceed . 6th Int . Cong . Electroenceph. and Clin . Neurophysiol ., Vienna, Austria, p 471 (1965) .
4.
D .P . PURPURA, T .L . FRIGYESI, J.G . McMURTRY and F . SCARFF, in : "The Thalamus ; D .P . PURPURA and M .D . Yahr (Eds .) Columbia Univ . Press, N.Y . p 153 (1966) .
5.
W .R . MEHLER, in : " The Thalamus ", D .P . Purpurs and M .D . Yahr Univ . Press, N.Y . p 109 (1966) .
6.
A. ELIZUR, B . BLUM and U . SANDHANK, Israel J . Med . Sc . 6,
7.
J. AUER,
S.
J.M . PETRAS, Anat . Rec. 148, 322 (1964)1 VIII Intern . Conqr . Anat ., Wiesbaden (1966) .
9.
D. BOWSHER, in : " The Thalamus " , D .P .~Purpura and M . Yahr Univ . Press N.Y . pp 99-127 (1966) .
J. Anat . 90, 30 - 41
(Eds .) Columbia
321 (1970) .
(1956) .
(Eda .) Columbia
1398
UNITS IN SENSORIMOTOR CORTEX
Vol. 9, No . 24
10 .
J . FORTUYN DROOGLEEVER and R. STEFENS, Electroenceph . and Clin . Neurophyei ol . 3 , 393 (1951) .
11 .
M.E . SCHIESEL and A.B . SCHIESEL, in : Brain Research Special Issue : "Forebrain Inhibitory Mechanisms", J . Schlag and A . Schiebel (Eds .) Elsevier Pub ., Amsterdam p 60 (1967) .
12 .
W.E . LEGROS, CLARK and R.H . BOGGON, Brain 56, 83
(1933) .
13 .
C. VOGT and O . VOGT, Psychol. U . Neurol .,
(1941) .
14 .
W.J .H . NAUTA and D.G . WHITELOCK, in : " Brain Mechanisms and Consciousness" J.F . Delafresnaye (Ed.), Charles C . Thomas, Springfield,Ill . pp 81-116 (1954)
15 .
T.P .S . POWEL and W.M . COWAN,
16 .
W.J .H . NAUTA and W.R . MEHLER, Anat . Rec ., 139, 260 (1961) .
17 .
T. SHIMAMOTO and M . VERZEANO, J . Neurophysiol ., 17, 278 (1954)
18 .
R. HASSLER, in : "Introduction to Steriotaxis with an Atlas of the Human Hrain", G . Scholtonbrand and P. Bailey (Eds .), Vol . I, Thieme, Stuttgart p 230 (1959) .
19 .
H. SLUM and B . FELDMAN, IEEE Transactions on Biomedical Engineering 12, 121 (1965) .
20 .
B . SLUM, L .M . HALPERN and A .A . WARD, Eimer . Neurology , 20, 156 (1968) .
21 .
W .R . HESS," Reitrage zur Physiologie Hirnstammes . Die Methodik der Lokali sierten Reisung und Ausschaltung Subortikaler Hirnabschnitte ", George Thieme, Leipzig (1932) .
22 .
R. HASSLER and K . MURS-CLEMENT, J . Hirnforschunq , ~,
23 .
P . BACH-Y-RITA, Exper . Neurology , 9,
50, 32
Brain , 79, 364 (1956) .
327 (1964) .
377
(1961) .
Pergamon Press
CHARACTERISTICS OF DRIVING OF UNITS IN THE SENSORIM(YTOR CORTE% HY CENTER MEDIAN NUCLEUS AND ITS INHIBITION BY ENTOPEDUNCUIJIR NUCLEUS* B. Blum ** Mount Zion Neurological Institute, San Francisco, California,U .S .A .
(Received 10 July 1970; in final form 20 October 1970) Interactions between the sensorimotor cortex (SM),thalamic nuclei, the striatum and the pallidum (1,2,3,4) may be assumed to depend on connectivitiea such as those schematized in Fiq . 1.
earoa erRUe t ~RE~ ~ s e) /ROREUD AllE1.e
erRw e-e)
Fig .
1
Proposed network emphaslzinq closed-circuit cornectivities of the cat SM . One circuit includes as a descending limb the cortico-putaminal projections (3) and as an ascending limb, projections from putamen (PUT) to entopeduncular nucleus (ENT),
the assumed cat homologue of primates' medial globus .pallidus (5), hence
to ventrolateral thalamus center median (CM)
(VL)
and then to SM .Another hypothetic circuit is from
to PUT and back to CM (5) . Projections from and to CM and VL
to and from SM are also shown (5,6,7,8,9 ,1p iHlum et al ., in preparation) . *This paper is dedicated to the memory of my friend and fellow scientist Warren S .Mc:Culloch . The results were presented in part to the lat Meeting of the European Brain and Behaviour Society, Marseilles, Oct . 1969 . Present address : Department of Physiology and Pharmacology, Tel Aviv University Medical School, Tel Aviv, Israel .
1389
139 0
iJNITS IN SENSORIMOTOR CORTEX
Vol. 9, No. 24
Accumulated information on CM-SM interactions are suggestive of the importance of CM for integration of movement at the sensorimotor cortex as well as at other levels
(2, and Blum et al . in preparation) . An intimate relationship has
been claimed for this nucleus also to the extrapyramidal system
(11,
12,13,14,15,
16,17) . Functionally, CM seems to be part of the thalamic reticular formation (11) and in fact it has been shown to play a role in gating excitability at cortical (1,2) and at subcortical levels
(4) .
An attempt was made to investigate some of the meanings of these relationships by a study of unitary responses in SM
to CM
stimulation, including the
effects upon these responses of preconditioning stimuli to ENT, VL, or to PUT . Since the location of CM in the cat is shown differently by different authors because of use of different criteria
(2,5) selection of CM targets in the
present work was based on microphysiological and electrophysiological consider ations, as guideline was used the often proposed division of that nucleus into medio-roatral and ventro-lateral portions
(5) . A preliminary report of our re-
sups will be presented here . METHODS Ten adult cats were prepared surgically under ether anesthesia and were studied electrographically under local procaine anesthesia, Gallamine HC1 paralysis and artificial respiration . Stimulation electrodes and microelectrodes were applied, using methods already reported in our previous studies (19,20), Bipolar stimuli were delivered to targets in CM,VL,PUT,ENT and pyramids which were selected according to Nissl and silver impregnation histological sections . Test stimuli delivered to CM consisted of single pulses 0 .1 to 0 .2 msec . in duration and close to threshold in intensity which amounted to about 0 .06-1 mAmp . currents . Preconditioning stimuli delivered to ENT,PUT, or VL consisted of trains of stimuli . Each such train was 40 cosec . in duration, consisting of pulses at 125200 c/sec .,
each pulse 0 .1-0 .2 cosec . in duration and of threshold intensity for
evoking cortical field potentials . Curreht spread to neighbouring structures was
Vol. 9, No. 24
UNITS IN SENSORIMOTOR CORTEX
1391
minimized by use of short pulse durations and of threshold voltages . it was monitored by placing electrodes at critical sites . Current spread to the capsule interns was checked by having electrodes on the pyramids . Inter-stimuli intervals of 0 to BO cosec . were tested . Neurones were identified whether they were of pyramidal tract neurone (p .t .n .)
type or not (n .p .t .n .) before being studied
further . This was done by testing whether they gave antidromic responses following stimulation of the pyramd.d . Criteria used in this and also in defining unit responses to CM
whether they were antidromic or post-synaptic discharges
were those mentioned in our previous studies (20) " In some recent confirmatory experiments* safer answers to these questions were obtained by use of the col lision teat as follows : the spontaneous diechargea of the unit tested were made to trigger the oscilloscope and after a selected interval also to trigger the stimulator . Thus, the test atimulua could be given at a selected delay from the spontaneous unit discharge or, in same cases, from a spike triggered by stimulation through the microelectrode . This interval was then adjusted so that any antidromlc impulse generated by the test atimulua would meet, en route,
the
orthodromic impulse of the spontaneous discharge, and mutual annulment
would
occur . Therefore, observations of such annulment
or of lack of annulment of
unit responses under such conditions following the test Stimulus would provide supportive evidence whether the unit evoked otherwise by this stimulus is antidromic or orthodramic .** At the end of each experiment the actual locations of stimulation and of recording electrodes were confirmed hiatologically (21) .
* These experiments were done at the author's present address with aid of Mr . Deli whose technical assistantship was enabled by generous support from L.E .Phillipa Fund for psychobiological research . ** In extracellular recordings such a test can be carried out only with units which show spontaneous discharges, or that can be excited through the microelectrode . Other limitations of the test are that a spontaneous or evoked discharge of the soma may produce an impulse that may not travel under the conditions of the experiment into the fiber tested
(Slum et al . unpublished) .
1392
iJNITS IN 3EN30RIMOTOR CORTEX
Vol. 9, No . 24
RESULTS SM units were driven by CM stimulation with latencies which range from 2,8 to 15 msec, or more . A large number of these, which satisfied criteria for postsynaptic discharges, including lack of collision of the impulse generated by the CM stimulation with that of the spontaneous discharges showed the following characteristics : they lacked in individual variability among successive responses, they showed sharp thresholds, they were intensely stimulus-bound, they were widely scattered in SM in all its various parts as delimited by Hassler and Muhs-Clement (22), they were p .t .n . and n .p .t .n, and some were shown to be inhibited by high frequency train stimuli delivered as pre-conditioning to ENT (Fig . 2 and 3) .
Fig. 2 Extracellular SM unit responses following CM stimulation showing the characteristics enumerated in the text . In these tracings and in the following ones the time of stimulation is marked with dots at bottom . A,B,E taken from cat and C,D,F from squirrel monkey . In(A~are depicted stimulus-bound waves (f) recorded in area 4 which presumably are synaptic potentials . They simanate on intensifying tlhe stimulus until a spike (#) is triggered, the latter identified as p .t .n . In fib)
reversal of stimulus polarity evoked similar synaptic potentials and a spike
nt twice the latency (~) identified as n .p .t .n . In (C) a unit
(~) within phase
Vol. 9, No. 24
UNITS IN SENSORIMOTOR CORTEX
relationship to the EEG slow waves (upper channel)
1393
is driven by a stimulus deli-
vered to CM a short time after a spontaneous discharge of the unit
(lower chan-
nel) . Note lack of collision suggesting the orthodromic nature of the unit response . in (D) a unit ( ""
) is evoked at a latency of as much as 15 cosec . and
which was also confirmed as orthodromic response . In
(E) a unit is evoked phase-
locked to the recruiting wave . A notable low variability of latency value,
high
reliability and sharp threshold for one discharge at weak stimulus and with double discharge at stronger stimulus level were observed . In (F) three successiv® unit responses are shown which were each obtained with 2.5 cosec . delay after their spontaneous discharge, which is about half the latency of the unit response . Note lack of collision, high reliability for the double discharge and the practically constant latent value .
Fiq. 3 An illustration of the inhibition of CM-evoked area 6 unit by ENT preconditioning. In
(A) are shown successive control unit responses to CM stimulation at
1001 response rate and in
(B) the full inhibition by the preconditioning stimu-
1394
iJNITS IN SENSORIMOTOR CORTEX
Vol . 9, No. 24
lus obtained with inter-stimuli intervals not longer than 30 meet . In (C) only part of the responses (338) are inhibited when inter-stimulus interval is 36 msec ., and in
(D) the inhibition ie at nil when the interval is 50 meet . The
insert diagram shows the e-fold decline of the inhibition with increase in inter-stimulus interval . Sane of these units were evoked by ENT single pulse stimulation as well and evidence was obtained in some of these cases of ENT-driven units that they were post-synaptically discharged . DISCUSSION The characteristics of most SM unit responses to stimulation of CM, including those shown to be post-synaptically discharged, were found to be low variability of latency among successive responses of a unit, a sharp threshold,
and
reliability of response which approached unity . All of these characteristics are not claimed to be unique to CM . Low variability in successive units was shown also with unit responses in other regions (23) . They are in accord with an hypothetic gating function ascribed to this nucleus
(1,2,4) . They are shown all at
the same time with the CM-driven units . One may assume that, if appropriately synchronised, a CM input with such characteristics may provide a ramp of exitation for effective occurrence of hetero-synaptic summation with a dependable timing . It is noteworthy that these properties satisfy also the requirement of cybernetic theory that a gate should not display threshold jitter . It is rather significant that CM signals possessing all of these characteristics at the same time can also be inhibited by preconditioning stimuli to ENT, logue of globus pallidus medium . However,
the presumed homo-
it must be emphasized that the mechan-
ism of this latter inhibition is not yet clear and the possibility that it may be a result of action through axon collaterals of fibers en passage activated antidromically was not eliminated .
Vol . 9, No . 24
UNITS IN SENSORIMOTOR CORTEX
1395
SUMMARY Responses of neurones of the cat aenaorimotor cortes
(SM) are synoptically
evoked by single pulse stimulation of center median nucleus (CM) with latencies ranging from 2 .8 to 15 meet . or more . These were shown to be characteristically lacking in individual variability, to have great reliability of response, a very sharp threshold, to be widely distributed among each neuronal type of SM, and some to be inhibited by ENT preconditioning with high frequency 40 meet . train of stimuli, an inhibition which may last as long as 50 meet . or more . It has been proposed that the above mentioned characteristics are consistent with a function of gating of excitability which has been ascribed to the CM nucleus . Acknowledgement - The author is grateful to Professor B . Libet for his encouragement, advice and commenta, to Dre. W.W .Alberta, E.W .Wright,Jr ., and W .Mehler for their suggestions and discussions, and to Arthur Johnston and Ruth Blum for their assistance throughout this work . This investigation was supported , in part, by USPHS Grant NS-05061 from the National Institutes of Health, Bethesda, Md ., U .S .A . REFERENCES 1.
H .H . JASPER, Electroenceph . and Clin . Neurophysiol . 1, 405 (1949) . s
2.
H .H . JASPER, in : Handbook of Physiology, Neurophyaiology iI , S . Field, H .W . Maqoun, and V .E . Hall (Eds .) Amer . Physiol . Soc., Washington D .C . p 1307 (1960) .
3.
B . BLUM, M. MANOACH, S . GITTER and H. ASKENASY, Proceed . 6th Int . Cong . Electroenceph. and Clin . Neurophysiol ., Vienna, Austria, p 471 (1965) .
4.
D .P . PURPURA, T .L . FRIGYESI, J.G . McMURTRY and F . SCARFF, in : "The Thalamus ; D .P . PURPURA and M .D . Yahr (Eds .) Columbia Univ . Press, N.Y . p 153 (1966) .
5.
W .R . MEHLER, in : " The Thalamus ", D .P . Purpurs and M .D . Yahr Univ . Press, N.Y . p 109 (1966) .
6.
A. ELIZUR, B . BLUM and U . SANDHANK, Israel J . Med . Sc . 6,
7.
J. AUER,
S.
J.M . PETRAS, Anat . Rec. 148, 322 (1964)1 VIII Intern . Conqr . Anat ., Wiesbaden (1966) .
9.
D. BOWSHER, in : " The Thalamus " , D .P .~Purpura and M . Yahr Univ . Press N.Y . pp 99-127 (1966) .
J. Anat . 90, 30 - 41
(Eds .) Columbia
321 (1970) .
(1956) .
(Eda .) Columbia
1398
UNITS IN SENSORIMOTOR CORTEX
Vol. 9, No . 24
10 .
J . FORTUYN DROOGLEEVER and R. STEFENS, Electroenceph . and Clin . Neurophyei ol . 3 , 393 (1951) .
11 .
M.E . SCHIESEL and A.B . SCHIESEL, in : Brain Research Special Issue : "Forebrain Inhibitory Mechanisms", J . Schlag and A . Schiebel (Eds .) Elsevier Pub ., Amsterdam p 60 (1967) .
12 .
W.E . LEGROS, CLARK and R.H . BOGGON, Brain 56, 83
(1933) .
13 .
C. VOGT and O . VOGT, Psychol. U . Neurol .,
(1941) .
14 .
W.J .H . NAUTA and D.G . WHITELOCK, in : " Brain Mechanisms and Consciousness" J.F . Delafresnaye (Ed.), Charles C . Thomas, Springfield,Ill . pp 81-116 (1954)
15 .
T.P .S . POWEL and W.M . COWAN,
16 .
W.J .H . NAUTA and W.R . MEHLER, Anat . Rec ., 139, 260 (1961) .
17 .
T. SHIMAMOTO and M . VERZEANO, J . Neurophysiol ., 17, 278 (1954)
18 .
R. HASSLER, in : "Introduction to Steriotaxis with an Atlas of the Human Hrain", G . Scholtonbrand and P. Bailey (Eds .), Vol . I, Thieme, Stuttgart p 230 (1959) .
19 .
H. SLUM and B . FELDMAN, IEEE Transactions on Biomedical Engineering 12, 121 (1965) .
20 .
B . SLUM, L .M . HALPERN and A .A . WARD, Eimer . Neurology , 20, 156 (1968) .
21 .
W .R . HESS," Reitrage zur Physiologie Hirnstammes . Die Methodik der Lokali sierten Reisung und Ausschaltung Subortikaler Hirnabschnitte ", George Thieme, Leipzig (1932) .
22 .
R. HASSLER and K . MURS-CLEMENT, J . Hirnforschunq , ~,
23 .
P . BACH-Y-RITA, Exper . Neurology , 9,
50, 32
Brain , 79, 364 (1956) .
327 (1964) .
377
(1961) .