Responses evoked in nucleus medialis dorsalis of the thalamus by subcortical stimulation. A microelectrode study

BRAIN RESEARCH

35

RESPONSES EVOKED IN NUCLEUS MEDIALIS DORSALIS OF THE T H A L A M U S BY SUBCORTICAL STIMULATION. A M I C R O E L E C T R O D E STUDY

H O R A C I O ENCABO AND A R T U R O J O R G E B E K E R M A N

Centro de lnvestigaciones Neurol6gicas del lnstituto Torcuato Di Tella, Hospital de Ni~os, Buenos Aires (Argentina) (Accepted October 22nd, 1970)

INTRODUCTION

Previous studies have demonstrated the polysensory nature of the peripheral input to the nucleus medialis dorsalis (MD) of the thalamus 9,1°,2'~. Furthermore, the great majority of the subcortical projections to the MD, as described by various authors for different mammalian species 1,7,11,14,16,19-21,23-25,27-29, originate t,'om other nuclear masses with equally well-known polysensory afferents2,3,8,1°,17,zL The present work was designed to shed further light upon the nature of these connections. Five structures were selected for this study: the centromedian nucleus (CM), the mesencephalic reticular formation (MRF, FRM), the septum (Spt), the amygdala (Amg) and the posterior hypothalamus (Hpt). MATERIAL AND METHODS

Fifty-two adult cats were used. Five were anesthetized with a single intravenous dose of chloralose (80 mg/kg), whereas in 47 cats the surgical procedure was carried out under ether narcosis and procaine infiltration of the incision and pressure zones. All animals were placed in a standard stereotaxic apparatus, paralyzed with gallamine triethiodide and artificially ventilated. All the structures were approached by a dorsal route with the exception of the hypothalamus which was impaled horizontally from behind with an electrode introduced through the cerebellum and brain stem. The area under study was that encompassed by the coordinates A8-10, L 0.5-2 of Jasper and Ajmone Marsan a5 and Snider and Niemer 26. Stimulation was always ipsilateral with the following standard coordinates: CM: A7, L 2.7, H + 1; Amg: A 11, L 10, H - - 7; Spt: A 16, L0.5, H + 1; MRF: A0, L0.5, H + 1 and A 3, L 3, H--2;Hpt:A9, L 1, H - - 3 . The extracellular electrical activity was recorded with steel microelectrodes sharpened according to the technique described by Green 12 with an initial resistance Brain Research, 28 (1971) 35-46

36

11. E N C A B O A N D A. J. BEKERMAN

of 5-20 M ~ . The signals were ted through a bioelectric neutralized input capacity amplifier to a 122 Tektronix amplifier, and displayed on a 565 Tektronix CRO whose vertical signal output was connected to the input of an SP 300 Ampex tape recorder. The material stored on a tape was subsequently photographed: Stimulation was carried out through concentric macroelectrodes delivering short duration (0,5-1.5 msec) single rectangular (1-10 V) pulses or high frequency trains (200--300/sec). The physiological state of the preparations was carefully controlled, the rectal temperature monitored and kept between 37.5 and 38.5°C, and the cortical vascularization and pupillary size were watched. After the surgical procedure, the animal was allowed to recover for not less than 2 h. After routine hardening, 20 # m serial sections of the brain were stained with thionine for demonstration of electrode tracks. To diminish cerebral pulsation (a) the exposed cerebral cortex was covered with agar, (b) artificial ventilation was obtained with fast shallow strokes, under pneumothorax in the majority of the experiments, and (c) sometimes the cat's body was suspended in a hammock. RESULTS

General The study included 735 cells: 677 pertained to the nucleus MD while the remaining 58, which we shall call 'boundary cells', were located in the transition zones between the nucleus MD and various neighboring structures, particularly the nucleus paracentralis and centralis lateralis. This group was included in this series since the activity of these 'boundary cells' was similar in all respects to that of the units located within the MD. The 735 cells also included 51 studied under chloralose anesthesia whose latency and response pattern did not differ from that of the684 units observed in unanesthetized animals. The total of 735 cells will therefore be considered a homogeneous group. The spontaneous activity was similar to that described in a previous report 9 where the only technical difference was the use of glass microelectrodes. Positivenegative spikes of different amplitudes, but of constant duration of the positive phase (1-1.5 msec), were observed. The discharges were either irregular single spikes or somewhat regular rhythmic bursts. Silent units whose activity could only be aroused by stimulation were likewise observed.

Type of responses Many cells responded to single shocks, although in a significant number, the use of high frequency (200/sec) trains was more effective than increased intensity o r duration of single stimuli. We found neither particular response patterns t o any of the stimulating sites nor response modifications with changes in stimulus intensity ;however, no systematic observations on this subject were made.

Brain Research, 28 (1971) 3546

M D UNITS EVOKEDBY CENTRAL STIMULATION a

mslc

37

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~ ' FRM Fig. 1. Responses Type 1 and II. FRM, mesencephalic reticular formation stimulation, a, Single spike response in a silent cell. b, Long-lasting response in two silent cells, c, Response consisting of the arrest of firing in a spontaneously active unit. d, Response diminution with successive stimuli. Time calibration common to all records. Voltage calibration common to a, c and d. Positivity is upwards in this and subsequent figures.

The usual response was of an excitatory nature (Type I), i.e., brief discharges sometimes of a single spike (Fig. la), transient acceleration of spontaneous discharge, or more frequently the appearance of repeated bursts of 3-4 spikes. Long duration responses were only seen exceptionally (Fig. lb). Suppression of spontaneous activity was also observed for different periods of time (Type II, Fig. lc). In such cases a single spike was sometimes observed following stimulation, but since this was inconstant and the delay between the stimulus artifact and the succeeding spike was highly variable, it was accepted that this was not an excitatory phenomenon but rather the result of the time elapsed between stimulation and the development of suppression, spontaneous activity being still present. This diminution of the rate of discharge was often associated with brief complex excitatory phenomena, depending upon the preceding pattern of activity of the unit (Type III, Fig. 2). The lability of the responses was comparable with that of many other central structures. Stimulus frequencies above 0.5/sec usually led to the diminution or abolition of the response (Fig. ld). The latency could be from 2 to 2000 msec, but the usual range was between 200 and 600 msec (Fig. 3). Variations of the latency were observed for the same unit without changes of the stimulus parameters. Such variations were not large for short latencies (2-3 msec for 20-30 msec latencies) but were more significant (200-300 msec or more) for latencies above 500 msec (Fig. 3a and b). Fig. 3 also shows variations of the latency which depended on changing the site of stimulation. The efficiency of stimulation clearly depended upon the nuclear mass that was stimulated (Table I). Of the cells under study, 50 ~ responded to CM stimulation, the percentage of responsive ceils being much lower with stimulation of other structures, i.e., Spt 34.7, M R F 20.7, Amg 20.8, H p t 16.7 ~ . Neither specific projections from any particular region of the stimulated nuclei, nor topographical differences could be detected within the explored areas of the MD. Nevertheless a somewhat larger number

Brain Research, 28 (1971) 3546

38

H. ENCABO AND A. J. BEKERMAN

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Fig. 2. Responses Type III. a, b and c, Records of the same cell to center median stimulation (CM). a, Spontaneously silent, long latency burst response, b, Spontaneously active, long arrest of-ftring i c, Combination of a and b responses, d, e and f, Another unit, Amg: amygdatar stimulation, d, Spontaneously silent, single spike or brief response, e, Spontaneously active, pause and long latency response, f, Same response but with an additional brief, short latency discharge. 7.

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+ I Fig. 3. Latency histograms. The values are expressed as a percentage of responses of the total number of units studied. The numbers indicate the quantity of units recorded for each stimulated area. Insets a and b: the same cell stimulated by F R M and CM respectively, a, Constant, short duration latencies. b, Long and variable latencies. Stimulus artifacts at beginning of the sweep, a, time calibration 100 cycles, b, time calibration 1 cycle. Voltage calibration, 1 mV for both records. Spikes retouched in b. Brain Research, 28 (1971) 35-46

MD

39

U N I T S EVOKED BY C E N T R A L S T I M U L A T I O N

TABLE I M D RESPONSES TO SUBCORTICAL STIMULATION

Stimulation

CM MRF Spt Amg Hpt

Units tested

Responses

Total

Activation

Inhibition

Complex

254 260 311 342 216

128 (50.4~) 54 (20.7~) 108 (34.7~o) 71 (20.8~) 36 (16.7~)

106 (82.8~o) 36 (66.7 ~) 89 (82.5 ~) 46 (64.9 ~) 25 (69.4~)

12(9.4~) 14 (25.9~) 17 (15.7~) 16 (22.5 ~) 8(22.2%)

10(7.8~) 4 (7.4~) 2(1.8~) 9 (12.6~o) 3(8.4~o)

of responses in the ventral portion of the MD was disclosed, particularly when the CM and M R F were stimulated. Fig. 4 shows the uneven topographical distribution of the afferents to the MD. The abscissae of the histograms in this figure arbitrarily divide the nucleus MD into 5 dorsoventral zones; these divisions correspond approximately to the dimensions in mm of this nucleus as outlined in frontal Planes 8-9 of the Jasper and Ajmone Marsan atlaslS.The ordinates, on the other hand, show the percentage of the responses as recorded at various depths of the microelectrode track for each stimulated nucleus. The projections from the CM and M R F nuclei end mainly in the ventral zones whereas those from the hypothalamus, septum and amygdala are more homogeneously distributed. Stimulation of the centromedian nucleus A study was made of 254 cells. A high percentage (128 units or 50.4 ~ ) of these responded to the activation of this structure. The majority of the responses (106 units or 82.8 ~ ) were of excitatory Type I (Table I). Fig. 3 shows the latency histogram of 91 units. Responses with latencies below 300 msec were predominant, but only 7 cells were below 20 msec values. Two cells had latencies of 5 and 2 msec, respectively. The long latency responses were almost invariably composed of one or more high frequency spike bursts. In addition to the aforementioned latency variations for a given unit (see Results, General), two neurons showed latency variations related to the type of stimulation. In one of these, a much shorter latency was obtained with a single shock than with a train of stimuli. In the other unit, the latency diminished with increasing stimulus frequency (more than 700 msec at 0.1, but only 250 msec at 3/sec). In this particular experiment the decrease in latency with increased stimulus frequency only appeared after the second or third volley at the new frequency. Stimulation of the mesencephalic reticular formation Responses following stimulation of the M R F were observed in 54 of the 260 neurons (20.7 ~o). Thirty-six cells (66.7 ~ ) were of excitatory Type I (Table I). It must be stressed that M R F stimulation gave burst responses only exceptionally. The latency

Brain Research, 28 (1971) 35-46

40

H. ENCABO AND A. .I. BEKERMAN

histogram (Fig. 3) for 27 units shows a fairly uniform distribution, values below 300 msec being clearly predominant. Latencies below 10 msec or above 400 msec were never encountered. When the density of the projections from the M R F to the nucleus M D was analyzed, two different reticular zones could be outlined. One of these, more laterally located (L 2-3; H - - 1, - - 2) in the region of the nucleus reticularis pontis oralis and central tegmental tract, aroused fewer thalamic responses (11 out of t26 M D units). The other one, more medially located (L 0.5-1; H ..... 0.5, 1) in the central gray matter, activated a larger number of M D units (43 out of 134 units).

Septal stimulation The effect of septal stimulation was studied in 311 M D cells, 108 responsive units being observed (34.7 ~o): 89 (82.5 ~ ) were purely excitatory Type I cells (Table I). Patterns of two or three burst discharges occurring at variable intervals were clearly predominant. The latency histogram from 52 units (Fig. 3) shows a considerable dispersion of the values. Few of these were longer than 900 msec, and latencies below 20 msec were never seen.

Stimulation of the amygdala The effect of stimulation of the amygdaloid complex was studied in 342 M D cells, 71 responsive units (20.8 %) being found: 46 (64.9 ~ ) were of Type 1 (Table I). Burst responses, as seen with septal stimulation were clearly predominant. Latency analysis (Fig. 3) also shows a striking similarity with the behavior after septal stimulation: the latency histogram for 42 cells is similar and no latency below 20 msec was observed.

Hypothalamic stimulation Responses in M D following hypothalamic stimulation were scarce: 36 (16.7 ~/o) responsive units out of a total of 216 were observed: 25 (69.4 ~ ) were of Ty pe I (Table I). The latency histogram of 21 cells (Fig. 3) shows a large proportion of units with latencies below 300 msec. A short latency of 5 msec was recorded in two cells and one of 6 msec in another cell.

Convergence The experimental set-up employed for this study only permitted the insertion of one recording and two stimulating electrodes. Observations were therefore restricted to identifying cells responding to the stimulation of either one or two structures out of the five under study. No interaction study between two stimulation sites was undertaken, although convergence from two stimulated areas onto one recording site was disclosed in 72 (30.5 ~o) out of the 236 cells. Figs. 5-7 illustrate the characteristics of the responses of cells showing clear

Brain Research, 28 (1971) 35-46

MD

41

UNITS EVOKED BY CENTRAL STIMULATION

Hpt 36u

Spt 102u Amg 67u

CM 115u FRM 50u

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Fig. 4. Distribution of responses as a function of the recording sites (see text). F R M and Amg, dotted line. CM, Spt and Hpt, filled line. CM-Amg 28u

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Fig. 5. Convergence. The surface of each circle is proportional to the total number of units studied. The black sectors correspond to the percentage of units showing convergence from the indicated pairs of stimulated areas.

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Fig. 6. FRM CM convergence, a, b, c and d, Four different units, a and b, Type I and II responses respectively for both indicated stimulations, c, Type I response for F R M and Type II response for CM stimulation, d, A unit with the opposite response to that shown in c. The voltage calibration in c corresponds to records b, c and d. The time calibration is common to all records.

Brain Research, 28 (1971) 35-46

42 y. 1

H. ENCABOAND A. J. BEKERMAN CM 47 u

FRM 26 u

FRM CM

90 55msec 80

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200

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Fig. 7. Histograms of short latency responses produced by stimulation of the FRM and CM. Number of recorded units as indicated. To the right: table of pairs of latency values for 12 units with convergence to the FRM and CM stimulation.

evidence of convergence. Stimulation of either the CM or M R F in the 4 neurons shown in Fig. 6 led to similar responses (excitation a, inhibition b ) o r to dissimilar responses (c, d). The amygdala and septum as well as the hypothalamus and amygdala could also successively influence thalamic units. As can be deduced from the schemes of Fig. 5, the degree of convergence onto each group of M D cells depended upon the particular pair of nuclei that were activated. Most of the possible combinations were studied. The largest degree of convergence was found with interplay of Spt-Amg (convergence 17/total 20), C M - M R F (C 22/T 60) and Amg-Hpt (C 12/T 3t), and the least with C M - A m g (C 2/T 28) and M R F - S p t (C 3/T 22). Intermediate values were found for CM-Spt (C 4/T 15) and Spt-Hpt (C 12/T 60). The convergence from septal and amygdalar rhinencephalic structures was very conspicuous, the latencies from each of these nuclei being similar. In view of the high degree of convergence between CM and M R F and the great number of cells responding with latencies below 300 msec, more precise latency measurements were made. The observed differences indicated the independence of the activated projections. The histograms shown in Fig. 7 correspond only to the tatencies below 300 msec and exhibit a significantly different spectrum. Furthermore, of 12 cells grouped in the right columns (Fig. 7) and showing effective convergence, three had the same latency and, with only one exception, the remaining nine had much longer latencies after CM stimulation than after M R F activation, as already shown in Figs. 3a and b and 6a. DISCUSSION The present electrophysiological findings would apparently agree with the current anatomical literature (see Introduction), where projections from the explored nuclei towards the MD have been repeatedly described. But the conspicuous predominance of long latency responses, as shown by our experiments, is hard to reconcile with the monosynaptic connections suggested by the morphological data. On the other hand, the different zones of each of the structures under study Brain Research, 28 (1971) 3546

MD

UNITS EVOKED BY CENTRAL STIMULATION

43

exhibit a variable density of areas projecting towards MD. For instance, the pathway from the amygdala to the MD described by Valverde 28 originates orally to the zones of the Amg which were stimulated in our experiments. On the contrary, the septal and amygdalar zones stimulated by Sager and Butkhuzi 2~ and by Trembly and Sutin 27 were similar to those explored by us but we never found the low latencies (below 10 msec) reported by these authors with evoked potential technique. Responses following latencies greater than 300 msec were very numerous. This finding agrees with previous reports related to MDg, 10 or other2,a, 18 structures. That these long latency responses are usually high frequency spike bursts seems significant. The possible explanations of such findings could be one of the following: (a) a polysynaptic circuit, (b) a slow conduction velocity, (c) long duration inhibitory phenomena followed by a rebound discharge, or (d) various combinations of these mechanisms. The assumption that a polysynaptic circuit is involved does not entirely explain our findings. Latency variations of 100-200 msec (or more) for a given cell and stimulus locus and parameter, and the significant decrease of these values with the increase in frequency of stimulation, are findings that do not support such a simple interpretation. The Scheibels 24 have pointed out that many intrathalamic fibers are of very small diameter, hence of a very slow conduction velocity; but this as well cannot be the only explanation of our experimental results, in particular when the variations in latency are considered. The soundness of the third explanation - - a rebound discharge following a long duration inhibition4, 5 - - seems to be greater. Intracellular recording is mandatory to obtain a final answer, but some of the findings obtained extracellularly seem to favor this interpretation. In fact, while many of the cells responding with one or several long latency bursts were spontaneously silent, other units had their spontaneous discharge inhibited by stimulation with a burst after this pause. It could be argued that the response is actually similar in both cases, an initial long duration inhibitory potential being concealed in the first by the lack of spontaneous discharge. Extracellular recording, in spontaneously silent cells, could possibly be interpreted as a long latency response when actually it is a long duration inhibition followed by a rebound discharge. Probably, as finally proposed, more than one of these possible mechanisms play a role in the development of this phenomenon. Type III responses were frequently observed. Since the stimulation parameters were unchanged it can be assumed that the variability of the responses evoked at the same cell is due to the variable pattern of spontaneous activity at the time of stimulation. Stimulation might sometimes induce apparently spontaneous changes of neuronal activity. In fact, the synchronizing and spindle generation effect of CM stimulation and the simultaneous appearance of neuronal burst discharges at widespread subcortical zones are well known. Since the surface cortical electrical activity was not monitored during the experiments reported here it cannot be ruled out that the effect encountered could have been the result of the MD participation in diffuse spindle activity and not the result of specific connections. The activation of the nucleus reticularis thalami and the intrathalamic negative feed-back mechanisms consequently aroused 24,25 should be also taken into account as another possible indirect mechanism of burst responses. Brain Research, 28 (1971) 3546

44

H. ENCABO AND A. J. BEKERMAN

Previous reports have shown converging somatic projections towards the neurons of the M D 9,1° and to the structures stimulated in this work e,3.s,l°.tT,'-'z. The results reported here indicate certain peculiarities of the interconnections of different polysomatic systems. Both the CM and the Spt, the two structures whose stimulation acted upon the greatest number of MD neurons, evoked responses of a similar type (activation) in a high percentage of cases. Yet what was said above about inhibitory phenomena concealed by the extracellular recording technique must be remembered. and if such were so. the percentages of the various types of response would be significantly different. The responses following stimulation of the M R F showed a pattern that can lead to the assumption that these projections to the nucleus M D have distinctive electrophysiological characteristics: predominance o1 short latencies and lack of burst responses. The possible existence in the M D of various neuronal populations is suggested by the study of convergences. There is a group of cells where the rhmencephalic nuclei Spt, A m g and H p t project, while afferents from the M R F and CM converge upon another cellular group. In other words, afferents from these two groups of nuclei rarely converge upon the same M D cell. this being a significant negative finding. In addition to the convergence upon the same M D cell, the rhinencephalic afferents evoke similar responses with long latencies, similar latency distribution and burst-type discharges. Their distribution within studied territories of the M D is more uniform and contrasts with the preferential distribution of afferents from CM and M R F towards the ventral portions of this structure. The convergence between CM and M R F is significant. The connections from the brain stem reticular system to the CM have already been described 6. The CM could therefore be located within the mesencephalic projections towards the MD. and its stimulation might activate both cells and fibers of passage from the same system. Our findings indicate that this is not so. The latencies following the stimulation of CM are usually longer, and the histograms and the comparative table (Fig. 7) clearly indicate the independent characteristics of these two projections. Furthermore. stimulation of the CM and M R F sometimes evoked, at a given M D unit. opposite effects (activation-inhibition); and burst discharges were rarely evoked by reticular stimulation. It must therelbre be accepted that the intbrmation converging from the CM and M R F to the M D has a completely independent origin. Finally, our observations lead to the assumption that there is an organization of the central afferents with at least two cellular populations, one receiving rhinencephalic or limbic projections (Spt, Amg, Hpt) and the other distinguished by the convergence of pathways from the M R F and CM. To this complex spectrum of subcortical afferents should be added those originating in the caudate nucleus t° and hippocampus 13 as previously described in the literature. SUMMARY

The afferents to 735 cells of the dorsomedian nucleus (MD) of the cat's thalamus, Brain Research, 28 (1971) 35-46

M D UNITS EVOKED BY CENTRAL STIMULATION

45

from various subcortical structures, s e p t u m (Spt), a m y g d a l a (Amg), mesencephalic reticular f o r m a t i o n ( M R F ) , p o s t e r i o r h y p o t h a l a m u s (Hpt) and c e n t r o m e d i a n nucleus ( C M ) were studied in unanesthetized curarized acute p r e p a r a t i o n s carefully infiltrated with p r o c a i n e at the sites indicated. Some animals were also chloralosed. The extracellular unit activity was recorded with steel microelectrodes, and short d u r a t i o n square pulses were delivered t h r o u g h concentric macroelectrodes. O f the M D cells, 50.4~o r e s p o n d e d to s t i m u l a t i o n o f the C M , 3 4 . 7 ~ to the Spt, 2 0 . 7 ~ to the M R F , 2 0 . 8 ~ to the A m g and 1 6 . 7 ~ to the Hpt. The responses were o f an excitatory type or consisted o f a transient arrest o f the s p o n t a n e o u s discharge. A c o m b i n a t i o n o f b o t h types o f response was also observed. The latencies ranged between 2 and 2000 msec. N u m e r o u s responses with latencies greater than 500 msec were evoked f r o m A m g , Spt a n d C M , whereas latencies a b o v e 400 msec were never recorded following s t i m u l a t i o n o f the M R F . Seventy-two cells r e s p o n d e d to stimulation o f m o r e t h a n one structure. The convergence between the rhinencephalic nuclei (Amg, Spt) on the one hand, and between the C M and R M F on the other, were conspicuous. The latencies following s t i m u l a t i o n o f the C M were greater t h a n those after M R F stimulation, a finding that would be in favor o f the concept t h a t these two afferent systems to M D are independent. ACKNOWLEDGEMENT

This w o r k was s u p p o r t e d by G r a n t 2546 A and B o f the Consejo N a c i o n a l de lnvestigaciones Cientificas y T6cnicas, Argentina.

REFERENCES 1 AJMONE MARSAN, C., The thalamus. Data on its functional anatomy and on some aspects of thalamo-cortical integration, Arch. ital. BioL, 103 (1965) 847-882. 2 ALBE-FESSARD,D., AND KRUGER, L., Duality of unit discharges from cat centrum medianum in response to natural and electrical stimulation, J. Neurophysiol., 25 (1962) 3-20. 3 AMASSIAN,V. E., AND DEVITO, R. V., Unit activity in reticular formation and nearby structures, J. Neurophysiol., 17 (1954) 575-603. 4 ANDERSEN,P., Rhythmic 10/sec activity in the thalamus. In D. P. PURPURA AND M. D. YAHR (Eds.), The Thalamus, Columbia Univ. Press, New York, 1966, pp. 143-151. 5 ANDERSEN, P., BROOKS, C. McC., AND ECCLES, J. C., Electrical responses of the ventro-basal nucleus of the thalamus. In W. BARGMANNANDJ. P. SCHAD~(Eds.), Lectures on the Diencephalon Progress in Brain Research, Vol. 5, Elsevier, Amsterdam, 1964, pp. 100-113. 6 BOWSHER, D., MALLART, A., PETIT, D.. AND ALBE-FESSARD, D., A bulbar relay to the centre median, J. Neurophysiol., 31 (1968)288-300. 7 CRAGG, B. G., The connections of the habenula in the rabbit, Exp. Neurol., 3 (1961) 388~-09. 8 ENCABO, H., Y SEGUNDO, J. P., Respuestas unitarias a estimulos aferentes en el septum, Rev. Med. Estud. gen. Navarra, 6 (1962) 157-165. 9 ENCABO, H., AND VOLKIND, R., Evoked somatic activity in nucleus medialis dorsalis: a microelectrode study, Electroenceph. clin. Neurophysiol., 25 (1968) 252-258. 10 FELTZ, P., KRAUTHAMER,G., AND ALBE-FESSARD,D., Neurons of the medial diencephalon. I. Somato-sensory responses and caudate inhibition, J. Neurophysiol., 30 (1967) 55 80. 11 Fox, C. A., Amygdalo-thalamic connections in Macaca mulatta, Anat. Rec., 103 (1949) 537. Brain Research, 28 (1971) 35-46

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