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Excitatory and inhibitory interactions between the thalamic VPM nuclei of the two sides
SHORT COMMUNICATIONS
391
Excitatory and inhibitory interactions between the thalamic VPM nuclei of the two sides The possibility of reciprocal interactions between the thalamic nuclei ventrales posterolaterales (VPL) of the two sides through subcortical pathways was shown by previous experiments in the cat z-a. The present experiments were planned to investigate whether similar interactions could also be found between the partes arcuatae of the ventrobasal complex (nucleus ventralis posteromedialis, VPM). To this effect, a sample population of units belonging to this nucleus was tested for reactivity to impulses originated by stimulating, under suitable conditions, the contralateral homonymous structure and the ascending trigeminal paths. Twenty-two curarized (ether during surgery; local anaesthesia with procaine 2 ~ in surgical wounds and friction points), artificially-ventilated cats were used. To prevent possible interthalamic activation via cortico-callosal pathways ~, 18 animals were submitted to the acute removal (suction or coagulation) of most of the hemicortex ipsilateral to the stimulated VPM, and 4 animals to the complete section of the corpus eallosum (Magni, Melzack and Smith's techniqueg). Five out of the 22 preparations also underwent ipsilateral hemisection of the mesencephalon to rule out the possibility of interthalamic effects due to the utilization of more caudally located loops (see, however, Eisenman et al.7). The experimental evidence was gathered by stereotaxic exploration of the thalamus with tungsten microelectrodes and by extracellular recording of unitary, all-or-none activity (CRO display). All neurones encountered within the VPM nucleus were identified by testing on them the excitatory effects of peripheral stimulation (both physiological and electrical) and were further tested for the excitatory and the inhibitory effects of contralateral VPM stimulation (bipolar concentric electrodes, 0.5 mm in outer diameter). Some units were also tested for their reactivity to both the stimulation of ipsilateral somatosensory cortical areas and of the contralateral nucleus trigemini sensibilis principalis (NVsnpr). In addition, the cortical evoked potentials elicited by stimulation of the latter were recorded in a few instances. All electrode placements were checked histologically on frozen sections (haematoxylin-eosin staining). The present results are based on the evidence obtained from 146 VPM neurones, which were all fired by physiological or electrical stimulation of the skin of muzzle or of intraoral structures (located within trigeminal receptive areas). In this connection, all these units exhibited specific properties, in keeping with the descriptions by previous authors (cf Darian-Smith's recent review6). As became apparent, a good proportion of the neurones tested was also sensitive to the stimulation of contralateral VPM. Both excitatory and inhibitory effects were observed, according to a pattern which can be summarized as follows. Out of the 146 VPM units identified, 27 neurones were found to be excited by the 'transversal' impulses elicited by contralateral VPM stimulation. Eighteen such units were caused to discharge by applying single shocks to the contralateral homonymous nucleus, whereas the remaining 9 units required short repetitive trains (10-50/sec) to achieve this effect. Four of the former reacted with one spike only,
Brain Research, 6 (1967) 391-394
392
SltORT COMMIJNICATIONS
Fig. 1. Extracellular responses recorded from a single VPM neurone of a curarized, locally anaesthe tized cat preparation. The unit was functionally identified by recording (superimposed sweeps) the excitatory responses elicited upon single-shock stimulation of its peripheral field (A0 contralateral whisker zone), of the pontine relay station (B, contralateral NVsnpr), and by testing the effects of stimulation of the trigeminal cortical projection area (C, ipsilateral Sx; superimposed sweeps recorded during repetitive stimulation at 100/sec). The signs of antidromic invasion that may be observed in C make identity with a T C R cell highly probable. The 'transversal inhibition' brought about by contralateral VPM stimulation is shown in the right-hand row: D, test stimulation alone applied to the contralateral NVsnpr (single shocks; 13 superimposed sweeps); E, responses obtained (13 superimposed sweeps) when the conditioning stimulus to the con tralateral VPM nucleus (train of 5 shocks at 320/sec) preceded the test stimulation. The functional localization of the stimulating V P M electrode is shown in F, obtained upon stimulation of the related whisker zone (single electrical shocks; 7 superimposed sweeps). Vertical bar: 300 itV for A-E, 100/.tV for F. Time calibration: 500 c/sec for A-C, 100 c/sec for D - F .
Brain Research, 6 (1967) 391-394
SHORT COMMUNICATIONS
393
after short and constant latencies (0.7-1.2 msec; conduction distance, about 10 mm), and were seen to follow stimulus frequencies up to 400/sec. They were therefore regarded as antidromically activated. The latencies of the transsynaptic responses (which were all those remaining, consisting of one spike or, more frequently, of brief bursts of 2-7 spikes) ranged between 3 and 10 msec (6.6 ~ 0.62 S.E.). The inhibitory effects (Fig. 1) were tested on 65 neurones of our sample. We saw that in 18 of these units the contralateral VPM stimulation (single shocks or brief trains of 7-10 msec, 320/sec, 0.1 msec) was very effective in inhibiting the responses to peripheral stimuli. In all such units contralateral stimuli were devoid of apparent excitatory effects. The inhibitory effects would last as long as 150-180 msec following the conditioning 'transversal' volley and the shortest effective interval was 5-6 msec. It should be noted that the inhibitory phenomena were more frequently observed in units linked with cutaneous fields (16 out of 42 neurones), particularly with whiskers; only rarely did inhibition appear in units linked with intraoral structures (2 out of 23 neurones). Some experiments were devoted to ascertain whether the 'transversal inhibition' really occurred at the thalamic level itself. To this effect, in all neurones exhibiting such inhibition we used as a test the monosynaptic unitary responses brought about by maximal volleys elicited by direct stimulation of the second-order neurones located in the ventrolateral part of the contralateral NVsnpr. These responses, too, were consistently blocked by contralateral VPM stimulation. In two instances, moreover, the trigemino-thalamic responses were recorded with concentric electrodes as massdischarges. In keeping with the microphysiological findings, the inhibitory action of the transversal volleys was seen to be exerted under these conditions only on the postsynaptic component, whose amplitude was reduced to 7 0 ~ of the unconditioned responses, and not at all on the presynaptic one. We therefore concluded that the inhibitory volleys brought about by contralateral VPM stimulation really act on elements belonging to the VPM nucleus. It should be noted that, according to our findings, in their majority the VPM units exhibiting transversal inhibition send their axons to the somatosensory cortex. In fact, out of a sample of 13 such units which were tested for the effects of singleshock stimulation of the ipsilateral somatosensory cortex, as many as 11 showed the signs of antidromic invasion, and were thus identified as thalamo-cortical relay cells; 1 was discharged transsynaptically and 1 did not react at all. Conversely, only 4 out of 14 units similarly tested but not transversally inhibited were antidromically invaded from the cortex, the remainder being either excited transsynaptically (2) or not excited at all (8). The heavy presence of T C R cells in the ventromedial pool subjected to inhibition from the contralateral VPM might account for a collateral observation, namely, that the evoked potentials elicited in the somatic cortical area by applying single shocks to NVsnpr were strongly reduced in all their components (down to 3 0 ~ of unconditioned amplitude) if the shocks were preceded by a conditioning volley applied to the contralateral VPM. From the present evidence it might be concluded that (i) V P M - V P M interactions (both excitatory and inhibitory in sign) do exist and really occur at the thalamic
Brain Research, 6 (1967) 391-394
394
SHORT COMMUNICATIONS
level; (ii) these are not due to the activation of cortical or prethalamic trigeminal relays; (iii) these interactions, as is suggested by the very latency of the transversal responses, are more likely to be dependent on specific VPM-VPM linkages than on aspecific reticular connections1, 8. This investigation was supported in part by a grant from Consiglio Nazionale delle Ricerche. Institute of Human Physiology, University of Catania, Catania rItaly)
A N T O N I O BAVA TULLIO M A N Z O N I
1 APPELBERG, B., KITCHELL, R. L.. AND LANDGREN, S., Reticular influence upon thalamic and cortical potentials evoked by stimulation of the cat's tongue, Actaphysiol. scand., 45 (1959) 48-71. 2 BAVA, A.. F:ADIGA,E., AND MANZONLT., Interactive potentialities between thalamic relay-nuclei through subcortical commissural pathways, Arch. Sci. bioL (Bologna), 50 (1966) 101-133. 3 BAVA, A.. FADIGA, E., E MANZONL T., Deafferentazione cronica e proprietor funzionati dei nuclei talamici di relais somatico. Atti Accad. naz. Lincei, Classe Sci. fis., mat. nat.. Ser. VIII. 40 (1966) 912-920. 4 BAVA, A., FADIGA, E., AND MANZONI. T., Lemniscal afferents and extracallosal mechanisms for interhemispheric transmission of somato-sensory evoked potentials. In W. COBB AND C. MOROc t r r n (Eds.), The Evoked Potentials. Electroenceph. clin. NeurophysioL, Suppk 26 (1967) 182-187. 5 BREMER, F., ET TERZUOLO, C. A., Transfert interh6misph6rique d'informations sensorieltes par le corps calleux, J. PhysioL (Paris), 47 (1955) 105-107. 6 DARIAN-SMrrH, I., Neural mechanisms of facial sensation, Int. Rev. Neurobiol., 9 (1966) 301-395. 7 EISENMAN,J., FROMM, G., LANDGREN,S., AND NOVlN, D., The ascending projections oftrigeminal neurones in the cat, investigated by antidromic stimulation, Acta physioL scand., 60 (t964) 337-350. 8 MAEKAWA,K., AND PURPURA, D. P., Intracellular study of lemniscal and non-specific synaptic interactions in thalamic ventrobasal neurons, Brain Research, 4 (1967) 308-323. 9 MAGNL F., MELZACK, R., AND SMITH, C. J., A stereotaxic method for sectioning the corpus callosum in cat, Electroenceph. clin. Neurophysiol., 12 1.1960) 517-518. (Accepted July 3rd, 1967)
Brain Research, 6 (1967) 391-394
391
Excitatory and inhibitory interactions between the thalamic VPM nuclei of the two sides The possibility of reciprocal interactions between the thalamic nuclei ventrales posterolaterales (VPL) of the two sides through subcortical pathways was shown by previous experiments in the cat z-a. The present experiments were planned to investigate whether similar interactions could also be found between the partes arcuatae of the ventrobasal complex (nucleus ventralis posteromedialis, VPM). To this effect, a sample population of units belonging to this nucleus was tested for reactivity to impulses originated by stimulating, under suitable conditions, the contralateral homonymous structure and the ascending trigeminal paths. Twenty-two curarized (ether during surgery; local anaesthesia with procaine 2 ~ in surgical wounds and friction points), artificially-ventilated cats were used. To prevent possible interthalamic activation via cortico-callosal pathways ~, 18 animals were submitted to the acute removal (suction or coagulation) of most of the hemicortex ipsilateral to the stimulated VPM, and 4 animals to the complete section of the corpus eallosum (Magni, Melzack and Smith's techniqueg). Five out of the 22 preparations also underwent ipsilateral hemisection of the mesencephalon to rule out the possibility of interthalamic effects due to the utilization of more caudally located loops (see, however, Eisenman et al.7). The experimental evidence was gathered by stereotaxic exploration of the thalamus with tungsten microelectrodes and by extracellular recording of unitary, all-or-none activity (CRO display). All neurones encountered within the VPM nucleus were identified by testing on them the excitatory effects of peripheral stimulation (both physiological and electrical) and were further tested for the excitatory and the inhibitory effects of contralateral VPM stimulation (bipolar concentric electrodes, 0.5 mm in outer diameter). Some units were also tested for their reactivity to both the stimulation of ipsilateral somatosensory cortical areas and of the contralateral nucleus trigemini sensibilis principalis (NVsnpr). In addition, the cortical evoked potentials elicited by stimulation of the latter were recorded in a few instances. All electrode placements were checked histologically on frozen sections (haematoxylin-eosin staining). The present results are based on the evidence obtained from 146 VPM neurones, which were all fired by physiological or electrical stimulation of the skin of muzzle or of intraoral structures (located within trigeminal receptive areas). In this connection, all these units exhibited specific properties, in keeping with the descriptions by previous authors (cf Darian-Smith's recent review6). As became apparent, a good proportion of the neurones tested was also sensitive to the stimulation of contralateral VPM. Both excitatory and inhibitory effects were observed, according to a pattern which can be summarized as follows. Out of the 146 VPM units identified, 27 neurones were found to be excited by the 'transversal' impulses elicited by contralateral VPM stimulation. Eighteen such units were caused to discharge by applying single shocks to the contralateral homonymous nucleus, whereas the remaining 9 units required short repetitive trains (10-50/sec) to achieve this effect. Four of the former reacted with one spike only,
Brain Research, 6 (1967) 391-394
392
SltORT COMMIJNICATIONS
Fig. 1. Extracellular responses recorded from a single VPM neurone of a curarized, locally anaesthe tized cat preparation. The unit was functionally identified by recording (superimposed sweeps) the excitatory responses elicited upon single-shock stimulation of its peripheral field (A0 contralateral whisker zone), of the pontine relay station (B, contralateral NVsnpr), and by testing the effects of stimulation of the trigeminal cortical projection area (C, ipsilateral Sx; superimposed sweeps recorded during repetitive stimulation at 100/sec). The signs of antidromic invasion that may be observed in C make identity with a T C R cell highly probable. The 'transversal inhibition' brought about by contralateral VPM stimulation is shown in the right-hand row: D, test stimulation alone applied to the contralateral NVsnpr (single shocks; 13 superimposed sweeps); E, responses obtained (13 superimposed sweeps) when the conditioning stimulus to the con tralateral VPM nucleus (train of 5 shocks at 320/sec) preceded the test stimulation. The functional localization of the stimulating V P M electrode is shown in F, obtained upon stimulation of the related whisker zone (single electrical shocks; 7 superimposed sweeps). Vertical bar: 300 itV for A-E, 100/.tV for F. Time calibration: 500 c/sec for A-C, 100 c/sec for D - F .
Brain Research, 6 (1967) 391-394
SHORT COMMUNICATIONS
393
after short and constant latencies (0.7-1.2 msec; conduction distance, about 10 mm), and were seen to follow stimulus frequencies up to 400/sec. They were therefore regarded as antidromically activated. The latencies of the transsynaptic responses (which were all those remaining, consisting of one spike or, more frequently, of brief bursts of 2-7 spikes) ranged between 3 and 10 msec (6.6 ~ 0.62 S.E.). The inhibitory effects (Fig. 1) were tested on 65 neurones of our sample. We saw that in 18 of these units the contralateral VPM stimulation (single shocks or brief trains of 7-10 msec, 320/sec, 0.1 msec) was very effective in inhibiting the responses to peripheral stimuli. In all such units contralateral stimuli were devoid of apparent excitatory effects. The inhibitory effects would last as long as 150-180 msec following the conditioning 'transversal' volley and the shortest effective interval was 5-6 msec. It should be noted that the inhibitory phenomena were more frequently observed in units linked with cutaneous fields (16 out of 42 neurones), particularly with whiskers; only rarely did inhibition appear in units linked with intraoral structures (2 out of 23 neurones). Some experiments were devoted to ascertain whether the 'transversal inhibition' really occurred at the thalamic level itself. To this effect, in all neurones exhibiting such inhibition we used as a test the monosynaptic unitary responses brought about by maximal volleys elicited by direct stimulation of the second-order neurones located in the ventrolateral part of the contralateral NVsnpr. These responses, too, were consistently blocked by contralateral VPM stimulation. In two instances, moreover, the trigemino-thalamic responses were recorded with concentric electrodes as massdischarges. In keeping with the microphysiological findings, the inhibitory action of the transversal volleys was seen to be exerted under these conditions only on the postsynaptic component, whose amplitude was reduced to 7 0 ~ of the unconditioned responses, and not at all on the presynaptic one. We therefore concluded that the inhibitory volleys brought about by contralateral VPM stimulation really act on elements belonging to the VPM nucleus. It should be noted that, according to our findings, in their majority the VPM units exhibiting transversal inhibition send their axons to the somatosensory cortex. In fact, out of a sample of 13 such units which were tested for the effects of singleshock stimulation of the ipsilateral somatosensory cortex, as many as 11 showed the signs of antidromic invasion, and were thus identified as thalamo-cortical relay cells; 1 was discharged transsynaptically and 1 did not react at all. Conversely, only 4 out of 14 units similarly tested but not transversally inhibited were antidromically invaded from the cortex, the remainder being either excited transsynaptically (2) or not excited at all (8). The heavy presence of T C R cells in the ventromedial pool subjected to inhibition from the contralateral VPM might account for a collateral observation, namely, that the evoked potentials elicited in the somatic cortical area by applying single shocks to NVsnpr were strongly reduced in all their components (down to 3 0 ~ of unconditioned amplitude) if the shocks were preceded by a conditioning volley applied to the contralateral VPM. From the present evidence it might be concluded that (i) V P M - V P M interactions (both excitatory and inhibitory in sign) do exist and really occur at the thalamic
Brain Research, 6 (1967) 391-394
394
SHORT COMMUNICATIONS
level; (ii) these are not due to the activation of cortical or prethalamic trigeminal relays; (iii) these interactions, as is suggested by the very latency of the transversal responses, are more likely to be dependent on specific VPM-VPM linkages than on aspecific reticular connections1, 8. This investigation was supported in part by a grant from Consiglio Nazionale delle Ricerche. Institute of Human Physiology, University of Catania, Catania rItaly)
A N T O N I O BAVA TULLIO M A N Z O N I
1 APPELBERG, B., KITCHELL, R. L.. AND LANDGREN, S., Reticular influence upon thalamic and cortical potentials evoked by stimulation of the cat's tongue, Actaphysiol. scand., 45 (1959) 48-71. 2 BAVA, A.. F:ADIGA,E., AND MANZONLT., Interactive potentialities between thalamic relay-nuclei through subcortical commissural pathways, Arch. Sci. bioL (Bologna), 50 (1966) 101-133. 3 BAVA, A.. FADIGA, E., E MANZONL T., Deafferentazione cronica e proprietor funzionati dei nuclei talamici di relais somatico. Atti Accad. naz. Lincei, Classe Sci. fis., mat. nat.. Ser. VIII. 40 (1966) 912-920. 4 BAVA, A., FADIGA, E., AND MANZONI. T., Lemniscal afferents and extracallosal mechanisms for interhemispheric transmission of somato-sensory evoked potentials. In W. COBB AND C. MOROc t r r n (Eds.), The Evoked Potentials. Electroenceph. clin. NeurophysioL, Suppk 26 (1967) 182-187. 5 BREMER, F., ET TERZUOLO, C. A., Transfert interh6misph6rique d'informations sensorieltes par le corps calleux, J. PhysioL (Paris), 47 (1955) 105-107. 6 DARIAN-SMrrH, I., Neural mechanisms of facial sensation, Int. Rev. Neurobiol., 9 (1966) 301-395. 7 EISENMAN,J., FROMM, G., LANDGREN,S., AND NOVlN, D., The ascending projections oftrigeminal neurones in the cat, investigated by antidromic stimulation, Acta physioL scand., 60 (t964) 337-350. 8 MAEKAWA,K., AND PURPURA, D. P., Intracellular study of lemniscal and non-specific synaptic interactions in thalamic ventrobasal neurons, Brain Research, 4 (1967) 308-323. 9 MAGNL F., MELZACK, R., AND SMITH, C. J., A stereotaxic method for sectioning the corpus callosum in cat, Electroenceph. clin. Neurophysiol., 12 1.1960) 517-518. (Accepted July 3rd, 1967)
Brain Research, 6 (1967) 391-394