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Inhibitory synaptic pathways linking specific and nonspecific thalamic nuclei
542
SHORT COMMUNICATIONS
Inhibitory synaptic pathways linking specific and nonspecific thalamic nuclei Stimulation of medial thalamic nonspecific nuclei suppresses transmission of cerebellofugal activity to motor cortex by activation of intrathalamic pathways that generate prolonged inhibitory postsynaptic potentials (IPSPs) in ventrolateral (VL) thalamic relay cells 4. Elucidation of the synaptic inhibition underlying suppression of VL relay activity during evoked E E G synchronization has provided an adequate interpretation of the marked depression in specific evoked responses observed in VL during behavioral sleep 6. Similarly, findings of IPSP blockade, and augmentation in excitatory postsynaptic potentials (EPSPs) in VL cells during EEG desynchronization 5 have indicated a mechanism whereby VL relay activity is enhanced during behavioral arousal 6. In both instances, inhibition of VL relays during EEG synchronization and facilitation of VL activity during arousal, emphasis has been placed on the operation of internuclear pathways arising in nonspecific thalamic nuclei and distributing in VL neuronal organizations a. The question of whether stimulation in VL might exert similar synaptic effects on medial nonspecific neurons and thereby reveal the existence of reciprocal internuclear pathways has been examined in the present study. Intracellular recordings were obtained from neurons in thalamic nuclei comprising medial components of the nonspecific thalamic reticular system 1 (n. centralis medialis, n. reuniens, n. paracentralis, n. centrum medianum and n. parafascicularis). Stimulation of VL was accomplished by stereotaxic placement of concentrically bipolar electrodes in sites yielding specific evoked responses in motor cortex. Experiments were carried out in encdphale isold cats prepared in a manner similar to that described in previous intracellular studies of thalamic neurons4, 5. Results obtained from more than 100 medial thalamic neurons exhibiting prominent evoked PSPs during VL stimulation are summarized, in part, in Fig. 1. Approximately 40 ~ of impaled neurons in medial thalamic nuclei exhibited short-
A
C
B 50msec
Fig. 1. Examples of intracellular recordings (lower channel records) obtained with 2 M potassium citrate filled micropipettes from medial thalamic neurons in 4 different preparations. Specific responses to VL stimulation recorded monopolarly from motor cortex are shown in upper channel records (negative upwards). Amplitudes of cortical surface responses ranged from 200 250 ffV. A and B, cells exhibiting 3040 mV spike potentials prior to VL stimulation and short-latency IPSPs immediately following stimulation. C and D, cells partially depolarized following impalements. In these elements, as well as in A and B, IPSPs are not preceded by EPSPs. Dashed horizontal lines drawn through baseline membrane potential. Note that the IPSP characteristics in medial thalamic neurons are independent of the characteristics of primary evoked responses recorded in motor cortex.
Brain Research, 15 (1969) 542-543
SHORT COMMUNICATIONS
543
latency (1.5-6 msec) prolonged (50-100 msec) IPSPs in response to single shock VL stimulation. A larger proportion (50 ~ ) of medial thalamic neurons exhibited mediumlatency (8-15 msec) IPSPs that were frequently preceded by brief EPSPs. However, repetitive VL stimulation usually resulted in summation of prolonged IPSPs and suppression of spike discharges in these elements. Antidromic responses were not observed in medial thalamic neurons during VL simulation nor were PSPs and associated spike discharges detected prior to the onset of short-latency IPSPs (Fig. 1). These observations indicate that such IPSPs are not likely to be generated by inhibitory interneurons activated by recurrent collaterals of neurons with projections to VL. Rather the data favor the existence of oligosynaptic pathways arising in VL and distributing diffusely in medial thalamic nuclei. The present findings taken together with earlier observations 4 indicate that internuclear synaptic pathways linking nonspecific and VL nuclei are reciprocal in nature and operation, although differences exist largely in respect to internuclear transit time. This follows from the finding that the shortest latency inhibitory interactions have been observed with stimulation in VL and recording in medial nuclei (Fig. 1) than vice versa2,4, 5. The functional significance of the powerful inhibitory action exerted by pathways from VL to medial nonspecific nuclei remains unclarified. An obvious inference is that 'selection' of a specific VL input pathway to m o t o r cortex would be considerably facilitated by concomitant VL-induced inhibition of 1he inhibitory effects of nonspecific nuclei on VL relay cells 4. This could provide an effective thalamic mechanism for enhancing the significance of specific input channels to cortex by suppression of nonspecific thalamocortical background activity. This work was supported by the National Institute of Neurological Diseases and Stroke, N.I.H. (NB-07512). T. DESIRAJU* G. BROGGI* S. PRELEVIC* M. SANTINI D. P. PURPURA
Department of Anatomy, Albert Einstein College of Medicine, Bronx, N.Y. (U.S.A.)
1 JASPER,H. H., Diffuse projection systems: The integrative action of the thalamic reticular system, Electroenceph. clin. Neurophysiol., 1 (1949) 405-420. 2 PURPURA,D. P., ANDCOHEN,B., Intracellular recording from thalamic neurons during recruiting responses, J. Neurophysiol., 25 (1962) 621-635. 3 PURPtrRA,D. P., FRIGYESI, T. L., MCMURTRY,J. G., AND SCARFF,T., Synaptic mechanisms in thalamic regulation of cerebello-cortical projection activity. In D: P. PVRPURAAND M. D. YAI~R (Eds.), The Thalamus, Columbia University, New York, 1966, pp. 153-172. 4 PURPURA,D. P., SCARrF,T., ANDMcMURTRV,J. G., Intracellular study of internuclear inhibition in ventrolateral thalamic neurons, J. Neurophysiol., 28 (1965) 487-496. 5 PURPURA, D. P., AND SHOFER, R. J., Intracellular recording from thalamic neurons during reticulocortical activation, J. Neurophysiol., 26 (1963) 494-505. 6 STERIADE,M., IOSIF,G., AND APOSTOL,V., Responsiveness of thalamic and cortical motor relays during arousal and various stages of sleep, J. Neurophysiol., 32 (1969) 251-265. (Accepted July 4th, 1969) * International Post-doctoral Fellows, National Institutes of Health. Brain Research, 15 (1969) 542-543
SHORT COMMUNICATIONS
Inhibitory synaptic pathways linking specific and nonspecific thalamic nuclei Stimulation of medial thalamic nonspecific nuclei suppresses transmission of cerebellofugal activity to motor cortex by activation of intrathalamic pathways that generate prolonged inhibitory postsynaptic potentials (IPSPs) in ventrolateral (VL) thalamic relay cells 4. Elucidation of the synaptic inhibition underlying suppression of VL relay activity during evoked E E G synchronization has provided an adequate interpretation of the marked depression in specific evoked responses observed in VL during behavioral sleep 6. Similarly, findings of IPSP blockade, and augmentation in excitatory postsynaptic potentials (EPSPs) in VL cells during EEG desynchronization 5 have indicated a mechanism whereby VL relay activity is enhanced during behavioral arousal 6. In both instances, inhibition of VL relays during EEG synchronization and facilitation of VL activity during arousal, emphasis has been placed on the operation of internuclear pathways arising in nonspecific thalamic nuclei and distributing in VL neuronal organizations a. The question of whether stimulation in VL might exert similar synaptic effects on medial nonspecific neurons and thereby reveal the existence of reciprocal internuclear pathways has been examined in the present study. Intracellular recordings were obtained from neurons in thalamic nuclei comprising medial components of the nonspecific thalamic reticular system 1 (n. centralis medialis, n. reuniens, n. paracentralis, n. centrum medianum and n. parafascicularis). Stimulation of VL was accomplished by stereotaxic placement of concentrically bipolar electrodes in sites yielding specific evoked responses in motor cortex. Experiments were carried out in encdphale isold cats prepared in a manner similar to that described in previous intracellular studies of thalamic neurons4, 5. Results obtained from more than 100 medial thalamic neurons exhibiting prominent evoked PSPs during VL stimulation are summarized, in part, in Fig. 1. Approximately 40 ~ of impaled neurons in medial thalamic nuclei exhibited short-
A
C
B 50msec
Fig. 1. Examples of intracellular recordings (lower channel records) obtained with 2 M potassium citrate filled micropipettes from medial thalamic neurons in 4 different preparations. Specific responses to VL stimulation recorded monopolarly from motor cortex are shown in upper channel records (negative upwards). Amplitudes of cortical surface responses ranged from 200 250 ffV. A and B, cells exhibiting 3040 mV spike potentials prior to VL stimulation and short-latency IPSPs immediately following stimulation. C and D, cells partially depolarized following impalements. In these elements, as well as in A and B, IPSPs are not preceded by EPSPs. Dashed horizontal lines drawn through baseline membrane potential. Note that the IPSP characteristics in medial thalamic neurons are independent of the characteristics of primary evoked responses recorded in motor cortex.
Brain Research, 15 (1969) 542-543
SHORT COMMUNICATIONS
543
latency (1.5-6 msec) prolonged (50-100 msec) IPSPs in response to single shock VL stimulation. A larger proportion (50 ~ ) of medial thalamic neurons exhibited mediumlatency (8-15 msec) IPSPs that were frequently preceded by brief EPSPs. However, repetitive VL stimulation usually resulted in summation of prolonged IPSPs and suppression of spike discharges in these elements. Antidromic responses were not observed in medial thalamic neurons during VL simulation nor were PSPs and associated spike discharges detected prior to the onset of short-latency IPSPs (Fig. 1). These observations indicate that such IPSPs are not likely to be generated by inhibitory interneurons activated by recurrent collaterals of neurons with projections to VL. Rather the data favor the existence of oligosynaptic pathways arising in VL and distributing diffusely in medial thalamic nuclei. The present findings taken together with earlier observations 4 indicate that internuclear synaptic pathways linking nonspecific and VL nuclei are reciprocal in nature and operation, although differences exist largely in respect to internuclear transit time. This follows from the finding that the shortest latency inhibitory interactions have been observed with stimulation in VL and recording in medial nuclei (Fig. 1) than vice versa2,4, 5. The functional significance of the powerful inhibitory action exerted by pathways from VL to medial nonspecific nuclei remains unclarified. An obvious inference is that 'selection' of a specific VL input pathway to m o t o r cortex would be considerably facilitated by concomitant VL-induced inhibition of 1he inhibitory effects of nonspecific nuclei on VL relay cells 4. This could provide an effective thalamic mechanism for enhancing the significance of specific input channels to cortex by suppression of nonspecific thalamocortical background activity. This work was supported by the National Institute of Neurological Diseases and Stroke, N.I.H. (NB-07512). T. DESIRAJU* G. BROGGI* S. PRELEVIC* M. SANTINI D. P. PURPURA
Department of Anatomy, Albert Einstein College of Medicine, Bronx, N.Y. (U.S.A.)
1 JASPER,H. H., Diffuse projection systems: The integrative action of the thalamic reticular system, Electroenceph. clin. Neurophysiol., 1 (1949) 405-420. 2 PURPURA,D. P., ANDCOHEN,B., Intracellular recording from thalamic neurons during recruiting responses, J. Neurophysiol., 25 (1962) 621-635. 3 PURPtrRA,D. P., FRIGYESI, T. L., MCMURTRY,J. G., AND SCARFF,T., Synaptic mechanisms in thalamic regulation of cerebello-cortical projection activity. In D: P. PVRPURAAND M. D. YAI~R (Eds.), The Thalamus, Columbia University, New York, 1966, pp. 153-172. 4 PURPURA,D. P., SCARrF,T., ANDMcMURTRV,J. G., Intracellular study of internuclear inhibition in ventrolateral thalamic neurons, J. Neurophysiol., 28 (1965) 487-496. 5 PURPURA, D. P., AND SHOFER, R. J., Intracellular recording from thalamic neurons during reticulocortical activation, J. Neurophysiol., 26 (1963) 494-505. 6 STERIADE,M., IOSIF,G., AND APOSTOL,V., Responsiveness of thalamic and cortical motor relays during arousal and various stages of sleep, J. Neurophysiol., 32 (1969) 251-265. (Accepted July 4th, 1969) * International Post-doctoral Fellows, National Institutes of Health. Brain Research, 15 (1969) 542-543