RELATIVE CONTRIBUTIONS OF THALAMIC RETICULAR NUCLEUS NEURONS AND INTRINSIC INTERNEURONS TO INHIBITION OF THALAMIC NEURONS PROJECTING TO THE MOTOR CORTEX

1. Intracellular responses to stimulation of the cerebral cortex (Cx) and cerebellum were analyzed in thalamocortical neurons (TCNs) in the ventroanterior-ventrolateral (VA-VL) complex of the thalamus and neurons in the thalamic reticular nuclei (RNs) of anesthetized cats, and the contribution of reticular nucleus neurons (RNNs) and thalamic interneurons (TINs) to cerebral and cerebellar inhibition of TCNs was determined. 2. Single TCNs projecting to area 4 or 6 received convergent monosynaptic excitatory and disynaptic inhibitory inputs from both the dentate nucleus (DN) and the interpositus nucleus (IN). These TCNs also received monosynaptic excitatory postsynaptic potentials (EPSPs) and disynaptic inhibitory postsynaptic potentials (IPSPs) from the pericruciate cortex (areas 4 and 6). Each TCN received the strongest excitatory and inhibitory inputs from the cortical area to which that TCN projected, and weaker inhibitory inputs from adjacent cortical areas. 3. RNNs were identified morphologically by intracellular injection of horseradish peroxidase (HRP). Stimulation of the brachium conjunctivum (BC) evoked disynaptic EPSPs with a long decay phase in RNNs in the anterior ventrolateral part of the RN. Single RNNs received convergent disynaptic excitatory inputs from both the DN and the IN. Stimulation of the Cx produced monosynaptic long-lasting EPSPs with two different latencies in these RNNs: early EPSPs with latencies of 0.9-2.1 ms and late EPSPs with latencies of 1.8-3.5 ms. Collision experiments with BC- and Cx-evoked EPSPs in RNNs indicated that BC-evoked disynaptic EPSPs and Cx-evoked early EPSPs were produced by axon collaterals of TCNs to RNNs. The latencies of the Cx-evoked late EPSPs in RNNs were almost identical to those of Cx-evoked monosynaptic EPSPs in TCNs, indicating that corticothalamic neurons (CTNs) exert monosynaptic excitatory effects on RNNs and TCNs. 4. Stimulation of the Cx produced IPSPs in TCNs with short latencies of 1.8-2.7 ms and longer latencies of greater than or equal to 2.8 ms. The Cx-evoked early IPSPs with latencies of 1.8-2.7 ms were mediated by RNNs. The origin of Cx-evoked late IPSPs with latencies of greater than or equal to 2.8 ms in TCNs was twofold. Cx-induced early IPSPs in TCNs were facilitated by conditioning cortical stimulation that induced late IPSPs in the TCNs. The same conditioning cortical stimulation also facilitated BC-evoked disynaptic IPSPs. The time course of this facilitation indicated that CTNs produce long-lasting excitation in TINs. These results indicated that Cx-evoked IPSPs with latencies of >2.7 ms were mediated at least in part by RNNs and inhibitory TINs in the VA-VL complex. 5. The shortest latencies of BC-evoked IPSPs in TCNs were greater than or equal to 0.8 ms longer than those of BC-evoked monosynaptic EPSPs in TCNs, and were almost equal to the latencies of BC-evoked EPSPs in RNNs. Therefore these BC-evoked disynaptic IPSPs could not be mediated via RNNs. However, the interaction between Cx-induced early IPSPs and BC-evoked late IPSPs in TCNs indicated that BC-evoked IPSPs contained a trisynaptic component via RNNs. 6. These electrophysiological results were confirmed by the anatomic findings that the main axons of HRP-stained RNNs receiving disynaptic excitatory input from the BC and monosynaptic excitatory input from the Cx ran dorsomedially or caudomedially and spread into the VA-VL complex, where TCNs receiving cerebellar input were located.