A description of the GABAergic neurons and axon terminals in the motor nuclei of the cat thalamus

Abstract

The GABA neurons and their processes in the cat motor thalamic nuclei were identified and studied with glutamic acid decarboxylase (GAD) immunocytochemistry at both the light and electron microscopic levels. The three nuclei that comprise the motor thalamus, ventral anterior (VA), ventral medial (VM), and ventral lateral (VL), each displayed a characteristic distribution pattern of GAD-positive structures that was consistent with their afferent and intrinsic neuronal organization. All three thalamic nuclei displayed a population of small, GAD-positive cells the dendrites of which contained synaptic vesicles and participated in complex synaptic arrays such as serial synapses, triads, and glomeruli. Based on their ultrastructural features, these GAD-containing cells were identified as local circuit neurons. In contrast, the larger, GAD-negative cells were presumed to be the thalamocortical projection neurons. The axons of GAD-positive local circuit neurons could not be identified in these preparations. The number of GAD-positive dendrites in the neuropil was different for the three thalamic nuclei. In the VA and VM, the GAD-positive dendrites were numerous and formed symmetric synapses with dendrites of GAD-negative cells, mainly in association with corticothalamic boutons. Within VL, the GAD-containing dendrites were more numerous than in VA and VM and formed synapses at influential locations on presumed thalamocortical projection neurons, such as bases of primary dendrites, and bifurcation sites of primary and secondary dendrites. The VA and anterolateral VM nuclei that receive inhibitory GABAergic afferents from the entopeduncular nucleus and substantia nigra contained the highest concentration of large GAD-positive axon terminals. These boutons contained pleomorphic vesicles and numerous mitochondria and formed symmetric synapses and multiple puncta adherentes with dendrites and somata of presumed thalamocortical projection neurons. The size, ultrastructural features, and distribution of these GAD-positive boutons were similar to those features described for basal ganglia terminals in the motor thalamus of the cat. In addition, similar large-size GAD-positive boutons were observed in the medial VM, which receives basal ganglia afferents exclusively from the substantia nigra. The concentration of these terminals in medial VM along the dendrites of thalamocortical projection neurons was much less than that in VA and anterolateral VM. The VL nucleus which lacks basal ganglia input did not contain any large GAD-positive boutons. Instead, small and medium size GAD-positive boutons were found in VL, where they formed symmetric synapses with dendrites of GAD-negative neurons, often in association with synaptic glomeruli. Our findings indicate that most of the GABAergic inhibition in VA and VM is provided by basal ganglia afferents that synapse with thalamocortical projection neurons and thereby presumably control the output activity of these cells. In contrast, the VL lacks this massive extrinsic GABAergic input but has numerous presynaptic dendrites of GABAergic local circuit neurons that appear to provide a similar inhibitory control of thalamocortical projection neurons. Finally, the dendrites of thalamocortical neurons in all three nuclei receive cortical and cerebellar inputs that are often associated with GABAergic dendrodendritic synapses that probably act to modify these two sources of excitation.