Mode of termination of pallidal afferents to the thalamus: a light and electron microscopic study with anterograde tracers and immunocytochemistry in Macaca mulatta.

Abstract

The mode of termination of individual pallidothalamic fibers in the densicellular subdivision of the ventral anterior thalamic nucleus (VAdc) of Macaca mulatta was analyzed with light and electron microscopy after injections of anterograde tracers in the medial globus pallidus. Three tracers were utilized: tritiated leucine, biotinylated dextran amine, and wheat germ agglutinin conjugated to horseradish peroxidase in combination with postembedding immunocytochemsitry for gamma-aminobutyric acid (GABA). Pallidothalamic fibers, upon entering the VAdc, gave off several collaterals that formed plexuses of varicose terminal branches within different cell clusters. The varicosities were aligned along somata and proximal dendrites of projection neurons providing dense input to each individual cell. At the electron microscopic level, labeled boutons displayed a predominantly flat and elongated shape. They contained a moderate number of pleomorphic synaptic vesicles and very large amounts of mitochondria, displayed symmetric synaptic contacts, and were immunoreactive for GABA. In the total sample of 128 autoradiographically labeled terminals, 64% were in synaptic contact with somata and primary dendrites of projection neurons, 14% formed synapses on proximal dendrites of undefined order, and only 7% established synaptic contacts on distal dendrites. Fifteen percent of the labeled boutons established synapses on distal dendrites of GABAergic local circuit neurons (LCN). Pallidal boutons were also found in complex synaptic arrangements: triads with three GABAergic synapses, and serial synapses with LCN dendrites that in turn established synaptic contacts on projection neuron somata or dendrites. These anatomical results suggest a dual effect of pallidal afferents to projection neurons: direct inhibition and disinhibition mediated by LCN. The findings indicate that the fine structure of pallidothalamic terminals in the monkey is similar to that described earlier in the cat. There are, however, interspecies differences in the distribution of pallidal input on postsynaptic targets and its participation in complex synaptic arrangements.