Fine structure of the magnocellular subdivision of the ventral anterior thalamic nucleus (V Amc) of Macaca mulatta: I. Cell types and synaptology

Abstract

The nucleus ventralis anterior pars magnocellularis (V Amc) is recognized only in primates and is the major recipient of the nigrothalamic projections. The neuronal and synaptic composition of this nucleus in the rhesus monkey was studied with the use of a variety of neuroanatomical techniques that included quantitative morphometry, anterograde and retrograde labeling with WGA-HRP from the prefrontal cortex, and immunocytochemistry for glutamic acid decarboxylase (GAD). Two major cell types were identified in the nucleus: thalamocortical projection neurons (PN) that were multipolar cells of various sizes, and small GAD-immunoreactive cells, apparently local circuit neurons (LCN). The approximate ratio of the two types of cells was 10:1. The major type of bouton encountered in the neuropil was of medium to large-sized (areas from 1.5 to 12 μ²) and mostly of en passant type. These terminals formed symmetric contacts, contained moderate amounts of pleomorphic or mostly flat synaptic vesicles and large numbers of mitochondria, and displayed numerous puncta adhaerentia. All of these boutons exhibited positive GAD immunoreactivity. These boutons constituted the only synaptic population on somata and primary dendrites of PN and formed an overwhelming majority on the secondary PN dendrites. There were fewer of these axon terminals on tertiary PN and LCN dendrites. Additionally, boutons with similar features formed synapses on axon hillocks or initial axonal segments of PN, and somata or very proximal parts of primary dendrites of LCN. With the exception of the boutons in the last two locations, all of the other boutons in this group were shown to be terminals of the nigrothalamic afferents in the parallel EM autoradiographic study (Kultas-Ilinsky and Ilinsky: J. Comp Neurol. 294:479-489,'90). The second major bouton population in the VAmc was represented by small to mediumsized terminals (areas range from 0.2 to 2.0 μ²) that formed distinct asymmetric contacts and contained large numbers of round vesicles and few or no mitochondria. These boutons were labeled anterogradely from the cortex and dominated on distal PN and LCN dendrites. Some of them were found on secondary PN dendrites where they formed synapses either directly or indirectly via LCN dendrites and dendro-dendritic contacts. The latter arrangements, i. e., serial synapses, were also formed between the cortical boutons and PN somata or tertiary dendrites. The third population of axon terminals encountered in the V Amc was represented by medium to large-sized boutons (areas from 2.0 to 3.5 μ²) with round vesicles and asymmetric contacts, i. e., all features of these boutons except the size were similar to those of cortical afferents. However, they were not labeled after cortical injections and were presumed to be terminals of superior colliculus afferents to the thalamus. These boutons formed synapses on secondary and tertiary PN dendrites and distal LCN dendrites, but were encountered infrequently. No complex synaptic arrangements such as glomeruli or reciprocal synapses were found in the V Amc neuropil; triad relationships were also practically absent. The results demonstrate that the ultrastructural organization of the V Amc is quite different from that of many specific thalamic nuclei processing sensory modalities. The findings pose interesting questions with respect to the mechanism of functioning of V Amc projection neurons and the overall significance of the ascending basal ganglia output via the nigrothalamic pathway.