Fine structure of the ventral lateral nucleus (VL) of the Macaca mulatta thalamus: cell types and synaptology.

Ultrastructure of the major cerebellar territory of the monkey thalamus, or VL as delineated in sagittal maps by Ilinsky and Kultas-Ilinsky (J. Comp. Neurol.262:331–364, ′87), was analyzed by using neuroanatomical tracing, immunocytochemical, and quantitative morphometric techniques. The VL nucleus contains nerve cells of two types. Multipolar neurons (PN) retrogradely labeled with wheat germ agglutinin-horseradish peroxidase (WGA-HRP) from the precentral gyrus display a tufted branching pattern of the proximal dendrites and have a range of soma areas from 200 to 1,000 μm2 (mean 535.2 μm2, SD = 159.5). Small glutamic acid decarboxylase (GAD) immunoreactive cells (LCN) exhibit sizes from 65 to 210 μm2 (mean 122.5 μm2, SD = 32.8) and remain unlabeled after cortical injections. The two cell types can be further distinguished by ultrastructural features. Unlike PN, LCN display little perikaryal cytoplasm, a small irregularly shaped nucleolus, and synaptic vesicles in proximal dendrites. The ratio of PN to LCN is 3:1. The LCN dendrites establish synaptic contacts on PN somata and all levels of dendritic arbor either singly or as a part of complex synaptic arrangements. They are also presynaptic to other LCN dendrites. Terminals known as LR type, i.e., large boutons containing round vesicles, are the most conspicuous in the neuropil. They form asymmetric contacts on somata and proximal dendrites of PN as well as on distal dendrites of LCN. The areas of these boutons range from 0.7 to 12 μm2 and the appositional length on PN dendrites ranges from 1.1 to 14 μm. All LR boutons except the largest ones become anterogradely labeled from large WGA-HRP injections in the deep cerebellar nuclei. These boutons are also encountered as part of triads and glomeruli, but very infrequently since the latter complex synaptic arrangements are rare. The most numerous axon terminals in the neuropil are the SR type, i.e., small terminals (mean area 0.42 μm2) containing round vesicles. The SR boutons become anterogradely labeled after WGA-HRP injections in the precentral gyrus. They form distinct asymmetric contacts predominantly on distal PN and LCN dendrites; however, their domain partially overlaps that of LR boutons at intermediate levels of PN dendrites. The SR boutons are components of serial synapses with LCN dendrites which, in turn, contact somata and all levels of dendritic arbors of PN. They also participate in complex arrangements that consist of sequences of LCN dendrites, serial synapses, and occasional boutons with symmetric contacts. These structures termed small glomeruli are much more frequent in the monkey VL than classic glomeruli with LR boutons. The third group is composed of boutons known as F1 type. This is a heterogeneous population containing boutons of varying sizes ranging from 0.4 to 9 μm2. The terminals contain pleomorphic or almost cylindrical vesicles and display symmetric contacts. The F1 boutons form axosomatic and axodendritic synapses on both types of cells, and axoaxonic synapses on initial axon segments of PN. It is these boutons that participate in complex synaptic arrangements with vesicle-containing LCN dendrites and SR boutons, and they are also encountered as part of triads with three symmetric contacts. Representatives of this bouton population display positive GAD immunoreactivity. For measurements of the membrane and apposing structures, the identified PN dendrites were grouped into three categories. The group of “secondary” dendrites included all consecutive-order short dendritic segments within approximately a 60 μm radius around the soma where most of the branching occurred. It was found that the ratios of boutons with asymmetric contacts to those with symmetric contacts were 4:1 on primary dendrites, 9:1 on “secondary,” and 55:1 on distal dendrites. The ratios of symmetric dendrodendritic synapses to symmetric contacts formed by axon terminals were 3:1 on primary and “secondary” dendrites and 1:1 on distal dendrites. This suggests the overall predominance of excitatory inputs (LR and SR boutons) on PN dendrites with inhibitory inputs coming mainly from GABAergic LCN dendrites. Comparison of the present findings with earlier data on the cerebellar thelamic territory in the cat and the nigrothalamic territory in the monkey suggests significant interspecies and internuclear differences in the organization of mtor thalamic circuits.