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 microns2 (mean 535.2 microns2, SD = 159.5). Small glutamic acid decarboxylase (GAD) immunoreactive cells (LCN) exhibit sizes from 65 to 210 microns2 (mean 122.5 microns2, 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 microns2 and the appositional length on PN dendrites ranges from 1.1 to 14 microns. 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 micron2) 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.(ABSTRACT TRUNCATED AT 400 WORDS)