Terminals of cerebellar afferents (CB) to different regions of the ventral lateral nucleus (VL) of the rhesus monkey thalamus were labeled with wheat germ agglutinin-horseradish peroxidase following injections into the dentate nucleus. Synaptic relationships of 17 CB with projection neuron dendrites (PNd) and local circuit neuron dendrites (LCNd) were analyzed in serial ultrathin sections from dorsal and ventral VL regions, which are known to differ cytoarchitecturally and functionally. Three terminals were reconstructed using three-dimensional (3D) computer image analysis techniques to obtain volumetric and planar measurements. CB in the ventral VL were often flat and elongated with synaptic vesicles arranged in clusters. Each CB was engaged with one PNd and one to four LCNd. A single bouton formed 8-50 synaptic contacts, with those on PNd outnumbering the ones on LCNd 4.1:1. Only some CB in the ventral VL were engaged in complex synaptic arrangements such as triads and serial synapses. Most CB in the dorsal VL displayed a roundish shape and numerous uniformly distributed synaptic vesicles. They formed 5-25 synaptic contacts with a 3:1 ratio of contacts on PNd compared with those on LCNd. CB in the dorsal VL participated in a variety of complex synaptic arrangements. Two types of triads were found: classic with CB, PNd and LCNd, and unconventional with CB and two LCNd. CB were also involved in serial synapses with two LCNd or LCNd and another PNd, and serial sequential synapses with two LCNd and a PNd. Three glomerulus-like structures were encountered in the dorsal VL. 3D reconstruction and volumetric measurements revealed that synaptic contacts formed by CB on PNd had varying shapes and sizes (0.022-0.274 microns2). Synapses formed on LCNd were larger (0.09-0.407 microns2). The total area of all active zones of a single CB on LCNd was either equal to or about 40% smaller than that of synapses on PNd. The entire active zone area comprised 1-1.6% of the total CB surface area and did not seem to correlate with the volume. Synaptic contacts formed by associated LCNd on PNd in complex arrangements were usually small (0.021-0.044 micron2). The results suggest that: synapses formed by CB on PNd and LCNd, and synapses formed by LCNd on PNd may differ in strength; a variety of different circuits participate in the processing of cerebellar afferent information in the primate VL; and these circuits differ in functionally different VL subdivisions.

This study examined organization of the projection from the dentate nucleus of the cerebellum to the ventral lateral nucleus (VL) of the thalamus in Macaca mulatta. Small injections of biotinylated dextran amine were placed in the ventral parts of dentate nuclei. The distribution of all contralateral terminal fields in the thalamus was charted, and representative individual axons that terminated in the VL were traced in serial sections under the light microscope. These axons were reconstructed with all their branches and terminal fields in the thalamus. The geometry and size of the terminal fields as well as the number and distribution of boutons and neurons in them were analyzed. The terminal fields of all labeled axons were distributed widely over the VL either singly or in clusters. Two types of axons were found: simple axons formed only one terminal field and complex axons formed multiple terminal fields at a distance. Individual terminal fields were focal, had the form of flattened discs, and generated up to 200 boutons distributed between 10 and 29 nerve cell bodies. These findings suggest that a simple axon activates a small group of neurons at one site. The complex axons, in turn, influence similar size cell groups at different VL locations. The total number of boutons generated by a single complex axon was up to 300. Future studies should determine whether simple axons could be branches of complex axons that took off below the thalamus. The results reveal a complex organization of the input from the ventral dentate to the VL that only partially fits into the traditional concept of somatotopic organization of the nucleus.

This study examined organization of the projection from the dentate nucleus of the cerebellum to the ventral lateral nucleus (VL) of the thalamus in Macaca mulatta. Small injections of biotinylated dextran amine were placed in the ventral parts of dentate nuclei. The distribution of all contralateral terminal fields in the thalamus was charted, and representative individual axons that terminated in the VL were traced in serial sections under the light microscope. These axons were reconstructed with all their branches and terminal fields in the thalamus. The geometry and size of the terminal fields as well as the number and distribution of boutons and neurons in them were analyzed. The terminal fields of all labeled axons were distributed widely over the VL either singly or in clusters. Two types of axons were found: simple axons formed only one terminal field and complex axons formed multiple terminal fields at a distance. Individual terminal fields were focal, had the form of flattened discs, and generated up to 200 boutons distributed between 10 and 29 nerve cell bodies. These findings suggest that a simple axon activates a small group of neurons at one site. The complex axons, in turn, influence similar size cell groups at different VL locations. The total number of boutons generated by a single complex axon was up to 300. Future studies should determine whether simple axons could be branches of complex axons that took off below the thalamus. The results reveal a complex organization of the input from the ventral dentate to the VL that only partially fits into the traditional concept of somatotopic organization of the nucleus. J. Comp. Neurol. 421:412–428, 2000. © 2000 Wiley‐Liss, Inc.