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

Abstract

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)

Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia

“…Consistent with anatomical tracing studies in primates, we confirm a dual role for VA/VL thalamic nuclei that are connected with cortical, striatal, and pallidal regions. The connectivity pattern of the VA and VL nuclei supports the idea that they have a specific role integrating information from cortical motor areas with dorsal striatal output (Kultas-Ilinsky and Ilinsky, 1991;McFarland and Haber, 2002). Thus, we confirm at an anatomical level the notion that thalamic nuclei not only relay information through parallel pathways, but they also mediate integration between functionally specific cortical areas.…”

Organization of projections from the anterior pole of the nucleus reticularis thalami (NRT) to subdivisions of the motor thalamus: Light and electron microscopic studies in the Rhesus monkey

“…The only candidates for that are either dendrosomatic or axosomatic synapses made by local circuit neurons. In the primate VL, the GABAergic local circuit neurons are more numerous than in the VA subdivisions (Kultas- Ilinsky and Ilinsky, 1991). Because the NRT axons synapse on a large number of local circuit neuron dendrites, these may provide a conduit of an indirect NRT input to somata of projection neurons.…”

“…9a,c,d, 10b, 11a) or on small-diameter vesiclecontaining dendrites (Figs 9c, 10a-c, 11b-d). These were identified as distal dendrites of the two types of cells found in each nucleus, projection neurons and local circuit neurons, respectively (for normal ultrastructure of the nuclei see Ilinsky and Kultas-Ilinsky, 1990;Kultas-Ilinsky and Ilinsky, 1991;Kultas-Ilinsky et al, 1997). Just as in the double-labeled tissue, two or even three synaptic contacts per labeled bouton could be seen in a single section plane (Figs.…”

The thalamus as a monitor of motor outputs

“…We have not treated them as higher-order relays because we have previously defined higher-order relays as thalamic relays that receive their driving afferents directly from the cortex (Sherman & Guillery 2001, p. 231). The distinction that matters here is that a higher-order relay is sending messages to the cortex about the outputs of other cortical areas, whereas the mamillary and cerebellar afferents to the thalamus, which, on the basis of their synaptic relationships, must be regarded as the drivers at their thalamic termination (Harding 1973;Rinvik & Grofova 1974a,b;Somogyi et al 1978;Kultas-Ilinsky & Ilinsky 1991), are carrying messages from lower, non-telencephalic centres. 6 One might expect that as these two pathways are already carrying information about motor control mechanisms, they might differ from the other ascending pathways and go straight to the thalamus without sending any branches to yet other parts of motor control circuitry.…”