The morphology and synaptic organization of neurons in the ventroanterior-ventrolateral nucleus of rats was examined using in vivo intracellular staining techniques. Neurons were characterized electrophysiologically based on intrinsic membrane properties and synaptic responses to stimulation of motor cortex and cerebellar nuclei, as described in the companion paper. Cerebellar-responsive neurons were stained intracellularly with either horseradish peroxidase or biocytin. All stained ventroanteriorventrolateral nucleus neurons were identified as thalamocortical neurons on anatomical (and often electrophysiological) grounds, consistent with previous findings that rat ventroanterior-ventrolateral nucleus is interneuron-sparse. Ventroanterior-ventrolateral nucleus neurons had three to eight thick primary dendrites. Proximal dendrites often exhibited a tufted branching pattern, from which many thinner, higher order dendrites arose. Dendrites branched to form a funnel-like infiltration of the neuropil that resulted in a spherical, roughly homogeneous dendritic field. The axon originated from the cell body or a proximal dendrite and coursed laterally and dorsally to innervate motor cortex. One to five axon collaterals were emitted in the rostral dorsolateral sector of the thalamic reticular nucleus; collaterals were not observed in the ventroanterior-ventrolateral nucleus or other nuclei in dorsal thalamus. The synaptic organization of the ventroanterior-ventrolateral nucleus was examined with electron microscopy, including two intracellularly labeled ventroanterior-ventrolateral nucleus neurons that were shown electrophysiologically to receive monosynaptic inputs from the cerebellum. The neuropil of rat ventroanterior-ventrolateral nucleus lacked the complexity and diversity found in corresponding thalamic nuclei of felines and primates, due to the paucity of interneurons. Vesicle-containing dendrites, dendrodendritic synapses and glomeruli were not observed. Three broad classes of presynaptic terminals were identified. (1) Small round boutons: small boutons containing densely-packed, small round vesicles that formed asymmetric synapses predominantly with the distal dendrites of thalamocortical neurons. These were the most prevalent type of bouton in the ventroanterior-ventrolateral nucleus (78% of presynaptic elements) and likely arose from the cerebral cortex. (2) Large round boutons: large terminals with loosely packed small round vesicles that made multiple asymmetric synapses with proximal and intermediate dendrites. Large round boutons comprised 8% of the neuropil, and likely arose from the cerebellar nuclei. (3) Medium size boutons with pleomorphic vesicles: mediumsized profiles containing pleomorphic vesicles that formed symmetric synapses with proximal, intermediate and distal dendrites and, less frequently, with cell bodies. These boutons constituted 14% of the neuropil, and their morphology was similar to previous descriptions of GABAergic immunoreactive profiles in rat ventroanterior-ventrolateral nucleus, as well as boutons originating from the thalamic reticular nucleus (which is the primary source of GABAergic input to the ventroanterior-ventrolateral nucleus). The synaptic organization of thalamocortical neurons and the scarcity of interneurons in the ventroanterior-ventrolateral nucleus is discussed in relation to the critical role of the thalamic reticular nucleus in modulating the efficacy of cortical and cerebellar afferents in the ventroanterior-ventrolateral nucleus and in determining the functional state of ventroanterior-ventrolateral nucleus neurons.
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