Morphological analysis of 77 neurons in the ventroanterior (VA), ventrolateral (VL), ventromedial (VM), and central lateral (CL) nuclei was performed by intracellular HRP staining in combination with electrophysiological studies. The neurons were classified into four groups according to either electrophysiological or morphological criteria, i.e., 20 relay neurons (18 thalamocortical (T-C) and two thalamocaudate (T-Cd) relay neurons), 17 projection neurons, 36 unidentified neurons, and four presumed interneurons. All 36 unidentified neurons had morphological features similar to those of relay and projection neurons. All neurons except four presumed interneurons had dendrites sparsely covered with spinelike appendages. Most of their dendrites displayed a spherically radiating branching pattern, and a few showed a tufted or linearly oriented pattern. Sizes of somata and dendritic radii were compared in entopeduncular (Ent)-responsive (n = 25) and cerebellar (CN)-responsive groups (n = 37) in VA, VL, and VM nuclei. The soma size was similar in VL (18-21 X 29-34 micron) and VM (15-19 X 29-31 micron), but in VA, CN-responsive neurons (15 X 30 micron) seemed to be smaller than Ent-responsive ones (22 X 36 micron). The largest dendritic field of neurons in each thalamic nucleus was similar in both groups. They were about 250-320 micron in radius. Diameters of axons were also compared but no statistically significant difference was detected (i.e., 1.5 +/- 0.3 (mean +/- S.D.) micron for the Ent group and 1.7 +/- 0.5 micron for the CN group). Three types of axonal trajectories were noted, i.e., neurons projecting their axons dorsolaterally, ventrolaterally, or horizontally. Fourteen neurons out of 37 relay and projection neurons gave off several fine distal axon collaterals in the thalamic reticular nucleus, and one T-Cd, three projection, and one unidentified neurons gave off proximal axon collaterals near the soma-dendritic domain in addition to those in the thalamic reticular nucleus. Four neurons classified as presumed interneurons had smaller somata (9-13 X 18-23 micron) and varicose dendrites. Three of them received Ent-induced inhibitory postsynaptic potentials (IPSPs) or CN-induced excitatory postsynaptic potentials (EPSPs). Several presumed axon terminals were found to cover the soma of an adjacent neuron, which seemed to indicate their inhibitory nature. The proximal axon collaterals in the ventral thalamic nuclei may consist of local inhibitory circuits with presumed interneurons in addition to other inhibitory circuits with thalamic reticular neurons.