In vivo intracellular recordings were obtained from identified thalamocortical neurons in the ventroanterior-ventrolateral complex in urethane-anesthetized rats. This thalamic nucleus has few interneurons. Neurons that responded to cerebellar stimulation were injected intracellularly with horseradish peroxidase or biocytin and examined with light and electron microscopy (see companion paper). Intrinsic membrane properties and voltage-dependent rhythmic activity of cerebellar-responsive ventroanterior-ventrolateral neurons were similar to those described previously for thalamic neurons. Thus, in addition to conventional "fast" Na(+)-dependent spikes, rat ventroanterior-ventrolateral neurons had "slow" Ca(2+)-mediated low-threshold spikes and membrane conductances that supported rhythmic oscillations. Two modes of spontaneous activity were observed: (i) a tonic firing pattern that consisted of irregularly occurring fast spikes that predominated when the membrane potential was more positive than about -60 mV, and (ii) a rhythmic firing pattern, observed when the membrane potential was more negative than about -65 mV, composed of periodic (4-8 Hz) membrane hyperpolarizations and ramp depolarizations that often produced a low-threshold spike and a burst of fast spikes. In some neurons, spontaneous fast prepotentials were also observed, often with a relatively constant rate (up to 70 Hz). Cerebellar stimulation elicited excitatory postsynaptic potentials that in some cases appeared to be all-or-none and were similar in form to fast prepotentials. Stimulation of ipsilateral motor cortex elicited a short-latency antidromic response followed by a monosynaptic excitatory postsynaptic potential, which had a slower rise time than excitatory postsynaptic potentials evoked from cerebellum, suggesting that cortical inputs were electrotonically distal to cerebellar inputs. In the presence of moderate membrane hyperpolarization, the cortically evoked excitatory postsynaptic potential was followed by a long-lasting hyperpolarization (100-400 ms duration), a rebound depolarization and one or two cycles resembling spontaneous rhythmic activity. Membrane conductance was increased during the initial component of the long hyperpolarization, much of which was probably due to an inhibitory postsynaptic potential. In contrast, membrane conductance was unchanged or slightly decreased during the latter three-quarters of the long hyperpolarization. The amplitude of this component of the long hyperpolarization usually decreased when the membrane was hyperpolarized with intracellular current injection. Thus, both disfacilitation and an inhibitory postsynaptic potential may have contributed to the latter portion of the cortically-evoked long hyperpolarization. The cortically-evoked inhibitory postsynaptic potentials likely originated predominantly from feedforward activation of GABAergic neurons in the thalamic reticular nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)