Reticularis thalami neurons (RE neurons) were identified morphologically, and their electrophysiological properties were studied in cat under barbiturate anesthesia. Intracellular HRP injections showed that RE neurons possessed very long dendrites bearing numerous filopodia-like appendages and that their axons were directed toward main thalamic nuclei. As a rule, small axonal branches were also emitted within the RE nucleus itself. At rest, the membrane potential of RE neurons displayed 2 types of oscillations: a slow 0.1-0.2 Hz oscillation and fast 7-12 Hz oscillations occurring on the positive phase of the former. Episodes of spindle (7-12 Hz) waves lasted for 2-3 sec and were characterized by rhythmic depolarizations and burst discharges. Intracellular injections of QX314 and current pulse analyses revealed the presence in RE cells of 2 distinct inward currents: a persistent current that promoted tonic firing and a low-threshold current deinactivated by hyperpolarization that generated burst discharges. The low-threshold current deinactivated with large somatic hyperpolarizations (up to 30 mV) and produced depolarizing responses that lasted for about 70 msec. In addition, low-threshold responses appeared rhythmically at intervals of about 150 msec after recovery of the membrane potential from hyperpolarization. Because of their duration, voltage dependence, and persistence after intracellular injections of QX314, it is suggested that these responses resulted from activation of a low-threshold Ca2+ current at the dendritic level. In QX314-injected cells, selective components of spontaneous oscillations were abolished, among them the positive phase of the slow oscillation and late depolarizing humps that followed burst discharges within spindle sequences. However, the rhythmic occurrence of spindle episodes at 0.1-0.2 Hz was never affected by DC currents or by QX314 or Cl- injections, suggesting that oscillations within a particular RE neuron partly reflected the oscillatory behavior of a network of cells. On the basis of these electrophysiological results and the known morphological and neurochemical features, a new hypothesis is proposed to account for the rhythmicity of RE neurons.