Rhythmical oscillation of thalamic neuronal populations occurs under physiological conditions and in several disease states. In the present experiments we examined the network properties of population rhythmicity and the possible involvement of N-methyl-D-aspartate receptors in the frequency regulation and maintenance of rhythmic thalamic bursts. Multisite recording of neuronal activity and local microinjections of drugs were performed on the freely moving rat. Rhythmic thalamic population bursts at 6 to 9 Hz and concurrent neocortical high voltage spike-and-wave spindles were observed during awake immobility, with the thalamic rhythm leading the neocortical high voltage spindle. Even though all individual thalamocortical neurons fired in a phase-locked manner to the high-voltage spindle, the majority discharged at a significantly lower frequency than that of the population (multiunit) activity. In contrast, neurons in the nucleus reticularis thalami discharged at the frequency of the population bursts. Neurons in the extrapyramidal system and neocortex but not the hippocampal formation also fired in a phase-locked manner to the high-voltage spindle. Systemic administration or local microinjection of either non-competitive or competitive N-methyl-D-aspartate blockers (ketamine or ap-5) slowed the frequency of thalamic multiunit bursts and associated high-voltage spindles from 8 to 2 Hz, or completely blocked rhythmicity. Unilateral thalamic injection of ketamine or ap-5 resulted in a suppression of the amplitude of high-voltage spindles in the injected hemisphere. It is concluded that thalamic rhythmicity is not due to the "pacemaker" properties of thalamic cells but is rather an emergent property of the relay thalamus-nucleus reticularis network. Furthermore, we hypothesize that the frequency of network oscillation is regulated by the interplay between two major classes of voltage-dependent conductances in the thalamocortical cells: low-threshold calcium channels and high-threshold N-methyl-D-aspartate channels.