THE SLOW (LESS-THAN-1 HZ) OSCILLATION IN RETICULAR THALAMIC AND THALAMOCORTICAL NEURONS - SCENARIO OF SLEEP RHYTHM GENERATION IN INTERACTING THALAMIC AND NEOCORTICAL NETWORKS

As most afferent axons to the thalamus originate in the cerebral corte x, we assumed that the slow (< 1 Hz) cortical oscillation described in the two companion articles is reflected in reticular (RE) thalamic an d thalamocortical cells. We hypothesized that the cortically generated slow rhythm would appear in the thalamus in conjunction with delta an d spindle oscillations arising from intrinsic and network properties o f thalamic neurons. Intracellular recordings have been obtained in ane sthetized cats from RE (n = 51) and cortically projecting (n = 240) th alamic neurons. RE cells were physiologically identified by cortically evoked high-frequency spike bursts and depolarizing spindle oscillati ons. Thalamocortical cells were recognized by backfiring from appropri ate neocortical areas, spindle-related cyclic IPSPs, and hyperpolariza tion-activated delta oscillation consisting of rhythmic low-threshold spikes (LTSs) alternating with afterhyperpolarizing potentials (AHPs). The slow rhythm (0.3-0.5 Hz) was recorded in 65% of RE neurons. In al most-equal-to 90% of oscillating cells, the rhythm consisted of prolon ged depolarizations giving rise to trains of single action potentials. DC hyperpolarization increased the synaptic noise and, in a few cells , suppressed the long-lasting depolarizing phase of the slow rhythm, w ithout blocking the fast EPSPs. In almost-equal-to 10% of oscillating neurons, the hyperpolarizing phase of the oscillation was much more pr onounced, thus suggesting that the slow rhythm was produced by inhibit ory sculpturing of the background firing. The slow oscillation was ass ociated with faster rhythms (4-8 Hz) in the same RE neuron. The slow r hythm of RE neurons was closely related to EEG wave complexes recurrin g with the same frequency, and its strong dependency upon a synchroniz ed state of cortical EEG was observed during shifts in EEG patterns at different levels of anesthesia. In 44% of thalamocortical cells the s low rhythm of depolarizing sequences was apparent and it could coexist with delta or spindle oscillations in the same neuron. The occurrence of the slowly recurring depolarizing envelopes was delayed by the hyp erpolarizing spindle sequences or by the LTS-AHP sequences of delta os cillation. The hyperpolarization-activated delta potentials that tende d to dampen after a few cycles were grouped in sequences recurring wit h the slow rhythm. We finally propose a unified scenario of the genesi s of the three major sleep rhythms: slow, delta, and spindle oscillati ons.