Phasic activation of lateral geniculate and perigeniculate thalamic neurons during sleep with ponto-geniculo-occipital waves

Abstract

Ponto-geniculo-occipital (PGO) waves are spiky field potentials generated in cholinergic nuclei of the dorsolateral mesopontine tegmentum just prior to and during rapid-eye-movement (REM) sleep and transferred toward thalamic nuclei. These events are commonly regarded as physiological correlates of oneiric behavior. We have examined the PGO-related discharges of physiologically identified neurons located in the dorsal lateral geniculate (LG) nucleus and perigeniculate (PG) sector of the reticular thalamic complex in chronically implanted, naturally sleeping cats. PGO focal waves and associated unit discharges were simultaneously recorded by the same microelectrode. PGO waves herald the other signs of REM sleep (EEG desynchronization and muscular atonia), appearing 30-90 sec before REM sleep over the EEG-synchronized activity of slow-wave sleep (pre-REM epoch). (1) Most PG neurons discharged bursts of action potentials in relation to PGO waves during both pre-REM and REM sleep. (2) The PGO-related activity of LG neurons was quite different. During the pre-REM stage, PGO waves correlated with a short (7-15 msec), high-frequency (300-500 Hz) spike burst of LG neurons, followed by a long (0.2-0.4 sec) train of single spikes, whereas during REM sleep, the PGO-related activity lacked the initial burst and consisted of a spike train that only slightly exceeded the tonically increased background firing of LG cells. The stereotyped characteristics of the PGO-related spike bursts during the pre-REM epoch suggest that they are the extracellular reflection of a low-threshold spike deinactivated by the tonic membrane hyperpolarization of LG cells associated with the EEG-synchronized sleep state. Such bursts are inactivated during the tonic depolarization of LG cells that occurs in REM sleep. The synchronous spike bursts discharged by LG cells in relation with the PGO waves of the pre-REM epoch probably underlie the much larger amplitude of the PGO waves of the pre-REM epoch as compared with those of the REM-sleep state. Since LG neurons have relatively low spontaneous firing rates during the EEG-synchronized pre-REM epoch, the PGO-related activity of this transitional stage leads to a higher signal-to-noise ratio in the visual thalamocortical channel than during REM sleep. We suggest that the PGO-related activity during the pre-REM epoch is related to vivid imagery during this stage of sleep.