Waking Experience and Circadian Rhythms Result in Differential Modulation of Sleep and Wake States

Abstract

Sleep is thought to be tightly regulated by two processes, a homeostatic and a circadian process, which interact in a complex way to integrate prior wakefulness and circadian time (Borbély et al., 1982). Despite extensive research, however, little is known about how each contributes to the regulation of sleep and wake states. The goal of this study was to explore the regulation of sleep and wake during and after extended wakefulness and describe how different waking experiences may contribute to changes in brain-wide electrophysiological activity and neuronal activity reporters. In addition, sleep and wake regulation was compared in the presence and absence of circadian rhythms. This study demonstrates that waking experience during sleep deprivation (SD) changes sleep state dynamics following SD and results in experience-specific electroencephalography (EEG) patterns during wake. Sleep and wake regulation was shown to be different in rhythmic and arrhythmic animals. This difference was reflected in the percent of time spent in each state and in cumulative amounts of slow wave sleep (SWS) and rapid-eye movement (REM) sleep at baseline and during and after sleep deprivation. An automated pipeline for detecting whole brain neuronal activity reporters in 2D sections was also developed as a complement to EEG studies, allowing for the interrogation of changes in regional activity over time. Taken together, this study contributes to our understanding of sleep-wake regulation by demonstrating (1) that wake experiences differentially modulate sleep homeostatic responses and (2) that the homeostat responds differently to high sleep pressure in the absence of circadian rhythms.