A novel theory of rapid eye movement sleep as an integral component of the seasonal timekeeping apparatus

Although we have an increasingly sure grasp of much of its proximate circuitry, we continue to lack the ultimate physiological rationale of rapid eye movement (REM) sleep. In this paper, we propose that REM sleep derives both its proximate mechanisms as well as its ultimate cause from photoperiodism. (This refers to the means whereby many organisms translate information about day length into appropriately timed physiological adjustments ensuring their survival through the most challenging season—usually winter). First, the REM sleep interval serves, we suggest, as a sampling device attuned to a particular species of sidereal signal that materializes only in the crepuscular intervals of the day (when light slowly changes place with darkness) and that becomes fully available to the animal only in the shorter days (SDs) of the year. Second, REM sleep serves as an interval timer sensitive to the duration between shorter vs. longer phasic REM episodes, a distinction which a defined set of astrocytes then translates into that between, respectively, a temporal interval incapable of supporting aerobic glycolysis (AG) vs. one fully capable of doing so. Accordingly lactate, the product of AG, functions as a SD-specific signal triggering a behavioral, metabolic, and neuroprotective/neurogenetic program allowing the animal to survive winter. Outlined is the CNS seasonal module responsible for recognizing the lactate signal and disseminating it through the seasonal animal. This includes a novel photoperiodic role for the central extended amygdala and in particular the bed nucleus of the stria terminalis (BNST). Our model clarifies many different aspects of the REM sleep/seasonal amalgam including its coopting of basic arousal circuitry so as to support behavioral bistability, a key feature of the photoperiodic organism. Thus a remarkable but heretofore poorly understood phenomenon, a phase of hyperarousal preceding the descent into involution, falls into place as part of the strategy for surviving winter. Finally, our hypothesis is concordant with recent evidence demonstrating that the gene set subserving so-called lactate-mediated neural plasticity emerged well before that supporting traditional (explicit) memory, a specialty of mammals and their hippocampal tissue.