Sleep restores an optimal computational regime in cortical networks

Abstract

SUMMARYSleep is vitally important for brain function, yet its core restorative process remains an open question. Sleep is assumed to subserve homeostatic processes in the brain because sleep restores functional capacity, and stable function requires compensatory tuning of circuits in the face of experience. However, the set-point around which sleep tunes circuit computation is unknown; for more than four decades, the homeostatic aspect of sleep has been approximated by a heuristic model whose strongest correlate is Slow-wave Activity (SWA). While SWA can indicate sleep pressure, it fails to explain why animals need sleep. In contrast, criticality is a computational regime that optimizes information processing capacity, and is a homeostatically regulated set-point in isocortical circuits. Consistent with the effects of waking, criticality is degraded by experience-dependent plasticity. Whether criticality is the computational set-point of sleep is unknown. To address this question, we evaluated the effects of sleep and wake on emergent dynamics in ensembles of cortical neurons recorded continuously for 10-14 d in freely behaving rats. We show that normal waking experience progressively disrupts criticality, and that sleep functions to restore critical dynamics. Criticality is perturbed in a context-dependent manner depending on behavior and environmental variables, and waking experience is causal in driving these effects. The degree of deviation from criticality is robustly predictive of future sleep/wake behavior, more accurate than SWA, behavioral history, and other neural measures. Our results demonstrate that perturbation and recovery of criticality is a network homeostatic mechanism consistent with the core, restorative function of sleep.