Sleep restores an optimal computational regime in cortical networks

Sleep is vitally important for brain function, yet its core process by which brain function is restored remains an open question. Sleep is assumed to subserve brain homeostatic processes; the proper compensatory tuning of circuits is necessary for stable function. Criticality, a computational regime that optimizes information processing capacity, is a homeostatically regulated set-point in isocortical circuits. Criticality is susceptible to degradation by experience-dependent plasticity. Whether criticality is the computational set-point of daily sleep is unknown. To address this question, we evaluated the effects of sleep and wake on emergent, computational 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 a universal set-point across animals. We find that criticality is perturbed in a context-dependent manner depending on behavior and environmental variables, and that waking experience is causal in driving these effects. The degree of deviation from criticality is robustly predictive of future behavior. Our results demonstrate that perturbation and recovery of criticality is consistent with a network mechanism at the core of the heuristic Two Process Model, which has been used to describe sleep and wake cycles for 40 years. Summarily, our data suggest that restoration of an optimal computational regime is a key factor in determining why brains sleep.