In most animals, sleep is considered a global brain and behavioral state. However, recent intracortical recordings have shown that aspects of non-rapid eye movement (NREM) sleep and wakefulness can occur simultaneously in different parts of the cortex in mammals, including humans. Paradoxically, however, NREM sleep still manifests as a global behavioral shutdown. In this review, the authors examine this paradox from an evolutionary perspective. On the basis of strategic modeling, they suggest that in animals with brains composed of heavily interconnected and functionally interdependent units, a global regulator of sleep maintains the behavioral shutdown that defines sleep and thereby ensures that local use-dependent functions are performed in a safe and efficient manner. This novel perspective has implications for understanding deficits in human cognitive performance resulting from sleep deprivation, sleep disorders such as sleepwalking, changes in consciousness that occur during sleep, and the function of sleep itself.