Sleep viewed as a state of adaptive inactivity

Abstract

Sleep is often viewed as a vulnerable state that is incompatible with behaviours that nourish and propagate species. This has led to the hypothesis that sleep has survived because it fulfills some universal, but as yet unknown, vital function. I propose that sleep is best understood as a variant of dormant states seen throughout the plant and animal kingdoms and that it is itself highly adaptive because it optimizes the timing and duration of behaviour. Current evidence indicates that ecological variables are the main determinants of sleep duration and intensity across species.

Figure 1 |. A continuum of states, from adaptive inactivity to high activity, in homeotherms.

States of adaptive inactivity include hibernation, torpor and sleep. Hibernation is the deepest form of dormancy in mammals, taking many minutes to reverse. Some bats, many species of rodents, marsupials and insectivores hibernate. The term torpor has been used to include not only extended periods of inactivity termed hibernation but also shorter periods of greatly reduced metabolism that may last as little as one night and that are frequently seen in birds and small mammals, such as certain species of bats and rodents. The walrus has recently been observed to spontaneously stop sleeping for periods of several days. Birds exhibit greatly increased duration of waking during migratory periods. Cetacean mothers and calves are continuously active for several weeks after birth. Image credits: ground squirrel courtesy of H. Carey; humming bird courtesy of E. Sullivan; dog courtesy of P. K. Friedman, walrus courtesy of Y. Komine; white-crowned sparrow courtesy of W. Kitundu; killer whale courtesy of M. Aguilera/SeaWorld San Diego.

Figure 2 |. Diversity of sleep in tetrapods.

A phylogenetic tree, with representative animals, which shows that aspects of sleep such as rapid eye movement (REM)-like and non-REM-like cortical activity and brainstem activity differ greatly between species. Slow waves and spindles are electroencephalographic (EEG) patterns that are typical of non-REM sleep in mammals, but they are not seen in turtles. Indeed, turtles show little change in forebrain EEG between waking and sleep states, although EEG spikes may occur at certain temperatures. No REM sleep-like activation of brainstem neuronal activity has been observed during sleep states in the turtle. Slow waves are briefly asymmetrical in sleeping birds, always asymmetrical in cetaceans and mostly asymmetrical in fur seals when they are in water but not when they are on land. Sleep duration is greatly reduced during migration in the white-crowned sparrow and no long-duration periods of sleep-like behaviour occur in the postpartum period in examined cetacean species. Recordings of neuronal activity have not been performed during sleep in birds, cetaceans or seals. Sleep in studied marsupial mammals seems to resemble that in placental mammals.