Origin and evolution of sleep: roles of vision and endothermy.

Abstract The origin of both sleep and memory appears to be closely associated with the evolution of mechanisms of enhancement and maintenance of synaptic efficacy. After the origin of activity-dependent synaptic plasticity, whereby single activations of synapses led to short-term efficacy enhancements, lengthy maintenance of the enhancements probably was achieved by repetitive activations (“dynamic stabilization”). These are thought to have occurred either in the course of frequent functional use, or to have been induced spontaneously within the brain to maintain synaptic efficacies in circuits that were in infrequent use. The latter repetitive activations are referred to as ‘non-utilitarian’ dynamic stabilization. With the evolution of increasing repertories and complexities of behavioral and sensory capabilities—with vision usually being the vastly preeminent sense—brain complexity increased markedly. Accompanying the greater complexity, needs for storage and maintenance of hereditary and experiential information (memories) also increased greatly. It is suggested that these increases led to conflicts between sensory input processing during restful waking and concomitant ‘non-utilitarian’ dynamic stabilization of infrequently used memory circuits. The selective pressure for the origin of primitive sleep may have been a need to achieve greater depression of central processing of sensory inputs—largely complex visual information—than occurs during restful waking. The electrical activities of the brain during sleep (aside from those that subserve autonomic activities) may function largely to maintain sleep and to dynamically stabilize infrequently used circuitry encoding memories. Sleep may not have been the only evolutionary adaptation to conflicts between dynamic stabilization and sensory input processing. In some ectothermic vertebrates, sleep may have been postponed or rendered unnecessary by a more readily effected means of resolution of the conflicts, namely, extensive retinal processing of visual information during restful waking. By this means, processing of visual information in central regions of the brain may have been maintained at a sufficiently low level to allow adequate concomitant dynamic stabilization. As endothermy evolved, the skeletal muscle hypotonia of primitive sleep may have become insufficient to prevent sleep-disrupting skeletal muscle contractions during ‘non-utilitarian’ dynamic stabilization of motor circuitry at the accompanying higher body temperatures and metabolic rates. Selection against such disruption during dynamic stabilization of motor circuitry may have led to the inhibition of skeletal muscle tone during a portion of primitive sleep, the portion designated as “rapid-eye-movement sleep.” Many marine mammals that are active almost continuously engage only in unihemispheric non-rapid-eye-movement sleep. They apparently do not require rapid-eye-movement sleep and accompanying ‘non-utilitarian’ dynamic stabilization of motor circuitry because this circuitry is in virtually continuous use. Studies of hibernation by arctic ground squirrels suggest that each hour of sleep stabilizes brain synapses for as long as four hours.