Memory, sleep and the evolution of mechanisms of synaptic efficacy maintenance

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. The development of activity-dependent synaptic plasticity apparently was the first evolutionary adaptation of nervous systems beyond a capacity to respond to environmental stimuli by mere reflexive actions. After the origin of activity-dependent synaptic plasticity, whereby single activations of synapses led to short-term efficacy enhancement, lengthy maintenance of enhancements probably was achieved by repetitive activations (“dynamic stabilization”). One source of selective pressure for the evolutionary origin of neurons and neural circuits with oscillatory firing capacities may have been a need for repetitive spontaneous activations to maintain synaptic efficacy in circuits that were in infrequent use. This process is referred to as “non-utilitarian” dynamic stabilization. Dynamic stabilization of synapses in “simple” invertebrates occurs primarily through frequent use. In complex, locomoting forms, it probably occurs through both frequent use and non-utilitarian activations during restful waking. With the evolution of increasing repertories and complexities of behavioral and sensory capabilities—with vision usually being the vastly pre-eminent sense—brain complexity increased markedly. Accompanying the greater complexity, needs for storage and maintenance of hereditary and experiential information (memories) increased greatly. It is sugested 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 resulting 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 may stabilize brain synapses for as long as 4 h. Phasic irregularities in heart and respiratory rates during rapid-eye-movement sleep may be a consequence of superposition of dynamic stabilization of motor circuitry on the rhythmic autonomic control mechanisms. Some information encoded in circuitry being dynamically stabilized during sleep achieves unconscious awareness in authentic and variously modified form as dreams and other sleep mentation.