Response to commentary on evolution of slow-wave sleep and palliopallial connectivity in mammals and birds: A hypothesis

Mammals and birds are the only animals that exhibit high-amplitude slow-waves (SWs) in the electroencephalogram during sleep. The SWs that characterize slow-wave sleep (SWS) in mammals and birds reflect the large-scale synchronization of slow neuronal activity. In mammals, this synchronization is dependent upon the high degree of interconnectivity within the neocortex, a cytoarchitectonic trait also found in the avian hyperpallium, but not the reptilian dorsal cortex. Consequently, I recently proposed that the presence of SWs in sleeping mammals and birds, and their absence in sleeping reptiles, is attributable to the greater degree of interconnectivity within the neocortex and hyperpallium when compared to the dorsal cortex [N.C. Rattenborg, Evolution of slow-wave sleep and palliopallial connectivity in mammals and birds: A hypothesis, Brain Res. Bull. 69 (2006) 20-29]. Rial et al. (this issue) challenge this hypothesis by noting that high-amplitude SWs occur in awake reptiles. Based largely on this observation, they suggest that SWS in homeotherms evolved from reptilian wakefulness. SWs in awake reptiles do not seem to reflect neural processes comparable to those that generate sleep-related SWs in homeotherms, however. Moreover, the proposed conversion of reptilian wakefulness into SWS is untenable from behavioral, mechanistic and functional perspectives. A more parsimonious explanation is that the precursor state to SWS in homeotherms was a state comparable to reptilian sleep, rather than wakefulness, with the primary difference being that the reptilian dorsal cortex lacks the interconnectivity necessary to generate sleep-related SWs in the electroencephalogram.