Evolution of slow-wave sleep and palliopallial connectivity in mammals and birds: a hypothesis.
Mammals and birds are the only animals that exhibit rapid eye-movement (REM) sleep and slow-wave sleep (SWS). Whereas the electroencephalogram (EEG) during REM sleep resembles the low-amplitude, high-frequency EEG of wakefulness, the EEG during SWS displays high-amplitude, slow-waves (1-4Hz). The absence of similar slow-waves (SWs) in sleeping reptiles suggests that the neuroanatomical and neurophysiological traits necessary for the genesis of SWs evolved independently in the mammalian and avian ancestors. Advances in our understanding of comparative neuroanatomy and the genesis of mammalian SWs suggest that the absence of SWs in reptiles is due to limited connectivity within the pallium, the dorsal portion of the telencephalon that includes the mammalian neocortex, reptilian dorsal cortex and avian Wulst (hyperpallium), as well as the dorsal ventricular ridge in birds and reptiles and the mammalian claustrum and pallial amygdala. In mammals, the slow oscillation (<1Hz) of cortical neurons acts through reciprocal corticothalamic loops and corticocortical connections to synchronize the 1-4Hz activity of thalamocortical neurons in a manner sufficient to generate SWs detectable in the EEG. Given the role that corticocortical (or palliopallial) connections play in the genesis of SWs in mammals, the degree of palliopallial connectivity might explain why birds show SWs and reptiles do not. Indeed, whereas the mammalian neocortex and avian pallium show extensive palliopallial connectivity, the reptilian pallium exhibits limited intrapallial connections. I thus propose that the evolution of SWs is linked to the independent evolution of extensive palliopallial connectivity in mammals and birds. As suggested by experiments functionally linking SWs to performance enhancements, the palliopallial connections that give rise to SWs might also depend on SWs to maintain their efficacy.
Rattenborg
Niels C
NC
Max Planck Institute for Ornithology, Seewiesen, Postfach 1564, Starnberg D-82305, Germany. rattenborg@orn.mpg.de
D000818:Animals; D005075:Biological Evolution; D001717:Birds / Q000033:anatomy & histology / Q000502:physiology*; D001921:Brain / Q000166:cytology / Q000502:physiology*; D004569:Electroencephalography; D008322:Mammals / Q000033:anatomy & histology / Q000502:physiology*; D009434:Neural Pathways / Q000166:cytology / Q000502:physiology; D010802:Phylogeny; D012890:Sleep / Q000502:physiology*