Call it sleep — what animals without backbones can tell us about the phylogeny of intrinsically generated neuromotor rhythms during early development

Abstract

A comprehensive overview is presented of the literature dealing with the development of sleep-like motility and neuronal activity patterns in non-vertebrate animals. it has been established that spontaneous, periodically modulated, neurogenic bursts of movement appear to be a universal feature of prenatal behavior. New empirical data are presented showing that such 'seismic sleep' or 'rapid-body-movement' bursts in cuttlefish persist for some time after birth. Extensive ontogenetic research in both vertebrates and non-vertebrates is thus essential before current hypotheses about the phylogeny of motorically active sleep-like states can be taken seriously.

Sleep and Development in Genetically Tractable Model Organisms

“…Similar trends, where the amount of total sleep, or vertebrate REM sleep, is highest early in development, have been observed in mammals, fish, birds, insects, and nematodes (Jouvet-Mounier et al 1970;McGinty et al 1977;Szymczak 1987;Shaw et al 2000;Kirov and Moyanova 2002;Paredes et al 2006;Raizen et al 2008;Hasan et al 2012;Todd et al 2012;Sorribes 2013). These findings led to the hypothesis that during early life, REM sleep and invertebrate sleep may play an important role in the development of the nervous system, by establishing a period of globally heightened plasticity and/ or providing endogenous, specialized activity in certain neural circuits (O'Donovan 1999;Blumberg 2008, 2010;Blumberg et al 2013;Corner 2013). Such specialized activity could, for instance, promote appropriate neurodevelopment through feedback by coupling function (such as recurring limb movement) to the refinement of neural connections.…”

Perchance to dream? Primordial motor activity patterns in vertebrates from fish to mammals: their prenatal origin, postnatal persistence during sleep, and pathological reemergence during REM sleep behavior disorder

“…as the most appropriate appelation for this fourth broad category of behavior (see Corner 2013) [4] . S u b s e q u e n t l y, t h e o n t o g e n y o f t h i s s t r i k i n g phenomenon -which has been referred to as 'seismic' sleep [5] or, more generally, motorically 'active sleep'…”

“…(MAS) -was reviewed across a wide spectrum of [4] . Although the so-called mature form of MAS (viz., rapid eye movement (REM) or 'paradoxical' sleep [5][6][7] ) appears to have evolved independently in birds and mammals [2,8,9] , many ectothermic vertebrates are also on record as…”

“…Deafferentation experiments in situ soon confirmed the intrinsic, nonreflexogenic, nature of motility in the chick embryo [20] , while in vitro experiments led to the same conclusion for amphibian and mammalian neuromotor systems [15,21,22] . It could be relevant for the understanding of sleep-related movement and behavioral pathologies in later life [23] that stereotyped, well organized, muscular contractions are in fact present from the onset of spontaneous motility both ontogenetically [24][25][26] and phylogenetically [3,4] . REM sleep behavior disorder (RBD) [27] for instance, mimicks in many respects normal fetal and early postnatal motor movement patterns.…”

“…4) has evidently taken over the control of behavior. The period of development between this early stage of putative wakefulness and sleep in adults has hardly been looked into for ectotherms, but it can be surmised that a similar waning of overall sleep time as takes place in birds and mammals -and also in the cuttlefi sh, a highly evolved cephalopod mollusc [4,57] will be observed as these animals grow older. It will be of special interest to see if their sleep shows spontaneous bouts of stereotyped movements, since these have been reported recently in sensescent cuttlefi sh [58] .…”