Skip to main content
PMC home page
Neuroscience Bulletin logoLink to Neuroscience Bulletin
. 2013 Mar 8;29(3):373–380. doi: 10.1007/s12264-013-1313-3

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

Michael A Corner 11313,21313,✉
PMCID: PMC5561840  PMID: 23471866

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.

Keywords: sleep phylogeny, behavior development, spontaneous motility, neuronal networks, cuttlefish

References

  • [1].Corner M, van der Togt C. No phylogeny without ontogeny: a comparative and developmental search for the sources of sleep-like neural and behavioral rhythms. Neurosci Bull. 2012;28:25–38. doi: 10.1007/s12264-012-1062-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [2].Fuller PM, Saper CB, Lu J. The pontine REM switch: past and present. J Physiol. 2007;584:735–741. doi: 10.1113/jphysiol.2007.140160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [3].Jouvet M. Paradoxical Sleep—a Study of its Nature and Mechanisms. Prog Brain Res. 1965;18:20–62. doi: 10.1016/S0079-6123(08)63582-7. [DOI] [PubMed] [Google Scholar]
  • [4].Jouvet M. The Paradox of Sleep/ Le Sommeil et le Rêve. Cambridge, MA: MiT Press; 1999. [Google Scholar]
  • [5].Siegel JM. Functional implications of sleep development. PLoS Biol. 2005;3:e178. doi: 10.1371/journal.pbio.0030178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [6].Valatx JL. The ontogeny and physiology confirms the dual nature of sleep states. Arch Ital Biol. 2004;142:569–580. [PubMed] [Google Scholar]
  • [7].Siegel JM. Do all animals sleep? Trends Neurosci. 2008;31:208–213. doi: 10.1016/j.tins.2008.02.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [8].Lee Kavanau J. REM and NREM sleep as natural accompaniments of the evolution of warm-bloodedness. Neurosci Biobehav Rev. 2002;26:889–906. doi: 10.1016/S0149-7634(02)00088-X. [DOI] [PubMed] [Google Scholar]
  • [9].Lesku JA, Martinez-Gonzalez D, Rattenborg NC. Sleep and sleep states: phylogeny and ontogeny. In: Squire LR, editor. Encyclopedia of Neuroscience. oxford: Academic Press; 2009. pp. 963–971. [Google Scholar]
  • [10].Corner M. Spontaneous motor rhythms in early life3—phenomenological and neurophysiological aspects. Prog Brain Res. 1978;48:349–366. doi: 10.1016/S0079-6123(08)61034-1. [DOI] [PubMed] [Google Scholar]
  • [11].Corner MA. Sleep and the beginnings of behavior in the animal kingdom—studies of ultradian motility cycles in early life. Prog Neurobiol. 1977;8:279–295. doi: 10.1016/0301-0082(77)90008-9. [DOI] [PubMed] [Google Scholar]
  • [12].Jouvet M. Le Chateau des Songes (The Castle of Dreams) Paris: Odile Jacob; 1992. [Google Scholar]
  • [13].Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, Sundaram MV, et al. Lethargus is a Caenorhabditis elegans sleep-like state. Nature. 2008;451:569–572. doi: 10.1038/nature06535. [DOI] [PubMed] [Google Scholar]
  • [14].Mahowald MW, Cramer Bornemann MA, Schenck CH. State dissociation, human behavior, and consciousness. Curr Top Med Chem. 2011;11:2392–2402. doi: 10.2174/156802611797470277. [DOI] [PubMed] [Google Scholar]
  • [15].French KA, Chang J, Reynolds S, Gonzalez R, Kristan WB, 3rd, Kristan WB., Jr Development of swimming in the medicinal leech, the gradual acquisition of a behavior. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005;191:813–821. doi: 10.1007/s00359-005-0003-7. [DOI] [PubMed] [Google Scholar]
  • [16].Reynolds SA, French KA, Baader A, Kristan WB., Jr Development of spontaneous and evoked behaviors in the medicinal leech. J Comp Neurol. 1998;402:168–180. doi: 10.1002/(SICI)1096-9861(19981214)402:2<168::AID-CNE3>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]
  • [17].Zega G, Thorndyke MC, Brown ER. Development of swimming behaviour in the larva of the ascidian Ciona intestinalis. J Exp Biol. 2006;209:3405–3412. doi: 10.1242/jeb.02421. [DOI] [PubMed] [Google Scholar]
  • [18].Ohmori H, Sasaki S. Development of neuromuscular transmission in a larval tunicate. J Physiol. 1977;269:221–254. doi: 10.1113/jphysiol.1977.sp011900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [19].Corner M. Rhythmicity in the Early Swimming of Anuran Larvae. J Embryol Exp Morphol. 1964;12:665–671. [PubMed] [Google Scholar]
  • [20].Fenelon V, Le Feuvre Y, Bem T, Meyrand P. Maturation of rhythmic neural network: role of central modulatory inputs. J Physiol Paris. 2003;97:59–68. doi: 10.1016/j.jphysparis.2003.10.007. [DOI] [PubMed] [Google Scholar]
  • [21].Rehm KJ, Deeg KE, Marder E. Developmental regulation of neuromodulator function in the stomatogastric ganglion of the lobster, Homarus americanus. J Neurosci. 2008;28:9828–9839. doi: 10.1523/JNEUROSCI.2328-08.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [22].Richards KS, Miller WL, Marder E. Maturation of lobster stomatogastric ganglion rhythmic activity. J Neurophysiol. 1999;82:2006–2009. doi: 10.1152/jn.1999.82.4.2006. [DOI] [PubMed] [Google Scholar]
  • [23].O’Donovan MJ. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol. 1999;9:94–104. doi: 10.1016/S0959-4388(99)80012-9. [DOI] [PubMed] [Google Scholar]
  • [24].Swanson LW. Quest for the basic plan of nervous system circuitry. Brain Res Rev. 2007;55:356–372. doi: 10.1016/j.brainresrev.2006.12.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [25].Pereanu W, Spindler S, Im E, Buu N, Hartenstein V. The emergence of patterned movement during late embryogenesis of Drosophila. Dev Neurobiol. 2007;67:1669–1685. doi: 10.1002/dneu.20538. [DOI] [PubMed] [Google Scholar]
  • [26].Crisp S, Evers JF, Fiala A, Bate M. The development of motor coordination in Drosophila embryos. Development. 2008;135:3707–3717. doi: 10.1242/dev.026773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [27].van Swinderen B, Nitz DA, Greenspan RJ. Uncoupling of brain activity from movement defines arousal states in Drosophila. Curr Biol. 2004;14:81–87. [PubMed] [Google Scholar]
  • [28].Eban-Rothschild AD, Bloch G. Differences in the sleep architecture of forager and young honeybees (Apis mellifera) J Exp Biol. 2008;211:2408–2416. doi: 10.1242/jeb.016915. [DOI] [PubMed] [Google Scholar]
  • [29].BBC Natural History Unit. Wild Film History. 1983. Aliens from inner space. [Google Scholar]
  • [30].Boletsky S, Boletsky MVv. Observations on the embryonic and early post-embryonic development of Rossia macrosoma (Mollusca, Cephalopoda) Helgolaender Wiss Meeresuntersuch. 1973;25:135–161. doi: 10.1007/BF01609965. [DOI] [Google Scholar]
  • [31].Tranter DJ, Augustine O. Observations on the life history of the blue-ringed octopus, Hapalochlaena maculosa. Marine Biol. 1973;18:115–128. doi: 10.1007/BF00348686. [DOI] [Google Scholar]
  • [32].von Boletzky S. Biology of early life stages in cephalopod molluscs. Adv Mar Biol. 2003;44:143–203. doi: 10.1016/S0065-2881(03)44003-0. [DOI] [PubMed] [Google Scholar]
  • [33].Meisel DV, Byrne RA, Mather JA, Kuba M. Behavioral sleep in octopus vulgaris. Vie et Milieu. 2011;61:185–190. [Google Scholar]
  • [34].Brown ER, Piscopo S, De Stefano R, Giuditta A. Brain and behavioural evidence for rest-activity cycles in octopus vulgaris. Behav Brain Res. 2006;172:355–359. doi: 10.1016/j.bbr.2006.05.009. [DOI] [PubMed] [Google Scholar]
  • [35].Frank MG, Waldrop RH, Dumoulin M, Aton S, Boal JG. A preliminary analysis of sleep-like states in the cuttlefish Sepia officinalis. PLoS One. 2012;7:e38125. doi: 10.1371/journal.pone.0038125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [36].Hanlon RT, Messenger JB. Adaptive coloration in young cuttlefish (Sepia offcinalis L.): the morphology and development of body patterns and their relation to behaviour. Phil Trans Roy Soc B (London) 1987;320:437–487. doi: 10.1098/rstb.1988.0087. [DOI] [Google Scholar]
  • [37].Siegel JM, Manger PR, Nienhuis R, Fahringer HM, Pettigrew JD. Monotremes and the evolution of rapid eye movement sleep. Philos Trans R Soc Lond B Biol Sci. 1998;353:1147–1157. doi: 10.1098/rstb.1998.0272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [38].Koizumi O, Mizumoto H, Sugiyama T, Bode HR. Nerve net formation in the primitive nervous system of Hydra—an overview. Neurosci Res Suppl. 1990;13:S165–170. doi: 10.1016/0921-8696(90)90046-6. [DOI] [PubMed] [Google Scholar]
  • [39].Tabak J, O’Donovan MJ, Rinzel J. Differential control of active and silent phases in relaxation models of neuronal rhythms. J Comput Neurosci. 2006;21:307–328. doi: 10.1007/s10827-006-8862-7. [DOI] [PubMed] [Google Scholar]
  • [40].Corner MA. Reciprocity of structure-function relations in developing neural networks: the odyssey of a self-organizing brain through research fads, fallacies and prospects. Prog Brain Res. 1994;102:3–31. doi: 10.1016/S0079-6123(08)60529-4. [DOI] [PubMed] [Google Scholar]
  • [41].Bosman L, Lodder JC, van ooyen A, Brussaard AB. Role of synaptic inhibition in spatiotemporal patterning of cortical activity. Prog Brain Res. 2005;147:201–204. doi: 10.1016/S0079-6123(04)47015-0. [DOI] [PubMed] [Google Scholar]
  • [42].Weiss PA. Deplantation of fragments of the nervous system in amphibians: central reorganization and the formation of nerves. J Exp Zool. 1950;113:397–461. doi: 10.1002/jez.1401130208. [DOI] [Google Scholar]

Articles from Neuroscience Bulletin are provided here courtesy of Springer

RESOURCES