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

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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.

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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.

    Article  PubMed  Google Scholar 

  2. Fuller PM, Saper CB, Lu J. The pontine REM switch: past and present. J Physiol 2007, 584: 735–741.

    Article  PubMed  CAS  Google Scholar 

  3. Jouvet M. Paradoxical Sleep—a Study of its Nature and Mechanisms. Prog Brain Res 1965, 18: 20–62.

    Article  PubMed  CAS  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.

    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  CAS  Google Scholar 

  7. Siegel JM. Do all animals sleep? Trends Neurosci 2008, 31: 208–213.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  9. Lesku JA, Martinez-Gonzalez D, Rattenborg NC. Sleep and sleep states: phylogeny and ontogeny. in: Squire LR (ed.), Encyclopedia of Neuroscience. oxford: Academic Press, 2009: 963–971

    Google Scholar 

  10. Corner M. Spontaneous motor rhythms in early life3—phenomenological and neurophysiological aspects. Prog Brain Res 1978, 48: 349–366.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  14. Mahowald MW, Cramer Bornemann MA, Schenck CH. State dissociation, human behavior, and consciousness. Curr Top Med Chem 2011, 11: 2392–2402.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  PubMed  Google Scholar 

  18. Ohmori H, Sasaki S. Development of neuromuscular transmission in a larval tunicate. J Physiol 1977, 269: 221–254.

    PubMed  CAS  Google Scholar 

  19. Corner M. Rhythmicity in the Early Swimming of Anuran Larvae. J Embryol Exp Morphol 1964, 12: 665–671.

    PubMed  CAS  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.

    Article  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.

    Article  PubMed  CAS  Google Scholar 

  22. Richards KS, Miller WL, Marder E. Maturation of lobster stomatogastric ganglion rhythmic activity. J Neurophysiol 1999, 82: 2006–2009.

    PubMed  CAS  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.

    Article  PubMed  Google Scholar 

  24. Swanson LW. Quest for the basic plan of nervous system circuitry. Brain Res Rev 2007, 55: 356–372.

    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.

    Article  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.

    Article  PubMed  CAS  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.

    Article  PubMed  Google Scholar 

  29. BBC Natural History Unit. Aliens from inner space. Wild Film History 1983 [video].

    Google Scholar 

  30. Boletsky Sv, Boletsky MVv. Observations on the embryonic and early post-embryonic development of Rossia macrosoma (Mollusca, Cephalopoda). Helgolaender Wiss Meeresuntersuch 1973, 25: 135–161.

    Article  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.

    Article  Google Scholar 

  32. von Boletzky S. Biology of early life stages in cephalopod molluscs. Adv Mar Biol 2003, 44: 143–203.

    Article  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.

    Article  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.

    Article  PubMed  CAS  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.

    Article  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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.

    Article  Google Scholar 

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Correspondence to Michael A. Corner.

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Corner, M.A. Call it sleep — what animals without backbones can tell us about the phylogeny of intrinsically generated neuromotor rhythms during early development. Neurosci. Bull. 29, 373–380 (2013). https://doi.org/10.1007/s12264-013-1313-3

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