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14 - Phenomenology and function of myoclonic twitching in developing rats

from Section III - Neuronal regulation

Published online by Cambridge University Press:  07 September 2011

Mark S. Blumberg
Affiliation:
The University of Iowa
Birendra N. Mallick
Affiliation:
Jawaharlal Nehru University
S. R. Pandi-Perumal
Affiliation:
Somnogen Canada Inc, Toronto
Robert W. McCarley
Affiliation:
Harvard University, Massachusetts
Adrian R. Morrison
Affiliation:
University of Pennsylvania
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Summary

Summary

The development of adult sleep is a complex process comprising the emergence and coalescence of sleep components and the consolidation of sleep into progressively longer bouts. Achieving adequate descriptions of infant sleep and its development requires the use of methods that are scaled to the structural and temporal properties of sleep at early ages. This chapter reviews work demonstrating in infant rats how measures of sleep–wake behavior (e.g., myoclonic twitching during REM sleep, high-amplitude movements during wakefulness) coupled with electromyography of skeletal muscle (e.g., nuchal muscle) reveal sleep–wake cycles that are highly structured in space and time. Consideration of other measures – for example, extraocular muscle and cortical activity – provides further support for the notion that adult sleep is constructed in an orderly fashion through the addition of components (e.g., delta waves) and alterations in the statistical structure of sleep and wake bouts. Neurophysiological recordings and lesions in the medulla, mesopontine region, hypothalamus, and forebrain indicate that the brain critically contributes to sleep–wake processes as early as the first postnatal week. Finally, sensory feedback produced by twitches of the limbs is transmitted to the contralateral somatosensory cortex (where cortical activity is also modulated by the corpus callosum) before being transmitted to the hippocampus. Thus, we are moving closer to a full description of sleep–wake processes in the newborn as well as an understanding of the contributions of sleep-related spontaneous activity to the self-organization of the nervous system.

Type
Chapter
Information
Rapid Eye Movement Sleep
Regulation and Function
, pp. 130 - 139
Publisher: Cambridge University Press
Print publication year: 2011

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References

Adrien, J. & Lanfumey, L. (1984) Neuronal activity of the developing raphe dorsalis: its relation with the states of vigilance. Exp Brain Res, Suppl. 8: –78.Google Scholar
Blumberg, M. S., Karlsson, K. Æ., Seelke, A. M. H. & Mohns, E. J. (2005). The ontogeny of mammalian sleep: A response to Frank and Heller (2003). J Sleep Res 14: –101.CrossRefGoogle Scholar
Blumberg, M. S. & Lucas, D. E. (1996) A developmental and component analysis of active sleep. Dev Psychobiol 29: –22.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Blumberg, M. S. & Seelke, A. M. (2010) The form and function of infant sleep: from muscle to neocortex. In The Oxford Handbook of Developmental Behavioral Neuroscience, eds. Blumberg, M. S., , J. H. Freeman, & Robinson, S. R.. New York: Oxford University Press, pp. 391–423.Google Scholar
Burgess, C., Lai, D., Siegel, J. & Peever, J. (2008) An endogenous glutamatergic drive onto somatic motoneurons contributes to the stereotypical pattern of muscle tone across the sleep-wake cycle. J Neurosci 28: –60.CrossRefGoogle ScholarPubMed
Chase, M. H. & Morales, F. R. (1983) Subthreshold excitatory activity and motoneuron discharge during REM periods of active sleep. Science 221: –8.CrossRefGoogle ScholarPubMed
Corner, M. A. (1977) Sleep and the beginnings of behavior in the animal kingdom: studies of ultradian motility cycles in early life. Prog Neurobiol 8: –95.CrossRefGoogle ScholarPubMed
Corner, M. A., Mirmiran, M., Bour, H. L. . (1980) Does rapid-eye-movement sleep play a role in brain development?Prog Brain Res 53: –56.CrossRefGoogle ScholarPubMed
Frank, M. G. & Heller, H. C. (2003) The ontogeny of mammalian sleep: a reappraisal of alternative hypotheses. J Sleep Res 12: –34.CrossRefGoogle ScholarPubMed
Gramsbergen, A. (1976) The development of the EEG in the rat. Dev Psychobiol 9: –15.CrossRefGoogle ScholarPubMed
Gramsbergen, A., Schwartze, P. & Prechtl, H. F. R. (1970) The postnatal development of behavioral states in the rat. Dev Psychobiol 3: –80.CrossRefGoogle ScholarPubMed
Hamburger, V. (1973) Anatomical and physiological bases of embryonic motility in birds and mammals. In Studies on the Development of Behavior and the Nervous System, Behavioral Embryology, Volume 1. ed. Gottlieb, G.. New York: Academic Press, pp. 51–76.Google Scholar
Hanganu, I. L., Ben-Ari, Y. & Khazipov, R. (2006) Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci 26: –36.CrossRefGoogle ScholarPubMed
Hanganu, I. L., Staiger, J. F., Ben-Ari, Y. & Khazipov, R. (2007) Cholinergic modulation of spindle bursts in the neonatal rat visual cortex in vivo. J Neurosci 27: –705.CrossRefGoogle ScholarPubMed
Hendricks, J. C., Sehgal, A. & Pack, A. (2000) The need for a simple animal model to understand sleep. Prog Neurobiol 61: –51.CrossRefGoogle ScholarPubMed
Innocenti, G. M. & Price, D. J. (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6: –65.CrossRefGoogle ScholarPubMed
Jouvet-Mounier, D., Astic, L. & Lacote, D. (1970) Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol 2: –39.Google ScholarPubMed
Karlsson, K. Æ. & Blumberg, M. S. (2005) Active medullary control of atonia in week-old rats. Neuroscience 130: –83.CrossRefGoogle ScholarPubMed
Karlsson, K. Æ., Gall, A. J., Mohns, E. J., Seelke, A. M. H. & Blumberg, M. S. (2005) The neural substrates of infant sleep in rats. PLoS Biol 3: –901.CrossRefGoogle ScholarPubMed
Karlsson, K. Æ., Mohns, E. J., Vianna di Prisco, G. & Blumberg, M. S. (2006) On the co-occurrence of startles and hippocampal sharp waves in newborn rats. Hippocampus 16: –65.CrossRefGoogle ScholarPubMed
Khazipov, R., Sirota, A., Leinekugel, X., . (2004) Early motor activity drives spindle-bursts in the developing somatosensory cortex. Nature 432: –61.CrossRefGoogle ScholarPubMed
Kilgard, M. P. & Merzenich, M. M. (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279: –18.CrossRefGoogle ScholarPubMed
Kreider, J. C. & Blumberg, M. S. (2000) Mesopontine contribution to the expression of active ‘twitch’ sleep in decerebrate week-old rats. Brain Res 872: –59.CrossRefGoogle ScholarPubMed
Leinekugel, X., Khazipov, R., Cannon, R. . (2002) Correlated bursts of activity in neonatal hippocampus in vivo. Science 296: –52.CrossRefGoogle ScholarPubMed
Marcano-Reik, A. J. & Blumberg, M. S. (2008) The corpus callosum modulates spindle-burst activity within homotopic regions of somatosensory cortex in newborn rats. Eur J Neurosci 28: –66.CrossRefGoogle ScholarPubMed
Minlebaev, M., Ben-Ari, Y. & Khazipov, R. (2007) Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol 97: –700.CrossRefGoogle ScholarPubMed
Mirmiran, M. (1995) The function of fetal/neonatal rapid eye movement sleep. Behav Brain Res 69: –22.CrossRefGoogle ScholarPubMed
Mohns, E. J. & Blumberg, M. S. (2008) Synchronous bursts of neuronal activity in the developing hippocampus: modulation by active sleep and association with emerging gamma and theta rhythms. J Neurosci 28: –44.CrossRefGoogle ScholarPubMed
Mohns, E. J. & Blumberg, M. S. (2010) Neocortical activation of the hippocampus during sleep in newborn rats. J Neurosci 30(9): –49.CrossRefGoogle Scholar
Morrison, A. R. (1988) Paradoxical sleep without atonia. Arch Ital Biol 126: –89.Google ScholarPubMed
Petersson, P., Waldenström, A., Fåhraeus, C. & Schouenborg, J. (2003) Spontaneous muscle twitches during sleep guide spinal self-organization. Nature 424: –5.CrossRefGoogle ScholarPubMed
Rechtschaffen, A. & Kales, A. eds. (1968) A Manual of Standardized Terminology, Techniques, and Scoring System for Sleep Stages of Human Subjects. Los Angeles: UCLA Brain Information Service/Brain Research Institute.Google Scholar
Robinson, S. R., Blumberg, M. S., Lane, M. S. & Kreber, L. A. (2000) Spontaneous motor activity in fetal and infant rats is organized into discrete multilimb bouts. Behav Neurosci 14: –36.Google Scholar
Roffwarg, H. P., Muzio, J. N. & Dement, W. C. (1966) Ontogenetic development of the human sleep–dream cycle. Science 152: –19.CrossRefGoogle ScholarPubMed
Schouenborg, J. (2010) Role of spontaneous movements in imprinting an action-based body representation in the spinal cord. In The Oxford Handbook of Developmental Behavioral Neuroscience, eds. Blumberg, M. S., Freeman, J. H. & Robinson, S. R.. New York: Oxford University Press, pp. 254–61.Google Scholar
Seelke, A. M. H. & Blumberg, M. S. (2008) The microstructure of active and quiet sleep as cortical delta activity emerges in infant rats. Sleep 31: –9.CrossRefGoogle ScholarPubMed
Seelke, A. M. H., Karlsson, K. Æ., Gall, A. J. & Blumberg, M. S. (2005) Extraocular muscle activity, rapid eye movements, and the development of active and quiet sleep. Eur J Neurosci 22: –20.CrossRefGoogle ScholarPubMed
Shaffery, J. P., Sinton, C. M., Bissette, G., Roffwarg, H. P. & Marks, G. A. (2002) Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience 110: –43.CrossRefGoogle ScholarPubMed
Siegel, J. M. (2005) REM sleep. In: Principles and Practice of Sleep Medicine. eds. Kryger, M. H., , T. Roth, & Dement, W. C.. Philadelphia: W. B. Saunders Company, pp. 120–35.Google Scholar
Van Someren, E. J. W., Mirmiran, M., Bos, N. P. A. . (1990) Quantitative analysis of eye movements during REM-sleep in developing rats. Dev Psychobiol 23: –61.CrossRefGoogle ScholarPubMed
Wong, R. O. (1999) Retinal waves and visual system development. Ann Rev Neurosci 22: –47.CrossRefGoogle ScholarPubMed

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