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6 - The ontogeny and function(s) of REM sleep

from Section II - General biology

Published online by Cambridge University Press:  07 September 2011

By
Marcos G. Frank
Edited by
Birendra N. Mallick ,
S. R. Pandi-Perumal ,
Robert W. McCarley  and
Adrian R. Morrison
Marcos G. Frank
Affiliation:
University of Pennsylvania School of Medicine
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

In the decade immediately following the discovery of REM sleep (Aserinsky and Kleitman, 1953), scientists in the United States and in Europe made a second, striking observation (Jouvet-Mounier et al., 1970; Roffwarg et al., 1966; Valatx et al., 1964). In several mammalian species, including humans, REM sleep amounts were two to three times higher in infancy than in adulthood, and then declined dramatically across development. This basic ontogenetic pattern has now been observed in a wide variety of mammals (Davis et al., 1999; Thurber et al., 2008; Walker and Berger, 1980) and suggests that REM sleep may play a crucial role in brain development. In this chapter, I review the evidence in support of this general hypothesis. I begin with an overview of several landmark events in the ontogenesis of sleep and sleep regulation to provide context to the more function-based discussions that follow. I then discuss the results of several studies that provide indirect or suggestive evidence of a role for REM sleep in general brain maturation. This is followed by a review of findings in the developing visual system that more specifically address a possible role for REM sleep in brain development and plasticity.

Type
Chapter
Information
Rapid Eye Movement Sleep
Regulation and Function
 , pp. 49 - 57
Publisher: Cambridge University Press
Print publication year: 2011

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References

Adlard, B. P. F. & Smart, J. L. (1974) Some aspects of the behavior of young and adult rats treated with p-chlorophenylalanine in infancy. Dev Psychobiol 7: –44.CrossRefGoogle Scholar
Aserinsky, E. & Kleitman, N. (1953) Regularly occurring periods of eye motility and concomitant phenomena during sleep. Science 118: –4.CrossRefGoogle ScholarPubMed
Aton, S. J., Seibt, J., Dumoulin, M. . (2009) Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 61: –66.CrossRefGoogle ScholarPubMed
Benington, J. H. & Frank, M. G. (2003) Cellular and molecular connections between sleep and synaptic plasticity. Prog Neurobiol 69: –101.CrossRefGoogle ScholarPubMed
Blumberg, M. S., Karlsson, K. A., Seelke, A. M. H. . (2005) The ontogeny of mammalian sleep: a response to Frank and Heller (2003). J Sleep Res 14: –8.CrossRefGoogle Scholar
Blumberg, M. S. & Lucas, D. E. (1994) Dual mechanisms of twitching during sleep in neonatal rats. Behav Neurosci 108: –202.CrossRefGoogle ScholarPubMed
Blumberg, M. S., Middlemis-Brown, J. E. & Johnson, E. D. (2004) Sleep homeostasis in infant rats. Behav Neurosci 118: –61.CrossRefGoogle ScholarPubMed
Bowe-Anders, C., Adrien, J. & Roffwarg, H. P. (1974) Ontogenesis of ponto-geniculo-occipital activity in the lateral geniculate nucleus of the kitten. Exp Neurology 43: –60.CrossRefGoogle ScholarPubMed
Caillard, O., Moreno, H., Schwaller, B. . (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. PNAS 97: –7.CrossRefGoogle ScholarPubMed
Chase, M. H. (1971) Brain stem somatic reflex activity in neonatal kittens during sleep and wakefulness. Physiol Behav 7: –72.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
Coyle, J. T. & Yamamura, H. I. (1976) Neurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain. Brain Res 118: –40.CrossRefGoogle ScholarPubMed
Daniels, J. D., Pettigrew, J. D. & Norman, J. L. (1978) Development of single-neuron responses in kitten’s lateral geniculate nucleus. J Neurophysiol 41: –93.CrossRefGoogle ScholarPubMed
Davenne, D. & Adrien, J. (1984) Suppression of PGO waves in the kitten: anatomical effects on the lateral geniculate nucleus. Neurosci Lett 45: –8.CrossRefGoogle ScholarPubMed
Davenne, D., Fregnac, Y., Imbert, M. . (1989) Lesion of the PGO pathways in the kitten. II. Impairment of physiological and morphological maturation of the lateral geniculate nucleus. Brain Res 485: –77.CrossRefGoogle ScholarPubMed
Davis, F. C., Frank, M. G. & Heller, H. C. (1999) Ontogeny of sleep and circadian rhythms. In Regulation of Sleep and Circadian Rhythms, eds. Zee, P. C & Turek, F W. New York: Marcel Dekker, Inc., pp. 19–80.Google Scholar
Dwyer, S. M. & Rosenwasser, A. M. (1998) Neonatal clomipramine treatment, alcohol intake and circadian rhythms in rats. Psychopharmacol 138: –83.CrossRefGoogle ScholarPubMed
Endo, T., Schwierin, B., Borbely, A. A. . (1997) Selective and total sleep deprivation: effect on the sleep EEG in the rat. Psychiatry Res 66: –110.CrossRefGoogle ScholarPubMed
Farabollini, F., Hole, D. R. & Wilson, C. A. (1988) Behavioral effects in adulthood of serotonin depletion by p-chorophenylalanine given neonatally to male rats. Int J Neurosci 41: –99.CrossRefGoogle ScholarPubMed
Feng, P. (2001) Postnatal REM sleep deprivation and depression: new findings and hypothesis. Actas de Fisiologica 7: .Google Scholar
Feng, P., Ma, Y. & Vogel, G. W. (2001) Ontogeny of REM rebound in postnatal rats. Sleep 24: –53.CrossRefGoogle ScholarPubMed
File, S. E. & Tucker, J. C. (1983) Neonatal clomipramine treatment in the rat does not affect social, sexual and exploratory behaviors in adulthood. Neurobehav Toxicol Teratol 5: –8.Google Scholar
Frank, M. G. & Heller, H. C. (1997a) Development of REM and slow wave sleep in the rat. Am J Physiol 272: –9.Google ScholarPubMed
Frank, M. G. & Heller, H. C. (1997b) Neonatal treatments with the serotonin uptake inhibitors clomipramine and zimelidine, but not the noradrenaline uptake inhibitor desipramine, disrupt sleep patterns in adult rats. Brain Res 768: –93.CrossRefGoogle Scholar
Frank, M. G. & Heller, H. C. (2003) The ontogeny of mammalian sleep: a reappraisal of alternative hypotheses. J Sleep Res 12: –34.CrossRefGoogle ScholarPubMed
Frank, M. G. & Heller, H. (2005) Unresolved issues in sleep ontogeny: a response to Blumberg . J Sleep Res 14: –101.CrossRefGoogle ScholarPubMed
Frank, M. G., Issa, N. P. & Stryker, M. P. (2001) Sleep enhances plasticity in the developing visual cortex. Neuron 30: –87.CrossRefGoogle ScholarPubMed
Frank, M. G., Morrissette, R. & Heller, H. C. (1998) Effects of sleep deprivation in neonatal rats. Am J Physiol 275: –57.Google ScholarPubMed
Garcia-Rill, E., Charlesworth, A., Heister, D. . (2008) The developmental decrease in REM sleep: the role of transmitters and electrical coupling. Sleep 31: –90.CrossRefGoogle ScholarPubMed
Gramsbergen, A. (1976) The development of the EEG in the rat. Dev Psychobiol 9: –15.CrossRefGoogle ScholarPubMed
Henderson, M. G., McConnaughey, M. M. & McMillen, B. A. (1991) Long-term consequences of prenatal exposure to cocaine or related drugs: effects on rat brain monoaminergic receptors. Brain Res Bull 26: –5.CrossRefGoogle ScholarPubMed
Hilakivi, L. A. & Hilakivi, I. (1987) Increased adult behavioral ‘despair’ in rats neonatally exposed to desipramine or zimeldine: an animal model of depression?Pharmacol Biochem Behav 28: –9.CrossRefGoogle ScholarPubMed
Hilakivi, L. A., Hilakivi, I., Ahtee, L. . (1987) Effect of neonatal nomifensine exposure on adult behavior and brain monoamines in rats. J Neural Transm 70: –116.CrossRefGoogle ScholarPubMed
Hilakivi, L. & Sinclair, J. D. (1986) Effect of neonatal clomipramine treatment on adult alcohol drinking in the AA and ANA rat lines. Pharmacol Biochem Behav 24: –5.CrossRefGoogle ScholarPubMed
Hogan, D., Roffwarg, H. P. & Shaffery, J. P. (2001) The effects of 1 week of REM sleep deprivation on parvalbumin and calbindin immunoreactive neurons in central visual pathways of kittens. J Sleep Res 10: –96.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. A. & Blumberg, M. S. (2002) The union of the state: myoclonic twitching is coupled with nuchal muscle atonia in infant rats. Behav Neurosci 116: –17.CrossRefGoogle ScholarPubMed
Karlsson, K. A. & Blumberg, M. S. (2003) Hippocampal theta in the newborn rat is revealed under conditions that promote REM sleep. J Neurosci 23: –18.CrossRefGoogle ScholarPubMed
Karlsson, K. A. & Blumberg, M. S. (2005) Active medullary control of atonia in week-old rats. Neuroscience 130: –83.CrossRefGoogle ScholarPubMed
Karlsson, K., Elig, A., Gall, A. J. . (2005a) The neural substrates of infant sleep in rats. PLoS Biology 3: .CrossRefGoogle ScholarPubMed
Karlsson, K. A., Gall, A. J., Mohns, E. J. . (2005b) The neural substrates of infant sleep in rats. PLoS Biol 3: .CrossRefGoogle ScholarPubMed
Karlsson, K. A., Kreider, J. C. & Blumberg, M. S. (2004) Hypothalamic contribution to sleep–wake cycle development. Neuroscience 123: –82.CrossRefGoogle ScholarPubMed
Kirkwood, A., Lee, H. K. & Bear, M. F. (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex. Nature 375: –31.CrossRefGoogle ScholarPubMed
Klemfuss, H. & Gillin, C. J. (1997) Neonatal scopolamine or antidepressant treatment: effect on development of hamster circadian rhythms. Pharmacol Biochem Behav 59: –73.Google Scholar
Lee, W., Nicklaus, K. J., Manning, D. R. . (1990) Ontogeny of cortical muscarinic receptor subtypes and muscarinic receptor-mediated responses in rat. J Pharmacol Exp Ther 252: –490.Google ScholarPubMed
Leinekugel, X., Khazipov, R., Cannon, R. . (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296: –52.CrossRefGoogle ScholarPubMed
Lopez, J., Roffwarg, H. P., Dreher, A. . (2008) Rapid eye movement sleep deprivation decreases long-term potentiation stability and affects some glutamatergic signaling proteins during hippocampal development. Neuroscience 153: –53.CrossRefGoogle ScholarPubMed
Marks, G. A., Roffwarg, H. P. & Shaffery, J. P. (1999) Neuronal activity in the lateral geniculate nucleus associated with ponto-geniculate-occipital waves lacks lamina specificity. Brain Res 815: –8.CrossRefGoogle Scholar
Marks, G. A., Shaffery, J. P., Oksenberg, A. . (1995) A functional role for REM sleep in brain maturation. Behav Brain Res 69: –11.CrossRefGoogle ScholarPubMed
McGinty, R. J., Stevenson, M., Hoppenbrouwers, T. . (1977) Polygraphic studies of kitten development: sleep state patterns. Dev Psychobiol 10: –69.CrossRefGoogle ScholarPubMed
Mirmiran, M. & Maas, Y. G. H. (1999) The function of fetal/neonatal REM sleep. In Rapid Eye Movement Sleep, eds. Mallick, B. N. & Inoue, S.. New Delhi: Narosa Publishing House, pp. 326–35.Google Scholar
Mirmiran, M., Scholtens, J., van de Poll, N. E. . (1983a) Effects of experimental suppression of active (REM) sleep during early development upon adult brain and behavior in the rat. Brain Res 283: –86.Google ScholarPubMed
Mirmiran, M., Uylings, H. B. & Corner, M. A. (1983b) Pharmacological suppression of REM sleep prior to weaning counteracts the effectiveness of subsequent environmental enrichment on cortical growth in rats. Brain Res 283: –5.Google ScholarPubMed
Mirmiran, M., van de Poll, N. E., Corner, M. A. . (1981) Suppression of active sleep by chronic treatment with chlorimipramine during early postnatal development: effects upon adult sleep and behavior in the rat. Brain Res 204: –46.CrossRefGoogle ScholarPubMed
Mirmiran, M., van den Dungen, H. & Uylings, H. B. (1982) Sleep patterns during rearing under different environmental conditions in juvenile rats. Brain Res 233: –98.CrossRefGoogle ScholarPubMed
Morrissey, M. J., Duntley, S. P., Anch, A. M. . (2004) Active sleep and its role in the prevention of apoptosis in the developing brain. Med Hypotheses 62: –9.CrossRefGoogle Scholar
Ninomiya, Y., Koyama, Y. & Kayama, Y. (2001) Postnatal development of choline acetyltransferase activity in the rat laterodorsal tegmental nucleus. Neurosci Lett 308: –40.CrossRefGoogle ScholarPubMed
Oksenberg, A., Shaffery, J. P., Marks, G. A. . (1996) Rapid eye movement sleep deprivation in kittens amplifies LGN cell-size disparity induced by monocular deprivation. Dev Brain Res 97: –61.CrossRefGoogle ScholarPubMed
Prathiba, J., Kumar, K. B. & Karanth, K. S. (1998) Hyperactivity of hypothalamic pituitary axis in neonatal clomipramine model of depression. J Neural Transm 105: –9.CrossRefGoogle Scholar
Prathiba, J., Kumar, K. B. & Karanth, K. S. (2000) Effects of REM sleep deprivation on cholinergic receptor sensitivity and passive avoidance behavior in clomipramine model of depression. Brain Res 867: –5.CrossRefGoogle Scholar
Roffwarg, H. P., Muzio, J. N. & Dement, W. C. (1966) Ontogenetic development of the human sleep–dream cycle. Science 152: –19.CrossRefGoogle ScholarPubMed
Roffwarg, H. P. & Shaffery, J. P. (1999) The ontogenetic hypothesis of REM sleep function: its history, current status and prospects for confirmation. Sleep Research Online 2: –15.Google Scholar
Seibt, J., Aton, S., Jha, S. K. . (2008) The non-benzodiazepine hypnotic Zolpidem impairs sleep-dependent cortical plasticity. Sleep 31: –92.Google ScholarPubMed
Sengpiel, F., Godecke, I., Stawinski, P. . (1998) Intrinsic and environmental factors in the development of functional maps in cat visual cortex. Neuropharmacology 37: –21.CrossRefGoogle ScholarPubMed
Shaffery, J. P., Oksenberg, A., Marks, G. A. . (1998) REM sleep deprivation in monocularly occluded kittens reduces the size of cells in LGN monocular segment. Sleep 21: –945.CrossRefGoogle ScholarPubMed
Shaffery, J. P., Roffwarg, H. P., Speciale, S. G. . (1999) Ponto-geniculo-occipital wave suppression amplifies lateral geniculate nuclues cell-size changes in monocularly deprived kittens. Dev Brain Res 114: –19.CrossRefGoogle Scholar
Shaffery, J. P., Sinton, C. M., Bissette, G. . (2002) Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience 110: –43.CrossRefGoogle ScholarPubMed
Shatz, C. J. (1996) Emergence of order in visual system development. PNAS 93: –8.CrossRefGoogle ScholarPubMed
Singer, W. (1979) Neuronal mechanisms in experience dependent modification of visual cortex function. In Development and Chemical Sensitivity of Neurons, vol. 31. eds. Cuenod, M., Kreutzberg, G. W. & Bloom, F. E.. Amsterdam: Elsevier/North-Holland Biomedical Press, pp. 457–77.Google Scholar
Sur, M. & Leamey, C. A. (2001) Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2: –62.CrossRefGoogle ScholarPubMed
Thurber, A., Jha, S. K., Coleman, T. . (2008) A preliminary study of sleep ontogenesis in the ferret (Mustela putorius furo)Behav Brain Res 189: –51.CrossRefGoogle Scholar
Valatx, J. L., Jouvet, D. & Jouvet, M. (1964) Evolution Electroencephalographique des differents etats de sommeil chez le chaton. Electroencephalogr Clin Neurophysiol 17: –33.Google Scholar
Van Someren, E. J., Mirmiran, M., Bos, N. P. . (1990) Quantitative analysis of eye movements during REM-sleep in developing rats. Dev Psychobiol 23: –61.CrossRefGoogle ScholarPubMed
Vogel, G., Neill, D., Hagler, M. . (1990a) A new animal model of endogenous depression: a summary of present findings. Neurosci Biobehav Rev 14: –91.Google ScholarPubMed
Vogel, G., Neill, D., Kors, D. . (1990b) REM sleep abnormalities in a new animal model of endogenous depression. Neurosci Biobehav Rev 14: –83.Google Scholar
Walker, J. M. & Berger, R J. (1980) The ontogenesis of sleep states, thermogenesis, and thermoregulation in the Virginia opossum. Dev Psychobiol 13: –54.CrossRefGoogle ScholarPubMed
Williams, A. L. & Jeffery, G. (2001) Growth dynamics of the developing lateral geniculate nucleus. J Comp Neurol 430: –42.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Wilson, C. A., Pearson, J. R., Hunter, A. J. . (1986) The effect of neonatal manipulation of hypothalamic serotonin levels on sexual activity in the adult rat. Pharmacol Biochem Behav 24: –83.CrossRefGoogle ScholarPubMed
Yannielli, P. C., Cutrera, R. A., Cardinali, D. P. . (1998) Neonatal clomipramine treatment of Syrian hamsters: effect on the circadian system. Eur J Pharmacol 349: –50.CrossRefGoogle ScholarPubMed

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