Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-8bljj Total loading time: 0 Render date: 2024-06-29T05:23:37.543Z Has data issue: false hasContentIssue false

29 - Neuronal models of REM-sleep control: evolving concepts

from Section IV - Neuroanatomy and neurochemistry

Published online by Cambridge University Press:  07 September 2011

James T. McKenna
Affiliation:
Harvard Medical School
Lichao Chen
Affiliation:
Harvard Medical School
Robert W. McCarley
Affiliation:
Harvard Medical School
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
Get access

Summary

Summary

In this chapter, we will review the recent developments relevant to understanding the neural systems that regulate REM sleep. We will review the initial discovery of REM sleep, followed by a brief description of the polysomnographic characterization of REM sleep. Our discussion will continue with a review of the principal brain-stem executive neurons responsible for REM generation. Pontine reticular formation neurons are involved in the expression of the majority of REM-sleep phenomena, including low-amplitude/high-frequency cortical EEG, the hippocampal theta rhythm, PGO waves/P-waves, and muscle atonia. Cholinergic brain-stem neurons are REM-on, promoting REM sleep; and serotonergic and noradrenergic brain-stem neurons are REM-off, suppressing REM sleep. GABAergic and glutamatergic mechanisms are also integral to REM sleep control. We will also survey the prominent nuclei of the midbrain and forebrain that promote, but do not generate, REM-sleep expression. The conclusion of this chapter will provide a review of three prominent models of REM-sleep regulation: the reciprocal-interaction model; the REM sleep “flip-flop” circuit model; and the revised model of paradoxical (REM) sleep control proposed by Luppi and colleagues.

Type
Chapter
Information
Rapid Eye Movement Sleep
Regulation and Function
, pp. 285 - 300
Publisher: Cambridge University Press
Print publication year: 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alam, N. M, Kumari, S. & Mallick, B. N. (1993) Role of GABA in acetylcholine-induced locus coeruleus mediated increases in REM. Sleep Res 22: .Google Scholar
Aserinsky, E. & Kleitman, N. (1953) Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118: –4.CrossRefGoogle ScholarPubMed
Aston-Jones, G., Zhu, Y. & Card, J. P. (2004) Numerous GABAergic afferents to locus ceruleus in the pericerulear dendritic zone: possible interneuronal pool. J Neurosci 24: –21.CrossRefGoogle ScholarPubMed
Boissard, R., Fort, P., Gervasoni, D., Barbagli, B. & Luppi, P. H. (2003) Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur J Neurosci 18: –39.CrossRefGoogle ScholarPubMed
Boissard, R., Gervasoni, D., Schmidt, M. H. . (2002) The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur J Neurosci 16: –73.CrossRefGoogle ScholarPubMed
Brown, R. E. (2003) Involvement of hypocretins/orexins in sleep disorders and narcolepsy. Drug News Perspect 16: –9.CrossRefGoogle ScholarPubMed
Brown, R. E., McKenna, J. T., Winston, S. . (2008) Characterization of GABAergic neurons in rapid-eye-movement sleep controlling regions of the brainstem reticular formation in GAD67-green fluorescent protein knock-in mice. Eur J Neurosci 27: –63.CrossRefGoogle ScholarPubMed
Brown, R. E., Sergeeva, O. A., Eriksson, K. S. & Haas, H. L. (2002) Convergent excitation of dorsal raphe serotonin neurons by multiple arousal systems (orexin/hypocretin, histamine and noradrenaline). J Neurosci 22: –9.CrossRefGoogle Scholar
Brown, R. E., Winston, S., Basheer, R., Thakkar, M. M. & McCarley, R. W. (2006) Electrophysiological characterization of neurons in the dorsolateral pontine rapid-eye-movement sleep induction zone of the rat: intrinsic membrane properties and responses to carbachol and orexins. Neuroscience 143: –55.CrossRefGoogle ScholarPubMed
Chase, M. H. & Morales, F. R. (1990) The atonia and myoclonia of active (REM) sleep. Ann Rev Psychol 41: –84.CrossRefGoogle ScholarPubMed
Chemelli, R. M., Willie, J. T., Sinton, C. M. . (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98: –51.CrossRefGoogle ScholarPubMed
Chen, L., Brown, R. E., McKenna, J. T. & McCarley, R. W. (2009) Animal models of narcolepsy. CNS Neurol Disord Drug Targets 8: –308.CrossRefGoogle ScholarPubMed
Chen, L., Thakkar, M. M., Winston, S. . (2006) REM sleep changes in rats induced by siRNA-mediated orexin knockdown. Eur J Neurosci 24: –48.CrossRefGoogle ScholarPubMed
El Mansari, M., Sakai, K. & Jouvet, M. (1989) Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep–waking cycle in freely moving cats. Exp Brain Res 76: –29.CrossRefGoogle ScholarPubMed
Ennis, M. & Aston-Jones, G. (1989a) GABA-mediated inhibition of locus coeruleus from the dorsomedial rostral medulla. J Neurosci 9: –81.CrossRefGoogle ScholarPubMed
Ennis, M. & Aston-Jones, G. (1989b) Potent inhibitory input to locus coeruleus from the nucleus prepositus hypoglossi. Brain Res Bull 22: –803.CrossRefGoogle ScholarPubMed
Ford, B., Holmes, C. J., Mainville, L. & Jones, B. E. (1995) GABAergic neurons in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J Comp Neurol 363: –96.CrossRefGoogle ScholarPubMed
Fort, P., Bassetti, C. L. & Luppi, P. H. (2009) Alternating vigilance states: new insights regarding neuronal networks and mechanisms. Eur J Neurosci 29: –53.CrossRefGoogle ScholarPubMed
Gerber, U., Stevens, D. R., McCarley, R. W. & Greene, R. W. (1991) Muscarinic agonists activate an inwardly rectifying potassium conductance in medial pontine reticular formation neurons of the rat in vitro. J Neurosci 11: –7.CrossRefGoogle ScholarPubMed
Gervasoni, D., Darracq, L., Fort, P. . (1998) Electrophysiological evidence that noradrenergic neurons of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur J Neurosci 10: –70.CrossRefGoogle ScholarPubMed
Gervasoni, D., Peyron, C., Rampon, C., . (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20: –25.CrossRefGoogle ScholarPubMed
Hagan, J. J., Leslie, R. A., Patel, S. . (1999) Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci U S A 96: –16.CrossRefGoogle ScholarPubMed
Hassani, O. K., Lee, M. G. & Jones, B. E. (2009) Melanin-concentrating hormone neurons discharge in a reciprocal manner to orexin neurons across the sleep–wake cycle. Proc Natl Acad Sci U S A 106: –22.CrossRefGoogle Scholar
Hendricks, J. C., Morrison, A. R. & Mann, G. L. (1982) Different behaviors during paradoxical sleep without atonia depend on pontine lesion site. Brain Res 239: –105.CrossRefGoogle ScholarPubMed
Hobson, J. A., McCarley, R. W. & Wyzinski, P. W. (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189: –8.CrossRefGoogle ScholarPubMed
Horvath, T. L., Peyron, C., Diano, S. . (1999) Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J Comp Neurol 415: –59.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Ito, K., Yanagihara, M., Imon, H., Dauphin, L. & McCarley, R. W. (2002) Intracellular recordings of pontine medial gigantocellular tegmental field neurons in the naturally sleeping cat: behavioral state-related activity and soma size difference in order of recruitment. Neuroscience 114: –37.CrossRefGoogle ScholarPubMed
Jouvet, M. (1962) [Research on the neural structures and responsible mechanisms in different phases of physiological sleep.] Arch Ital Biol 100: –206.Google ScholarPubMed
Jouvet, M. (1994) Paradoxical sleep mechanisms. Sleep 17: –83.CrossRefGoogle ScholarPubMed
Jouvet, M., Jeannerod, M. & Delorme, F. (1965) [Organization of the system responsible for phase activity during paradoxal sleep]. C R Seances Soc Biol Fil 159: –604.Google ScholarPubMed
Jouvet, M., Michel, F. & Courjon, J. (1959a) [Electric activity of the rhinencephalon during sleep in cats.]. C R Seances Soc Biol Fil 153: –5.Google ScholarPubMed
Jouvet, M., Michel, F. & Courjon, J. (1959b) [On a stage of rapid cerebral electrical activity in the course of physiological sleep.]. C R Seances Soc Biol Fil 153: –8.Google ScholarPubMed
Jouvet, M., Michel, F. & Courjon, J. (1959c) [Recording and stimulation of the subcortical structures in the chronic decorticated animal.] Rev Neurol (Paris) 101: –6.Google ScholarPubMed
Kantor, S., Mochizuki, T., Janisiewicz, A. M. . (2009) Orexin neurons are necessary for the circadian control of REM sleep. Sleep 32: –34.CrossRefGoogle ScholarPubMed
Kaur, S., Panchal, M., Faisal, M. . (2004) Long term blocking of GABA-A receptor in locus coeruleus by bilateral microinfusion of picrotoxin reduced rapid eye movement sleep and increased brain Na-K ATPase activity in freely moving normally behaving rats. Behav Brain Res 151: –90.CrossRefGoogle ScholarPubMed
Kaur, S., Saxena, R. N. & Mallick, B. N. (2001) GABAergic neurons in prepositus hypoglossi regulate REM sleep by its action on locus coeruleus in freely moving rats. Synapse 42: –50.CrossRefGoogle ScholarPubMed
Kiyashchenko, L. I., Mileykovskiy, B. Y., Maidment, N. . (2002) Release of hypocretin (orexin) during waking and sleep states. J Neurosci 22: –6.CrossRefGoogle ScholarPubMed
Kovacs, K. J. (2008) Measurement of immediate-early gene activation- c-fos and beyond. J Neuroendocrinol 20: –72.CrossRefGoogle Scholar
Lee, M. G., Hassani, O. K. & Jones, B. E. (2005) Discharge of identified orexin/hypocretin neurons across the sleep–waking cycle. J Neurosci 25: –20.CrossRefGoogle ScholarPubMed
Lee, M. L., Swanson, B. E. & de la Iglesia, H. O. (2009) Circadian timing of REM sleep is coupled to an oscillator within the dorsomedial suprachiasmatic nucleus. Curr Biol 19: –52.CrossRefGoogle Scholar
Levine, E. S. & Jacobs, B. L. (1992) Neurochemical afferents controlling the activity of serotonergic neurons in the dorsal raphe nucleus: microiontophoretic studies in the awake cat. J Neurosci 12: –44.CrossRefGoogle ScholarPubMed
Li, X., Rainnie, D. G., McCarley, R. W. & Greene, R. W. (1998) Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18: –12.CrossRefGoogle ScholarPubMed
Lim, A. S., Lozano, A. M., Moro, E. . (2007) Characterization of REM-sleep associated ponto-geniculo-occipital waves in the human pons. Sleep 30: –7.CrossRefGoogle ScholarPubMed
Lin, L., Faraco, J., Li, R. . (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98: –76.CrossRefGoogle ScholarPubMed
Liu, R. J., van den Pol, A. N. & Aghajanian, G. K. (2002) Hypocretins (orexins) regulate serotonin neurons in the dorsal raphe nucleus by excitatory direct and inhibitory indirect actions. J Neurosci 22: –64.CrossRefGoogle ScholarPubMed
Lu, J., Bjorkum, A. A., Xu, M., . (2002) Selective activation of the extended ventrolateral preoptic nucleus during rapid eye movement sleep. J Neurosci 22: –76.CrossRefGoogle ScholarPubMed
Lu, J., Greco, M. A., Shiromani, P. & Saper, C. B. (2000) Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 20: –42.CrossRefGoogle ScholarPubMed
Lu, J., Jhou, T. C. & Saper, C. B. (2006a) Identification of wake–active dopaminergic neurons in the ventral periaqueductal gray matter. J Neurosci 26: –202.CrossRefGoogle ScholarPubMed
Lu, J., Sherman, D., Devor, M. & Saper, C. B. (2006b) A putative flip-flop switch for control of REM sleep. Nature 441: –94.CrossRefGoogle ScholarPubMed
Luppi, P. H., Gervasoni, D., Verret, L. . (2006) Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J Physiol (Paris) 100: –83.CrossRefGoogle ScholarPubMed
Mallick, B. N., Kaur, S. & Saxena, R. N. (2001) Interactions between cholinergic and GABAergic neurotransmitters in and around the locus coeruleus for the induction and maintenance of rapid eye movement sleep in rats. Neuroscience 104: –85.CrossRefGoogle ScholarPubMed
Mallick, B. N., Majumdar, S., Faisal, M. . (2002) Role of norepinephrine in the regulation of rapid eye movement sleep. J Biosci 27: –51.CrossRefGoogle ScholarPubMed
Mallick, B. N., Thankachan, S. & Islam, F. (1998) Differential responses of brain stem neurons during spontaneous and stimulation-induced desynchronization of the cortical EEG in freely moving cats. Sleep Res Online 1: –46.Google ScholarPubMed
Maloney, K. J., Mainville, L. & Jones, B. E. (1999) Differential c-Fos expression in cholinergic, monoaminergic, and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J Neurosci 19: –72.CrossRefGoogle ScholarPubMed
Maloney, K. J., Mainville, L. & Jones, B. E. (2000) c-Fos expression in GABAergic, serotonergic, and other neurons of the pontomedullary reticular formation and raphe after paradoxical sleep deprivation and recovery. J Neurosci 20: –79.CrossRefGoogle ScholarPubMed
McCarley, R. W. (2004) Mechanisms and models of REM sleep control. Arch Ital Biol 142: –67.Google ScholarPubMed
McCarley, R. W. (2007) Neurobiology of REM and NREM sleep. Sleep Med 8: –30.CrossRefGoogle ScholarPubMed
McCarley, R. W. & Hobson, J. A. (1975a) Discharge patterns of cat pontine brain stem neurons during desynchronized sleep. J Neurophysiol 38: –66.CrossRefGoogle ScholarPubMed
McCarley, R. W. & Hobson, J. A. (1975b) Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 189: –60.CrossRefGoogle ScholarPubMed
McCarley, R. W. & Massaquoi, S. G. (1986a) Further discussion of a model of the REM sleep oscillator. Am J Physiol 251: –6.Google ScholarPubMed
McCarley, R. W. & Massaquoi, S. G. (1986b) A limit cycle mathematical model of the REM sleep oscillator system. Am J Physiol 251: –29.Google ScholarPubMed
McCarley, R. W., Nelson, J. P. & Hobson, J. A. (1978) Ponto-geniculo-occipital (PGO) burst neurons: correlative evidence for neuronal generators of PGO waves. Science 201: –72.CrossRefGoogle ScholarPubMed
McGinty, D. & Szymusiak, R. (2001) Brain structures and mechanisms involved in the generation of NREM sleep: focus on the preoptic hypothalamus. Sleep Med Rev 5: –42.CrossRefGoogle ScholarPubMed
Merchant-Nancy, H., Vazquez, J., Garcia, F. & Drucker-Colin, R. (1995) Brain distribution of c-fos expression as a result of prolonged rapid eye movement (REM) sleep period duration. Brain Res 681: –22.CrossRefGoogle ScholarPubMed
Mileykovskiy, B. Y., Kiyashchenko, L. I. & Siegel, J. M. (2005) Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46: –98.CrossRefGoogle ScholarPubMed
Mitani, A., Ito, K., Hallanger, A. E. . (1988) Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res 451: –402.CrossRefGoogle ScholarPubMed
Mochizuki, T., Crocker, A., McCormack, S. . (2004) Behavioral state instability in orexin knock-out mice. J Neurosci 24: –300.CrossRefGoogle ScholarPubMed
Moruzzi, G. & Magoun, H. W. (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1: –73.CrossRefGoogle ScholarPubMed
Nitz, D. & Siegel, J. (1997a) GABA release in the dorsal raphe nucleus: role in the control of REM sleep. Am J Physiol 273: –5.Google ScholarPubMed
Nitz, D. & Siegel, J. M. (1997b) GABA release in the locus coeruleus as a function of sleep/wake state. Neuroscience 78: –801.CrossRefGoogle ScholarPubMed
Pal, D. & Mallick, B. N. (2009) GABA in pedunculopontine tegmentum increases rapid eye movement sleep in freely moving rats: possible role of GABA-ergic inputs from substantia nigra pars reticulata. Neuroscience 164: –14.CrossRefGoogle ScholarPubMed
Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.Google Scholar
Peigneux, P., Laureys, S., Fuchs, S. . (2001) Generation of rapid eye movements during paradoxical sleep in humans. Neuroimage 14: –8.CrossRefGoogle ScholarPubMed
Peyron, C., Sapin, E., Leger, L., Luppi, P. H. & Fort, P. (2009) Role of the melanin-concentrating hormone neuropeptide in sleep regulation. Peptides 30: –9.CrossRefGoogle ScholarPubMed
Peyron, C., Tighe, D. K., van den Pol, A. N. . (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18: –10,015.CrossRefGoogle ScholarPubMed
Portas, C. M. & McCarley, R. W. (1994) Behavioral state-related changes of extracellular serotonin concentration in the dorsal raphe nucleus: a microdialysis study in the freely moving cat. Brain Res 648: –12.CrossRefGoogle ScholarPubMed
Sakai, K. & Crochet, S. (2001) Role of dorsal raphe neurons in paradoxical sleep generation in the cat: no evidence for a serotonergic mechanism. Eur J Neurosci 13: –12.Google ScholarPubMed
Sakai, K., Petitjean, F. & Jouvet, M. (1976) Effects of ponto-mesencephalic lesions and electrical stimulation upon PGO waves and EMPs in unanesthetized cats. Electroencephalogr Clin Neurophysiol 41: –63.CrossRefGoogle ScholarPubMed
Saper, C. B., Chou, T. C. & Scammell, T. E. (2001) The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci 24: –31.CrossRefGoogle ScholarPubMed
Sapin, E., Lapray, D. & Berod, A. . (2009) Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS One 4: .CrossRefGoogle ScholarPubMed
Sastre, J. P., Buda, C., Kitahama, K. & Jouvet, M. (1996) Importance of the ventrolateral region of the periaqueductal gray and adjacent tegmentum in the control of paradoxical sleep as studied by muscimol microinjections in the cat. Neuroscience 74: –26.CrossRefGoogle ScholarPubMed
Sastre, J. P. & Jouvet, M. (1979) [Oneiric behavior in cats]. Physiol Behav 22: –89.Google ScholarPubMed
Sherin, J. E., Elmquist, J. K., Torrealba, F. & Saper, C. B. (1998) Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18: –21.CrossRefGoogle ScholarPubMed
Steriade, M. & McCarley, R. W. (2005) Brainstem Control of Wakefulness and Sleep. New York: Plenum Press.Google Scholar
Steriade, M., Pare, D., Datta, S., Oakson, G. & Curro Dossi, R. (1990) Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves. J Neurosci 10: –79.CrossRefGoogle ScholarPubMed
Thakkar, M. M., Ramesh, V., Cape, E. G. . (1999) REM sleep enhancement and behavioral cataplexy following orexin (hypocretin)-II receptor antisense perfusion in the pontine reticular formation. Sleep Res Online 2: –20.Google ScholarPubMed
Thakkar, M. M., Strecker, R. E. & McCarley, R. W. (1998) Behavioral state control through differential serotonergic inhibition in the mesopontine cholinergic nuclei: a simultaneous unit recording and microdialysis study. J Neurosci 18: –7.CrossRefGoogle ScholarPubMed
Thakkar, M. M., Strecker, R. E. & McCarley, R. W. (2002) Phasic but not tonic REM-selective discharge of periaqueductal gray neurons in freely behaving animals: relevance to postulates of GABAergic inhibition of monoaminergic neurons. Brain Res 945: –80.CrossRefGoogle Scholar
Torterolo, P., Sampogna, S., Morales, F. R. & Chase, M. H. (2006) MCH-containing neurons in the hypothalamus of the cat: searching for a role in the control of sleep and wakefulness. Brain Res 1119: –14.CrossRefGoogle ScholarPubMed
Trulson, M. E. & Jacobs, B. L. (1979) Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res 163: –50.CrossRefGoogle ScholarPubMed
Verret, L., Fort, P., Gervasoni, D., Leger, L. & Luppi, P. H. (2006) Localization of the neurons active during paradoxical (REM) sleep and projecting to the locus coeruleus noradrenergic neurons in the rat. J Comp Neurol 495: –86.CrossRefGoogle ScholarPubMed
Verret, L., Goutagny, R., Fort, P. . (2003) A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci 4: .CrossRefGoogle ScholarPubMed
Vertes, R. P., Hoover, W. B. & Viana di Prisco, G. (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3: –200.CrossRefGoogle ScholarPubMed
Vertes, R. P. & Kocsis, B. (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81: –926.Google ScholarPubMed
Xi, M. C., Morales, F. R. & Chase, M. H. (1999a) Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J Neurophysiol 82: –19.CrossRefGoogle ScholarPubMed
Xi, M. C., Morales, F. R. & Chase, M. H. (1999b) A GABAergic pontine reticular system is involved in the control of wakefulness and sleep. Sleep Res Online 2: –8.Google ScholarPubMed
Xi, M. C., Morales, F. R. & Chase, M. H. (2001a) Induction of wakefulness and inhibition of active (REM) sleep by GABAergic processes in the nucleus pontis oralis. Arch Ital Biol 139: –45.Google ScholarPubMed
Xi, M. C., Morales, F. R. & Chase, M. H. (2001b) The motor inhibitory system operating during active sleep is tonically suppressed by GABAergic mechanisms during other states. J Neurophysiol 86: –15.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×