Neurophysiological mechanisms of sleep and wakefulness: a question of balance.

Following a summary of the stages of sleep and wakefulness as monitored with the electroencephalogram and electromyogram, important aspects of the neurophysiology and neuroanatomy of the circuits of vigilance state control are reviewed. A homeostatic drive for sleep and a circadian influence work in concert to determine sleepiness. These processes influence sleep-promoting and central arousing neuronal systems, the former dependent on a group of neurons in the hypothalamic ventrolateral preoptic area and the latter governed by neurons in the pons and basal forebrain. The interactive neuronal circuit that is formed by these cell groups ensures the balance between sleep and wakefulness and the rapid transition to and from sleep. As sleep deepens, the switch to rapid eye movement (REM) sleep occurs. This transition can also be viewed as a balance between one group of pontine neurons that discharge only during REM sleep and another group that cease to discharge during REM sleep. This article concludes with future perspectives based on the recent discovery of the orexin cell group. Orexinergic neurons may be critical both for promoting wakefulness at certain times in the daily cycle and for controlling the switch into REM sleep.

[1]  C. Economo SLEEP AS A PROBLEM OF LOCALIZATION , 1930 .

[2]  M. Sterman,et al.  Forebrain inhibitory mechanisms: sleep patterns induced by basal forebrain stimulation in the behaving cat. , 1962, Experimental neurology.

[3]  M. Jouvet,et al.  Effets du refroidissement et de la stimulation des noyaux du systeme du raphe sur les etats de vigilance chez le chat , 1979 .

[4]  M. Jouvet What does a cat dream about? , 1979, Trends in Neurosciences.

[5]  F. Bloom,et al.  Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R. McCarley,et al.  Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat , 1988, Brain Research.

[7]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  D. McCormick Cholinergic and noradrenergic modulation of thalamocortical processing , 1989, Trends in Neurosciences.

[9]  M. Steriade,et al.  Brainstem Control of Wakefulness and Sleep , 1990, Springer US.

[10]  G Oakson,et al.  Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  M. Steriade,et al.  Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Y. Lai,et al.  Enhancement of acetylcholine release during REM sleep in the caudomedial medulla as measured by in vivo microdialysis , 1992, Brain Research.

[13]  R. McCarley,et al.  Neurobiological structure of the revised limit cycle reciprocal interaction model of REM cycle control , 1992, Journal of sleep research.

[14]  J. Monti,et al.  Involvement of histamine in the control of the waking state. , 1993, Life sciences.

[15]  L. Sanford,et al.  Central administration of two 5-HT receptor agonists: Effect on REM sleep initiation and PGO waves , 1994, Pharmacology Biochemistry and Behavior.

[16]  R. McCarley Neurophysiology of Sleep: Basic Mechanisms Underlying Control of Wakefulness and Sleep , 1994 .

[17]  W. Dement,et al.  Circadian rhythms in narcolepsy: studies on a 90 minute day. , 1994, Electroencephalography and clinical neurophysiology.

[18]  Derk-Jan Dijk,et al.  Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans , 1994, Neuroscience Letters.

[19]  R. McCarley,et al.  Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal. , 1994, Science.

[20]  R. Llinás,et al.  Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling rem sleep: An in vitro electrophysiological study , 1994, Neuroscience.

[21]  D.G.M. Dijk,et al.  Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  R Szymusiak,et al.  Magnocellular nuclei of the basal forebrain: substrates of sleep and arousal regulation. , 1995, Sleep.

[23]  R. McCarley,et al.  Chronic low-amplitude electrical stimulation of the laterodorsal tegmental nucleus of freely moving cats increases REM sleep , 1996, Brain Research.

[24]  R. McCarley,et al.  Activation of Ventrolateral Preoptic Neurons During Sleep , 1996, Science.

[25]  D. Rainnie,et al.  Microdialysis perfusion of 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH- DPAT) in the dorsal raphe nucleus decreases serotonin release and increases rapid eye movement sleep in the freely moving cat , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  R. Lydic,et al.  Pontine Nitric Oxide Modulates Acetylcholine Release, Rapid Eye Movement Sleep Generation, and Respiratory Rate , 1997, The Journal of Neuroscience.

[27]  A I Pack,et al.  Serotonin at the Laterodorsal Tegmental Nucleus Suppresses Rapid-Eye-Movement Sleep in Freely Behaving Rats , 1997, The Journal of Neuroscience.

[28]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.

[29]  C. Saper,et al.  Innervation of Histaminergic Tuberomammillary Neurons by GABAergic and Galaninergic Neurons in the Ventrolateral Preoptic Nucleus of the Rat , 1998, The Journal of Neuroscience.

[30]  C. Guilleminault,et al.  Narcolepsy and idiopathic hypersomnolence. , 1998, Clinics in chest medicine.

[31]  S. Carr,et al.  Orexins and Orexin Receptors: A Family of Hypothalamic Neuropeptides and G Protein-Coupled Receptors that Regulate Feeding Behavior , 1998, Cell.

[32]  A. N. van den Pol,et al.  Neurons Containing Hypocretin (Orexin) Project to Multiple Neuronal Systems , 1998, The Journal of Neuroscience.

[33]  Jon T. Willie,et al.  Narcolepsy in orexin Knockout Mice Molecular Genetics of Sleep Regulation , 1999, Cell.

[34]  Takeshi Sakurai,et al.  Distribution of orexin neurons in the adult rat brain 1 Published on the World Wide Web on 17 March 1999. 1 , 1999, Brain Research.

[35]  G. Aston-Jones,et al.  Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system , 1999, The Journal of comparative neurology.

[36]  Emmanuel Mignot,et al.  The Sleep Disorder Canine Narcolepsy Is Caused by a Mutation in the Hypocretin (Orexin) Receptor 2 Gene , 1999, Cell.

[37]  T. Sakurai,et al.  Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Sebastiaan Overeem,et al.  A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains , 2000, Nature Medicine.

[39]  Stephen R. Morairty,et al.  Adenosinergic modulation of basal forebrain and preoptic/anterior hypothalamic neuronal activity in the control of behavioral state , 2000, Behavioural Brain Research.

[40]  R. McCarley,et al.  Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study , 2000, Neuroscience.

[41]  Michael Aldrich,et al.  Reduced Number of Hypocretin Neurons in Human Narcolepsy , 2000, Neuron.

[42]  E. Mignot,et al.  Changes in CSF hypocretin-1 (orexin A) levels in rats across 24 hours and in response to food deprivation , 2001, Neuroreport.

[43]  R. Szymusiak,et al.  Subregional organization of preoptic area /anterior hypothalamic projections to arousal‐related monoaminergic cell groups , 2001, The Journal of comparative neurology.

[44]  M. Xi,et al.  Effects on sleep and wakefulness of the injection of hypocretin-1 (orexin-A) into the laterodorsal tegmental nucleus of the cat , 2001, Brain Research.

[45]  J. Yesavage,et al.  CSF hypocretin/orexin levels in narcolepsy and other neurological conditions , 2001, Neurology.

[46]  J. Sutcliffe,et al.  The hypocretins: Setting the arousal threshold , 2002, Nature Reviews Neuroscience.

[47]  Ming-Fung Wu,et al.  Release of Hypocretin (Orexin) during Waking and Sleep States , 2002, The Journal of Neuroscience.

[48]  E. Mignot,et al.  The role of cerebrospinal fluid hypocretin measurement in the diagnosis of narcolepsy and other hypersomnias. , 2002, Archives of neurology.

[49]  K. J. Parker,et al.  Circadian and Homeostatic Regulation of Hypocretin in a Primate Model: Implications for the Consolidation of Wakefulness , 2003, The Journal of Neuroscience.

[50]  D. J. Woodward,et al.  Bistability, switches and working memory in a two-neuron inhibitory-feedback model , 1993, Biological Cybernetics.

[51]  Takeshi Sakurai,et al.  Expression of a Poly-Glutamine-Ataxin-3 Transgene in Orexin Neurons Induces Narcolepsy–Cataplexy in the Rat , 2004, The Journal of Neuroscience.