Sleep homeostasis in the rat in the light and dark period

Sleep is regulated by the interaction of a homeostatic (Process S) and a circadian component. The duration of prior wakefulness is the main factor influencing subsequent sleep duration and its intensity. We investigated in the rat whether the sleep-wake history before sleep deprivation (SD) contributes to the effects of sleep loss incurred during the SD. A 24-h baseline recording was followed by 6 h SD at light onset (SD-Light, n=7), or at dark onset (SD-Dark, n=8) and 18 h recovery. Both SDs led to a pronounced increase in slow wave activity (SWA, EEG power between 0.75 and 4.0 Hz) in NREM sleep and increased sleep consolidation. The prolongation of sleep episodes was associated with increased intra-episode SWA. The amount of waking before the SD correlated positively with the SWA increase during recovery, and SWA levels before SD were negatively correlated with their subsequent increase. The time-course of SWA (Process S) as well as of single frequency bins within the SWA band was successfully simulated based on vigilance-state distribution. The time constant of the exponential monotonic decay (Td) was higher for the 0.75-1.0 Hz bin compared to all remaining frequency bins of the SWA band, reflecting a slower process determining the slow EEG component during sleep. The data show that the homeostatic response after SD, consisting of increased sleep intensity and sleep consolidation is determined by a combination of SD and the preceding vigilance-state history. The slower dynamics of low frequency delta power compared to fast delta frequencies point to heterogeneity within the traditionally defined SWA band.

[1]  Giulio Tononi,et al.  Sleep homeostasis in Drosophila melanogaster. , 2004, Sleep.

[2]  R. Huber,et al.  Topography of EEG dynamics after sleep deprivation in mice. , 2000, Journal of neurophysiology.

[3]  I Tobler,et al.  Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. , 1991, The American journal of physiology.

[4]  I Tobler,et al.  The dynamics of spindles and EEG slow-wave activity in NREM sleep in mice. , 2004, Archives italiennes de biologie.

[5]  M. Kas,et al.  Circadian timed wakefulness at dawn opposes compensatory sleep responses after sleep deprivation in Octodon degus. , 1999, Sleep.

[6]  Vladyslav V Vyazovskiy,et al.  Interhemispheric sleep EEG asymmetry in the rat is enhanced by sleep deprivation. , 2002, Journal of neurophysiology.

[7]  S. Daan,et al.  EEG Power Density during Nap Sleep: Reflection of an Hourglass Measuring the Duration of Prior Wakefulness , 1987, Journal of biological rhythms.

[8]  A. Reißland Electrophysiology of trichobothria in orb-weaving spiders (Agelenidae, Araneae) , 1978, Journal of comparative physiology.

[9]  T. Deboer,et al.  Sleep regulation in the Djungarian hamster: comparison of the dynamics leading to the slow-wave activity increase after sleep deprivation and daily torpor. , 2003, Sleep.

[10]  M. Lancel,et al.  Effects of circadian phase and duration of sleep deprivation on sleep and EEG power spectra in the cat , 1991, Brain Research.

[11]  A. Borbély A two process model of sleep regulation. , 1982, Human neurobiology.

[12]  P. Achermann,et al.  Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. , 1997, Electroencephalography and clinical neurophysiology.

[13]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  P. Achermann,et al.  Low-frequency (<1Hz) oscillations in the human sleep electroencephalogram , 1997, Neuroscience.

[15]  Reto Huber,et al.  Effects of sleep deprivation on sleep and sleep EEG in three mouse strains: empirical data and simulations , 2000, Brain Research.

[16]  H. Heller,et al.  Homeostatic regulation of sleep in arrhythmic Siberian hamsters. , 2004, American Journal of Physiology. Regulatory Integrative and Comparative Physiology.

[17]  S. Daan,et al.  Dissimilarity of slow-wave activity enhancement by torpor and sleep deprivation in a hibernator. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[18]  V. Vyazovskiy,et al.  Running wheel accessibility affects the regional electroencephalogram during sleep in mice. , 2006, Cerebral cortex.

[19]  D. Dijk,et al.  Dynamics of electroencephalographic sleep spindles and slow wave activity in men: effect of sleep deprivation , 1993, Brain Research.

[20]  I Tobler,et al.  Electroencephalogram analysis of non-rapid eye movement sleep in rats. , 1988, The American journal of physiology.

[21]  D. Dijk,et al.  Separation of circadian and wake duration-dependent modulation of EEG activation during wakefulness , 2002, Neuroscience.

[22]  S. Daan,et al.  Timing of human sleep: recovery process gated by a circadian pacemaker. , 1984, The American journal of physiology.

[23]  D Chollet,et al.  The Homeostatic Regulation of Sleep Need Is under Genetic Control , 2001, The Journal of Neuroscience.

[24]  M Steriade,et al.  Electrophysiological correlates of sleep delta waves. , 1998, Electroencephalography and clinical neurophysiology.

[25]  A. Borbély,et al.  Sleep EEG in the rat as a function of prior waking. , 1986, Electroencephalography and clinical neurophysiology.

[26]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[27]  Alexander A. Borbély,et al.  Sleep-deprivation: Effects on sleep and EEG in the rat , 1979, Journal of comparative physiology.

[28]  V. Vyazovskiy,et al.  Regional differences in NREM sleep slow‐wave activity in mice with congenital callosal dysgenesis , 2005, Journal of sleep research.

[29]  I. Feinberg,et al.  Homeostatic behavior of fast fourier transform power in very low frequency non-rapid eye movement human electroencephalogram , 2006, Neuroscience.

[30]  A. Borbély,et al.  Effect of sleep deprivation on EEG slow wave activity within non-REM sleep episodes in the rat. , 1989, Electroencephalography and clinical neurophysiology.

[31]  M. Bonnet,et al.  Effect of 64 hours of sleep deprivation upon sleep in geriatric normals and insomniacs , 1986, Neurobiology of Aging.

[32]  I Tobler,et al.  Prolonged effects of 24-h total sleep deprivation on sleep and sleep EEG in the rat , 1999, Neuroscience Letters.

[33]  A. Borbély,et al.  Sleep regulation in rats: effects of sleep deprivation, light, and circadian phase. , 1986, The American journal of physiology.

[34]  Alexander A. Borbély,et al.  The effect of 3-h and 6-h sleep deprivation on sleep and EEG spectra of the rat , 1990, Behavioural Brain Research.

[35]  M. Kryger,et al.  Principles and Practice of Sleep Medicine , 1989 .

[36]  Alexander A. Borbély,et al.  Sleep homeostasis in the rat: Simulation of the time course of EEG slow-wave activity , 1991, Neuroscience Letters.

[37]  T. Deboer,et al.  Sleep and Sleep Regulation in Normal and Prion Protein-Deficient Mice , 1997, The Journal of Neuroscience.

[38]  A. Borbély,et al.  The effect of light on sleep and the EEG of young rats , 1990, Pflügers Archiv.

[39]  Gerard A. Kerkhof,et al.  Effects of repeated sleep deprivation in the dark- or light-period on sleep in rats , 1989, Physiology & Behavior.

[40]  Peter Achermann,et al.  A model of human sleep homeostasis based on EEG slow-wave activity: Quantitative comparison of data and simulations , 1993, Brain Research Bulletin.

[41]  Peter Achermann,et al.  Sleep continuity and the REM-nonREM cycle in the rat under baseline conditions and after sleep deprivation , 1991, Physiology & Behavior.