Inter-individual differences in the dynamics of sleep homeostasis.

STUDY OBJECTIVES The two-process model posits that sleep is regulated by 2 independent processes, a circadian Process C and a homeostatic Process S. EEG slow-wave activity (SWA) is a marker of NREM sleep intensity and is used as an indicator of sleep homeostasis. So far, parameters of the two-process model have been derived mainly from average data. Our aim was to quantify inter-individual differences. DESIGN Polysomnographic recordings (analysis of existing data). SETTING Sound attenuated sleep laboratory. PATIENTS OR PARTICIPANTS Eight healthy young males. INTERVENTIONS 40-h sustained wakefulness. MEASUREMENTS AND RESULTS Process S was modeled by a saturating exponential function during wakefulness and an exponential decline during sleep. Empirical mean SWA (derivation C3A2) per NREM sleep episode at episode midpoint were used for parameter estimation. Parameters were estimated simultaneously by minimizing the mean square error between data and simulations of Process S. This approach was satisfactory for average data and most individual data. We further improved our methodological approach by limiting the time constants to a physiologically meaningful range. This allowed a satisfactory fit also for the one individual whose parameters were beyond a physiological range. The time constants of the buildup of Process S ranged from 14.1 h to 26.4 h and those of the decline from 1.2 h to 2.9 h with similar inter-individual variability of the buildup and decline of Process S. CONCLUSIONS We established a robust method for parameter estimation of Process S on an individual basis.

[1]  J. Carrier,et al.  Age‐related modifications of NREM sleep EEG: from childhood to middle age , 2001, Journal of sleep research.

[2]  Sharon L. Weinberg,et al.  Data Analysis for the Behavioral Sciences Using SPSS , 2002 .

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

[4]  P Achermann,et al.  Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep , 2000, Neuroscience.

[5]  D. Dijk,et al.  Age-Related Reduction in the Maximal Capacity for Sleep—Implications for Insomnia , 2008, Current Biology.

[6]  J. R. Matthews,et al.  Evidence from the waking electroencephalogram that short sleepers live under higher homeostatic sleep pressure than long sleepers , 2001, Neuroscience.

[7]  H. Landolt,et al.  A functional genetic variation of adenosine deaminase affects the duration and intensity of deep sleep in humans , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Achermann,et al.  Sleep homeostasis in the rat in the light and dark period , 2007, Brain Research Bulletin.

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

[10]  M. Carskadon,et al.  Spectral analysis of the sleep electroencephalogram during adolescence. , 2004, Sleep.

[11]  S. Daan,et al.  Evidence for differential human slow‐wave activity regulation across the brain , 2009, Journal of sleep research.

[12]  Peter Achermann,et al.  Individual ‘Fingerprints’ in Human Sleep EEG Topography , 2001, Neuropsychopharmacology.

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

[14]  Domien G. M. Beersma,et al.  All night spectral analysis of EEG sleep in young adult and middle-aged male subjects , 1989, Neurobiology of Aging.

[15]  P. Achermann,et al.  Effect of age on the sleep EEG: slow-wave activity and spindle frequency activity in young and middle-aged men , 1996, Brain Research.

[16]  J. Carrier,et al.  Circadian and homeostatic sleep regulation in morningness–eveningness , 2006, Journal of sleep research.

[17]  P. Achermann,et al.  Insufficient non-REM sleep intensity in narcolepsy-cataplexy. , 2007, Sleep.

[18]  Pierre Philip,et al.  The circadian and homeostatic modulation of sleep pressure during wakefulness differs between morning and evening chronotypes , 2003, Journal of sleep research.

[19]  Elizabeth B Klerman,et al.  Interindividual variation in sleep duration and its association with sleep debt in young adults. , 2005, Sleep.

[20]  D. Dijk,et al.  Sex differences in the sleep EEG of young adults: visual scoring and spectral analysis. , 1989, Sleep.

[21]  A. Wirz-Justice,et al.  Power density in theta/alpha frequencies of the waking EEG progressively increases during sustained wakefulness. , 1995, Sleep.

[22]  H C Thode,et al.  Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density. , 1990, Journal of theoretical biology.

[23]  H. Landolt.  Genotype-dependent differences in sleep, vigilance, and response to stimulants. , 2008, Current pharmaceutical design.

[24]  P. Achermann,et al.  Challenging sleep homeostasis in narcolepsy-cataplexy: implications for non-REM and REM sleep regulation. , 2008, Sleep.

[25]  H. Landolt,et al.  Similar sleep EEG topography in middle-aged depressed patients and healthy controls. , 2005, Sleep.

[26]  D. Dijk,et al.  PER3 Polymorphism Predicts Sleep Structure and Waking Performance , 2007, Current Biology.

[27]  A. Besset,et al.  Sleep architecture, slow wave activity, and sleep spindles in adult patients with sleepwalking and sleep terrors , 2000, Clinical Neurophysiology.

[28]  D. Dijk,et al.  EEG power density during recovery sleep in the morning. , 1991, Electroencephalography and clinical neurophysiology.

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

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

[31]  I Feinberg,et al.  Systematic trends across the night in human sleep cycles. , 1979, Psychophysiology.

[32]  D. Dinges,et al.  Individual differences in adult human sleep and wakefulness: Leitmotif for a research agenda. , 2005, Sleep.

[33]  Julie Carrier,et al.  Difference in sleep regulation between morning and evening circadian types as indexed by antero‐posterior analyses of the sleep EEG , 2006, The European journal of neuroscience.

[34]  Peter Achermann,et al.  Homeostatic sleep regulation in adolescents. , 2005, Sleep.

[35]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[36]  Manuel Schabus,et al.  Homeostatic Sleep Pressure and Responses to Sustained Attention in the Suprachiasmatic Area , 2009, Science.

[37]  T. Wehr,et al.  Two circadian rhythms in the human electroencephalogram during wakefulness. , 1999, The American journal of physiology.

[38]  G. Rondouin,et al.  Sleep deprivation in narcoleptic subjects: effect on sleep stages and EEG power density. , 1992, Electroencephalography and clinical neurophysiology.

[39]  N. Kajimura,et al.  Ultradian oscillations in cranial thermoregulation and electroencephalographic slow-wave activity during sleep are abnormal in humans with annual winter depression , 2000, Brain Research.

[40]  A A Borbély,et al.  Time course of EEG power density during long sleep in humans. , 1990, The American journal of physiology.

[41]  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.

[42]  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.

[43]  P. Achermann.  The two-process model of sleep regulation revisited. , 2004, Aviation, space, and environmental medicine.