Human Circadian Physiology and Sleep-Wake Regulation

Periodic daily cycles have been observed in a wide range of physiologic and behavioral variables in humans. These include cyclic variations in sleep propensity, neurobehavioral performance, motor performance, as well as thermoregulatory, endocrine, cardiac, gastrointestinal, pulmonary, renal, and neurologic functions, including sensory sensitivity. The rhythms of all of these variables exhibit a specific temporal relationship with each other and with the environmental light—dark cycle. The mechanisms underlying these rhythms, their temporal relationships, and their functional significance have been the subject of numerous investigations (Conroy & Mills, 1970).

[1]  Derk-Jan Dijk,et al.  EEG slow waves and sleep spindles: windows on the sleeping brain , 1995, Behavioural Brain Research.

[2]  R L Williams,et al.  Effect on sleep of a sleep period time displacement. , 1971, Aerospace medicine.

[3]  A. Lewy,et al.  The role of melatonin and circadian phase in age-related sleep-maintenance insomnia: assessment in a clinical trial of melatonin replacement. , 1998, Sleep.

[4]  C A Czeisler,et al.  Timing of REM sleep is coupled to the circadian rhythm of body temperature in man. , 1980, Sleep.

[5]  M. Carskadon,et al.  Cumulative effects of sleep restriction on daytime sleepiness. , 1981, Psychophysiology.

[6]  C A Czeisler,et al.  Short‐term memory, alertness and performance: a reappraisal of their relationship to body temperature , 1992, Journal of sleep research.

[7]  Paolo Sassone-Corsi,et al.  A Web of Circadian Pacemakers , 2002, Cell.

[8]  M Terman,et al.  Light Treatment for Sleep Disorders: Consensus Report , 1995, Journal of biological rhythms.

[9]  REM sleep deprivation during 5 hours leads to an immediate REM sleep rebound and to suppression of non-REM sleep intensity. , 1990, Electroencephalography and clinical neurophysiology.

[10]  F. G. Benedict STUDIES IN BODY-TEMPERATURE.— I. INFLUENCE OF THE INVERSION OF THE DAILY ROUTINE; THE TEMPERATURE OF NIGHT-WORKERS , 1904 .

[11]  C A Czeisler,et al.  Timing of REM and stages 3 + 4 sleep during temporal isolation in man. , 1980, Sleep.

[12]  R. Kronauer,et al.  Photopic transduction implicated in human circadian entrainment , 1997, Neuroscience Letters.

[13]  J. N. Mills Circadian rhythms during and after three months in solitude underground , 1964, The Journal of physiology.

[14]  C A Czeisler,et al.  Phase-Amplitude Resetting of the Human Circadian Pacemaker via Bright Light: A Further Analysis , 1994, Journal of biological rhythms.

[15]  Jürgen Zulley,et al.  Interaction Between the Sleep-Wake Cycle and the Rhythm of Rectal Temperature , 1982 .

[16]  I Feinberg,et al.  EEG sleep patterns as a function of normal and pathological aging in man. , 1967, Journal of psychiatric research.

[17]  Alexander A. Borbély,et al.  Sleep Regulation: Circadian Rhythm and Homeostasis , 1982 .

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

[19]  T. Åkerstedt,et al.  Sleepiness and shift work: field studies. , 1982, Sleep.

[20]  J. C. Zimmerman,et al.  Cortisol secretion is inhibited during sleep in normal man. , 1983, The Journal of clinical endocrinology and metabolism.

[21]  A. Pack,et al.  Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4-5 hours per night. , 1997, Sleep.

[22]  Richard E Kronauer,et al.  Human circadian pacemaker is sensitive to light throughout subjective day without evidence of transients. , 1997, The American journal of physiology.

[23]  R. H. van den Hoofdakker,et al.  Endogenous and exogenous components in the circadian variation of core body temperature in humans , 1997, Journal of sleep research.

[24]  D. Dijk,et al.  Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance , 1992, Journal of sleep research.

[25]  Arthur T. Winfree,et al.  The timing of biological clocks , 1986 .

[26]  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.

[27]  Richard E. Kronauer,et al.  Erratum: Quantifying human circadian pacemaker response to brief, extended, and repeated light stimuli over the photopic range (Journal of Biological Rhythms) , 2000 .

[28]  T H Monk,et al.  Rhythmic vs homeostatic influences on mood, activation, and performance in young and old men. , 1992, Journal of gerontology.

[29]  P. Achermann,et al.  Sleep Initiation and Initial Sleep Intensity: Interactions of Homeostatic and Circadian Mechanisms , 1989, Journal of biological rhythms.

[30]  E. Cauter,et al.  Diurnal and ultradian rhythms in human endocrine function: a minireview. , 1990 .

[31]  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.

[32]  S. Campbell,et al.  Napping behavior during "spontaneous internal desynchronization": sleep remains in synchrony with body temperature. , 1985, Human neurobiology.

[33]  Charles A. Czeisler,et al.  The human circadian timing system and sleep-wake regulation , 2000 .

[34]  M. K. Vaughan,et al.  TWENTY-FOUR-HOUR CYCLE OF A MELATONIN-LIKE SUBSTANCE IN THE PLASMA OF HUMAN MALES , 1973 .

[35]  R. Kronauer,et al.  Simulations of light effects on the human circadian pacemaker: implications for assessment of intrinsic period. , 1996, The American journal of physiology.

[36]  C A Czeisler,et al.  Mathematical model of the human circadian system with two interacting oscillators. , 1982, The American journal of physiology.

[37]  P. Lavie,et al.  Ultrashort sleep-walking schedule. I. Evidence of ultradian rhythmicity in "sleepability'. , 1981, Electroencephalography and clinical neurophysiology.

[38]  D. Dijk,et al.  Later endogenous circadian temperature nadir relative to an earlier wake time in older people. , 1998, The American journal of physiology.

[39]  C A Czeisler,et al.  Circadian pacemaker interferes with sleep onset at specific times each day: role in insomnia. , 1987, The American journal of physiology.

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

[41]  M. Carskadon,et al.  Effects of Total Sleep Loss on Sleep Tendency , 1979, Perceptual and motor skills.

[42]  J. Carrier,et al.  Sleep propensity and sleep architecture after bright light exposure at three different times of day , 1995, Journal of sleep research.

[43]  A A Borbély,et al.  Electroencephalogram power density and slow wave sleep as a function of prior waking and circadian phase. , 1990, Sleep.

[44]  C. Czeisler,et al.  Gender differences in the temporal organization of proclactin (PRL) secretion: evidence for a sleep-independent circadian rhythm of circulating PRL levels- a clinical research center study. , 1996, The Journal of clinical endocrinology and metabolism.

[45]  J. Aschoff On the perception of time during prolonged temporal isolation. , 1985, Human neurobiology.

[46]  P. Badia,et al.  Immediate effects of different light intensities on body temperature and alertness , 1993, Physiology and Behavior.

[47]  P. Achermann,et al.  Concepts and models of sleep regulation: an overview , 1992, Journal of sleep research.

[48]  R. Cartwright,et al.  Principles and Practice of Sleep Medicine, 3rd ed. , 2001 .

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

[50]  N. Kleitman,et al.  Effect of non-twenty-four-hour routines of living on oral temperature and heart rate. , 1953, Journal of applied physiology.

[51]  A single pacemaker can produce different rates of reentrainment in different overt rhythms , 1992, Journal of sleep research.

[52]  J. C. Zimmerman,et al.  REM density is dissociated from REM sleep timing during free-running sleep episodes. , 1980, Sleep.

[53]  J. Aschoff,et al.  Desynchronization of human circadian rhythms. , 1967, The Japanese journal of physiology.

[54]  J. C. Zimmerman,et al.  Chronobiology of aging: Temperature, sleep-wake rhythms and entrainment , 1982, Neurobiology of Aging.

[55]  D. Dawson,et al.  The hypothermic effect of melatonin on core body temperature: Is more better? , 1996, Journal of pineal research.

[56]  W. Fishbein,et al.  Plasma 17-hydroxycorticosteroid levels during sleep in man. , 1966, The Journal of clinical endocrinology and metabolism.

[57]  P. Achermann,et al.  Dynamics of the sleep EEG after an early evening nap: experimental data and simulations. , 1996, The American journal of physiology.

[58]  R. Kronauer,et al.  Circadian sleep regulation in the absence of light perception: chronic non-24-hour circadian rhythm sleep disorder in a blind man with a regular 24-hour sleep-wake schedule. , 1993, Sleep.

[59]  S. Daan,et al.  Vertebrate Circadian Systems , 1982, Proceedings in Life Sciences.

[60]  C. Czeisler,et al.  Association of sleep-wake habits in older people with changes in output of circadian pacemaker , 1992, The Lancet.

[61]  M. Carskadon,et al.  Circadian variation of sleep tendency in elderly and young adult subjects. , 1982, Sleep.

[62]  D. Kass,et al.  Transient circadian internal desynchronization after light-dark phase shift in monkeys. , 1977, The American journal of physiology.

[63]  J. W. Hastings,et al.  A PERSISTENT DIURNAL RHYTHM OF LUMINESCENCE IN GONYAULAX POLYEDRA , 1958 .

[64]  C A Czeisler,et al.  Human sleep: its duration and organization depend on its circadian phase. , 1980, Science.

[65]  S H Strogatz,et al.  The mathematical structure of the human sleep-wake cycle , 1986 .

[66]  H. Agnew,et al.  THE EFFECTS OF STAGE FOUR SLEEP DEPRIVATION. , 1964, Electroencephalography and clinical neurophysiology.

[67]  D. Kripke,et al.  Bright light can delay human temperature rhythm independent of sleep. , 1989, The American journal of physiology.

[68]  E. Brown,et al.  The parathyroid hormone circadian rhythm is truly endogenous--a general clinical research center study. , 1997, The Journal of clinical endocrinology and metabolism.

[69]  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.

[70]  T. Åkerstedt,et al.  The circadian variation of experimentally displaced sleep. , 1981, Sleep.

[71]  M. Terman,et al.  A Circadian Pacemaker for Visual Sensitivity? a , 1985, Annals of the New York Academy of Sciences.

[72]  I Tobler,et al.  Effect of partial sleep deprivation on sleep stages and EEG power spectra: evidence for non-REM and REM sleep homeostasis. , 1990, Electroencephalography and clinical neurophysiology.

[73]  B M Stone,et al.  Human circadian rhythms in constant dim light (8 lux) with knowledge of clock time , 1996, Journal of sleep research.

[74]  A. Borbély,et al.  The effect of sleep deprivation on sleep in rats with suprachiasmatic lesions , 1983, Neuroscience Letters.

[75]  M. Orne,et al.  Temporal placement of a nap for alertness: contributions of circadian phase and prior wakefulness. , 1987, Sleep.

[76]  Daniel J Buysse,et al.  Circadian determinants of the postlunch dip in performance. , 1996, Chronobiology international.

[77]  C. L. Ralph,et al.  A melatonin rhythm persists in rat pineals in darkness. , 1971, Endocrinology.

[78]  Richard E. Kronauer,et al.  Light-induced suppression of endogenous circadian amplitude in humans , 1991, Nature.

[79]  T. Åkerstedt,et al.  Towards the Prediction of Alertness on Abnormal Sleep/Wake Schedules , 1989 .

[80]  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.

[81]  D. Dijk,et al.  Light Treatment for Sleep Disorders: Consensus Report , 1995, Journal of biological rhythms.

[82]  M. Moore-Ede,et al.  Mathematical Models of the Circadian Sleep-Wake Cycle. , 1984 .

[83]  C A Czeisler,et al.  ENTRAINMENT OF HUMAN ORCADIAN RHYTHMS BY LIGHT‐DARK CYCLES: A REASSESSMENT , 1981, Photochemistry and photobiology.

[84]  Daniel F. Kripke,et al.  Natural light exposure of young adults , 1986, Physiology & Behavior.

[85]  F. Steyvers,et al.  Vigilance and performance in automated systems , 1989 .

[86]  C A Czeisler,et al.  Variation of electroencephalographic activity during non‐rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans , 1997, The Journal of physiology.

[87]  J. Rizzo,et al.  Suppression of melatonin secretion in some blind patients by exposure to bright light. , 1995, The New England journal of medicine.

[88]  N. Kleitman,et al.  STUDIES ON THE PHYSIOLOGY OF SLEEP , 1926 .

[89]  Simon Folkard,et al.  Multi-oscillatory control of circadian rhythms in human performance , 1983, Nature.

[90]  J. Aschoff,et al.  Human Circadian Rhythms in Continuous Darkness: Entrainment by Social Cues , 1971, Science.

[91]  K. Lushington,et al.  The rhythms of human sleep propensity and core body temperature , 1996, Journal of sleep research.

[92]  H. Berg Cold Spring Harbor Symposia on Quantitative Biology.: Vol. LII. Evolution of Catalytic Functions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1987, ISBN 0-87969-054-2, xix + 955 pp., US $150.00. , 1989 .

[93]  W. Dement,et al.  The effect of dream deprivation. , 1960, Science.

[94]  D J Foley,et al.  Sleep complaints among elderly persons: an epidemiologic study of three communities. , 1995, Sleep.

[95]  G. Pincus A Diurnal Rhythm in the Excretion of Urinary Ketosteroids by Young Men1 , 1943 .

[96]  C A Czeisler,et al.  Light exposure induces equivalent phase shifts of the endogenous circadian rhythms of circulating plasma melatonin and core body temperature in men. , 1991, The Journal of clinical endocrinology and metabolism.

[97]  J. Aschoff,et al.  Exogenous and endogenous components in circadian rhythms. , 1960, Cold Spring Harbor symposia on quantitative biology.

[98]  A. Winfree The geometry of biological time , 1991 .

[99]  C. Czeisler,et al.  Resetting the Melatonin Rhythm with Light in Humans , 1997, Journal of biological rhythms.

[100]  R. Kronauer,et al.  Phase‐shifting human circadian rhythms: influence of sleep timing, social contact and light exposure. , 1996, The Journal of physiology.

[101]  N. Kleitman,et al.  STUDIES ON THE PHYSIOLOGY OF SLEEP: VII. The Effect of the Position of the Body and of Sleep on Rectal Temperature in Man , 1933 .

[102]  T F Gallagher,et al.  Cortisol is secreted episodically by normal man. , 1970, The Journal of clinical endocrinology and metabolism.

[103]  S Folkard,et al.  Complex interaction of the sleep-wake cycle and circadian phase modulates mood in healthy subjects. , 1997, Archives of general psychiatry.

[104]  P. Lavie Melatonin: Role in Gating Nocturnal Rise in Sleep Propensity , 1997, Journal of biological rhythms.

[105]  DM Edgar,et al.  Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[106]  M. Carskadon,et al.  Multiple sleep latency tests during the constant routine. , 1992, Sleep.

[107]  W C Dement,et al.  Sleep studies on a 90-minute day. , 1975, Electroencephalography and clinical neurophysiology.

[108]  Miles Le,et al.  Sleep and aging. , 1980 .

[109]  J. N. Mills,et al.  Human circadian rhythms. , 1966, Physiological reviews.

[110]  J. Waterhouse,et al.  Adaptation to abrupt time shifts of the oscillator(s) controlling human circadian rhythms. , 1978, The Journal of physiology.

[111]  M. Menaker,et al.  Circadian Rhythms in Cultured Mammalian Retina , 1996, Science.

[112]  J. Waterhouse,et al.  Masking in humans: the problem and some attempts to solve it. , 1989, Chronobiology international.

[113]  D. Beersma,et al.  No impact of physical activity on the period of the circadian pacemaker in humans. , 1998, Chronobiology international.

[114]  C. Czeisler,et al.  Persistence of the circadian thyrotropin rhythm under constant conditions and after light-induced shifts of circadian phase. , 1994, The Journal of clinical endocrinology and metabolism.

[115]  Anna Wirz-Justice,et al.  A human phase-response curve to light , 1991, Neuroscience Letters.

[116]  A. Lewy,et al.  Circadian rhythm abnormalities in totally blind people: incidence and clinical significance. , 1992, The Journal of clinical endocrinology and metabolism.

[117]  J. Sassin,et al.  Effects of a prolonged 3-hour sleep-wake cycle on sleep stages, plasma cortisol, growth hormone and body temperature in man. , 1974, The Journal of clinical endocrinology and metabolism.

[118]  R. Kronauer,et al.  Exposure to bright light and darkness to treat physiologic maladaptation to night work. , 1990, The New England journal of medicine.

[119]  R. Kronauer,et al.  Refinement of a limit cycle oscillator model of the effects of light on the human circadian pacemaker. , 1998, Journal of theoretical biology.

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

[121]  R. Wever,et al.  Re-entrainment of circadian rhythms after phase-shifts of the Zeitgeber. , 1975, Chronobiologia.

[122]  S. Daan,et al.  Reduction of human sleep duration after bright light exposure in the morning , 1987, Neuroscience Letters.

[123]  J. Taub The Sleep-Wakefulness Cycle in Mexican Adults , 1971 .

[124]  D. Edgar Sleep-wake circadian rhythms and aging: Potential etiologies and relevance to age-related changes in integrated physiological systems , 1994, Neurobiology of Aging.

[125]  C. Czeisler,et al.  Episodic 24-hour cortisol secretory patterns in patients awaiting elective cardiac surgery. , 1976, The Journal of clinical endocrinology and metabolism.

[126]  D. Kupfer,et al.  Sleep of healthy seniors: a revisit. , 1985, Sleep.

[127]  H. Heller,et al.  Sleep homeostasis in suprachiasmatic nuclei-lesioned rats: effects of sleep deprivation and triazolam administration , 1992, Brain Research.

[128]  P. Badia,et al.  Changes in circadian rhythms and sleep quality with aging: Mechanisms and interventions , 1995, Neuroscience & Biobehavioral Reviews.

[129]  Richard E. Kronauer,et al.  Dose-response relationships for resetting of human circadian clock by light , 1996, Nature.

[130]  M. Byrne,et al.  Nocturnal exercise phase delays circadian rhythms of melatonin and thyrotropin secretion in normal men. , 1994, The American journal of physiology.

[131]  H. Agnew,et al.  Stage 4 Sleep: Influence of Time Course Variables , 1971, Science.

[132]  W. K. Honig Operant behavior : areas of research and application , 1966 .

[133]  P. Achermann,et al.  Sleep Homeostasis and Models of Sleep Regulation , 1999 .

[134]  A. Mant,et al.  Sleep patterns and problems in elderly general practice attenders: an Australian survey. , 2010, Community health studies.

[135]  D. Dijk,et al.  Dynamics of EEG slow-wave activity and core body temperature in human sleep after exposure to bright light. , 1992, Sleep.

[136]  The Sleep-Wake Pattern of Cortisol and Growth Hormone Secretion during Non-Entrained (Free-Running) Conditions in Man , 1981 .

[137]  S. Yen,et al.  Melatonin: a major regulator of the circadian rhythm of core temperature in humans. , 1992, The Journal of clinical endocrinology and metabolism.

[138]  Joseph F Rizzo,et al.  Nonphotic entrainment of the human circadian pacemaker. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[139]  A. Renold,et al.  Reaction of the adrenal cortex to physical and emotional stress in college oarsmen. , 1951, The New England journal of medicine.

[140]  C. Simon,et al.  Nocturnal oscillations in plasma renin activity and REM-NREM sleep cycles in humans: a common regulatory mechanism? , 1988, Sleep.

[141]  M. Wilson,et al.  Blind man living in normal society has circadian rhythms of 24.9 hours. , 1977, Science.

[142]  J. Palmblad,et al.  Adrenocortical and gonadal steroids during sleep deprivation. , 1980, Sleep.

[143]  T. Monk,et al.  Circadian Determinants of Subjective Alertness , 1989, Journal of biological rhythms.

[144]  Torbjörn Åkerstedt,et al.  Melatonin excretion, body temperature and subjective arousal during 64 hours of sleep deprivation , 1979, Psychoneuroendocrinology.

[145]  R. Wever,et al.  The Circadian System of Man: Results of Experiments Under Temporal Isolation , 1979 .

[146]  R. Wurtman,et al.  Studies of the 24 hour rhythm of melatonin in man. , 1978, Journal of neural transmission. Supplementum.

[147]  R. Kronauer,et al.  Bright light induction of strong (type 0) resetting of the human circadian pacemaker. , 1989, Science.

[148]  Richard E. Kronauer,et al.  Quantifying Human Circadian Pacemaker Response to Brief, Extended, and Repeated Light Stimuli over the Phototopic Range , 1999, Journal of biological rhythms.