PHYSIOLOGY OF SLEEP (REVIEW)–Interactions between stress and sleep: from basic research to clinical situations

Abstract Acute stress is a fundamental adaptive response which enables an organism to cope with daily threatening environmental stimuli. If prolonged and uncontrollable, the stress response may become inadequate and ultimately result in health damage. Animal models of stress in rodents indicate that both acute and chronic stressors have pronounced effects on sleep architecture and circadian rhythms. One major physiological response elicited by stress is activation of the hypothalamo-pituitary-adrenal axis. In both animals and humans, the hypothalamo-pituitary-adrenal axis plays an important role in sleep–wake regulation and in alterations of the sleep–wake cycle secondary to exposure to acute or chronic stressors. In humans, dysfunction of the neuroendocrine regulation of sleep can lead to severe sleep disturbances. The progressive decay of the hypothalamo-pituitary-adrenal axis in elderly people, which mimics chronic exposure to stress, may contribute to fragmented and unstable sleep in ageing. Shift workers, chronic insomniacs or patients suffering from mental disorders show abnormal hypothalamo-pituitary-adrenal secretory activity and concomitant sleep disturbances. Those sleep disorders and possible underlying mechanisms are briefly reviewed.

[1]  Raymond Cespuglio,et al.  Sleep and stress in man: an approach through exercise and exposure to extreme environments , 1998 .

[2]  O. Reeth Sleep and circadian disturbances in shift work: strategies for their management. , 1998 .

[3]  K. Polonsky,et al.  Modulation of glucose regulation and insulin secretion by circadian rhythmicity and sleep. , 1991, The Journal of clinical investigation.

[4]  P. Lavie,et al.  Long-term effects of extreme situational stress on sleep and dreaming. , 1987, The American journal of psychiatry.

[5]  C. Jouny,et al.  Pulsatile cortisol secretion and EEG delta waves are controlled by two independent but synchronized generators. , 1998, The American journal of physiology.

[6]  R. Sapolsky Why Stress Is Bad for Your Brain , 1996, Science.

[7]  Daniel J Buysse,et al.  Electroencephalographic sleep in spousal bereavement and bereavement-related depression of late life , 1992, Biological Psychiatry.

[8]  L. Solberg,et al.  Sleep in the Wistar‐Kyoto rat, a putative genetic animal model for depression , 2000, Neuroreport.

[9]  M. Uchiyama,et al.  Sleep and mood disorders. , 1997, Sleep medicine reviews.

[10]  B. McEwen Protective and damaging effects of stress mediators. , 1998, The New England journal of medicine.

[11]  H. Selye A Syndrome produced by Diverse Nocuous Agents , 1936, Nature.

[12]  M. Demitrack Neuroendocrine correlates of chronic fatigue syndrome: a brief review. , 1997, Journal of psychiatric research.

[13]  T. Åkerstedt,et al.  Sleep on the night shift: 24-hour EEG monitoring of spontaneous sleep/wake behavior. , 1989, Psychophysiology.

[14]  Simon Folkard,et al.  Models of Shiftwork and Health: An Examination of the Influence of Stress on Shiftwork Theory , 1997, Hum. Factors.

[15]  C. Kirschbaum,et al.  Burnout, perceived stress, and cortisol responses to awakening. , 1999, Psychosomatic medicine.

[16]  G. Brandenberger,et al.  Internal dissociation of the circadian markers of the cortisol rhythm in night workers. , 1996, The American journal of physiology.

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

[18]  N. Barden,et al.  Regulation of corticosteroid receptor gene expression in depression and antidepressant action. , 1999, Journal of psychiatry & neuroscience : JPN.

[19]  J. Krueger,et al.  Sleep: A Physiologic Role for IL‐1β and TNF‐α a , 1998, Annals of the New York Academy of Sciences.

[20]  A. Steiger,et al.  Effects of an ACTH/MSH(4–9) analog (HOE 427) on the sleep EEG and nocturnal hormonal secretion in humans , 1991, Peptides.

[21]  J. Valatx,et al.  Effect of intracerebroventricular administration of α‐helical CRH (9–41) on the sleep/waking cycle in rats under normal conditions or after subjection to an acute stressful stimulus , 1997, Journal of sleep research.

[22]  W. F. Waters,et al.  Attention, stress and negative emotion in persistent sleep-onset and sleep-maintenance insomnia. , 1993, Sleep.

[23]  M. Le Moal,et al.  Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress , 1995, Journal of Neuroscience.

[24]  F. Turek,et al.  The effects of short periods of immobilization on the hamster circadian clock , 1991, Brain Research.

[25]  D J Kupfer,et al.  Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol. , 1996, The Journal of clinical endocrinology and metabolism.

[26]  Perceptions of life stress and chronic insomnia in older adults. , 1995 .

[27]  K. Spiegel,et al.  Impact of sleep debt on metabolic and endocrine function , 1999, The Lancet.

[28]  J. Born,et al.  Hypothalamus-pituitary-adrenal activity during human sleep: a coordinating role for the limbic hippocampal system. , 2009, Experimental and clinical endocrinology & diabetes.

[29]  T. Seeman,et al.  Aging and hypothalamic-pituitary-adrenal response to challenge in humans. , 1994, Endocrine reviews.

[30]  M. Irwin,et al.  Impaired natural killer cell activity during bereavement , 1987, Brain, Behavior, and Immunity.

[31]  S. Maier,et al.  A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. , 1995, Endocrinology.

[32]  R. Geenen,et al.  Relationships between cardiovascular and immunological changes in an experimental stress model , 1995, Psychological Medicine.

[33]  R. Conley,et al.  Effects of antidepressant treatment on neuroactive steroids in major depression. , 1998, The American journal of psychiatry.

[34]  A. Wirz-Justice,et al.  Circadian Rhythms and Depression: Clinical and Experimental Models , 1997 .

[35]  D. Suchecki,et al.  Increased ACTH and corticosterone secretion induced by different methods of paradoxical sleep deprivation , 1998, Journal of sleep research.

[36]  D. Kupfer,et al.  Reduced cortisol latency in depressive illness. , 1983, Archives of general psychiatry.

[37]  K. Miczek,et al.  Long-term impairment of autonomic circadian rhythms after brief intermittent social stress , 1993, Physiology & Behavior.

[38]  C. Berridge,et al.  Stress-induced behaviors require the corticotropin-releasing hormone (CRH) receptor, but not CRH. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Kiecolt-Glaser,et al.  Psychoneuroimmunology and health consequences: data and shared mechanisms. , 1995, Psychosomatic medicine.

[40]  J W Mason,et al.  Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder. , 1993, The American journal of psychiatry.

[41]  C. Kirschbaum,et al.  The cortisol response to awakening in relation to different challenge tests and a 12-hour cortisol rhythm. , 1999, Life sciences.

[42]  E. van Cauter,et al.  Sleep loss results in an elevation of cortisol levels the next evening. , 1997, Sleep.

[43]  R. Cartwright,et al.  Adjustment disorders of sleep: The sleep effects of a major stressful event and its resolution , 1991, Psychiatry Research.

[44]  S. West,et al.  Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder. , 1999, The American journal of psychiatry.

[45]  H. Moldofsky,et al.  The relationship of interleukin‐1 and immune functions to sleep in humans. , 1986, Psychosomatic medicine.

[46]  S Maccari,et al.  Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. , 1999, Journal of neurobiology.

[47]  S. Daan,et al.  Social stress induces high intensity sleep in rats , 1997, Neuroscience Letters.

[48]  F. Holsboer,et al.  Altered hypothalamic-pituitary-adrenocortical regulation in healthy subjects at high familial risk for affective disorders. , 1995, Neuroendocrinology.

[49]  T. Smith,et al.  Electroencephalographic sleep and natural killer activity in depressed patients and control subjects. , 1992, Psychosomatic medicine.

[50]  H. Selye The Stress of Life , 1958 .

[51]  C E Speicher,et al.  Marital quality, marital disruption, and immune function. , 1987, Psychosomatic medicine.

[52]  F. Holsboer,et al.  Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives , 1999, Trends in Neurosciences.

[53]  D. Papanicolaou,et al.  Rapid eye movement sleep correlates with the overall activities of the hypothalamic-pituitary-adrenal axis and sympathetic system in healthy humans. , 1997, The Journal of clinical endocrinology and metabolism.

[54]  A. Muzet,et al.  Cortisol secretion is related to electroencephalographic alertness in human subjects during daytime wakefulness. , 1998, The Journal of clinical endocrinology and metabolism.

[55]  T M McLellan,et al.  Low doses of melatonin and diurnal effects on thermoregulation and tolerance to uncompensable heat stress. , 1999, Journal of applied physiology.

[56]  F. Abboud,et al.  Sympathetic-nerve activity during sleep in normal subjects. , 1993, The New England journal of medicine.

[57]  W. Schwartz Sleep science : integrating basic research and clinical practice , 1997 .

[58]  P. Willner,et al.  Changes in sleep architecture following chronic mild stress , 1997, Biological Psychiatry.

[59]  G. Brandenberger,et al.  Comparative effect of night and daytime sleep on the 24-hour cortisol secretory profile. , 1995, Sleep.

[60]  Jan Born,et al.  Timing the end of nocturnal sleep , 1999, Nature.

[61]  G. Brandenberger,et al.  Disturbances in Hormonal Profiles of Night Workers during Their Usual Sleep and Work Times , 1998, Journal of biological rhythms.

[62]  U. Knigge,et al.  Serotonergic involvement in stress-induced ACTH release , 1998, Brain Research.

[63]  F. Holsboer,et al.  The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety. , 1999, Journal of psychiatric research.

[64]  J. Krueger,et al.  Somnogenic relationships between tumor necrosis factor and interleukin-1. , 1999, The American journal of physiology.

[65]  Robert M. Sapolsky,et al.  Stress, the Aging Brain, and the Mechanisms of Neuron Death , 1992 .

[66]  R. Thisted,et al.  Sleep and Psychiatric Disorders: A Meta-analysis , 1992 .

[67]  N. Porter,et al.  Stress hormones and brain aging: adding injury to insult? , 1998, Nature Neuroscience.

[68]  E. D. de Kloet,et al.  Altered reactivity of the hypothalamic-pituitary-adrenal axis in the primary fibromyalgia syndrome. , 1993, The Journal of rheumatology.

[69]  B. McEwen,et al.  Stress and cognitive function , 1995, Current Opinion in Neurobiology.

[70]  M. Joëls,et al.  Brain corticosteroid receptor balance in health and disease. , 1998, Endocrine reviews.

[71]  C. Dugovic,et al.  Sleep-wakefulness patterns in the helpless rat , 1991, Physiology & Behavior.

[72]  P. Lavie,et al.  Elevated awaking thresholds during sleep: characteristics of chronic war-related posttraumatic stress disorder patients , 1998, Biological Psychiatry.

[73]  S. Checkley,et al.  Treatment of major depression with metyrapone and hydrocortisone. , 1995, Journal of affective disorders.

[74]  C. Bonnet,et al.  Influence of stress duration on the sleep rebound induced by immobilization in the rat: a possible role for corticosterone , 1999, Neuroscience.

[75]  T. Monk,et al.  Hours of work : temporal factors in work scheduling , 1985 .

[76]  N. Schneiderman,et al.  Posttraumatic Stress Symptoms, Intrusive Thoughts, Loss, and Immune Function after Hurricane Andrew , 1997, Psychosomatic medicine.

[77]  V. Baubet,et al.  Evidence for a sleep-promoting influence of stress. , 1995, Advances in neuroimmunology.

[78]  D. H. Stott Follow‐up Study from Birth of the Effects of Prenatal Stresses , 1973, Developmental medicine and child neurology.

[79]  Gillin Jc Are sleep disturbances risk factors for anxiety, depressive and addictive disorders? , 1998 .

[80]  M. Dallman,et al.  Feast and Famine: Critical Role of Glucocorticoids with Insulin in Daily Energy Flow , 1993, Frontiers in Neuroendocrinology.

[81]  G. Debilly,et al.  Influence of a 1 h immobilization stress on sleep states and corticotropin-like intermediate lobe peptide (CLIP or ACTH18–39, Ph-ACTH18–39) brain contents in the rat , 1997, Brain Research.

[82]  S. Ancoli-Israel,et al.  Identification and treatment of sleep problems in the elderly. , 1997, Sleep medicine reviews.

[83]  F. Turek,et al.  High Corticosterone Levels in Prenatally Stressed Rats Predict Persistent Paradoxical Sleep Alterations , 1999, The Journal of Neuroscience.

[84]  A. Guidotti,et al.  Fluoxetine-elicited changes in brain neurosteroid content measured by negative ion mass fragmentography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[85]  B. Lemmer,et al.  Physiology and Pharmacology of Biological Rhythms , 1997, Handbook of Experimental Pharmacology.

[86]  F. Goodwin,et al.  Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2) , 1988, The New England journal of medicine.

[87]  M. Roden,et al.  The circadian melatonin and cortisol secretion pattern in permanent night shift workers. , 1993, The American journal of physiology.

[88]  D. Swaab,et al.  Increased numbers of corticotropin-releasing hormone expressing neurons in the hypothalamic paraventricular nucleus of depressed patients. , 1994, Neuroendocrinology.

[89]  W. Cannon ORGANIZATION FOR PHYSIOLOGICAL HOMEOSTASIS , 1929 .

[90]  E. Bixler,et al.  Chronic insomnia and activity of the stress system: a preliminary study. , 1998, Journal of psychosomatic research.

[91]  M. Opp Corticotropin-releasing hormone involvement in stressor-induced alterations in sleep and in the regulation of waking. , 1995, Advances in neuroimmunology.

[92]  M. Johns,et al.  Relationship Between Sleep Habits, Adrenocortical Activity and Personality , 1971, Psychosomatic medicine.

[93]  Claude Gronfier,et al.  Twenty-four-hour melatonin and core body temperature rhythms: their adaptation in night workers. , 1997, The American journal of physiology.

[94]  D S Weiss,et al.  Sleep disturbances in the Vietnam generation: findings from a nationally representative sample of male Vietnam veterans. , 1998, The American journal of psychiatry.

[95]  G. Debilly,et al.  Role of the locus coeruleus in the sleep rebound following two different sleep deprivation methods in the rat , 1996, Brain Research.

[96]  D. Filipini,et al.  Possible use of glucocorticoid receptor antagonists in the treatment of major depression: preliminary results using RU 486. , 1993, Journal of psychiatry & neuroscience : JPN.

[97]  J. Muller,et al.  Circadian variation in cardiovascular events. , 1999, American journal of hypertension.

[98]  P. Linkowski,et al.  The dexamethasone suppression test and sleep electroencephalogram in nonbipolar major depressed inpatients: A multivariate analysis , 1998, Biological Psychiatry.

[99]  A. Steiger,et al.  The hypothalamic-pituitary-adrenocortical system and sleep in man. , 1995, Advances in neuroimmunology.

[100]  F. Holsboer,et al.  Prediction of medium-term outcome by cortisol response to the combined dexamethasone-CRH test in patients with remitted depression. , 1999, The American journal of psychiatry.

[101]  K. Felszeghy,et al.  Neuroendocrine and neurochemical consequences of long-term sleep deprivation in rats: similarities to some features of depression. , 1991, Homeostasis in health and disease : international journal devoted to integrative brain functions and homeostatic systems.

[102]  D. Dinges,et al.  Rapid eye movement sleep disturbance in posttraumatic stress disorder , 1994, Biological Psychiatry.

[103]  C. Reynolds,et al.  Sleep and affective disorders. A minireview. , 1987, The Psychiatric clinics of North America.

[104]  F. Turek,et al.  Stimulated activity mediates phase shifts in the hamster circadian clock induced by dark pulses or benzodiazepines , 1989, Nature.

[105]  Dumont,et al.  Sleep Quality of Former Night-shift Workers. , 1997, International journal of occupational and environmental health.