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Sleep Deprivation and Circadian Disruption Stress, Allostasis, and Allostatic Load

Published:April 23, 2022DOI:https://doi.org/10.1016/j.jsmc.2022.03.005

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      References

        • Sterling P.
        • Eyer J.
        Allostasis: a new paradigm to explain arousal pathology.
        in: Fisher S. Reason J. Handbook of life stress, cognition and health. John Wiley & Sons, New York1988: 629-649
        • McEwen B.S.
        • Stellar E.
        Stress and the individual: mechanisms leading to disease.
        Arch Intern Med. 1993; 153: 2093-2101
        • McEwen B.S.
        Protective and damaging effects of stress mediators.
        N Engl J Med. 1998; 338: 171-179
        • Munck A.
        • Guyre P.M.
        Glucocorticoids and immune function.
        in: Ader R. Felten D.L. Cohen N. Psychoneuroimmunology. Academic Press, San Diego (CA)1991: 447-474
        • Sapolsky R.M.
        Physiological and pathophysiological implications of social stress in mammals. Coping with the environment: neural and endocrine mechanisms.
        Oxford University Press, New York2000: 517-532
        • Borovikova L.V.
        • Ivanova S.
        • Zhang M.
        • et al.
        Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin.
        Nature. 2000; 405: 458-462
        • Bierhaus A.
        • Wolf J.
        • Andrassy M.
        • et al.
        A mechanism converting psychosocial stress into mononuclear cell activation.
        Proc Natl Acad Sci U S A. 2003; 100: 1920-1925
        • Sapolsky R.M.
        • Romero L.M.
        • Munck A.U.
        How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions.
        Endocr Rev. 2000; 21: 55-89
        • McEwen B.S.
        • Wingfield J.C.
        The concept of allostasis in biology and biomedicine.
        Horm Behav. 2003; 43: 2-15
        • McEwen B.S.
        Structural plasticity of the adult brain: how animal models help us understand brain changes in depression and systemic disorders related to depression.
        Dialogues Clin Neurosci. 2004; 6: 119-133
        • McEwen B.S.
        Mood disorders and allostatic load.
        Biol Psychiatry. 2003; 54: 200-207
        • Sheline Y.I.
        Neuroimaging studies of mood disorder effects on the brain.
        Biol Psychiatry. 2003; 54: 338-352
        • Pitman R.K.
        Hippocampal diminution in PTSD: more (or less?) than meets the eye.
        Hippocampus. 2001; 11: 73-74
        • Bremner J.D.
        Neuroimaging studies in posttraumatic stress disorder.
        Curr Psychiatry Rep. 2002; 4: 254-263
        • Butler M.P.
        • Kriegsfeld L.J.
        • Silver R.
        Circadian regulation of endocrine functions.
        in: Pfaff D. Arnold A. Etgen A. Hormones, brain and behavior. 2nd edition. Academic Press, San Diego (CA)2009: 473-505
        • Cearley C.
        • Churchill L.
        • Krueger J.M.
        Time of day differences in ILIbeta and TNFalpha mRNA levels in specific regions of the rat brain.
        Neurosci Lett. 2003; 352: 61-63
        • Lange T.
        • Dimitrov S.
        • Born J.
        Effects of sleep and circadian rhythm on the human immune system.
        Ann N Yacad Sci. 2010; 1193: 48-59
        • Jacobson L.
        • Akana S.F.
        • Cascio C.S.
        • et al.
        Circadian variations in plasma corticosterone permit normal termination of adrenocorticotropin responses to stress.
        Endocrinology. 1988; 122: 1343-1348
        • Boivin D.B.
        • Tremblay G.M.
        • James F.O.
        Working on atypical schedules.
        Sleep Med. 2007; 8: 578-589
        • Knutsson A.
        Health disorders of shift workers.
        Occup Med (Lond). 2003; 53: 103-108
        • Moore-Ede M.C.
        Physiology of the circadian timing system: predictive versus reactive homeostasis.
        Am J Phys. 1986; 250: R735-R752
        • Moore R.Y.
        • Eichler V.B.
        Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat.
        Brain Res. 1972; 42: 201-206
        • Klein D.C.
        • Moore R.Y.
        • Reppert S.M.
        Suprachiasmatic nucleus: the mind's clock.
        Oxford University Press, New York1991
        • Balsalobre A.
        • Brown S.A.
        • Marcacci L.
        • et al.
        Resetting of circadian time in peripheral tissues by glucocorticoid signaling.
        Science. 2000; 289: 2344-2347
        • Segall L.A.
        • Perrin J.S.
        • Walker C.D.
        • et al.
        Glucocorticoid rhythms control the rhythm of expression of the clock protein, Period2, in oval nucleus of the bed nucleus of the stria terminalis and central nucleus of the amygdala in rats.
        Neuroscience. 2006; 140: 753-757
        • Lamont E.W.
        • Robinson B.
        • Stewart J.
        • et al.
        The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2.
        Proc Natl Acad Sci U S A. 2005; 102: 4180-4184
        • Karatsoreos I.N.
        • McEwen B.S.
        Psychobiological allostasis: resistance, resilience and vulnerability.
        Trends Cogn Sci. 2011; 15: 576-584
        • Gilbertson M.W.
        • Paulus L.A.
        • Williston S.K.
        • et al.
        Neurocognitive function in monozygotic twins discordant for combat exposure: relationship to posttraumatic stress disorder.
        J Abnorm Psychol. 2006; 115: 484-495
        • Gilbertson M.W.
        • Shenton M.E.
        • Ciszewski A.
        • et al.
        Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma.
        Nat Neurosci. 2002; 5: 1242-1247
        • Yoo S.S.
        • Gujar N.
        • Hu P.
        • et al.
        The human emotional brain without sleep-a prefrontal amygdala disconnect.
        Curr Biol. 2007; 17: R877-R878
        • Gianaros P.J.
        • Jennings J.R.
        • Sheu L.K.
        • et al.
        Heightened functional neural activation to psychological stress covaries with exaggerated blood pressure reactivity.
        Hypertension. 2007; 49: 134-140
        • Gianaros P.J.
        • Sheu L.K.
        A review of neuroimaging studies of stressor-evoked blood pressure reactivity: emerging evidence for a brain-body pathway to coronary heart disease risk.
        Neuroimage. 2009; 47: 922-936
        • Gianaros P.J.
        • Sheu L.K.
        • Matthews K.A.
        • et al.
        Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala.
        J Neurosci. 2008; 28: 990-999
        • Karatsoreos I.N.
        • Bhagat S.
        • Bloss E.B.
        • et al.
        Disruption of circadian clocks has ramifications for metabolism, brain, and behavior.
        Proc Natl Acad Sci U S A. 2011; 108: 1657-1662
        • McEwen B.S.
        Effects of adverse experiences for brain structure and function.
        Biol Psychiatry. 2000; 48: 721-731
        • McEwen B.S.
        Protective and damaging effects of stress mediators: central role of the brain.
        Dialogues Clin Neurosci. 2006; 8: 367-381
        • McEwen B.S.
        • Coirini H.
        • Westlind-Danielsson A.
        • et al.
        Steroid hormones as mediators of neural plasticity.
        J Steroid Biochem Mol Biol. 1991; 39: 223-232
        • Davis S.
        • Mirick D.K.
        • Stevens R.G.
        Night shift work, light at night, and risk of breast cancer.
        J Natl Cancer Inst. 2001; 93: 1557-1562
        • Suwazono Y.
        • Dochi M.
        • Sakata K.
        • et al.
        A longitudinal study on the effect of shift work on weight gain in male Japanese workers.
        Obesity (Silver Spring). 2008; 16: 1887-1893
        • Lowden A.
        • Moreno C.
        • Holmback U.
        • et al.
        Eating and shift work - effects on habits, metabolism and performance.
        Scand J Work Environ Health. 2010; 36: 150-162
        • Leproult R.
        • Copinschi G.
        • Buxton O.
        • et al.
        Sleep loss results in an elevation of cortisol levels the next evening.
        Sleep. 1997; 20: 865-870
        • Spiegel K.
        • Leproult R.
        • Van Cauter E.
        Impact of sleep debt on metabolic and endocrine function.
        Lancet. 1999; 354: 1435-1439
        • Spiegel K.
        • Tasali E.
        • Penev P.
        • et al.
        Brief communication: sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite.
        Ann Intern Med. 2004; 141: 846-850
        • Gangwisch J.E.
        • Malaspina D.
        • Boden-Albala B.
        • et al.
        Inadequate sleep as a risk factor for obesity: analyses of the NHANES I.
        Sleep. 2005; 28: 1289-1296
        • Matthews K.A.
        • Dahl R.E.
        • Owens J.F.
        • et al.
        Sleep duration and insulin resistance in healthy black and white adolescents.
        Sleep. 2012; 35: 1353-1358
        • St-Onge M.P.
        • O'Keeffe M.
        • Roberts A.L.
        • et al.
        Short sleep duration, glucose dysregulation and hormonal regulation of appetite in men and women.
        Sleep. 2012; 35: 1503-1510
        • Vetrivelan R.
        • Fuller P.M.
        • Yokota S.
        • et al.
        Metabolic effects of chronic sleep restriction in rats.
        Sleep. 2012; 35: 1511-1520
        • Vgontzas A.N.
        • Zoumakis E.
        • Bixler E.O.
        • et al.
        Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines.
        J Clin Endocrinol Metab. 2004; 89: 2119-2126
        • Friedman E.M.
        • Hayney M.S.
        • Love G.D.
        • et al.
        Social relationships, sleep quality, and interleukin-6 in aging women.
        Proc Natl Acad Sci U S A. 2005; 102: 18757-18762
        • Pearson G.L.
        • Savenkova M.
        • Barnwell J.J.
        • et al.
        Circadian desynchronization alters metabolic and immune responses following lipopolysaccharide inoculation in male mice.
        Brain Behav Immun. 2020; 88: 220-229https://doi.org/10.1016/j.bbi.2020.05.033
        • Phillips D.J.
        • Savenkova M.I.
        • Karatsoreos I.N.
        Environmental disruption of the circadian clock leads to altered sleep and immune responses in mouse.
        Brain Behav Immun. 2015; 47: 14-23https://doi.org/10.1016/j.bbi.2014.12.008
        • Lewy A.J.
        • Lefler B.J.
        • Emens J.S.
        • et al.
        The circadian basis of winter depression.
        Proc Natl Acad Sci U S A. 2006; 103: 7414-7419
        • Karatsoreos I.N.
        Links between circadian rhythms and psychiatric disease.
        Front Behav Neurosci. 2014; 8: 162
        • Vogel G.W.
        • Thompson Jr., F.C.
        • Thurmond A.
        • et al.
        The effect of REM deprivation on depression.
        Psychosomatics. 1973; 14: 104-107
        • Wirz-Justice A.
        • Van den Hoofdakker R.H.
        Sleep deprivation in depression: what do we know, where do we go?.
        Biol Psychiatry. 1999; 46: 445-453
        • Kuhn M.
        • Maier J.G.
        • Wolf E.
        • et al.
        Indices of cortical plasticity after therapeutic sleep deprivation in patients with major depressive disorder.
        J Affect Disord. 2020; 277: 425-435https://doi.org/10.1016/j.jad.2020.08.052
        • Morley-Fletcher S.
        • Mairesse J.
        • Soumier A.
        • et al.
        Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats.
        Psychopharmacology. 2011; 217: 301-313
        • Keller J.
        • Flores B.
        • Gomez R.G.
        • et al.
        Cortisol circadian rhythm alterations in psychotic major depression.
        Biol Psychiatry. 2006; 60: 275-281
        • Rintamaki R.
        • Grimaldi S.
        • Englund A.
        • et al.
        Seasonal changes in mood and behavior are linked to metabolic syndrome.
        PLoS One. 2008; 3: e1482
        • Martino T.A.
        • OuditGY
        • Herzenberg A.M.
        • et al.
        Circadian rhythm disorganization produces profound cardiovascular and renal disease in hamsters.
        Am J Physiol Regul Integr Comp Physiol. 2008; 294: R1675-R1683
        • McEwen B.S.
        • Chattarji S.
        Molecular mechanisms of neuroplasticity and pharmacological implications: the example of tianeptine.
        Eur Neuropsychopharmacol. 2004; 14: S497-S502
        • Taishi P.
        • Chen Z.
        • Obal F.J.
        • et al.
        Sleep-associated changes in interleukin-1beta mRNA in the brain.
        J Interferon Cytokine Res. 1998; 18: 793-798
        • Clark R.A.
        • Valente A.J.
        Nuclear factor kappa B activation by NADPH oxidases.
        Mech Ageing Dev. 2004; 125: 799-810
        • Tang J.
        • Liu J.
        • Zhou C.
        • et al.
        Role of NADPH oxidase in the brain injury of intracerebral hemorrhage.
        J Neurochem. 2005; 94: 1342-1350
        • Silva R.H.
        • Abilio V.C.
        • Takatsu A.L.
        • et al.
        Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice.
        Neuropharmacology. 2004; 46: 895-903
        • Kong J.
        • Shepel P.N.
        • Holden C.P.
        • et al.
        Brain glycogen decreases with increased periods to wakefulness: implications for homeostatic drive to sleep.
        J Neurosci. 2002; 22: 5581-5587
        • Brown A.M.
        Brain glycogen re-awakened.
        J Neurochem. 2004; 89: 537-552
        • Wender R.
        • Brown A.M.
        • Fern R.
        • et al.
        Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter.
        J Neurosci. 2000; 20: 6804-6810
        • Youngblood B.D.
        • Zhou J.
        • Smagin G.N.
        • et al.
        Sleep deprivation by the “flower pot” technique and spatial reference memory.
        Physiol Behav. 1997; 61: 249-256
        • Kim E.Y.
        • Mahmoud G.S.
        • Grover L.M.
        REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus.
        Neurosci Lett. 2005; 388: 163-167
        • Graves L.A.
        • Heller E.A.
        • Pack A.I.
        • et al.
        Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning.
        Learn Mem. 2003; 10: 168-176
        • Guan Z.
        • Peng X.
        • Fang J.
        Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus.
        Brain Res. 2004; 1018: 38-47
        • Romcy-Pereira R.
        • Pavlides C.
        Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP.
        Eur J Neurosci. 2004; 20: 3453-3462
        • Lu H.J.
        • Lv J.
        β-Adrenergic receptor activity in the hippocampal dentate gyrus Participates in spatial learning and memory impairment in sleep-deprived rats.
        Exp Neurobiol. 2021; 30: 144-154
        • Vecsey C.G.
        • Huang T.
        • Abel T.
        Sleep deprivation impairs synaptic tagging in mouse hippocampal slices.
        Neurobiol Learn Mem. 2018; 154: 136-140
        • Wong L.W.
        • Chong Y.S.
        • Wong W.L.E.
        • et al.
        Inhibition of Histone Deacetylase Reinstates hippocampus-dependent long-term synaptic plasticity and associative memory in sleep-deprived mice.
        Cereb Cortex. 2020; 30: 4169-4182
        • de Paula H.M.
        • Hoshino K.
        Correlation between the fighting rates of REM sleep-deprived rats and susceptibility to the 'wild running' of audiogenic seizures.
        Brain Res. 2002; 926: 80-85
        • Musty R.E.
        • Consroe P.F.
        Phencyclidine produces aggressive behavior in rapid eye movement sleep- deprived rats.
        Life Sci. 1982; 30: 1733-1738
        • Russell J.W.
        • Singer G.
        Relations between muricide, circadian rhythm and consummatory behavior.
        Physiol Behav. 1983; 30: 23-27
        • Wood G.E.
        • Young L.T.
        • Reagan L.P.
        • et al.
        Acute and chronic restraint stress alter the incidence of social conflict in male rats.
        Horm Behav. 2003; 43: 205-213
        • Guzman-Marin R.
        • Suntsova N.
        • Stewart D.R.
        • et al.
        Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats.
        J Physiol. 2003; 549: 563-571
        • Rajizadeh M.A.
        • Esmaeilpour K.
        • Haghparast E.
        • et al.
        Voluntary exercise modulates learning & memory and synaptic plasticity impairments in sleep deprived female rats.
        Brain Res. 2020; 1729: 146598https://doi.org/10.1016/j.brainres.2019.146598
        • Roman V.
        • Van der Borght K.
        • Leemburg S.A.
        • et al.
        Sleep restriction by forced activity reduces hippocampal cell proliferation.
        Brain Res. 2005; 1065: 53-59
        • Hairston I.S.
        • Little M.T.
        • Scanlon M.D.
        • et al.
        Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning.
        J Neurophysiol. 2005; 94: 4224-4233
        • Prince T.M.
        • Wimmer M.
        • Choi J.
        • et al.
        Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory.
        Neurobiol Learn Mem. 2014; 109: 122-130
        • Ognjanovski N.
        • Maruyama D.
        • Lashner N.
        • et al.
        CA1 hippocampal network activity changes during sleep- dependent memory consolidation.
        Front Syst Neuro-sci. 2014; 8: 61
        • Aton S.J.
        • Seibt J.
        • Dumoulin M.
        • et al.
        Mechanisms of sleep-dependent consolidation of cortical plasticity.
        Neuron. 2009; 61: 454-466
        • Aton S.J.
        • Broussard C.
        • Dumoulin M.
        • et al.
        Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons.
        Proc Natl Acad Sci U S A. 2013; 110: 3101-3106
        • Aton S.J.
        • Suresh A.
        • Broussard C.
        • et al.
        Sleep promotes cortical response potentiation following visual experience.
        Sleep. 2014; 37: 1163-1170
        • Gais S.
        • Born J.
        Declarative memory consolidation: mechanisms acting during human sleep.
        Learn Mem. 2004; 11: 679-685
        • Atkinson G.
        • Davenne D.
        Relationships between sleep, physical activity and human health.
        Physiol Behav. 2007; 90: 229-236
        • Karlson B.
        • Eek F.C.
        • Hansen A.M.
        • et al.
        Diurnal Cortisol pattern of shift workers on workday and a day off.
        Scand J Work Environ Health. 2006; Suppl: 27-34
        • Cho K.
        Chronic 'jet lag' produces temporal lobe atrophy and spatial cognitive deficits.
        Nat Neurosci. 2001; 4: 567-568
        • Hendrickx H.
        • McEwen B.S.
        • van der Ouderaa F.
        Metabolism, mood and cognition in aging: the importance of lifestyle and dietary intervention.
        Neurobiol Aging. 2005; 26S: S1-S5
        • Gold S.M.
        • Dziobek I.
        • Sweat V.
        • et al.
        Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes.
        Diabetologia. 2007; 50: 711-719
        • Arvanitakis Z.
        • Wilson R.S.
        • Bienias J.L.
        • et al.
        Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function.
        Arch Neurol. 2004; 61: 661-666
        • Rasgon N.
        • Jarvik L.
        Insulin resistance, affective disorders, and Alzheimer's disease: review and hypothesis.
        J Gerontol. 2004; 59A: 178-183
        • Tsuno N.
        • Besset A.
        • Ritchie K.
        Sleep and depression.
        J Clin Psychiatry. 2005; 66: 1254-1269