Sleep deprivation and stress: a reciprocal relationship

Mathieu Nollet, William Wisden, Nicholas P Franks, Mathieu Nollet, William Wisden, Nicholas P Franks

Abstract

Sleep is highly conserved across evolution, suggesting vital biological functions that are yet to be fully understood. Animals and humans experiencing partial sleep restriction usually exhibit detrimental physiological responses, while total and prolonged sleep loss could lead to death. The perturbation of sleep homeostasis is usually accompanied by an increase in hypothalamic-pituitary-adrenal (HPA) axis activity, leading to a rise in circulating levels of stress hormones (e.g. cortisol in humans, corticosterone in rodents). Such hormones follow a circadian release pattern under undisturbed conditions and participate in the regulation of sleep. The investigation of the consequences of sleep deprivation, from molecular changes to behavioural alterations, has been used to study the fundamental functions of sleep. However, the reciprocal relationship between sleep and the activity of the HPA axis is problematic when investigating sleep using traditional sleep-deprivation protocols that can induce stress per se. This is especially true in studies using rodents in which sleep deprivation is achieved by exogenous, and potentially stressful, sensory-motor stimulations that can undoubtedly confuse their conclusions. While more research is needed to explore the mechanisms underlying sleep loss and health, avoiding stress as a confounding factor in sleep-deprivation studies is therefore crucial. This review examines the evidence of the intricate links between sleep and stress in the context of experimental sleep deprivation, and proposes a more sophisticated research framework for sleep-deprivation procedures that could benefit from recent progress in biotechnological tools for precise neuromodulation, such as chemogenetics and optogenetics, as well as improved automated real-time sleep-scoring algorithms.

Keywords: glucocorticoids; non-rapid eye movement sleep; rapid eye movement sleep.

Conflict of interest statement

We declare we have no competing interests.

© 2020 The Authors.

References

    1. Weber F, Dan Y. 2016. Circuit-based interrogation of sleep control. Nature 538, 51–59. (10.1038/nature19773)
    1. Franken P, Malafosse A, Tafti M. 1999. Genetic determinants of sleep regulation in inbred mice. Sleep 22, 155–169.
    1. Schmidt MH. 2014. The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness. Neurosci. Biobehav. Rev. 47, 122–153. (10.1016/j.neubiorev.2014.08.001)
    1. Albrecht U, Ripperger JA. 2018. Circadian clocks and sleep: impact of rhythmic metabolism and waste clearance on the brain. Trends Neurosci. 41, 677–688. (10.1016/j.tins.2018.07.007)
    1. Blaxton JM, Bergeman CS, Whitehead BR, Braun ME, Payne JD. 2017. Relationships among nightly sleep quality, daily stress, and daily affect. J. Gerontol. B Psychol. Sci. Soc. Sci. 72, 363–372.
    1. Tononi G, Cirelli C. 2014. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81, 12–34. (10.1016/j.neuron.2013.12.025)
    1. Bringmann H. 2019. Genetic sleep deprivation: using sleep mutants to study sleep functions. EMBO Rep. 20, e46807 (10.15252/embr.201846807)
    1. Cirelli C, Tononi G. 2008. Is sleep essential? PLoS Biol. 6, e216 (10.1371/journal.pbio.0060216)
    1. Colavito V, Fabene PF, Grassi-Zucconi G, Pifferi F, Lamberty Y, Bentivoglio M, Bertini G. 2013. Experimental sleep deprivation as a tool to test memory deficits in rodents. Front. Syst. Neurosci. 7, 106 (10.3389/fnsys.2013.00106)
    1. Longordo F, Kopp C, Luthi A. 2009. Consequences of sleep deprivation on neurotransmitter receptor expression and function. Eur. J. Neurosci. 29, 1810–1819. (10.1111/j.1460-9568.2009.06719.x)
    1. Bentivoglio M, Grassi-Zucconi G. 1997. The pioneering experimental studies on sleep deprivation. Sleep 20, 570–576. (10.1093/sleep/20.7.570)
    1. Waters F, Chiu V, Atkinson A, Blom JD. 2018. Severe sleep deprivation causes hallucinations and a gradual progression toward psychosis with increasing time awake. Front. Psychiatry 9, 303 (10.3389/fpsyt.2018.00303)
    1. Selye H. 1998. A syndrome produced by diverse nocuous agents. [Reprinted from Nature 1936; 138, 32.]. J. Neuropsychiatry Clin. Neurosci. 10, 230–231. (10.1176/jnp.10.2.230a)
    1. Mark J, Heiner L, Mandel P, Godin Y. 1969. Norepinephrine turnover in brain and stress reactions in rats during paradoxical sleep deprivation. Life Sci. 8, 1085–1093. (10.1016/0024-3205(69)90161-1)
    1. Kollar EJ, Slater GR, Palmer JO, Doctor RF, Mandell AJ. 1966. Stress in subjects undergoing sleep deprivation. Psychosom. Med. 28, 101–113. (10.1097/00006842-196603000-00002)
    1. Selye H. 1950. Stress and the general adaptation syndrome. Br. Med. J. 1, 1383–1392. (10.1136/bmj.1.4667.1383)
    1. Kvetnansky R, Pacak K, Fukuhara K, Viskupic E, Hiremagalur B, Nankova B, Goldstein DS, Sabban EL, Kopin IJ. 1995. Sympathoadrenal system in stress. Interaction with the hypothalamic-pituitary-adrenocortical system. Ann. N. Y. Acad. Sci. 771, 131–158. (10.1111/j.1749-6632.1995.tb44676.x)
    1. Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, Scheimann J, Myers B. 2016. Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr. Physiol. 6, 603–621. (10.1002/cphy.c150015)
    1. Son GH, Cha HK, Chung S, Kim K. 2018. Multimodal regulation of circadian glucocorticoid rhythm by central and adrenal clocks. J. Endocr. Soc. 2, 444–459. (10.1210/js.2018-00021)
    1. Kalsbeek A, van der Spek R, Lei J, Endert E, Buijs RM, Fliers E. 2012. Circadian rhythms in the hypothalamo-pituitary-adrenal (HPA) axis. Mol. Cell. Endocrinol. 349, 20–29. (10.1016/j.mce.2011.06.042)
    1. Born J, Spath-Schwalbe E, Schwakenhofer H, Kern W, Fehm HL. 1989. Influences of corticotropin-releasing hormone, adrenocorticotropin, and cortisol on sleep in normal man. J. Clin. Endocrinol. Metab. 68, 904–911. (10.1210/jcem-68-5-904)
    1. Gvilia I, Suntsova N, Kumar S, McGinty D, Szymusiak R. 2015. Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 309, R1092–R1100. (10.1152/ajpregu.00176.2015)
    1. Romanowski CP, Fenzl T, Flachskamm C, Wurst W, Holsboer F, Deussing JM, Kimura M. 2010. Central deficiency of corticotropin-releasing hormone receptor type 1 (CRH-R1) abolishes effects of CRH on NREM but not on REM sleep in mice. Sleep 33, 427–436. (10.1093/sleep/33.4.427)
    1. Bradbury MJ, Dement WC, Edgar DM. 1998. Effects of adrenalectomy and subsequent corticosterone replacement on rat sleep state and EEG power spectra. Am. J. Physiol. 275, R555–R565. (10.1152/ajpcell.1998.275.2.C555)
    1. Spath-Schwalbe E, Gofferje M, Kern W, Born J, Fehm HL. 1991. Sleep disruption alters nocturnal ACTH and cortisol secretory patterns. Biol. Psychiatry. 29, 575–584. (10.1016/0006-3223(91)90093-2)
    1. Follenius M, Brandenberger G, Bandesapt JJ, Libert JP, Ehrhart J. 1992. Nocturnal cortisol release in relation to sleep structure. Sleep 15, 21–27. (10.1093/sleep/15.1.21)
    1. Meerlo P, Sgoifo A, Suchecki D. 2008. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med. Rev. 12, 197–210. (10.1016/j.smrv.2007.07.007)
    1. Pejovic S, et al. 2013. Effects of recovery sleep after one work week of mild sleep restriction on interleukin-6 and cortisol secretion and daytime sleepiness and performance. Am. J. Physiol. Endocrinol. Metab. 305, E890–E896. (10.1152/ajpendo.00301.2013)
    1. Leproult R, Van Cauter E. 2011. Effect of 1 week of sleep restriction on testosterone levels in young healthy men. JAMA 305, 2173–2174. (10.1001/jama.2011.710)
    1. Voderholzer U, Piosczyk H, Holz J, Feige B, Loessl B, Kopasz M, Riemann D, Nissen C. 2012. The impact of increasing sleep restriction on cortisol and daytime sleepiness in adolescents. Neurosci. Lett. 507, 161–166. (10.1016/j.neulet.2011.12.014)
    1. Nedeltcheva AV, Kessler L, Imperial J, Penev PD. 2009. Exposure to recurrent sleep restriction in the setting of high caloric intake and physical inactivity results in increased insulin resistance and reduced glucose tolerance. J. Clin. Endocrinol. Metab. 94, 3242–3250. (10.1210/jc.2009-0483)
    1. Guyon A, Balbo M, Morselli LL, Tasali E, Leproult R, L'Hermite-Baleriaux M, Van Cauter E, Spiegel K. 2014. Adverse effects of two nights of sleep restriction on the hypothalamic-pituitary-adrenal axis in healthy men. J. Clin. Endocrinol. Metab. 99, 2861–2868. (10.1210/jc.2013-4254)
    1. Leproult R, Copinschi G, Buxton O, Van Cauter E. 1997. Sleep loss results in an elevation of cortisol levels the next evening. Sleep 20, 865–870.
    1. Reynolds AC, Dorrian J, Liu PY, Van Dongen HP, Wittert GA, Harmer LJ, Banks S. 2012. Impact of five nights of sleep restriction on glucose metabolism, leptin and testosterone in young adult men. PLoS ONE 7, e41218 (10.1371/journal.pone.0041218)
    1. Spiegel K, Leproult R, L'Hermite-Baleriaux M, Copinschi G, Penev PD, Van Cauter E. 2004. Leptin levels are dependent on sleep duration: relationships with sympathovagal balance, carbohydrate regulation, cortisol, and thyrotropin. J. Clin. Endocrinol. Metab. 89, 5762–5771. (10.1210/jc.2004-1003)
    1. Spiegel K, Leproult R, Van Cauter E. 1999. Impact of sleep debt on metabolic and endocrine function. Lancet 354, 1435–1439. (10.1016/S0140-6736(99)01376-8)
    1. Omisade A, Buxton OM, Rusak B. 2010. Impact of acute sleep restriction on cortisol and leptin levels in young women. Physiol. Behav. 99, 651–656. (10.1016/j.physbeh.2010.01.028)
    1. Guyon A, Morselli LL, Balbo ML, Tasali E, Leproult R, L'Hermite-Baleriaux M, Van Cauter E, Spiegel K. 2017. Effects of insufficient sleep on pituitary-adrenocortical response to CRH stimulation in healthy men. Sleep 40, zsx064 (10.1093/sleep/zsx064)
    1. Abell JG, Shipley MJ, Ferrie JE, Kivimaki M, Kumari M. 2016. Recurrent short sleep, chronic insomnia symptoms and salivary cortisol: a 10-year follow-up in the Whitehall II study. Psychoneuroendocrinology 68, 91–99. (10.1016/j.psyneuen.2016.02.021)
    1. Weitzman ED, Zimmerman JC, Czeisler CA, Ronda J. 1983. Cortisol secretion is inhibited during sleep in normal man. J. Clin. Endocrinol. Metab. 56, 352–358. (10.1210/jcem-56-2-352)
    1. Wu H, Zhao Z, Stone WS, Huang L, Zhuang J, He B, Zhang P, Li Y. 2008. Effects of sleep restriction periods on serum cortisol levels in healthy men. Brain Res. Bull. 77, 241–245. (10.1016/j.brainresbull.2008.07.013)
    1. Leproult R, Colecchia EF, L'Hermite-Baleriaux M, Van Cauter E. 2001. Transition from dim to bright light in the morning induces an immediate elevation of cortisol levels. J. Clin. Endocrinol. Metab. 86, 151–157. (10.1210/jc.86.1.151)
    1. Gil-Lozano M, Hunter PM, Behan LA, Gladanac B, Casper RF, Brubaker PL. 2016. Short-term sleep deprivation with nocturnal light exposure alters time-dependent glucagon-like peptide-1 and insulin secretion in male volunteers. Am. J. Physiol. Endocrinol. Metab. 310, E41–E50. (10.1152/ajpendo.00298.2015)
    1. Schussler P, Uhr M, Ising M, Weikel JC, Schmid DA, Held K, Mathias S, Steiger A. 2006. Nocturnal ghrelin, ACTH, GH and cortisol secretion after sleep deprivation in humans. Psychoneuroendocrinology 31, 915–923. (10.1016/j.psyneuen.2006.05.002)
    1. Chapotot F, Buguet A, Gronfier C, Brandenberger G. 2001. Hypothalamo-pituitary-adrenal axis activity is related to the level of central arousal: effect of sleep deprivation on the association of high-frequency waking electroencephalogram with cortisol release. Neuroendocrinology 73, 312–321. (10.1159/000054648)
    1. von Treuer K, Norman TR, Armstrong SM. 1996. Overnight human plasma melatonin, cortisol, prolactin, TSH, under conditions of normal sleep, sleep deprivation, and sleep recovery. J. Pineal Res. 20, 7–14. (10.1111/j.1600-079X.1996.tb00232.x)
    1. Benedict C, Hallschmid M, Lassen A, Mahnke C, Schultes B, Schioth HB, Born J, Lange T. 2011. Acute sleep deprivation reduces energy expenditure in healthy men. Am. J. Clin. Nutr. 93, 1229–1236. (10.3945/ajcn.110.006460)
    1. Vgontzas AN, Mastorakos G, Bixler EO, Kales A, Gold PW, Chrousos GP. 1999. Sleep deprivation effects on the activity of the hypothalamic-pituitary-adrenal and growth axes: potential clinical implications. Clin. Endocrinol. (Oxf.) 51, 205–215. (10.1046/j.1365-2265.1999.00763.x)
    1. Cedernaes J, Osler ME, Voisin S, Broman JE, Vogel H, Dickson SL, Zierath JR, Schioth HB,, Benedict C. 2015. Acute sleep loss induces tissue-specific epigenetic and transcriptional alterations to circadian clock genes in men. J. Clin. Endocrinol. Metab. 100, E1255–E1261. (10.1210/JC.2015-2284)
    1. Klumpers UM, Veltman DJ, van Tol MJ, Kloet RW, Boellaard R, Lammertsma AA, Hoogendijk WJG. 2015. Neurophysiological effects of sleep deprivation in healthy adults, a pilot study. PLoS ONE 10, e0116906 (10.1371/journal.pone.0116906)
    1. Vargas I, Lopez-Duran N. 2017. The cortisol awakening response after sleep deprivation: is the cortisol awakening response a ‘response’ to awakening or a circadian process? J. Health Psychol. 1359105317738323 (10.1177/1359105317738323)
    1. Trivedi MS, Holger D, Bui AT, Craddock TJA, Tartar JL. 2017. Short-term sleep deprivation leads to decreased systemic redox metabolites and altered epigenetic status. PLoS ONE 12, e0181978 (10.1371/journal.pone.0181978)
    1. Born J, Schenk U, Spath-Schwalbe E, Fehm HL. 1988. Influences of partial REM sleep deprivation and awakenings on nocturnal cortisol release. Biol. Psychiatry 24, 801–811. (10.1016/0006-3223(88)90256-9)
    1. Stamatakis KA, Punjabi NM. 2010. Effects of sleep fragmentation on glucose metabolism in normal subjects. Chest 137, 95–101. (10.1378/chest.09-0791)
    1. Chennaoui M, et al. 2011. Effect of one night of sleep loss on changes in tumor necrosis factor alpha (TNF-alpha) levels in healthy men. Cytokine 56, 318–324. (10.1016/j.cyto.2011.06.002)
    1. Pejovic S, Vgontzas AN, Basta M, Tsaoussoglou M, Zoumakis E, Vgontzas A, Bixler E, Chrousos G. 2010. Leptin and hunger levels in young healthy adults after one night of sleep loss. J. Sleep Res. 19, 552–558. (10.1111/j.1365-2869.2010.00844.x)
    1. Honma A, Revell VL, Gunn PJ, Davies SK, Middleton B, Raynaud FI, Skene DJ. 2020. Effect of acute total sleep deprivation on plasma melatonin, cortisol and metabolite rhythms in females. Eur. J. Neurosci. 51, 366–378. (10.1111/ejn.14411)
    1. Schwarz J, Gerhardsson A, van Leeuwen W, Lekander M, Ericson M, Fischer H, Kecklund G, Åkerstedt T. 2018. Does sleep deprivation increase the vulnerability to acute psychosocial stress in young and older adults? Psychoneuroendocrinology 96, 155–165. (10.1016/j.psyneuen.2018.06.003)
    1. Vargas I, Lopez-Duran N. 2017. Investigating the effect of acute sleep deprivation on hypothalamic-pituitary-adrenal-axis response to a psychosocial stressor. Psychoneuroendocrinology 79, 1–8. (10.1016/j.psyneuen.2017.01.030)
    1. Massar SAA, Liu JCJ, Mohammad NB, Chee MWL. 2017. Poor habitual sleep efficiency is associated with increased cardiovascular and cortisol stress reactivity in men. Psychoneuroendocrinology 81, 151–156. (10.1016/j.psyneuen.2017.04.013)
    1. Bassett SM, Lupis SB, Gianferante D, Rohleder N, Wolf JM. 2015. Sleep quality but not sleep quantity effects on cortisol responses to acute psychosocial stress. Stress 18, 638–644. (10.3109/10253890.2015.1087503)
    1. Steiger A. 2002. Sleep and the hypothalamo-pituitary-adrenocortical system. Sleep Med. Rev. 6, 125–138. (10.1053/smrv.2001.0159)
    1. Buckley TM, Schatzberg AF. 2005. On the interactions of the hypothalamic-pituitary-adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rhythm, exemplary sleep disorders. J. Clin. Endocrinol. Metab. 90, 3106–3114. (10.1210/jc.2004-1056)
    1. Pawlyk AC, Morrison AR, Ross RJ, Brennan FX. 2008. Stress-induced changes in sleep in rodents: models and mechanisms. Neurosci. Biobehav. Rev. 32, 99–117. (10.1016/j.neubiorev.2007.06.001)
    1. Kim EJ, Dimsdale JE. 2007. The effect of psychosocial stress on sleep: a review of polysomnographic evidence. Behav. Sleep Med. 5, 256–278. (10.1080/15402000701557383)
    1. Mendelson W, Guthrie RD, Guynn R, Harris RL, Wyatt RJ. 1974. Rapid eye movement (REM) sleep deprivation, stress and intermediary metabolism. J. Neurochem. 22, 1157–1159. (10.1111/j.1471-4159.1974.tb04353.x)
    1. Stern WC, Miller FP, Cox RH, Maickel RP. 1971. Brain norepinephrine and serotonin levels following REM sleep deprivation in the rat. Psychopharmacologia 22, 50–55. (10.1007/BF00401466)
    1. Stefurak SJ, Stefurak ML, Mendelson WB, Gillin JC, Wyatt RJ. 1977. A method for sleep depriving rats. Pharmacol. Biochem. Behav. 6, 137–139. (10.1016/0091-3057(77)90169-1)
    1. Levitt RA. 1966. Sleep deprivation in the rat. Science 153, 85–87. (10.1126/science.153.3731.85)
    1. Ferguson J, Dement W. 1967. The effect of variations in total sleep time on the occurrence of rapid eye movement sleep in cats. Electroencephalogr Clin. Neurophysiol. 22, 2–10. (10.1016/0013-4694(67)90003-X)
    1. Tobler I, Murison R, Ursin R, Ursin H, Borbely AA. 1983. The effect of sleep deprivation and recovery sleep on plasma corticosterone in the rat. Neurosci. Lett. 35, 297–300. (10.1016/0304-3940(83)90333-6)
    1. Roman V, Hagewoud R, Luiten PG, Meerlo P. 2006. Differential effects of chronic partial sleep deprivation and stress on serotonin-1A and muscarinic acetylcholine receptor sensitivity. J. Sleep Res. 15, 386–394. (10.1111/j.1365-2869.2006.00555.x)
    1. Campbell IG, Guinan MJ, Horowitz JM. 2002. Sleep deprivation impairs long-term potentiation in rat hippocampal slices. J. Neurophysiol. 88, 1073–1076. (10.1152/jn.2002.88.2.1073)
    1. Tartar JL, Ward CP, Cordeira JW, Legare SL, Blanchette AJ, McCarley RW, Strecker RE. 2009. Experimental sleep fragmentation and sleep deprivation in rats increases exploration in an open field test of anxiety while increasing plasma corticosterone levels. Behav. Brain Res. 197, 450–453. (10.1016/j.bbr.2008.08.035)
    1. Sgoifo A, Buwalda B, Roos M, Costoli T, Merati G, Meerlo P. 2006. Effects of sleep deprivation on cardiac autonomic and pituitary-adrenocortical stress reactivity in rats. Psychoneuroendocrinology 31, 197–208. (10.1016/j.psyneuen.2005.06.009)
    1. Meerlo P, Koehl M, van der Borght K, Turek FW. 2002. Sleep restriction alters the hypothalamic-pituitary-adrenal response to stress. J. Neuroendocrinol. 14, 397–402. (10.1046/j.0007-1331.2002.00790.x)
    1. McCarthy A, Loomis S, Eastwood B, Wafford KA, Winsky-Sommerer R, Gilmour G. 2017. Modelling maintenance of wakefulness in rats: comparing potential non-invasive sleep-restriction methods and their effects on sleep and attentional performance. J. Sleep Res. 26, 179–187. (10.1111/jsr.12464)
    1. Dispersyn G, Sauvet F, Gomez-Merino D, Ciret S, Drogou C, Leger D, Gallopin T, Chennaoui M. 2017. The homeostatic and circadian sleep recovery responses after total sleep deprivation in mice. J. Sleep Res. 26, 531–538. (10.1111/jsr.12541)
    1. Feng L, Wu HW, Song GQ, Lu C, Li YH, Qu LN, Chen S, Liu X, Chang Q. 2016. Chronical sleep interruption-induced cognitive decline assessed by a metabolomics method. Behav. Brain Res. 302, 60–68. (10.1016/j.bbr.2015.12.039)
    1. Pierard C, et al. 2007. Modafinil restores memory performance and neural activity impaired by sleep deprivation in mice. Pharmacol. Biochem. Behav. 88, 55–63. (10.1016/j.pbb.2007.07.006)
    1. Pierard C, Liscia P, Chauveau F, Coutan M, Corio M, Krazem A, Beracochea D. 2011. Differential effects of total sleep deprivation on contextual and spatial memory: modulatory effects of modafinil. Pharmacol. Biochem. Behav. 97, 399–405. (10.1016/j.pbb.2010.09.016)
    1. Fenzl T, Romanowski CP, Flachskamm C, Honsberg K, Boll E, Hoehne A, Kimura M. 2007. Fully automated sleep deprivation in mice as a tool in sleep research. J. Neurosci. Methods. 166, 229–235. (10.1016/j.jneumeth.2007.07.007)
    1. Bergmann BM, Everson CA, Kushida CA, Fang VS, Leitch CA, Schoeller DA, Refetoff S, Rechtschaffen A. 1989. Sleep deprivation in the rat: V. Energy use and mediation. Sleep 12, 31–41. (10.1093/sleep/12.1.31)
    1. Rechtschaffen A, Bergmann BM. 1995. Sleep deprivation in the rat by the disk-over-water method. Behav. Brain Res. 69, 55–63. (10.1016/0166-4328(95)00020-T)
    1. Rechtschaffen A, Gilliland MA, Bergmann BM, Winter JB. 1983. Physiological correlates of prolonged sleep deprivation in rats. Science 221, 182–184. (10.1126/science.6857280)
    1. Everson CA, Bergmann BM, Rechtschaffen A. 1989. Sleep deprivation in the rat: III. Total sleep deprivation. Sleep 12, 13–21. (10.1093/sleep/12.1.13)
    1. Everson CA, Crowley WR. 2004. Reductions in circulating anabolic hormones induced by sustained sleep deprivation in rats. Am. J. Physiol. Endocrinol. Metab. 286, E1060–E1070. (10.1152/ajpendo.00553.2003)
    1. Everson CA, Szabo A. 2011. Repeated exposure to severely limited sleep results in distinctive and persistent physiological imbalances in rats. PLoS ONE 6, e22987 (10.1371/journal.pone.0022987)
    1. Lopez-Rodriguez F, Kim J, Poland RE. 2004. Total sleep deprivation decreases immobility in the forced-swim test. Neuropsychopharmacology 29, 1105–1111. (10.1038/sj.npp.1300406)
    1. Yang CK, Tsai HD, Wu CH, Cho CL. 2019. The role of glucocorticoids in ovarian development of sleep deprived rats. Taiwan. J. Obstet. Gynecol. 58, 122–127. (10.1016/j.tjog.2018.11.023)
    1. Ringgold KM, Barf RP, George A, Sutton BC, Opp MR. 2013. Prolonged sleep fragmentation of mice exacerbates febrile responses to lipopolysaccharide. J. Neurosci. Methods. 219, 104–112. (10.1016/j.jneumeth.2013.07.008)
    1. Leenaars CH, Dematteis M, Joosten RN, Eggels L, Sandberg H, Schirris M, Feenstra MGP, Van Someren EJW. 2011. A new automated method for rat sleep deprivation with minimal confounding effects on corticosterone and locomotor activity. J. Neurosci. Methods. 196, 107–117. (10.1016/j.jneumeth.2011.01.014)
    1. Ramesh V, Kaushal N, Gozal D. 2009. Sleep fragmentation differentially modifies EEG delta power during slow wave sleep in socially isolated and paired mice. Sleep Sci. 2, 64–75,
    1. Yonglin G, Brandon A, Michael BR, Rif SE-M. 2017. Corticosterone response in sleep deprivation and sleep fragmentation. J. Sleep Disord. Manage. 3, 018 (10.23937/2572-4053.1510018)
    1. Dumaine JE, Ashley NT. 2015. Acute sleep fragmentation induces tissue-specific changes in cytokine gene expression and increases serum corticosterone concentration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 308, R1062–R1069. (10.1152/ajpregu.00049.2015)
    1. Wallace E, et al. 2015. Differential effects of duration of sleep fragmentation on spatial learning and synaptic plasticity in pubertal mice. Brain Res. 1615, 116–128. (10.1016/j.brainres.2015.04.037)
    1. Endo T, Schwierin B, Borbely AA, Tobler I. 1997. Selective and total sleep deprivation: effect on the sleep EEG in the rat. Psychiatry Res. 66, 97–110. (10.1016/S0165-1781(96)03029-6)
    1. Franken P, Dijk DJ, Tobler I, Borbely AA. 1991. Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am. J. Physiol. 261, R198–R208.
    1. Tobler I, Deboer T, Fischer M. 1997. Sleep and sleep regulation in normal and prion protein-deficient mice. J. Neurosci. 17, 1869–1879. (10.1523/JNEUROSCI.17-05-01869.1997)
    1. Mongrain V, Hernandez SA, Pradervand S, Dorsaz S, Curie T, Hagiwara G, Gip P, Heller HC, Franken P. 2010. Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis. Sleep 33, 1147–1157. (10.1093/sleep/33.9.1147)
    1. Sanchez-Alavez M, Conti B, Moroncini G, Criado JR. 2007. Contributions of neuronal prion protein on sleep recovery and stress response following sleep deprivation. Brain Res. 1158, 71–80. (10.1016/j.brainres.2007.05.010)
    1. Palchykova S, Winsky-Sommerer R, Meerlo P, Durr R, Tobler I. 2006. Sleep deprivation impairs object recognition in mice. Neurobiol. Learn. Mem. 85, 263–271. (10.1016/j.nlm.2005.11.005)
    1. Hagewoud R, Havekes R, Novati A, Keijser JN, Van der Zee EA, Meerlo P. 2010. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J. Sleep Res. 19, 280–288. (10.1111/j.1365-2869.2009.00799.x)
    1. Naidoo N, Davis JG, Zhu J, Yabumoto M, Singletary K, Brown M, Galante R, Agarwal B, Baur JA. 2014. Aging and sleep deprivation induce the unfolded protein response in the pancreas: implications for metabolism. Aging Cell 13, 131–141. (10.1111/acel.12158)
    1. Onaolapo JO, Onaolapo YA, Akanmu AM, Olayiwola G. 2016. Caffeine and sleep-deprivation mediated changes in open-field behaviours, stress response and antioxidant status in mice. Sleep Sci. 9, 236–243. (10.1016/j.slsci.2016.10.008)
    1. Kawakami M, Kimura F, Tsai CW. 1983. Correlation of growth hormone secretion to sleep in the immature rat. J. Physiol. 339, 325–337. (10.1113/jphysiol.1983.sp014719)
    1. Zant JC, Leenaars CH, Kostin A, Van Someren EJ, Porkka-Heiskanen T. 2011. Increases in extracellular serotonin and dopamine metabolite levels in the basal forebrain during sleep deprivation. Brain Res. 1399, 40–48. (10.1016/j.brainres.2011.05.008)
    1. Gip P, Hagiwara G, Sapolsky RM, Cao VH, Heller HC, Ruby NF. 2004. Glucocorticoids influence brain glycogen levels during sleep deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R1057–R1062. (10.1152/ajpregu.00528.2003)
    1. Melgarejo-Gutierrez M, Acosta-Pena E, Venebra-Munoz A, Escobar C, Santiago-Garcia J, Garcia-Garcia F. 2013. Sleep deprivation reduces neuroglobin immunoreactivity in the rat brain. Neuroreport 24, 120–125. (10.1097/WNR.0b013e32835d4b74)
    1. Hairston IS, Ruby NF, Brooke S, Peyron C, Denning DP, Heller HC, Sapolsky RM. 2001. Sleep deprivation elevates plasma corticosterone levels in neonatal rats. Neurosci. Lett. 315, 29–32. (10.1016/S0304-3940(01)02309-6)
    1. Meerlo P, Turek FW. 2001. Effects of social stimuli on sleep in mice: non-rapid-eye-movement (NREM) sleep is promoted by aggressive interaction but not by sexual interaction. Brain Res. 907, 84–92. (10.1016/S0006-8993(01)02603-8)
    1. Kopp C, Longordo F, Nicholson JR, Luthi A. 2006. Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. J. Neurosci. 26, 12 456–12 465. (10.1523/JNEUROSCI.2702-06.2006)
    1. Kalinchuk AV, McCarley RW, Porkka-Heiskanen T, Basheer R. 2010. Sleep deprivation triggers inducible nitric oxide-dependent nitric oxide production in wake-active basal forebrain neurons. J. Neurosci. 30, 13 254–13 264. (10.1523/JNEUROSCI.0014-10.2010)
    1. Longordo F, Fan J, Steimer T, Kopp C, Luthi A. 2011. Do mice habituate to ‘gentle handling?’ A comparison of resting behavior, corticosterone levels and synaptic function in handled and undisturbed C57BL/6. J. Mice. Sleep 34, 679–681. (10.1093/sleep/34.5.679)
    1. Vecsey CG, Wimmer ME, Havekes R, Park AJ, Perron IJ, Meerlo P, Abel T, 2013. Daily acclimation handling does not affect hippocampal long-term potentiation or cause chronic sleep deprivation in mice. Sleep 36, 601–607. (10.5665/sleep.2556)
    1. van Driel KS, Talling JC. 2005. Familiarity increases consistency in animal tests. Behav. Brain Res. 159, 243–245. (10.1016/j.bbr.2004.11.005)
    1. Sorge RE, et al. 2014. Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat. Methods 11, 629–632. (10.1038/nmeth.2935)
    1. Cirelli C, Faraguna U, Tononi G. 2006. Changes in brain gene expression after long-term sleep deprivation. J. Neurochem. 98, 1632–1645. (10.1111/j.1471-4159.2006.04058.x)
    1. Cirelli C, Tononi G. 2000. Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J. Neurosci. 20, 9187–9194. (10.1523/JNEUROSCI.20-24-09187.2000)
    1. Gompf HS, Mathai C, Fuller PM, Wood DA, Pedersen NP, Saper CB, Lu J. 2010. Locus ceruleus and anterior cingulate cortex sustain wakefulness in a novel environment. J. Neurosci. 30, 14 543–14 551. (10.1523/JNEUROSCI.3037-10.2010)
    1. Bellesi M, de Vivo L, Chini M, Gilli F, Tononi G, Cirelli C. 2017. Sleep loss promotes astrocytic phagocytosis and microglial activation in mouse cerebral cortex. J. Neurosci. 37, 5263–5273. (10.1523/JNEUROSCI.3981-16.2017)
    1. Penalva RG, Lancel M, Flachskamm C, Reul JM, Holsboer F, Linthorst AC. 2003. Effect of sleep and sleep deprivation on serotonergic neurotransmission in the hippocampus: a combined in vivo microdialysis/EEG study in rats. Eur. J. Neurosci. 17, 1896–1906. (10.1046/j.1460-9568.2003.02612.x)
    1. Kopp C, Longordo F, Luthi A. 2007. Experience-dependent changes in NMDA receptor composition at mature central synapses. Neuropharmacology 53, 1–9. (10.1016/j.neuropharm.2007.03.014)
    1. Jouvet D, Vimont P, Delorme F. 1964. Study of selective deprivation of the paradoxal phase of sleep in the cat. J. Physiol. (Paris) 56, 381.
    1. Mendelson WB, Guthrie RD, Frederick G, Wyatt RJ. 1974. The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol. Biochem. Behav. 2, 553–556. (10.1016/0091-3057(74)90018-5)
    1. Morden B, Mitchell G, Dement W. 1967. Selective REM sleep deprivation and compensation phenomena in the rat. Brain Res. 5, 339–349. (10.1016/0006-8993(67)90042-X)
    1. Murison R, Ursin R, Coover GD, Lien W, Ursin H. 1982. Sleep deprivation procedure produces stomach lesions in rats. Physiol. Behav. 29, 693–694. (10.1016/0031-9384(82)90240-2)
    1. Galvão MD, Sinigaglia-Coimbra R, Kawakami SE, Tufik S, Suchecki D. 2009. Paradoxical sleep deprivation activates hypothalamic nuclei that regulate food intake and stress response. Psychoneuroendocrinology 34, 1176–1183. (10.1016/j.psyneuen.2009.03.003)
    1. Kim EY, Mahmoud GS, Grover LM. 2005. REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus. Neurosci. Lett. 388, 163–167. (10.1016/j.neulet.2005.06.057)
    1. Machado RB, Tufik S, Suchecki D. 2008. Chronic stress during paradoxical sleep deprivation increases paradoxical sleep rebound: association with prolactin plasma levels and brain serotonin content. Psychoneuroendocrinology 33, 1211–1224. (10.1016/j.psyneuen.2008.06.007)
    1. Mathangi DC, Shyamala R, Subhashini AS. 2012. Effect of REM sleep deprivation on the antioxidant status in the brain of Wistar rats. Ann. Neurosci. 19, 161–164. (10.5214/ans.0972.7531.190405)
    1. Sallanon-Moulin M, Touret M, Didier-Bazes M, Roudier V, Fages C, Tardy M, Jouvet M. 1994. Glutamine synthetase modulation in the brain of rats subjected to deprivation of paradoxical sleep. Brain Res. Mol. Brain Res. 22, 113–120. (10.1016/0169-328X(94)90038-8)
    1. Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB. 1997. Sleep deprivation by the ‘flower pot’ technique and spatial reference memory. Physiol. Behav. 61, 249–256. (10.1016/S0031-9384(96)00363-0)
    1. Mirescu C, Peters JD, Noiman L, Gould E. 2006. Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc. Natl Acad. Sci. USA 103, 19 170–19 175. (10.1073/pnas.0608644103)
    1. Machado RB, Tufik S, Suchecki D. 2013. Role of corticosterone on sleep homeostasis induced by REM sleep deprivation in rats. PLoS ONE 8, e63520 (10.1371/journal.pone.0063520)
    1. van Hulzen ZJ, Coenen AM. 1981. Paradoxical sleep deprivation and locomotor activity in rats. Physiol. Behav. 27, 741–744. (10.1016/0031-9384(81)90250-X)
    1. Coenen AM, van Luijtelaar EL. 1985. Stress induced by three procedures of deprivation of paradoxical sleep. Physiol. Behav. 35, 501–504. (10.1016/0031-9384(85)90130-1)
    1. Suchecki D, Tiba PA, Tufik S. 2002. Paradoxical sleep deprivation facilitates subsequent corticosterone response to a mild stressor in rats. Neurosci. Lett. 320, 45–48. (10.1016/S0304-3940(02)00024-1)
    1. Andersen ML, Bignotto M, Machado RB, Tufik S. 2004. Different stress modalities result in distinct steroid hormone responses by male rats. Braz. J. Med. Biol. Res. 37, 791–797. (10.1590/S0100-879X2004000600003)
    1. Brianza-Padilla M, Sanchez-Munoz F, Vazquez-Palacios G, Huang F, Almanza-Perez JC, Bojalil R, Bonilla-Jaime H. 2018. Cytokine and microRNA levels during different periods of paradoxical sleep deprivation and sleep recovery in rats. PeerJ 6, e5567 (10.7717/peerj.5567)
    1. Ma C, Wu G, Wang Z, Wang P, Wu L, Zhu G, Zhao H. 2014. Effects of chronic sleep deprivation on the extracellular signal-regulated kinase pathway in the temporomandibular joint of rats. PLoS ONE 9, e107544 (10.1371/journal.pone.0107544)
    1. Palma BD, Suchecki D, Tufik S. 2000. Differential effects of acute cold and footshock on the sleep of rats. Brain Res. 861, 97–104. (10.1016/S0006-8993(00)02024-2)
    1. Suchecki D, Tufik S. 2000. Social stability attenuates the stress in the modified multiple platform method for paradoxical sleep deprivation in the rat. Physiol. Behav. 68, 309–316. (10.1016/S0031-9384(99)00181-X)
    1. Mueller AD, Pollock MS, Lieblich SE, Epp JR, Galea LA, Mistlberger RE. 2008. Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1693–R1703. (10.1152/ajpregu.00858.2007)
    1. Solanki N, Atrooz F, Asghar S, Salim S. 2016. Tempol protects sleep-deprivation induced behavioral deficits in aggressive male Long-Evans rats. Neurosci. Lett. 612, 245–250. (10.1016/j.neulet.2015.12.032)
    1. Zhang L, et al. 2017. Melatonin prevents sleep deprivation-associated anxiety-like behavior in rats: role of oxidative stress and balance between GABAergic and glutamatergic transmission. Am. J. Transl. Res. 9, 2231–2242.
    1. Tiba PA, Oliveira MG, Rossi VC, Tufik S, Suchecki D. 2008. Glucocorticoids are not responsible for paradoxical sleep deprivation-induced memory impairments. Sleep 31, 505–515. (10.1093/sleep/31.4.505)
    1. Suchecki D, Lobo LL, Hipolide DC, Tufik S. 1998. Increased ACTH and corticosterone secretion induced by different methods of paradoxical sleep deprivation. J. Sleep Res. 7, 276–281. (10.1046/j.1365-2869.1998.00122.x)
    1. De Lorenzo BH, de Oliveira Marchioro L, Greco CR, Suchecki D. 2015. Sleep-deprivation reduces NK cell number and function mediated by beta-adrenergic signalling. Psychoneuroendocrinology 57, 134–143. (10.1016/j.psyneuen.2015.04.006)
    1. Mueller AD, Parfyonov M, Pavlovski I, Marchant EG, Mistlberger RE. 2014. The inhibitory effect of sleep deprivation on cell proliferation in the hippocampus of adult mice is eliminated by corticosterone clamp combined with interleukin-1 receptor 1 knockout. Brain Behav. Immun. 35, 182–188. (10.1016/j.bbi.2013.10.001)
    1. Arthaud S, Varin C, Gay N, Libourel PA, Chauveau F, Fort P, Luppi P-H, Peyron C. 2015. Paradoxical (REM) sleep deprivation in mice using the small-platforms-over-water method: polysomnographic analyses and melanin-concentrating hormone and hypocretin/orexin neuronal activation before, during and after deprivation. J. Sleep Res. 24, 309–319. (10.1111/jsr.12269)
    1. Chanana P, Kumar A. 2016. GABA-BZD receptor modulating mechanism of Panax quinquefolius against 72-h sleep deprivation induced anxiety like behavior: possible roles of oxidative stress, mitochondrial dysfunction and neuroinflammation. Front. Neurosci. 10, 84 (10.3389/fnins.2016.00084)
    1. Han C, Li F, Ma J, Liu Y, Li W, Mao Y, Song Y, Guo S, Liu J. 2017. Distinct behavioral and brain changes after different durations of the modified multiple platform method on rats: an animal model of central fatigue. PLoS ONE 12, e0176850 (10.1371/journal.pone.0176850)
    1. da Silva Rocha-Lopes J, Machado RB, Suchecki D. 2018. Chronic REM sleep restriction in juvenile male rats induces anxiety-like behavior and alters monoamine systems in the amygdala and hippocampus. Mol. Neurobiol. 55, 2884–2896. (10.1007/s12035-017-0541-3)
    1. Pardo GV, Goularte JF, Hoefel AL, de Castro AL, Kucharski LC, da Rosa Araujo AS, Lucion AB. 2016. Effects of sleep restriction during pregnancy on the mother and fetuses in rats. Physiol. Behav. 155, 66–76. (10.1016/j.physbeh.2015.11.037)
    1. Hajali V, Sheibani V, Esmaeili-Mahani S, Shabani M. 2012. Female rats are more susceptible to the deleterious effects of paradoxical sleep deprivation on cognitive performance. Behav. Brain Res. 228, 311–318. (10.1016/j.bbr.2011.12.008)
    1. Hajali V, Sheibani V, Ghazvini H, Ghadiri T, Valizadeh T, Saadati H, Shabani M. 2015. Effect of castration on the susceptibility of male rats to the sleep deprivation-induced impairment of behavioral and synaptic plasticity. Neurobiol. Learn. Mem. 123, 140–148. (10.1016/j.nlm.2015.05.008)
    1. Cohen S, Kozlovsky N, Matar MA, Kaplan Z, Zohar J, Cohen H. 2012. Post-exposure sleep deprivation facilitates correctly timed interactions between glucocorticoid and adrenergic systems, which attenuate traumatic stress responses. Neuropsychopharmacology 37, 2388–2404. (10.1038/npp.2012.94)
    1. Porkka-Heiskanen T, Smith SE, Taira T, Urban JH, Levine JE, Turek FW, Stenberg D. 1995. Noradrenergic activity in rat brain during rapid eye movement sleep deprivation and rebound sleep. Am. J. Physiol. 268, R1456–R1463. (10.1152/ajpregu.1995.268.6.R1456)
    1. Porter NM, et al. 2012. Hippocampal CA1 transcriptional profile of sleep deprivation: relation to aging and stress. PLoS ONE 7, e40128 (10.1371/journal.pone.0040128)
    1. Guzman-Marin R, Bashir T, Suntsova N, Szymusiak R, McGinty D. 2007. Hippocampal neurogenesis is reduced by sleep fragmentation in the adult rat. Neuroscience 148, 325–333. (10.1016/j.neuroscience.2007.05.030)
    1. Cheng O, Li R, Zhao L, Yu L, Yang B, Wang J, Chen B, Yang J. 2015. Short-term sleep deprivation stimulates hippocampal neurogenesis in rats following global cerebral ischemia/reperfusion. PLoS ONE 10, e0125877 (10.1371/journal.pone.0125877)
    1. Grassi Zucconi G, Cipriani S, Balgkouranidou I, Scattoni R. 2006. ‘One night’ sleep deprivation stimulates hippocampal neurogenesis. Brain Res. Bull. 69, 375–381. (10.1016/j.brainresbull.2006.01.009)
    1. Novati A, Roman V, Cetin T, Hagewoud R, den Boer JA, Luiten PG, Meerlo P. 2008. Chronically restricted sleep leads to depression-like changes in neurotransmitter receptor sensitivity and neuroendocrine stress reactivity in rats. Sleep 31, 1579–1585. (10.1093/sleep/31.11.1579)
    1. Wang PK, Cao J, Wang H, Liang L, Zhang J, Lutz BM, Shieh K-R, Bekker A, Tao Y-X. 2015. Short-term sleep disturbance-induced stress does not affect basal pain perception, but does delay postsurgical pain recovery. J. Pain. 16, 1186–1199. (10.1016/j.jpain.2015.07.006)
    1. Vlasov K, Van Dort CJ, Solt K. 2018. Optogenetics and chemogenetics. Methods Enzymol. 603, 181–196. (10.1016/bs.mie.2018.01.022)
    1. McGinty DJ, Sterman MB. 1968. Sleep suppression after basal forebrain lesions in the cat. Science 160, 1253–1255. (10.1126/science.160.3833.1253)
    1. Nauta WJ. 1946. Hypothalamic regulation of sleep in rats; an experimental study. J. Neurophysiol. 9, 285–316. (10.1152/jn.1946.9.4.285)
    1. Vetrivelan R, Fuller PM, Yokota S, Lu J, Saper CB. 2012. Metabolic effects of chronic sleep restriction in rats. Sleep 35, 1511–1520. (10.5665/sleep.2200)
    1. Lu J, Greco MA, Shiromani P, Saper CB. 2000. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J. Neurosci. 20, 3830–3842. (10.1523/JNEUROSCI.20-10-03830.2000)
    1. Chung S, et al. 2017. Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 545, 477–481. (10.1038/nature22350)
    1. Kroeger D, et al. 2018. Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nat. Commun. 9, 4129 (10.1038/s41467-018-06590-7)
    1. Venner A, Anaclet C, Broadhurst RY, Saper CB, Fuller PM. 2016. A novel population of wake-promoting GABAergic neurons in the ventral lateral hypothalamus. Curr. Biol. 26, 2137–2143. (10.1016/j.cub.2016.05.078)
    1. Anaclet C, Pedersen NP, Ferrari LL, Venner A, Bass CE, Arrigoni E, Fuller PM. 2015. Basal forebrain control of wakefulness and cortical rhythms. Nat. Commun. 6, 8744 (10.1038/ncomms9744)
    1. Qiu MH, Chen MC, Fuller PM, Lu J. 2016. Stimulation of the pontine parabrachial nucleus promotes wakefulness via extra-thalamic forebrain circuit nodes. Curr. Biol. 26, 2301–2312. (10.1016/j.cub.2016.07.054)
    1. Yu X, et al. 2019. GABA and glutamate neurons in the VTA regulate sleep and wakefulness. Nat. Neurosci. 22, 106–119. (10.1038/s41593-018-0288-9)
    1. Pedersen NP, Ferrari L, Venner A, Wang JL, Abbott SBG, Vujovic N, Arrigoni E, Saper CB, Fuller PM. 2017. Supramammillary glutamate neurons are a key node of the arousal system. Nat. Commun. 8, 1405 (10.1038/s41467-017-01004-6)
    1. Holth JK, et al. 2019. The sleep-wake cycle regulates brain interstitial fluid tau in mice and CSF tau in humans. Science 363, 880–884. (10.1126/science.aav2546)
    1. Yaghouby F, Schildt CJ, Donohue KD, O'Hara BF, Sunderam S. 2014. Validation of a closed-loop sensory stimulation technique for selective sleep restriction in mice. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2014, 3771–3774. (10.1109/EMBC.2014.6944444)
    1. Libourel PA, Corneyllie A, Luppi PH, Chouvet G, Gervasoni D. 2015. Unsupervised online classifier in sleep scoring for sleep deprivation studies. Sleep 38, 815–828. (10.5665/sleep.4682)
    1. Gross BA, Vanderheyden WM, Urpa LM, Davis DE, Fitzpatrick CJ, Prabhu K, Poe GR. 2015. Stress-free automatic sleep deprivation using air puffs. J. Neurosci. Methods. 251, 83–91. (10.1016/j.jneumeth.2015.05.010)
    1. Minakawa EN, Wada K, Nagai Y. 2019. Sleep disturbance as a potential modifiable risk factor for Alzheimer's disease. Int. J. Mol. Sci. 20, 803 (10.3390/ijms20040803)
    1. Palagini L, Bastien CH, Marazziti D, Ellis JG, Riemann D. 2019. The key role of insomnia and sleep loss in the dysregulation of multiple systems involved in mood disorders: a proposed model. J. Sleep Res. 28, e12841 (10.1111/jsr.12841)
    1. Morin CM, Drake CL, Harvey AG, Krystal AD, Manber R, Riemann D, Spiegelhalder K, 2015. Insomnia disorder. Nat. Rev. Dis. Primers 1, 15026 (10.1038/nrdp.2015.26)
    1. Irwin MR. 2015. Why sleep is important for health: a psychoneuroimmunology perspective. Annu. Rev. Psychol. 66, 143–172. (10.1146/annurev-psych-010213-115205)
    1. Shochat T. 2012. Impact of lifestyle and technology developments on sleep. Nat. Sci. Sleep 4, 19–31. (10.2147/NSS.S18891)

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