Circadian regulation of sleep in mammals: Role of the suprachiasmatic nucleus

Mistlberger, Ralph E.

doi:10.1016/j.brainresrev.2005.01.005

Cited by 318Circadian rhythm and melatoninSleep and Wakefulness ResearchSleep and Work-Related Fatigue

Circadian regulation of sleep in mammals: Role of the suprachiasmatic nucleus

Mistlberger, Ralph E.·2005·Brain Research Reviews

DOI 10.1016/j.brainresrev.2005.01.005

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Abstract

Despite significant progress in elucidating the molecular basis for circadian oscillations, the neural mechanisms by which the circadian clock organizes daily rhythms of behavioral state in mammals remain poorly understood. The objective of this review is to critically evaluate a conceptual model that views sleep expression as the outcome of opponent processes-a circadian clock-dependent alerting process that opposes sleep during the daily wake period, and a homeostatic process by which sleep drive builds during waking and is dissipated during sleep after circadian alerting declines. This model is based primarily on the evidence that in a diurnal primate, the squirrel monkey (Saimiri sciureus), ablation of the master circadian clock (the suprachiasmatic nucleus; SCN) induces a significant expansion of total daily sleep duration and a reduction in sleep latency in the dark. According to this model, the circadian clock actively promotes wake but only passively gates sleep; thus, loss of circadian clock alerting by SCN ablation impairs the ability to sustain wakefulness and causes sleep to expand. For comparison, two additional conceptual models are described, one in which the circadian clock actively promotes sleep but not wake, and a third in which the circadian clock actively promotes both sleep and wake, at different circadian phases. Sleep in intact and SCN-damaged rodents and humans is first reviewed, to determine how well the data fit these conceptual models. Neuroanatomical and neurophysiological studies are then reviewed, to examine the evidence for direct and indirect interactions between the SCN circadian clock and sleep-wake circuits. Finally, sleep in SCN-ablated squirrel monkeys is re-examined, to consider its compatibility with alternative models of circadian regulation of sleep. In aggregate, the behavioral and neurobiological evidence suggests that in rodents and humans, the circadian clock actively promotes both wake and sleep, at different phases of the circadian cycle. The hypersomnia of SCN-ablated squirrel monkeys is unique in magnitude, but is not incompatible with a role for the SCN pacemaker in actively promoting sleep.

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The central clock of the brain is located in the hypothalamic suprachiasmatic nucleus (SCN) and drives many physiological and behavioral rhythms, including promotion of sleep during one part of the circadian cycle and wakefulness during the other part.
“The central clock of our brain is located in the hypothalamic suprachiasmatic nucleus (SCN) and drives many physiological and behavioral rhythms including the promotion of sleep during one part of the circadian cycle and wakefulness during the other part [59], in humans respectively night and day.”
From Sleep, vigilance, and thermosensitivity (2012) · cites this paper as [59]

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Neural Circuitry of Wakefulness and Sleep
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Neurobiology of the Sleep-Wake Cycle: Sleep Architecture, Circadian Regulation, and Regulatory Feedback
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SCN Outputs and the Hypothalamic Balance of Life
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PDF Cells Are a GABA-Responsive Wake-Promoting Component of the Drosophila Sleep Circuit
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Neurobiology of food anticipatory circadian rhythms
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Self-citation
Functional neuroanatomy of the central noradrenergic system
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Neurobiological mechanisms for the regulation of mammalian sleep–wake behavior: Reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence
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Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat
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PERIOD3, circadian phenotypes, and sleep homeostasis
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Food-anticipatory circadian rhythms: concepts and methods
Mistlberger, R. E. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06965.x · Cited by 224 · see citing works
Self-citation
Calcitonin Gene-Related Peptide Neurons Mediate Sleep-Specific Circadian Output in Drosophila
Kunst, M., Hughes, M. E., Raccuglia, D., Felix, M., Li, M., Barnett, G., Duah, J., & Nitabach, M. N. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.077 · Cited by 213 · see citing works
The Neurobiology of Sleep and Wakefulness
Schwartz, M. D., & Kilduff, T. S. (2015) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2015.07.002 · Cited by 207 · see citing works
How to fix a broken clock
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Guidelines for the Recording and Evaluation of Pharmaco-EEG Data in Man: The International Pharmaco-EEG Society (IPEG)
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The role of environmental light in sleep and health: Effects of ocular aging and cataract surgery
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Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats
Landry, G. J., Simon, M. M., Webb, I. C., & Mistlberger, R. E. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00874.2005 · Cited by 179 · see citing works
Self-citation
How sleep and wakefulness influence circadian rhythmicity: effects of insufficient and mistimed sleep on the animal and human transcriptome
Archer, S. N., & Oster, H. (2015) · Journal of Sleep Research · doi:10.1111/jsr.12307 · Cited by 171 · see citing works
An Autonomous Circadian Clock in the Inner Mouse Retina Regulated by Dopamine and GABA
Ruan, G.-X., Allen, G. C., Yamazaki, S., & McMahon, D. G. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060249 · Cited by 164 · see citing works
Light, Sleep, and Circadian Rhythms: Together Again
Dijk, D., & Archer, S. N. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000145 · Cited by 167 · see citing works
Gonadal- and Sex-Chromosome-Dependent Sex Differences in the Circadian System
Kuljis, D. A., Loh, D. H., Truong, D. A., Vosko, A. M., Ong, M. L., McClusky, R., Arnold, A. P., & Colwell, C. S. (2013) · Endocrinology · doi:10.1210/en.2012-1921 · Cited by 151 · see citing works
Sleep and circadian rhythmicity as entangled processes serving homeostasis
Franken, P., & Dijk, D.-J. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00764-z · Cited by 147 · see citing works
Experimental sleep deprivation as a tool to test memory deficits in rodents
Colavito, V., Fabene, P. F., Grassi-Zucconi, G., Pifferi, F., Lamberty, Y., Bentivoglio, M., & Bertini, G. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00106 · Cited by 142 · see citing works
Suprachiasmatic VIP neurons are required for normal circadian rhythmicity and comprised of molecularly distinct subpopulations
Todd, W. D., Venner, A., Anaclet, C., Broadhurst, R. Y., Luca, R. D., Bandaru, S. S., Issokson, L., Hablitz, L. M., Cravetchi, O., Arrigoni, E., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17197-2 · Cited by 142 · see citing works
African trypanosome infections of the nervous system: Parasite entry and effects on sleep and synaptic functions
Kristensson, K., Nygård, M., Bertini, G., & Bentivoglio, M. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.12.001 · Cited by 140 · see citing works
Effects of prolonged‐release melatonin, zolpidem, and their combination on psychomotor functions, memory recall, and driving skills in healthy middle aged and elderly volunteers
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The Sleep-Immunity Relationship
Gamaldo, C. E., Shaikh, A. K., & McArthur, J. C. (2012) · Neurologic Clinics · doi:10.1016/j.ncl.2012.08.007 · Cited by 124 · see citing works
The dorsomedial hypothalamic nucleus is not necessary for food‐anticipatory circadian rhythms of behavior, temperature or clock gene expression in mice
Moriya, T., Aida, R., Kudo, T., Akiyama, M., Doi, M., Hayasaka, N., Nakahata, N., Mistlberger, R. E., Okamura, H., & Shibata, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06697.x · Cited by 124 · see citing works
Self-citation
Functional neuroanatomy of sleep and circadian rhythms
Rosenwasser, A. M. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.08.001 · Cited by 122 · see citing works
Circadian Timing of REM Sleep Is Coupled to an Oscillator within the Dorsomedial Suprachiasmatic Nucleus
Lee, M. L., Swanson, B. E., & de la Iglesia, H. O. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.051 · Cited by 120 · see citing works
Circadian control of the sleep–wake cycle
Beersma, D. G. M., & Gordijn, M. C. M. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.09.010 · Cited by 117 · see citing works
Orbitofrontal Gray Matter Relates to Early Morning Awakening: A Neural Correlate of Insomnia Complaints?
Stoffers, D., Moens, S., Benjamins, J. S., van Tol, M., Penninx, B. W. J. H., Veltman, D. J., van der Wee, N. J. A., & Someren, E. J. W. V. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00105 · Cited by 114 · see citing works
The dynamics of GABA signaling: Revelations from the circadian pacemaker in the suprachiasmatic nucleus
Albers, H. E., Walton, J. C., Gamble, K. L., McNeill, J. K., & Hummer, D. L. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.11.003 · Cited by 113 · see citing works
Neurobiological studies of fatigue
Harrington, M. E. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.07.004 · Cited by 112 · see citing works
“The SCN may also function to increase sleep during the inactive period (Mistlberger, 2005).”
Orexin Neurons Are Necessary for the Circadian Control of REM Sleep
Kántor, S., Mochizuki, T., Janisiewicz, A. M., Clark, E. L., Nishino, S., & Scammell, T. E. (2009) · SLEEP · doi:10.1093/sleep/32.9.1127 · Cited by 111 · see citing works
The Methamphetamine-Sensitive Circadian Oscillator (MASCO) in Mice
Tataroğlu, Ö., Davidson, A. J., Benvenuto, L. J., & Menaker, M. (2006) · Journal of Biological Rhythms · doi:10.1177/0748730406287529 · Cited by 109 · see citing works
Adenosine, Caffeine, and Performance: From Cognitive Neuroscience of Sleep to Sleep Pharmacogenetics
Urry, E., & Landolt, H. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_274 · Cited by 108 · see citing works
Circadian desynchronization of core body temperature and sleep stages in the rat
Cambras, T., Weller, J. R., Anglès‐Pujolràs, M., Lee, M. L., Christopher, A. S., Dı́ez-Noguera, A., Krueger, J. M., & de la Iglesia, H. O. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702424104 · Cited by 107 · see citing works
Sleep, vigilance, and thermosensitivity
Romeijn, N., Raymann, R. J. E. M., Møst, E., Te Lindert, B., Van Der Meijden, W. P., Fronczek, R., Gomez-Herrero, G., & Van Someren, E. J. W. (2012) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1042-2 · Cited by 105 · see citing works
Abnormal Sleep, Circadian Rhythm Disruption, and Delirium in the ICU: Are They Related?
Daou, M., Telías, I., Younes, M. K., Brochard, L. J., & Wilcox, M. E. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.549908 · Cited by 106 · see citing works
A Time to Fast, a Time to Feast: The Crosstalk between Metabolism and the Circadian Clock
Kovac, J., Husse, J., & Oster, H. (2009) · Molecules and Cells · doi:10.1007/s10059-009-0113-0 · Cited by 100 · see citing works
Adolescent sleep patterns in humans and laboratory animals
Hagenauer, M. H., & Lee, T. M. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.01.013 · Cited by 101 · see citing works
Melatonin and anesthesia: a clinical perspective
Naguib, M., Gottumukkala, V. N. R., & Goldstein, P. A. (2006) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2006.00384.x · Cited by 96 · see citing works
Circadian clock genes: Non-circadian roles in sleep, addiction, and psychiatric disorders?
Rosenwasser, A. M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.03.004 · Cited by 92 · see citing works
Sleep and energy balance: interactive homeostatic systems
VanItallie, T. B. (2006) · Metabolism · doi:10.1016/j.metabol.2006.07.010 · Cited by 89 · see citing works
Role of biological rhythms in gastrointestinal health and disease
Hoogerwerf, W. A. (2009) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-009-9119-3 · Cited by 87 · see citing works
A New Perspective for Parkinson’s Disease: Circadian Rhythm
Li, S., Wang, Y., Wang, F., Hu, L., & Liu, C. (2016) · Neuroscience Bulletin · doi:10.1007/s12264-016-0089-7 · Cited by 86 · see citing works
Buying time: a rationale for examining the use of circadian rhythm and sleep interventions to delay progression of mild cognitive impairment to Alzheimerâ€™s disease
Landry, G. J., & Liu-Ambrose, T. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00325 · Cited by 84 · see citing works
Rodent models of insomnia: A review of experimental procedures that induce sleep disturbances
Revel, F. G., Gottowik, J., Gatti, S., Wettstein, J. G., & Moreau, J. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.03.002 · Cited by 82 · see citing works
Bidirectional interactions between the circadian and reward systems: is restricted food access a unique zeitgeber?
Webb, I. C., Baltazar, R. M., Lehman, M. N., & Coolen, L. M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06966.x · Cited by 79 · see citing works
Influence of Age, Circadian and Homeostatic Processes on Inhibitory Motor Control: A Go/Nogo Task Study
Sagaspe, P., Taillard, J., Amieva, H., Beck, A., Rascol, O., Dartigues, J., Capelli, A., & Philip, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039410 · Cited by 77 · see citing works
Circadian Neurobiology and the Physiologic Regulation of Sleep and Wakefulness
Schwartz, W. J., & Klerman, E. B. (2019) · Neurologic Clinics · doi:10.1016/j.ncl.2019.03.001 · Cited by 75 · see citing works
What keeps us awake?–the role of clocks and hourglasses, light, and melatonin
Cajochen, C., Chellappa, S., & Schmidt, C. (2010) · International review of neurobiology · doi:10.1016/s0074-7742(10)93003-1 · Cited by 73 · see citing works
Delayed Orexin Signaling Consolidates Wakefulness and Sleep: Physiology and Modeling
Behn, C. D., Kopell, N., Brown, E. N., Mochizuki, T., & Scammell, T. E. (2008) · Journal of Neurophysiology · doi:10.1152/jn.01243.2007 · Cited by 70 · see citing works
Sleep timing and the circadian clock in mammals: Past, present and the road ahead
Sanchez, R. E. A., Kalume, F. K., & de la Iglesia, H. O. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.034 · Cited by 71 · see citing works
Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework
Phillips, A. J. K., Robinson, P. A., Kedziora, D. J., & Abeysuriya, R. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000826 · Cited by 70 · see citing works
Jet lag syndrome: circadian organization, pathophysiology, and management strategies
Avidan, A. Y., & Colwell, C. S. (2010) · Nature and Science of Sleep · doi:10.2147/nss.s6683 · Cited by 67 · see citing works
Reproductive hormone replacement alters sleep in mice
Paul, K. N., Laposky, A. D., & Turek, F. W. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.07.081 · Cited by 68 · see citing works
Nocturia in Parkinson's Disease: Why Does It Occur and How to Manage?
Batla, A., Phé, V., Min, L. D., & Panicker, J. N. (2016) · Movement Disorders Clinical Practice · doi:10.1002/mdc3.12374 · Cited by 68 · see citing works
The role of the circadian system in the etiology of depression
de Leeuw, M., Verhoeve, S. I., van der Wee, N. J. A., van Hemert, A. M., Vreugdenhil, E., & Coomans, C. P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105383 · Cited by 72 · see citing works
A Comprehensive Overview of the Neural Mechanisms of Light Therapy
Huang, X., Tao, Q., & Ren, C. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01089-8 · Cited by 71 · see citing works
Sleep deprivation in a quantitative physiologically based model of the ascending arousal system
Phillips, A. J. K., & Robinson, P. A. (2008) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2008.08.022 · Cited by 65 · see citing works
Sleep and hippocampal neurogenesis: Implications for Alzheimer’s disease
Kent, B. A., & Mistlberger, R. E. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.02.004 · Cited by 64 · see citing works
Self-citation
Trace amine-associated receptor 1: a multimodal therapeutic target for neuropsychiatric diseases
Schwartz, M. D., Canales, J. J., Zucchi, R., Espinoza, S., Sukhanov, I., & Gainetdinov, R. R. (2018) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2018.1480723 · Cited by 63 · see citing works
Basic Science Review on Circadian Rhythm Biology and Circadian Sleep Disorders
Toh, K. L. (2008) · Annals of the Academy of Medicine Singapore · doi:10.47102/annals-acadmedsg.v37n8p662 · Cited by 61 · see citing works
Dietary heat-killed Lactobacillus brevis SBC8803 promotes voluntary wheel-running and affects sleep rhythms in mice
Miyazaki, K., Itoh, N., Yamamoto, S., Higo-Yamamoto, S., Nakakita, Y., Kaneda, H., Shigyo, T., & Oishi, K. (2014) · Life Sciences · doi:10.1016/j.lfs.2014.07.009 · Cited by 61 · see citing works
GABAB receptors play an essential role in maintaining sleep during the second half of the night in Drosophila melanogaster
Gmeiner, F., Kołodziejczyk, A. M., Yoshii, T., Rieger, D., Nässel, D. R., & Helfrich‐Förster, C. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.085563 · Cited by 62 · see citing works
Sleep ability mediates individual differences in the vulnerability to sleep loss: Evidence from a PER3 polymorphism
Maire, M., Reichert, C., Gabel, V., Viola, A., Strobel, W. M., Krebs, J., Landolt, H., Bachmann, V., Cajochen, C., & Schmidt, C. (2013) · Cortex · doi:10.1016/j.cortex.2013.11.008 · Cited by 60 · see citing works
Serotonergic Integration of Circadian Clock and Ultradian Sleep–Wake Cycles
Miyamoto, H., Nakamaru‐Ogiso, E., Hamada, K., & Hensch, T. K. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0793-12.2012 · Cited by 57 · see citing works
Estradiol modulates recovery of REM sleep in a time-of-day-dependent manner
Schwartz, M. D., & Mong, J. A. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00474.2012 · Cited by 58 · see citing works
Sleep-Wake Regulation and Its Impact on Working Memory Performance: The Role of Adenosine
Reichert, C., Maire, M., Schmidt, C., & Cajochen, C. (2016) · Biology · doi:10.3390/biology5010011 · Cited by 56 · see citing works
Taking the Lag out of Jet Lag through Model-Based Schedule Design
Dean, D. A., Forger, D. B., & Klerman, E. B. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000418 · Cited by 57 · see citing works
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Authors: Mistlberger, R. E.
Affiliations: Simon Fraser University (CA)
Corresponding author: Mistlberger, Ralph E.
ORCID: Mistlberger, Ralph E.
Venue: Brain Research Reviews
Publisher: Elsevier BV
Published: 2005-11
Volume: 49
Issue: 3
Pages: 429-454
ISSN: 0165-0173 (ISSN-L)
DOI: 10.1016/j.brainresrev.2005.01.005
OpenAlex: W1984524952
Cited by: 318
References: 253
Citations by year: 2026: 5 · 2025: 8 · 2024: 12 · 2023: 15 · 2022: 11 · 2021: 11 · 2020: 11 · 2019: 18 · 2018: 10 · 2017: 14 · 2016: 22 · 2015: 14 · 2014: 14 · 2013: 24 · 2012: 26
FWCI: 1.24
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Brain Research Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
Keywords: suprachiasmatic nucleus, circadian clock, sleep-wake regulation, sleep homeostasis, sleep drive, hypersomnia, squirrel monkey, circadian pacemaker
MeSH terms: Animals, Circadian Rhythm, Humans, Mammals, Sleep, Sleep Deprivation, Suprachiasmatic Nucleus, Mice, Rats

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Circadian regulation of sleep in mammals: Role of the suprachiasmatic nucleus

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