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Adolescent Changes in the Homeostatic and Circadian Regulation of Sleep
Open accessAbstract
Sleep deprivation among adolescents is epidemic. We argue that this sleep deprivation is due in part to pubertal changes in the homeostatic and circadian regulation of sleep. These changes promote a delayed sleep phase that is exacerbated by evening light exposure and incompatible with aspects of modern society, notably early school start times. In this review of human and animal literature, we demonstrate that delayed sleep phase during puberty is likely a common phenomenon in mammals, not specific to human adolescents, and we provide insight into the mechanisms underlying this phenomenon.
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“For pubertal mice, this tendency was exaggerated, with the animals being clearly more sensitive to evening light than adults [70, 198].”
From The neuroendocrine control of the circadian system: Adolescent chronotype (2012) · cites this paper as [70]
In the citing paper
“Reduced sensitivity to the homeostatic sleep drive that builds during extended wakefulness may also contribute to later bedtimes in adolescents (Hagenauer, Perryman, Lee, & Carskadon, 2009).”
From Sleep and circadian contributions to adolescent alcohol use disorder (2015) · cites this paper as Hagenauer et al., 2009
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“Similar findings of a pubertal phase-delay shift of the circadian timing system have also been reported in other mammals (Hagenauer et al., 2009).”
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“A high correlation between age and eveningness was also expected and arises from the pubertal drift to eveningness (Carskadon et al., 1993; Hagenauer et al., 2009) and the expanding social roles of the maturing adolescent.”
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“The data that are available for this age group (10 to 17 years) are dominated by the observation that they go to bed considerably later in the evening (particularly if they have access to television or live in latitudes where summer evenings can be very long) and so tend to be sleepdeprived on school days [53-64].”
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“adolescent sleep patterns were different and that they needed late morning sleep for better learning (Carskadon, 1981, 1990; Dewald, 2010; Hagenauer, 2009; Hansen, 2005; Mitru, 2002).”
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Sleep quality and adolescent default mode network connectivity
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“Biological alterations during puberty contribute to a sleep phase delay, shifting the body’s internal clock and making it more difficult for adolescents to fall asleep before 11 p.m. (Hagenauer et al., 2009).”
BackgroundSleep and health-related physical fitness in children and adolescents: a systematic review
Fonseca, A. P. L. M., de Azevedo, C. V. M., & Santos, R. (2021) · Sleep Science · doi:10.5935/1984-0063.20200125 · Cited by 75
“During adolescence there is a higher sleep necessity than in adulthood, but lower than during childhood 14-16 .”
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Zerbini, G., van der Vinne, V., Otto, L., Kantermann, T., Krijnen, W. P., Roenneberg, T., & Merrow, M. W. (2017) · Scientific Reports · doi:10.1038/s41598-017-04076-y · Cited by 80
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The challenges of adolescent sleep
Illingworth, G. (2020) · Interface Focus · doi:10.1098/rsfs.2019.0080 · Cited by 62
“The circadian pacemaker shifts later with the progression of puberty [38], with a ‘phase delay’ in circadian timing occurring in humans as well as nonhuman mammals [39,40].”
BackgroundDíaz‐Morales, J. F., & Escribano, C. (2013) · Personality and Individual Differences · doi:10.1016/j.paid.2013.02.011 · Cited by 65
Jamieson, D., Broadhouse, K. M., Lagopoulos, J., & Hermens, D. F. (2019) · Sleep Medicine · doi:10.1016/j.sleep.2019.08.013 · Cited by 64
Seasonal and weather variation of sleep and physical activity in 12–14-year-old children
Quante, M., Wang, R., Weng, J. F., Kaplan, E. R., Rueschman, M., Taveras, E. M., Rifas‐Shiman, S. L., Gillman, M. W., & Redline, S. S. (2017) · Behavioral Sleep Medicine · doi:10.1080/15402002.2017.1376206 · Cited by 70
Ziporyn, T. D., Owens, J. A., Wahlstrom, K. L., Wolfson, A. R., Troxel, W., Saletin, J., Rubens, S. L., Pelayo, R., Payne, P. A., Hale, L. E., et al. (2022) · Sleep Health · doi:10.1016/j.sleh.2021.10.008 · Cited by 66
“Such a pattern of delayed sleep has also been found in nonhuman juvenile mammals of at least 6 species, indicating a strong biologic component.(24,25) In humans, this pattern manifests itself by both a later “chronotype,” a behavioral marker, as well as the secretion of melatonin later in the evening, a biologic marke…”
BackgroundGaragiola, E. R., Lam, Q., Wachsmuth, L. S., Tan, T. Y., Ghali, S., Asafo, S. M., & Swarna, M. (2022) · Behavioral Sciences · doi:10.3390/bs12070220 · Cited by 78
“During puberty, the circadian rhythm of adolescents shifts, such that they fall asleep later in the night and sleep later into the morning than young children and adults [61].”
BackgroundInsights into muscle stem cell dynamics during postnatal development
Bachman, J. F., & Chakkalakal, J. V. (2021) · FEBS Journal · doi:10.1111/febs.15856 · Cited by 57
Adverse Effects of Daylight Saving Time on Adolescents' Sleep and Vigilance
Medina, D., Ebben, M. R., Milrad, S. F., Atkinson, B., & Krieger, A. C. (2015) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.4938 · Cited by 59
“25,38,39 16 In our study, the effects of DST on total sleep time, subjective daytime sleepiness, and vigilance in adolescents were statistically significant during the week following DST as compared to the week prior to DST implementation.”
Adolescent Neurological Development and Implications for Health and Well-Being
Griffin, A. (2017) · Healthcare · doi:10.3390/healthcare5040062 · Cited by 69
MicroRNAs in the Onset of Schizophrenia
Thomas, K. T., & Zakharenko, S. S. (2021) · Cells · doi:10.3390/cells10102679 · Cited by 64
Arrona-Palacios, A., & Díaz-Morales, J. (2018) · British Journal of Educational Psychology · doi:10.1111/bjep.12196 · Cited by 49
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
“Short- and long-term alterations in the circulating ovarian hormone profile, either at major life events such as adolescence, pregnancy, and at menopause or across the menstrual cycle, are associated with elevated sleep disturbance (3, 23, 27, 33), suggesting that these hormones may play a role in the physiological re…”
BackgroundSleep, sleep timing and chronotype in animal behaviour
Randler, C. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.05.001 · Cited by 59
Circadian rhythms and risk for substance use disorders in adolescence
Hasler, B. P., Soehner, A. M., & Clark, D. B. (2014) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000107 · Cited by 62
“Reduced sensitivity to the homeostatic sleep drive that builds during extended wakefulness may also contribute to later bedtimes in adolescents [16].”
BackgroundEvening adolescents: The role of family relationships and pubertal development
Díaz‐Morales, J. F., Escribano, C., Jankowski, K. S., Vollmer, C., & Randler, C. (2014) · Journal of Adolescence · doi:10.1016/j.adolescence.2014.03.001 · Cited by 57
“After reaching adolescence, most people gradually become more and more morning-types (Hur, 2007).”
BackgroundFigueiro, M. G. (2013) · Journal of Light & Visual Environment · doi:10.2150/jlve.ieij130000503 · Cited by 54
Deficient Sleep in Mouse Models of Fragile X Syndrome
Saré, R. M., Harkless, L. H., Levine, M., Torossian, A., Sheeler, C. A., & Smith, C. B. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00280 · Cited by 54
“However, circadian rhythm in P21 animals is not as defined as in adult animals (Hagenauer et al., 2009), which may mask potential differences between genotypes.”
BackgroundPregnancy Induces an Earlier Chronotype in Both Mice and Women
Martin‐Fairey, C. A., Zhao, P., Wan, L., Roenneberg, T., Fay, J. C., Ma, X., McCarthy, R., Jungheim, E. S., England, S. K., & Herzog, E. D. (2019) · Journal of Biological Rhythms · doi:10.1177/0748730419844650 · Cited by 55
“Shifts in chronotype at the time of puberty have been attributed to sex hormones in rats, common degus, and macaques (Golub et al., 2002; Hagenauer et al., 2009; Hagenauer et al., 2011a, 2011b; Hagenauer and Lee, 2012) and could underlie the pregnancy-induced shifts in daily rhythms.”
New determinants of mental health: the role of noise pollution. A narrative review
Tortorella, A. A. V., Menculini, G., Moretti, P., Attademo, L., Balducci, P. M., Bernardini, F., Cirimbilli, F., Chieppa, A. G., Ghiandai, N., & Erfurth, A. (2022) · International Review of Psychiatry · doi:10.1080/09540261.2022.2095200 · Cited by 58
“Indeed, circadian systems progressively develop from childhood to adolescence through the transition from a previous to a later chronotype around puberty (Carpenter et al., 2015; Hagenauer et al., 2009; Roenneberg et al., 2004).”
BackgroundGiddens, N. T., Juneau, P. L., Manza, P., Wiers, C. E., & Volkow, N. D. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2120009119 · Cited by 53
Dissipation of sleep pressure is stable across adolescence
Tarokh, L., Carskadon, M. A., & Achermann, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.055 · Cited by 53
“Studies in humans and animals support the notion that changes to the circadian timing system underlie the delayed bedtimes observed in adolescents (reviewed in (Hagenauer et al., 2009)).”
BackgroundEvening daylight may cause adolescents to sleep less in spring than in winter
Figueiro, M. G., & Rea, M. S. (2010) · Chronobiology International · doi:10.3109/07420528.2010.487965 · Cited by 52
“…Copyright © 2010 Informa Healthcare USA, Inc. ISSN 0742-0528 print/1525-6073 online DOI: 10.3109/07420528.2010.487965 mechanisms are believed to underlie the tendency toward later bed and rise times experienced by adolescents (Carskadon et al., 1993, 1999; reviewed in Hagenauer et al., 2009).”
InfluentialSleep in adolescent depression: physiological perspectives
Urrila, A. S., Paunio, T., Palomäki, E., & MARTTUNEN, M. J. (2015) · Acta Physiologica · doi:10.1111/apha.12449 · Cited by 56
“Published by John Wiley & Sons Ltd, doi: 10.1111/apha.12449760 chronotype seems to have at least partly a biological background, as it has been observed in different types of societies and also in other mammalian species (reviewed in Hagenauer et al. 2009).”
BackgroundInfluentialCohen‐Zion, M., & Shiloh, E. (2017) · Chronobiology International · doi:10.1080/07420528.2017.1387792 · Cited by 51
“…this sleepiness is then combined with a lack of intrinsic arousal during morning hours [a function of the delayed phase of Process C in adolescence (Hagenauer et al. 2009)], the teen in essence acquires a “second” layer of sleepiness or at least lack the protective alerting function of Process C…”
BackgroundCarvalho-Mendes, R. P., Dunster, G. P., de la Iglesia, H. O., & Menna-Barreto, L. S. (2020) · Journal of Biological Rhythms · doi:10.1177/0748730420927603 · Cited by 54
“…et al., 2014; Fischer et al., 2017; Frey et al., 2009; Randler, 2011; Roenneberg et al., 2004; Tonetti et al., 2008), and in some animal models, sex differences in the timing of puberty are also reflected by differences in the delay of circadian timing (see review in Hagenauer et al., 2009).”
BackgroundLight Exposure Among Adolescents With Delayed Sleep Phase Disorder: A Prospective Cohort Study
Auger, R. R., Burgess, H. J., Dierkhising, R., Sharma, R. G., & Slocumb, N. L. (2011) · Chronobiology International · doi:10.3109/07420528.2011.619906 · Cited by 50
“Given the combined prospect of a blunted phase advance response among pubertal humans (Hagenauer et al., 2009), it would seem that therapies aimed at augmenting exposure to this PRC region would be most fruitful.”
BackgroundSynchronizing education to adolescent biology: ‘let teens sleep, start school later.’
Kelley, P., Lockley, S. W., Foster, R. G., & Kelley, J. (2015) · Learning, Media and Technology · doi:10.1080/17439884.2014.942666 · Cited by 56
“…communication, decreased concentration and cognitive performance, unintended sleeps, decreased motor performance, increased risk taking and changes in mood pattern, specifically depression (Millman 2005; Knutson et al. 2007; Hagenauer et al. 2009; Foster et al. 2013; de Souza and Hidalgo 2014).”
BackgroundInfluentialAssociation Between Substance Use and Insufficient Sleep in U.S. High School Students
Kwon, M., Seo, Y. S., Park, E., & Chang, Y. (2020) · The Journal of School Nursing · doi:10.1177/1059840519901161 · Cited by 48
“In terms of sleep, it is reported that more mature teenagers are slower to fall asleep even after being awake for an extended period than younger teenagers (Hagenauer et al., 2009), which may indicate that older high school students are able to better tolerate longer waking episodes but, to the degree in which the use…”
BackgroundDanielsson, K., Jansson‐Fröjmark, M., Broman, J., & Markström, A. (2015) · Behavioral Sleep Medicine · doi:10.1080/15402002.2014.981817 · Cited by 48
Metadata
- Authors
- Hagenauer, M. H., Perryman, J. I., Lee, T. M., & Carskadon, M. A.
- Affiliations
- University of Michigan (US)
- Brown University (US)
- Venue
- Developmental Neuroscience
- Publisher
- S. Karger AG
- Published
- 2009
- Volume
- 31
- Issue
- 4
- Pages
- 276-284
- ISSN
- 0378-5866 (ISSN-L)
- 1421-9859
- PMC
- PMC2820578
- OpenAlex
- W2032467619
- Cited by
- 593
- References
- 67
- Citations by year
- 2026: 42 · 2025: 40 · 2024: 32 · 2023: 34 · 2022: 55 · 2021: 49 · 2020: 53 · 2019: 31 · 2018: 59 · 2017: 44 · 2016: 21 · 2015: 31 · 2014: 28 · 2013: 22 · 2012: 17
- FWCI
- 1.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Developmental Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- National Science Foundation
- National Institutes of Health (5k05mh001358-03, 5r01nr004279-04)
- National Institute of Mental Health (R01MH045945, MH52415, MH01358, R01MH052415, R01MH076969, MH076969)
- National Institute of Nursing Research (NR04279)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007048)
- 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 related disorders
- Keywords
- adolescent sleep, sleep deprivation, pubertal development, sleep homeostasis, circadian rhythm, delayed sleep phase, evening light exposure, school start time, mammals
- MeSH terms
- Adolescent, Adolescent Behavior, Animals, Biological Clocks, Circadian Rhythm, Female, Homeostasis, Humans, Light, Male, Puberty, Sleep, Sleep Deprivation, Photoperiod, Gonadal Hormones
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