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, the tendency to be more responsive to light at subjective night was exaggerated, with the animals being clearly more sensitive to evening light than adults.
“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]
Reduced sensitivity to the homeostatic sleep drive that builds during extended wakefulness may contribute to later bedtimes in adolescents.
“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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“and by a slowing of homeostatic build up, shifting the major sleep period to a later phase of the circadian rhythm [5,7].”
BackgroundEmergence of Sex Differences in Insomnia Symptoms in Adolescents: A Large-Scale School-Based Study
Zhang, J., Chan, N. Y., Lam, S. P., Li, S. X., Liu, Y., Chan, J. W. Y., Kong, A. P. S., Ronald, C. W., Chan, K. C. C., Li, A. M., et al. (2016) · SLEEP · doi:10.5665/sleep.6022 · Cited by 205 · see citing works
Neuroscience and education: prime time to build the bridge
Sigman, M., Peña, M., Goldin, A. P., & Ribeiro, S. T. G. (2014) · Nature Neuroscience · doi:10.1038/nn.3672 · Cited by 196 · see citing works
Grandner, M. A., Martin, J. L., Patel, N. P., JACKSON, N. J., Gehrman, P., Pien, G. W., Perlis, M. L., Xie, D., Sha, D., Weaver, T. E., et al. (2012) · SLEEP · doi:10.5665/sleep.1704 · Cited by 183 · see citing works
MODIFICATIONS TO WEEKEND RECOVERY SLEEP DELAY CIRCADIAN PHASE IN OLDER ADOLESCENTS
Crowley, S. J., & Carskadon, M. A. (2010) · Chronobiology International · doi:10.3109/07420528.2010.503293 · Cited by 172 · see citing works
“Similar findings of a pubertal phase-delay shift of the circadian timing system have also been reported in other mammals (Hagenauer et al., 2009).”
ResultCircadian Photoentrainment in Mice and Humans
Foster, F., Hughes, S., & Peirson, S. N. (2020) · Biology · doi:10.3390/biology9070180 · Cited by 163 · see citing works
Re-evaluating the effect of age on physical activity over the lifespan
Varma, V. R., Dey, D., Leroux, A., Di, J., Urbanek, J. K., Xiao, L., & Zipunnikov, V. (2017) · Preventive Medicine · doi:10.1016/j.ypmed.2017.05.030 · Cited by 164 · see citing works
Outdoor Light at Night (LAN) Is Correlated With Eveningness in Adolescents
Vollmer, C., Michel, U., & Randler, C. (2012) · Chronobiology International · doi:10.3109/07420528.2011.635232 · Cited by 162 · see citing works
“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.”
BackgroundPsychometric properties of the A dolescent S leep H ygiene S cale
Storfer‐Isser, A., LeBourgeois, M. K., Harsh, J., Tompsett, C. J., & Redline, S. S. (2013) · Journal of Sleep Research · doi:10.1111/jsr.12059 · Cited by 153 · see citing works
“Sleep Foundation, 2006, 2011), shifts in sleep–wake patterns (Hagenauer et al., 2009; National Sleep Foundation, 2006), decreased sleep quality (Roberts et al.”
BackgroundA review of sleep disturbance in children and adolescents with anxiety
Brown, W. J., Wilkerson, A. K., Boyd, S. J., Dewey, D., Mesa, F., & Bunnell, B. E. (2018) · Journal of Sleep Research · doi:10.1111/jsr.12635 · Cited by 153 · see citing works
The Need for Sleep in the Adolescent Brain
Galván, A. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.11.002 · Cited by 154 · see citing works
The neuroendocrine control of the circadian system: Adolescent chronotype
Hagenauer, M. H., & Lee, T. M. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.04.003 · Cited by 143 · see citing works
“Pubertal stage was assigned with respect to secondary sex development in the same manner as discussed in Hagenauer et al. (2009). Note”
BackgroundMethodInfluentialEveningness, Sleep Patterns, Daytime Functioning, and Quality of Life in Israeli Adolescents
Tzischinsky, O., & Shochat, T. (2011) · Chronobiology International · doi:10.3109/07420528.2011.560698 · Cited by 126 · see citing works
“A review of human and animal studies provides evidence that these changes may be a common phenomenon among mammals during the sexual maturation period (Hagenauer et al., 2009).”
BackgroundSleep and circadian contributions to adolescent alcohol use disorder
Hasler, B. P., Soehner, A. M., & Clark, D. B. (2015) · Alcohol · doi:10.1016/j.alcohol.2014.06.010 · Cited by 123 · see citing works
Circadian Misalignment, Reward‐Related Brain Function, and Adolescent Alcohol Involvement
Hasler, B. P., & Clark, D. B. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12003 · Cited by 120 · see citing works
“Later sleep schedules result, in part, from the timing of the circadian clock becoming relatively delayed (shifting later), and also because adolescents appear to become resistant to the homeostatic sleep drive that accumulates with time spent awake (Hagenauer et al., 2009).”
BackgroundSchool-based sleep promotion programs: Effectiveness, feasibility and insights for future research
Cassoff, J., Knäuper, B., Michaelsen, S., & Gruber, R. (2013) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2012.07.001 · Cited by 118 · see citing works
Inadequate sleep as a contributor to type 2 diabetes in children and adolescents
Dutil, C., & Chaput, J. (2017) · Nutrition and Diabetes · doi:10.1038/nutd.2017.19 · Cited by 118 · see citing works
Sleep’s role in the development and resolution of adolescent depression
Gradisar, M., Kahn, M., Micic, G., Short, M. A., Reynolds, C. M., Orchard, F., Bauducco, S., Bartel, K., & Richardson, C. E. (2022) · Nature Reviews Psychology · doi:10.1038/s44159-022-00074-8 · Cited by 129 · see citing works
Sustained benefits of delaying school start time on adolescent sleep and well-being
Lo, J. C., Lee, S. M., Lee, X. K., Sasmita, K., Chee, N. I. Y. N., Tandi, J., Cher, W. S., Gooley, J. J., & Chee, M. W. L. (2018) · Sleep · doi:10.1093/sleep/zsy052 · Cited by 114 · see citing works
“In addition, the maturational delay in circadian timing and slower accumulation of sleep pressure [13], as well as technology use before bedtime [14], all lead to delays in bedtime.”
BackgroundBorisenkov, M. F., Perminova, E. V., & Kosova, A. L. (2010) · Chronobiology International · doi:10.3109/07420528.2010.487624 · Cited by 116 · see citing works
“changes in chronotype are mainly determined by biological factors (Hagenauer et al., 2009; Roenneberg et al., 2004).”
BackgroundSleep Problems Across Development: A Pathway to Adolescent Risk Taking Through Working Memory
Thomas, A. G., Monahan, K. C., Lukowski, A. F., & Cauffman, E. (2015) · Journal of Youth and Adolescence · doi:10.1007/s10964-014-0179-7 · Cited by 116 · see citing works
“During puberty, adolescents experience significant reductions in slow wave sleep (Carskadon 2002), as well as changes in their circadian rhythm known as a ‘‘delayed phase preference,’’ which involves a desire to stay up later in the evening and sleep in later in the morning (Hagenauer et al. 2009).”
BackgroundDaily rhythms of the sleep-wake cycle
Waterhouse, J. M., Fukuda, Y., & Morita, T. (2012) · Journal of PHYSIOLOGICAL ANTHROPOLOGY · doi:10.1186/1880-6805-31-5 · Cited by 116 · see citing works
“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].”
BackgroundSleep habits, academic performance, and the adolescent brain structure
Urrila, A. S., Eric Artiges, A., Massicotte, J., Miranda, R., Vulser, H., Frère, P., Lapidaire, W., Lemaître, H., Penttilä, J., Conrod, P., et al. (2017) · Scientific Reports · doi:10.1038/srep41678 · Cited by 115 · see citing works
“Based on the six voxel-wise correlation analyses between sleep habits and GMV, three region-of interest masks were identified for the following variables: (1) wake-up time during weekends (including areas of the left frontal medial orbital cortex and the left ACC); (2) bedtime during weekends (including areas of the r…”
The Effect of One Night's Sleep Deprivation on Adolescent Neurobehavioral Performance
Louca, M., & Short, M. A. (2014) · SLEEP · doi:10.5665/sleep.4174 · Cited by 105 · see citing works
Sleep’s effects on cognition and learning in adolescence
Carskadon, M. A. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53817-8.00008-6 · Cited by 111 · see citing works
Making long-term memories in minutes: a spaced learning pattern from memory research in education
Kelley, P., & Whatson, T. S. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00589 · Cited by 106 · see citing works
“The mismatch between educational timings and circadian neuroscience evidence strongly suggest major readjustment of current educational practice is required (Czeisler, 2009; Hagenauer et al., 2009; Lockley and Foster, 2012).”
BackgroundHasler, B. P., Franzen, P. L., de Zambotti, M., Prouty, D., Brown, S. A., Tapert, S. F., Pfefferbaum, A., Pohl, K. M., Sullivan, E. V., Bellis, M. D. D., et al. (2017) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13401 · Cited by 102 · see citing works
“All rights reserved. other drug involvement, evidence is lacking on earlier adolescence when eveningness tendencies start increasing (Hagenauer et al., 2009).”
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
“…Carskadon et al., 1999; Hagenauer et al., 2011a; Hummer, 2006; Hummer et al., 2007; McGinnis et al., 2007) and sensitivity to environmental time cues (Borisenkov, 2011; Crowley and Carskadon, 2010; Hagenauer et al., 2009; Sharkey et al., 2011; Weinert and Kompauerova, 1998; Weinert et al., 1994).”
Sleep during development: Sex and gender differences
Franco, P., Putois, B., Guyon, A., Raoux, A., Papadopoulou, M. T., Guignard‐Perret, A., Bat‐Pitault, F., Hartley, S., & Plancoulaine, S. (2020) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2020.101276 · Cited by 102 · see citing works
Suleiman, A. B., & Dahl, R. E. (2017) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2016.12.010 · Cited by 95 · see citing works
Danielsson, K., Sakarya, A., & Jansson‐Fröjmark, M. (2019) · Chronobiology International · doi:10.1080/07420528.2018.1564322 · Cited by 92 · see citing works
“There is a known delay of circadian rhythms during puberty, and eveningness CT is high in adolescence (Borisenkov et al. 2010; Hagenauer et al. 2009).”
BackgroundDelayed sleep phase disorder in youth
Gradisar, M., & Crowley, S. J. (2013) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e328365a1d4 · Cited by 94 · see citing works
“These data have been replotted as a PRC separately by age [23], and illustrated that the phase delay portion of the PRC was greater for the pubertal compared with the adult mice.”
ResultNovati, A., Hulshof, H. J., Koolhaas, J. M., Lucassen, P. J., & Meerlo, P. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.027 · Cited by 94 · see citing works
“One contributing factor is that adolescence is characterized by spontaneous changes in circadian organization resulting in a stronger tendency for evening activities and delayed sleep timing (Crowley et al., 2007; Roenneberg et al., 2007; Hagenauer et al., 2009).”
Hasler, B. P., Kirisci, L., & Clark, D. B. (2016) · Journal of Studies on Alcohol and Drugs · doi:10.15288/jsad.2016.77.649 · Cited by 87 · see citing works
“…crosssectional literature indicating that variability in sleep timing during adolescence is associated with a host of problems, including substance involvement, mood disorders, and academic problems (Fuligni & Hardway, 2006; Haraszti et al., 2014; O’Brien & Mindell, 2005; Pasch et al., 2010).”
BackgroundThe etiology of delayed sleep phase disorder
Micic, G., Lovato, N., Gradisar, M., Ferguson, S. A., Burgess, H. J., & Lack, L. C. (2016) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.06.004 · Cited by 84 · see citing works
Sleep-Related Problems and the Effects of Anxiety Treatment in Children and Adolescents
Caporino, N. E., Read, K. L., Shiffrin, N. D., Settipani, C. A., Kendall, P. C., Compton, S. N., Sherrill, J. T., Piacentini, J. C., Walkup, J. T., Ginsburg, G. S., et al. (2015) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2015.1063429 · Cited by 85 · see citing works
Time to learn: H ow chronotype impacts education
Zerbini, G., & Merrow, M. W. (2017) · PsyCh Journal · doi:10.1002/pchj.178 · Cited by 85 · see citing works
“A delay in chronotype is observed also in animals (some mammals, such as rhesus monkeys, and laboratory rats and mice), suggesting that systematic changes occur during puberty that delay the circadian clock as opposed to purely societal structures (Hagenauer et al., 2009).”
BackgroundMorningness/eveningness and school performance among Spanish adolescents: Further evidence
Escribano, C., Díaz‐Morales, J. F., Delgado, P., & Mateo, M. J. C. (2011) · Learning and Individual Differences · doi:10.1016/j.lindif.2011.12.008 · Cited by 79 · see citing works
Later high school start times associated with longer actigraphic sleep duration in adolescents
Nahmod, N. G., Lee, S., Master, L., Chang, A., Hale, L. E., & Buxton, O. M. (2018) · SLEEP · doi:10.1093/sleep/zsy212 · Cited by 82 · see citing works
Sleep behaviors in traditional‐age college students
Owens, H., Christian, B. J., & Polivka, B. J. (2017) · Journal of the American Association of Nurse Practitioners · doi:10.1002/2327-6924.12520 · Cited by 80 · see citing works
Energy drink consumption, health complaints and late bedtime among young adolescents
Koivusilta, L., Kuoppamäki, H., & Rimpelä, A. (2016) · International Journal of Public Health · doi:10.1007/s00038-016-0797-9 · Cited by 73 · see citing works
“Along with later bedtimes in modern societies, the insufficiency of sleep among children and adolescents has become a topic of considerable concern (Hagenauer et al. 2009; Matricciani et al. 2012; Carskadon 2011).”
BackgroundThe emerging role of educational neuroscience in education reform
Zadina, J. N. (2015) · Psicologí a Educativa · doi:10.1016/j.pse.2015.08.005 · Cited by 80 · see citing works
“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).”
BackgroundWahlstrom, K. L., Dretzke, B. J., Gordon, M., Peterson, K., Edwards, K., & Gdula, J. (2014) · University of Minnesota Digital Conservancy (University of Minnesota) · Cited by 76 · see citing works
Sleep quality and adolescent default mode network connectivity
Tashjian, S. M., Goldenberg, D., Monti, M. M., & Galván, A. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy009 · Cited by 73 · see citing works
“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 · see citing works
“During adolescence there is a higher sleep necessity than in adulthood, but lower than during childhood 14-16 .”
BackgroundCircadian Rhythms and Measures of CNS/Autonomic Interaction
Riganello, F., Prada, V., Soddu, A., Perri, C. D., & Sannita, W. G. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16132336 · Cited by 72 · see citing works
Human Adolescent Phase Response Curves to Bright White Light
Crowley, S. J., & Eastman, C. I. (2017) · Journal of Biological Rhythms · doi:10.1177/0748730417713423 · Cited by 69 · see citing works
“, 2004) and other young mammals, such as rhesus monkey, degu, laboratory rat, laboratory mouse, and fat sand rat (Hagenauer et al., 2009), show a puberty-related delay of the circadian timing system.”
BackgroundLower school performance in late chronotypes: underlying factors and mechanisms
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 72 · see citing works
Understanding the Need for Sleep to Improve Cognition
Leong, R. L. F., & Chee, M. W. L. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-032620-034127 · Cited by 89 · see citing works
Sleep complaints among adolescent outpatients with major depressive disorder
Urrila, A. S., Karlsson, L., Kiviruusu, O. H., Pelkonen, M. U. I., Strandholm, T., & MARTTUNEN, M. J. (2012) · Sleep Medicine · doi:10.1016/j.sleep.2012.04.012 · Cited by 68 · see citing works
The challenges of adolescent sleep
Illingworth, G. (2020) · Interface Focus · doi:10.1098/rsfs.2019.0080 · Cited by 74 · see citing works
“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 · see citing works
Jamieson, D., Broadhouse, K. M., Lagopoulos, J., & Hermens, D. F. (2019) · Sleep Medicine · doi:10.1016/j.sleep.2019.08.013 · Cited by 63 · see citing works
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 64 · see citing works
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 64 · see citing works
“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 71 · see citing works
“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 61 · see citing works
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 · see citing works
“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 · see citing works
MicroRNAs in the Onset of Schizophrenia
Thomas, K. T., & Zakharenko, S. S. (2021) · Cells · doi:10.3390/cells10102679 · Cited by 59 · see citing works
Arrona‐Palacios, A., & Díaz‐Morales, J. F. (2017) · British Journal of Educational Psychology · doi:10.1111/bjep.12196 · Cited by 59 · 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
“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 56 · see citing works
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 56 · see citing works
“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 54 · see citing works
“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 · see citing works
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 · see citing works
“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 54 · see citing works
“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 53 · see citing works
“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 52 · see citing works
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 · see citing works
“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 · see citing works
“…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 52 · see citing works
“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 · see citing works
“…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 50 · see citing works
“…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 · see citing works
“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 · see citing works
“…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 · see citing works
“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 · see citing works
- 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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