An Approach to Studying Circadian Rhythms of Adolescent Humans
Abstract
The "long nights" protocol was designed to evaluate sleep processes and circadian rhythm parameters in young humans. A total of 19 children (10 boys, ages 11.2 to 14.1 years [mean = 12.7 +/- 1.0], and 9 girls, ages 12.2 to 14.4 years [mean = 13.1 +/- 0.7]) took part in the study. Sleep/wake initially was assessed at home using actigraphy and diary for 1 week on each child's self-selected schedule followed by an 8-night fixed light-dark (LD) condition, while sleeping from 22:00 to 08:00 h and wearing an eye mask to exclude as much light as possible. Phase measurements included 4-night mean actigraphically estimated sleep onset and offset as well as 1-night dim light salivary melatonin onset (DLSMO) phase at the end of each condition. Subjects then lived in the laboratory for 6 consecutive cycles: Day 1 LD = 14:10 h, lights out 22:00 to 08:00 h; Days 2-4 LD = 6:18 h, lights out 18:00 to 12:00 h; Days 5-6 = constant routine in continuous dim light (about 20 lux); Night 6 = 14 h recovery sleep. Phase markers (sleep onset, sleep offset, DLSMO) were significantly less dispersed after the fixed LD as compared to the self-selected condition, indicating efficacy of the LD protocol. Phase markers were correlated at the self-selected assessment (sleep onset vs. sleep offset r = .72; DLSMO vs. sleep onset r = .82; DLSMO vs. sleep offset r = .76) but not on the fixed schedule, probably due to restricted range. The constant routine provided additional phase markers, melatonin offset and midphase. Offset phase of melatonin secretion was significantly correlated with age (r = .62) and Tanner stage (r = .62). In conclusion, these preliminary data indicate a relationship between adolescent development and circadian phase. Thus, the long nights protocol is a feasible way in which to assess circadian parameters in young humans as well as to examine intrinsic sleep processes.
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The delayed circadian phase is maintained under controlled laboratory conditions in which there is limited possibility for social influence.
“This delay is also maintained under controlled laboratory conditions in which there is limited possibility for social influence [31, 32].”
From The neuroendocrine control of the circadian system: Adolescent chronotype (2012) · cites this paper as [32]
Delayed circadian phase correlates with secondary-sex development in both home-based and laboratory studies of adolescents.
“Both home-based and laboratory studies of adolescents show that delayed circadian phase correlates with secondary-sex development [31, 32, 33, 164], and this correlation holds true for subjective ratings of chronotype and puberty even when grade level in school is held constant [36].”
From The neuroendocrine control of the circadian system: Adolescent chronotype (2012) · cites this paper as [32]
Cites
Two-Process Model of Sleep Regulation
Binder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_6166 · Cited by 3,895 · see citing works
Tanner, J. M. (1978) · Medical Entomology and Zoology · Cited by 3,742 · see citing works
Guidelines for the Multiple Sleep Latency Test (MSLT): A Standard Measure of Sleepiness
Carskadon, M. A. (1986) · SLEEP · doi:10.1093/sleep/9.4.519 · Cited by 1,607 · see citing works
Self-citationActivity-Based Sleep-Wake Identification: An Empirical Test of Methodological Issues
Sadeh, A., Sharkey, M., & Carskadon, M. A. (1994) · Sleep · doi:10.1093/sleep/17.3.201 · Cited by 1,487 · see citing works
Self-citationAssociation between Puberty and Delayed Phase Preference
Carskadon, M. A., Vieira, C., & Acebo, C. (1993) · Sleep · doi:10.1093/sleep/16.3.258 · Cited by 1,167 · see citing works
Self-citationMelatonin Shifts Human Orcadian Rhythms According to a Phase-Response Curve
Lewy, A. J., Ahmed, S., Jackson, J. M. L., & Sack, R. L. (1992) · Chronobiology International · doi:10.3109/07420529209064550 · Cited by 693 · see citing works
Edgar, D. M., Dement, W., & Fuller, C. A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-01065.1993 · Cited by 685 · see citing works
Wever, R. (1979) · Topics in environmental physiology and medicine · doi:10.1007/978-1-4612-6142-1 · Cited by 623 · see citing works
Monk, T. H., Reynolds, C. F., Kupfer, D. J., Buysse, D. J., Coble, P. A., HAYES, A. J., Machen, M. A., PETRIE, S. R., & Ritenour, A. (1994) · Journal of Sleep Research · doi:10.1111/j.1365-2869.1994.tb00114.x · Cited by 537 · see citing works
The circadian system of man—Results of experiments under temporal isolation
(1980) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/s0300-9629(80)80040-5 · Cited by 515 · see citing works
The Dim Light Melatonin Onset as a Marker for Orcadian Phase Position
Lewy, A. J., & Sack, R. L. (1989) · Chronobiology International · doi:10.3109/07420528909059144 · Cited by 418 · see citing works
Conservation of photoperiod-responsive mechanisms in humans
Wehr, T. A., Moul, D. E., Barbato, G., Giesen, H. A., Seidel, J. A., Barker, C., & Bender, C. (1993) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1993.265.4.r846 · Cited by 334 · see citing works
The Social Rhythm Metric An Instrument to Quantify the Daily Rhythms of Life
Monk, T. H., Flaherty, J. F., Frank, E., Hoskinson, K., & Kupfer, D. J. (1990) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-199002000-00007 · Cited by 295 · see citing works
Adaptation to abrupt time shifts of the oscillator(s) controlling human circadian rhythms.
Mills, J. N., Minors, D. S., & Waterhouse, J. M. (1978) · The Journal of Physiology · doi:10.1113/jphysiol.1978.sp012582 · Cited by 285 · see citing works
Sleep characteristics of adolescents: A longitudinal study
de Andrade, M. M. M., Benedito‐Silva, A. A., Domenice, S., Arnhold, I. J. P., & Menna-Barreto, L. S. (1993) · Journal of Adolescent Health · doi:10.1016/s1054-139x(08)80016-x · Cited by 216 · see citing works
Cauter, E. V., Sturis, J., Byrne, M. M., Blackman, J. D., Leproult, R., Ofek, G., L’Hermite‐Balériaux, M., Refetoff, S., Turek, F. W., & Reeth, O. V. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.266.6.e953 · Cited by 142 · see citing works
Adolescent sleepiness: increased risk in a high-risk population
Carskadon, M. A. (1990) · Journal of Safety Research · doi:10.1016/0022-4375(90)90038-d · Cited by 125 · see citing works
Self-citationSleep habits of children and the identification of pathologically sleepy children
Anders, T. F., Carskadon, M. A., Dement, W. C., & Harvey, K. (1978) · Child Psychiatry & Human Development · doi:10.1007/bf01463220 · Cited by 110 · see citing works
Self-citationKirmil‐Gray, K., Eagleston, J. R., Gibson, E., & Thoresen, C. E. (1984) · Journal of Youth and Adolescence · doi:10.1007/bf02088636 · Cited by 102 · see citing works
Deacon, S., & Arendt, J. (1994) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1994.tb03940.x · Cited by 67 · see citing works
Busby, K., & Pivik, R. T. (1983) · Pediatric Research · doi:10.1203/00006450-198310000-00007 · Cited by 27 · see citing works
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The Role of Actigraphy in the Study of Sleep and Circadian Rhythms
Ancoli-Israel, S., Cole, R., Alessi, C., Chambers, M., Moorcroft, W., & Pollak, C. P. (2003) · Sleep · doi:10.1093/sleep/26.3.342 · Cited by 2,751 · see citing works
Sleep Patterns and Predictors of Disturbed Sleep in a Large Population of College Students
Lund, H. G., Reider, B. D., Whiting, A. B., & Prichard, J. R. (2010) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2009.06.016 · Cited by 1,907 · see citing works
Sleep Schedules and Daytime Functioning in Adolescents
Wolfson, A. R., & Carskadon, M. A. (1998) · Child Development · doi:10.1111/j.1467-8624.1998.tb06149.x · Cited by 1,676 · see citing works
Self-citationSleep, circadian rhythms, and delayed phase in adolescence
Crowley, S. J., Acebo, C., & Carskadon, M. A. (2007) · Sleep Medicine · doi:10.1016/j.sleep.2006.12.002 · Cited by 1,127 · see citing works
Self-citationRegulation of adolescent sleep: Implications for behavior
CARSKADON, M. A., ACEBO, C., & JENNI, O. G. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.032 · Cited by 792 · see citing works
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Carskadon, M. A., Wolfson, A. R., Acebo, C., Tzischinsky, O., & Seifer, R. (1998) · Sleep · doi:10.1093/sleep/21.8.871 · Cited by 769 · see citing works
Self-citationCircadian preference, sleep and daytime behaviour in adolescence
Giannotti, F., Cortesi, F., Sebastiani, T., & Ottaviano, S. (2002) · Journal of Sleep Research · doi:10.1046/j.1365-2869.2002.00302.x · Cited by 703 · see citing works
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Hagenauer, M. H., Perryman, J. I., Lee, T. M., & Carskadon, M. A. (2009) · Developmental Neuroscience · doi:10.1159/000216538 · Cited by 593 · see citing works
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Fredriksen, K., Rhodes, J., Reddy, R., & Way, N. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00655.x · Cited by 510 · see citing works
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Jenni, O. G., Achermann, P., & Carskadon, M. A. (2005) · Sleep · doi:10.1093/sleep/28.11.1446 · Cited by 469 · see citing works
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Self-citationRegulation of sleepiness in adolescents: update, insights, and speculation
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Self-citationSleep EEG changes during adolescence: An index of a fundamental brain reorganization
Feinberg, I., & Campbell, I. G. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.09.008 · Cited by 280 · see citing works
Crowley, S. J., Van Reen, E., LeBourgeois, M. K., Acebo, C., Tarokh, L., Seifer, R., Barker, D. H., & Carskadon, M. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112199 · Cited by 273 · see citing works
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Moore, M., & Meltzer, L. J. (2008) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2008.01.001 · Cited by 235 · see citing works
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School-based sleep promotion programs: Effectiveness, feasibility and insights for future research
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Raniti, M. B., Allen, N. B., Schwartz, O., Waloszek, J. M., Byrne, M. L., Woods, M. J., Bei, B., Nicholas, C. L., & Trinder, J. (2017) · Behavioral Sleep Medicine · doi:10.1080/15402002.2015.1120198 · Cited by 117 · see citing works
Bonmati-Carrion, M. A., Middleton, B., Revell, V., Skene, D. J., Rol, M. A., & Madrid, J. A. (2014) · Chronobiology International · doi:10.3109/07420528.2013.820740 · Cited by 116 · see citing works
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Ming, X., Koransky, R., Kang, V., Buchman, S., Sarris, C. E., & Wagner, G. C. (2011) · Clinical Medicine Insights: Circulatory, Respiratory and Pulmonary Medicine · doi:10.4137/ccrpm.s7955 · Cited by 91 · see citing works
Hummer, D. L., Jechura, T. J., Mahoney, M. M., & Lee, T. M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00043.2006 · Cited by 52 · see citing works
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Vedaa, Ø., West Saxvig, I., Wilhelmsen-Langeland, A., Bjorvatn, B., & Pallesen, S. (2012) · Scandinavian Journal of Educational Research · doi:10.1080/00313831.2011.567396 · Cited by 39 · see citing works
Richardson, C. E., Gradisar, M., Short, M. A., & Lang, C. (2017) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2016.06.010 · Cited by 38 · see citing works
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Self-citation
- Authors
- Carskadon, M. A., Acebo, C., Richardson, G. S., Tate, B. A., & Seifer, R.
- Affiliations
- Brown University (US)
- Venue
- Journal of Biological Rhythms
- Publisher
- SAGE Publications
- Published
- 1997-06
- Volume
- 12
- Issue
- 3
- Pages
- 278-289
- ISSN
- 0748-7304 (ISSN-L)
- 1552-4531
- OpenAlex
- W2144397115
- Cited by
- 301
- References
- 21
- Citations by year
- 2026: 11 · 2025: 16 · 2024: 13 · 2023: 15 · 2022: 18 · 2021: 8 · 2020: 14 · 2019: 8 · 2018: 12 · 2017: 17 · 2016: 13 · 2015: 19 · 2014: 11 · 2013: 17 · 2012: 15
- FWCI
- 0.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Biological Rhythms (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH52415, R01MH052415)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- circadian rhythm, adolescents, dim light melatonin onset, sleep onset, sleep offset, constant routine, recovery sleep, puberty, Tanner stages, age differences, actigraphy
- MeSH terms
- Adolescent, Child, Child Development, Child, Preschool, Circadian Rhythm, Humans, Sleep
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