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A Longitudinal Assessment of Sleep Timing, Circadian Phase, and Phase Angle of Entrainment across Human Adolescence
Open accessAbstract
The aim of this descriptive analysis was to examine sleep timing, circadian phase, and phase angle of entrainment across adolescence in a longitudinal study design. Ninety-four adolescents participated; 38 (21 boys) were 9-10 years ("younger cohort") and 56 (30 boys) were 15-16 years ("older cohort") at the baseline assessment. Participants completed a baseline and then follow-up assessments approximately every six months for 2.5 years. At each assessment, participants wore a wrist actigraph for at least one week at home to measure self-selected sleep timing before salivary dim light melatonin onset (DLMO) phase - a marker of the circadian timing system - was measured in the laboratory. Weekday and weekend sleep onset and offset and weekend-weekday differences were derived from actigraphy. Phase angles were the time durations from DLMO to weekday sleep onset and offset times. Each cohort showed later sleep onset (weekend and weekday), later weekend sleep offset, and later DLMO with age. Weekday sleep offset shifted earlier with age in the younger cohort and later in the older cohort after age 17. Weekend-weekday sleep offset differences increased with age in the younger cohort and decreased in the older cohort after age 17. DLMO to sleep offset phase angle narrowed with age in the younger cohort and became broader in the older cohort. The older cohort had a wider sleep onset phase angle compared to the younger cohort; however, an age-related phase angle increase was seen in the younger cohort only. Individual differences were seen in these developmental trajectories. This descriptive study indicated that circadian phase and self-selected sleep delayed across adolescence, though school-day sleep offset advanced until no longer in high school, whereupon offset was later. Phase angle changes are described as an interaction of developmental changes in sleep regulation interacting with psychosocial factors (e.g., bedtime autonomy).
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![Figure 3 A proposed model to explain phase angle to sleep onset differences in the younger (top) and older (bottom) adolescent cohorts. Black horizontal bars illustrate average sleep times for each cohort (younger: 21:55–06:35; older: 23:02–06:40). Bold lines illustrate sleep pressure accumulation and dissipation functions predicted by the homeostatic sleep system. The upward facing arrow indicates the average DLMO phase for each age group (younger: 20:42; older: 20:54), and the right-facing block arrow shows the interval between DLMO phase and sleep onset (phase angle to sleep onset). Based on previous modeling work, [27] the saturating exponential function reaches it maximum more quickly and therefore at an earlier clock time in the younger cohort compared to the older cohort. We propose that the older adolescents are able to stay awake for a longer period of time (∼2 h) after DLMO phase compared to the younger adolescents (∼1 h) because of this developmental difference in homeostatic sleep pressure at the end of the waking day.](/paper-figures/3541c22d806f4e9e8531eb3570c4fd3a/a-longitudinal-assessment-of-sleep-timing-circadian-phase-and-phase-angle-of-figure-3.jpg)
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In the citing paper
“In general, the timing of sleep onset and waking and other biological rhythms (for example, fluctuations in melatonin levels) is earlier relative to adults during early childhood8,9 and shifts later during adolescence, and this shift in timing may be conserved among rodents and non-human primates (NHPs)10.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [10]
In the citing paper
“Early school start times, which are typically more than an hour earlier in US high schools (ages 15–18 years) than in elementary schools (ages 9–10 years) or middle schools (ages 11–13 years), may contribute to these problems of shorter sleep10,148.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [10]
In the citing paper
“circadian rhythms naturally delay”
From Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents (2018) · cites this paper as [38]
In the citing paper
“Changes in sleep/circadian timing appear to result from both phase delays in the timing of the circadian clock (38), and a slower accumulation in homeostatic sleep drive (37).”
From Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents (2018) · cites this paper as [38]
In the citing paper
“Decreased sleep duration and increased sleep disturbance may be a consequence of delayed sleep timing, conflicting with school start times on weekdays, (typically earlier in high school than in elementary or middle school), resulting in circadian misalignment and sleep loss (38,45).”
From Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents (2018) · cites this paper as [38]
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Citations
Cites
Tanner, J. M. (1978) · Medical Entomology and Zoology · Cited by 3,742
Social Jetlag: Misalignment of Biological and Social Time
Wittmann, M., Dinich, J., Merrow, M., & Roenneberg, T. (2006) · Chronobiology International · doi:10.1080/07420520500545979 · Cited by 2,625 · cited 1×
“Larger degrees of social jetlag have been associated with reduced alertness and performance [40,41,42,43], greater use of alcohol, nicotine and caffeine, and an increased risk for depression and obesity [39,44,45].”
BackgroundSleep 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 · cited 1×
“A previous crosssectional comparison [38] and longitudinal assessment [23] of sleep times across the transition from high school to college also showed a pattern of delayed wake-up times.”
BackgroundSleep 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 · cited 4×
“Other previous cross-sectional survey findings showed a similar delayed pattern across the adolescent years [1,21], though not as large as that reported by Roenneberg and colleagues.”
BackgroundResultInfluentialSelf-citationA marker for the end of adolescence
Roenneberg, T., Kuehnle, T., Pramstaller, P. P., Ricken, J., Havel, M., Guth, A., & Merrow, M. (2004) · Current Biology · doi:10.1016/j.cub.2004.11.039 · Cited by 1,585 · cited 2×
“A shift toward ‘‘eveningness’’ also emerges as youngsters age [10], and this shift appears to be linked to pubertal development [11,12].”
BackgroundActivity-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 · cited 1×
“, Ardsley, NY, USA) to estimate sleep/wake using the validated ‘‘Sadeh’’ algorithm [34].”
MethodSelf-citationRoenneberg, T., Allebrandt, K. V., Merrow, M., & Vetter, C. (2012) · Current Biology · doi:10.1016/j.cub.2012.03.038 · Cited by 1,407 · cited 2×
“Roenneberg and colleagues [39] reported that the degree to which weekend and weekday sleep timing differ increases over the second decade of life, and they relate the phenomenon to the construct of ‘‘social jetlag’’ (i.”
BackgroundSleep Duration From Infancy to Adolescence: Reference Values and Generational Trends
Iglowstein, I., Jenni, O. G., Molinari, L., & Largo, R. H. (2003) · PEDIATRICS · doi:10.1542/peds.111.2.302 · Cited by 1,318 · cited 1×
“sleep time [1,9,13,14,15,16,17,18,19].”
Association 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 · cited 1×
“A shift toward ‘‘eveningness’’ also emerges as youngsters age [10], and this shift appears to be linked to pubertal development [11,12].”
BackgroundSelf-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 · cited 1×
“times on non-school or vacation mornings as youngsters age [1,2,3,4,5,6,7].”
BackgroundSelf-citation
Cited by
Sorted by citations
Rhythms of life: circadian disruption and brain disorders across the lifespan
Logan, R. W., & McClung, C. A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0088-y · Cited by 713
An update on adolescent sleep: New evidence informing the perfect storm model ☆
Crowley, S. J., Wolfson, A. R., Tarokh, L., & Carskadon, M. A. (2018) · Journal of Adolescence · doi:10.1016/j.adolescence.2018.06.001 · Cited by 684
Self-citationSleep in adolescence: Physiology, cognition and mental health
Tarokh, L., Saletin, J. M., & Carskadon, M. A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.008 · Cited by 552
Self-citationChronotypes in the US–influence of age and sex
Fischer, D., Lombardi, D. A., Marucci-Wellman, H., & Roenneberg, T. (2017) · PLOS ONE · doi:10.1371/journal.pone.0178782 · Cited by 502
Circadian disruption and human health
Fishbein, A. B., Knutson, K. L., & Zee, P. C. (2021) · Journal of Clinical Investigation · doi:10.1172/jci148286 · Cited by 468
“Because adolescents are susceptible to phase delays (8, 186, 187), circadian misalignment is commonly associated with greater metabolic effects in this population (188, 189) and potentially effects on the CV system (190).”
Background
Metadata
- Authors
- Crowley, S. J., Van Reen, E., LeBourgeois, M. K., Acebo, C., Tarokh, L., Seifer, R., Barker, D. H., & Carskadon, M. A.
- Affiliations
- Rush University Medical Center (US)
- University of Colorado Boulder (US)
- Brown University (US)
- University of Bern (CH)
- University of South Australia (AU)
- Corresponding author
- Crowley, Stephanie J.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-11-07
- Volume
- 9
- Issue
- 11
- Pages
- e112199
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4224451
- OpenAlex
- W2090080078
- Cited by
- 273
- References
- 60
- Citations by year
- 2026: 27 · 2025: 19 · 2024: 21 · 2023: 31 · 2022: 25 · 2021: 26 · 2020: 22 · 2019: 33 · 2018: 25 · 2017: 21 · 2016: 15 · 2015: 8
- FWCI
- 7.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- BORIS (University Library Bern) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UniSA Research Outputs Repository (University of South Australia) (submittedVersion)
- Open Access CRIS of the University of Bern
- Funders
- Brown University
- Jazz Pharmaceuticals
- National Institutes of Health
- National Institute on Alcohol Abuse and Alcoholism (AA 13252, R01AA013252)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- sleep timing, circadian phase, adolescence, dim light melatonin onset, sleep onset, sleep offset, circadian entrainment, salivary melatonin
- MeSH terms
- Adolescent, Aging, Child, Circadian Rhythm, Female, Humans, Longitudinal Studies, Male, Melatonin, Saliva, Sex Characteristics, Sleep, Time Factors, Actigraphy
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