CoChat
Sign Up
Cited by 143Circadian rhythm and melatoninSleep and Wakefulness ResearchHypothalamic control of reproductive hormones

The neuroendocrine control of the circadian system: Adolescent chronotype

Open access
Hagenauer, Megan Hastings, Lee, Theresa M.·2012·Frontiers in Neuroendocrinology
DOI 10.1016/j.yfrne.2012.04.003PMC PMC4762453
Open this paper in CoChat — free account

Abstract

Scientists, public health and school officials are paying growing attention to the mechanism underlying the delayed sleep patterns common in human adolescents. Data suggest that a propensity towards evening chronotype develops during puberty, and may be caused by developmental alterations in internal daily timekeeping. New support for this theory has emerged from recent studies which show that pubertal changes in chronotype occur in many laboratory species similar to human adolescents. Using these species as models, we find that pubertal changes in chronotype differ by sex, are internally generated, and driven by reproductive hormones. These chronotype changes are accompanied by alterations in the fundamental properties of the circadian timekeeping system, including endogenous rhythm period and sensitivity to environmental time cues. After comparing the developmental progression of chronotype in different species, we propose a theory regarding the ecological relevance of adolescent chronotype, and provide suggestions for improving the sleep of human adolescents.

AI snapshot

Written from the paper’s full text.

TL;DR

This review argues that adolescent evening chronotype is driven in part by pubertal gonadal hormones acting on the circadian system, supported by cross-species evidence that rest/activity timing shifts during puberty and by hormone manipulations in rats and degus. It proposes that multiple circadian properties change during puberty and adolescence, with implications for sleep, clinical care, and school start times.

Key findings

  • Human adolescents require as much as 9–10 hours of sleep per night, yet over 45% in the United States report less than 8 hours on school nights; a meta-analysis of 13 studies from 9 countries found weekend bedtimes delayed by ~2.75 hours between ages 11–18. Girls begin the sleep-timing delay one year earlier than boys, with maximum delay at 19.5 years in girls versus 20.9 years in boys, and boys show more extreme chronotype changes across adolescence.
  • In laboratory rats and degus, pubertal rest/activity rhythms shifted by 2–4 hours, with male degus and rats showing 3–5 hour changes; gonadectomy before puberty either eliminated or diminished the shift, and in male rats the mechanism likely involves activational testosterone converted locally to estrogen. The shift persisted under constant conditions, indicating it is internally generated rather than a passive masking response to light.
  • Human adolescents had an endogenous circadian period of 24.27 h, significantly longer than the 24.12 h found in adults using similar forced-desynchrony protocols. Pubertal mice were more sensitive to evening light than adults, and some human evidence suggests adolescents are less responsive to morning light, though findings are mixed.
  • Later school start times by 30 min–1 h increased weekday total sleep by 15–45 minutes, reduced daytime sleepiness and unhappiness reports, and a 1 h delay was associated with a 16% drop in adolescent car accident rate; another study found 16–19% fewer teen car accidents per year per capita in a city with 75–80 minutes later start times.

Methods

  • Narrative review combined with original rodent experiments: the authors monitored secondary sex development and daily wheel-running activity rhythms in nocturnal rats and diurnal degus under varying hormonal conditions, monitored sleep electrophysiology in pubertal degus, and performed gonadectomy and hormone-replacement studies.
  • They also placed juvenile rats in constant lighting conditions to test whether pubertal activity changes were internally generated, and conducted an intensive review of existing developmental sleep and circadian literature to assess generalization across mammalian species, including humans.
  • Main analysis was qualitative cross-species comparison of developmental chronotype progression, circadian free-running period, light sensitivity, rhythm consolidation, and gonadal hormone dependence.

Limitations

  • The paper states that multiple experiments remain necessary: human chronotype correlations with circulating testosterone and estrogen need confirmation, some light-sensitivity studies lacked child or older adult control groups, rodent puberty is not necessarily analogous to human puberty, and species differences in hormonal effects on circadian rhythms are substantial. The authors also note that a previous study observed chronotype changes in both male and female degus during puberty, making their female degu conclusion tentative, and that unpublished SCN clock-gene data found little physiological evidence for altered circadian phasing.
  • Evident from the text: this is a narrative review rather than a systematic review, many human studies cited are cross-sectional or retrospective, and causal claims about hormonal mechanisms in humans remain indirect because much of the strongest experimental evidence comes from rodent models with different pubertal timing and reproductive physiology.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.yfrne.2012.04.003

Cites

208 of 208 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 237 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Pubertal changes in chronotype are internally generated.

    “Using these species as models, we find that pubertal changes in chronotype differ by sex, are internally generated, and driven by reproductive hormones.”
    Quote in the paperSubstantial claim
  • Findingown data

    Chronotype changes during puberty are accompanied by alterations in fundamental properties of the circadian timekeeping system, including endogenous rhythm period and sensitivity to environmental time cues.

    “These chronotype changes are accompanied by alterations in the fundamental properties of the circadian timekeeping system, including endogenous rhythm period and sensitivity to environmental time cues.”
    Quote in the paperSubstantial claim
  • Findingown data

    Pubertal changes in chronotype differ by sex.

    “Using these species as models, we find that pubertal changes in chronotype differ by sex, are internally generated, and driven by reproductive hormones.”
    Quote in the paperSubstantial claim
  • Findingcitation

    The pubertal shift in timing of daily rest and activity occurs whether measured by wheel-running activity or general sleep patterns using sleep electrophysiology.

    “This shift in the timing of daily rest and activity occurred whether we were observing wheel-running activity or general sleep patterns using sleep electrophysiology (degus: [148]; similar data are presented for a small sample size of rats in [76]).”
    Quote in the paperSubstantial claim
  • Findingown data

    Both rodent species showed a large (2-4) hr shift in the phasing of their rest/activity rhythms during pubertal development.

    “This meant that, overall, both rodent species showed a large (2-4) hr shift in the phasing of their rest/activity rhythms during pubertal development, similar to human adolescents (Figure 2C-D, [66-67, 75, 114, 185]).”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [66] Hagenauer MH King AF Possidente B McGinnis MY Lumia AR Peckham EM Lee TM Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency Horm Behav 2011 60 46 57 21397604 PMC3112245 source

      Not checked in the free run.

    • cites [67] Hagenauer MH Ku JH Lee TM Chronotype changes during puberty depend on gonadal hormones in the slow-developing rodent, Octodon degus Horm Behav 2011 60 37 45 21316365 PMC3112253 source

      Not checked in the free run.

    • cites [75] Hummer DL Jechura TJ Mahoney MM Lee TM Gonadal hormone effects on entrained and free-running rhythms in the developing diurnal rodent, Octodon degus Am J Physiol Regul Integr Comp Physiol 2007 292 R586 R597 16917014 source

      Not checked in the free run.

    • cites [114] McGinnis MY Lumia AR Tetel MJ Molenda-Figueira HA Possidente B Effects of anabolic androgenic steroids on the development and expression of running wheel activity and circadian rhythms in male rats Physiol Behav 2007 92 1010 1018 17716697 PMC4476530 source

      Not checked in the free run.

  • May combine two claims. 64
  • Classified as probably not a substantial claim. 28

  • May combine two claims.

    Findingown data

    Gonadectomized animals either completely lacked a shift in chronotype during the normal pubertal period (degus) or showed a much diminished shift (rats).

    “We found that gonadectomized animals either completely lacked a shift in chronotype during the normal pubertal period (degus: [67, 75]) or showed a much diminished shift in chronotype (rats: [66]).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [67] Hagenauer MH Ku JH Lee TM Chronotype changes during puberty depend on gonadal hormones in the slow-developing rodent, Octodon degus Horm Behav 2011 60 37 45 21316365 PMC3112253 source

      Not checked in the free run.

    • cites [75] Hummer DL Jechura TJ Mahoney MM Lee TM Gonadal hormone effects on entrained and free-running rhythms in the developing diurnal rodent, Octodon degus Am J Physiol Regul Integr Comp Physiol 2007 292 R586 R597 16917014 source

      Not checked in the free run.

    • cites [66] Hagenauer MH King AF Possidente B McGinnis MY Lumia AR Peckham EM Lee TM Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency Horm Behav 2011 60 46 57 21397604 PMC3112245 source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    The activity patterns of animals gonadectomized before puberty resembled those of prepubertal rodents, as well as those of animals gonadectomized during adulthood in previous studies.

    “The activity patterns of the animals gonadectomized before puberty resembled those of prepubertal rodents, as well as those of animals that were gonadectomized during adulthood in previous studies.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingcitation

    In degus, females did not seem to shift their activity rhythms at all during puberty, despite males showing large changes in chronotype.

    “For degus, the sex difference was absolute: females did not seem to shift their activity rhythms at all during puberty, despite the fact that males showed large changes in chronotype [67].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Hagenauer MH Ku JH Lee TM Chronotype changes during puberty depend on gonadal hormones in the slow-developing rodent, Octodon degus Horm Behav 2011 60 37 45 21316365 PMC3112253 source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    The crepuscular-like activity distribution in juvenile rats persisted under constant conditions and was immediately exaggerated, with even more activity occurring at the end of the active period.

    “To our surprise, the crepuscular-like activity distribution not only persisted under constant conditions, it was immediately exaggerated, with even more activity occurring at the end of the active period.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingcitation

    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].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [70] Hagenauer MH Perryman JI Lee TM Carskadon MA Adolescent changes in the homeostatic and circadian regulation of sleep Dev Neurosci 2009 31 276 284 19546564 PMC2820578 source

      Not checked in the free run.

    • cites [198] Weinert D Kompauerova V Light induced phase and period responses of circadian activity rhythms in laboratory mice of different age Zoology 1998 101 45 52 source

      Not checked in the free run.

  • May combine two claims.

    Findingnone given

    In rats, both males and females show changes in free-running period around the time of puberty, but these changes differ by sex, with males showing a lengthening and females showing a shortening.

    “In rats, both males and females show changes in free-running period around the time of puberty, but these changes differ by sex, with males showing a lengthening of free-running period and females showing a shortening.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Findingnone given

    In rats, the hormone responsible for pubertal chronotype change is testosterone, which is converted locally into estrogen.

    “Finally, in rats, we have learned that the hormone responsible for pubertal chronotype change is testosterone, which is converted locally into estrogen.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    These changes exhibited sex differences and are, at least partially, dependent on gonadal hormones.

    “These changes exhibited sex differences and are, at least partially, dependent on gonadal hormones.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Other fundamental circadian properties change during puberty and adolescence, including free-running period and circadian sensitivity to light.

    “We also demonstrated that other fundamental circadian properties change during puberty and adolescence, including free-running period and circadian sensitivity to light.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingcitation

    In rats, the increase in the amplitude of rest/activity rhythms during puberty is particularly notable and strongly related to pubertal hormones: prepubertal gonadectomy prevents activity levels from increasing much beyond prepubertal levels in both males and females.

    “In rats, the increase in the amplitude of rest/activity rhythms during puberty is particularly notable and strongly related to pubertal hormones: prepubertal gonadectomy prevents activity levels from increasing much beyond prepubertal levels in both males and females [66].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [66] Hagenauer MH King AF Possidente B McGinnis MY Lumia AR Peckham EM Lee TM Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency Horm Behav 2011 60 46 57 21397604 PMC3112245 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    In the degu, there is a brief increase in activity levels during puberty that appears only to be related to gonadal hormones in females, and which then disappears as the animals mature, so the increase in activity level cannot explain the development of more consolidated, phase-advanced rest/activity rhythms during puberty.

    “In the degu, there is a brief increase in activity levels during puberty that appears only to be related to gonadal hormones in females, and which then disappears as the animals mature [67], so the increase in activity level cannot explain the development of more consolidated, phase-advanced rest/activity rhythms during puberty.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Hagenauer MH Ku JH Lee TM Chronotype changes during puberty depend on gonadal hormones in the slow-developing rodent, Octodon degus Horm Behav 2011 60 37 45 21316365 PMC3112253 source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Circadian phase is more delayed during puberty than adulthood in rats and degus, as it is in humans and macaques.

    “However, the observation was clearly replicated that circadian phase is more delayed during puberty than adulthood [75, 114] as it is in humans and macaques [60, 160].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [75] Hummer DL Jechura TJ Mahoney MM Lee TM Gonadal hormone effects on entrained and free-running rhythms in the developing diurnal rodent, Octodon degus Am J Physiol Regul Integr Comp Physiol 2007 292 R586 R597 16917014 source

      Not checked in the free run.

    • cites [114] McGinnis MY Lumia AR Tetel MJ Molenda-Figueira HA Possidente B Effects of anabolic androgenic steroids on the development and expression of running wheel activity and circadian rhythms in male rats Physiol Behav 2007 92 1010 1018 17716697 PMC4476530 source

      Not checked in the free run.

    • cites [60] Golub MS Takeuchi PT Hoban-Higgins TM Carskadon MA Nutrition and circadian activity offset in adolescent rhesus monkeys Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 50 68 Cambridge University Press source

      Not checked in the free run.

    • cites [160] Roenneberg T Kuehnle T Pramstaller PP Ricken J Havel M Guth A Merrow M A marker for the end of adolescence Curr Biol 2004 14 R1038 R1039 15620633 source

      Not checked in the free run.

  • May combine two claims.

    Findingreasoning

    A number of components of the circadian system change during puberty, including free-running period, circadian light sensitivity, rhythm consolidation, and rhythm amplitude.

    “These data suggest that a number of components of the circadian system change during puberty, including free-running period, circadian light sensitivity, rhythm consolidation, and rhythm amplitude.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In Iceland over 70% of individuals between the ages of 16-21 reported frequent daytime sleepiness.

    “In Iceland over 70% of individuals between the ages of 16-21 reported frequent daytime sleepiness [188].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [188] Thorleifsdottir B Bjornsson JK Benediktsdottir B Gislason TH Kristbjarnarson H Sleep and sleep habits from childhood to young adulthood over a 10-year period J Psychosom Res 2002 53 529 537 12127168 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Similar trends of insufficient sleep have been observed in other modern societies, including Korea, Brazil, and Italy.

    “Similar trends have been observed in other modern societies, including Korea, Brazil, and Italy [11, 59, 62, 209].”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [11] Andrade M Menna-Barreto L Carskadon MA Sleep Patterns of High School Students Living in Sao Paulo, Brazil Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 118 131 Cambridge University Press source

      Not checked in the free run.

    • cites [59] Giannotti F Cortesi F Carskadon MA Sleep Patterns and Daytime Function in Adolescence: An Epidemiological Survey of an Italian High School Student Sample Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 132 147 Cambridge University Press source

      Not checked in the free run.

    • cites [62] Gradisar M Gardner G Dohnt H Recent worldwide sleep patterns and problems during adolesence: A review and meta-analysis of age, region, and sleep Sleep Med 2011 12 110 118 21257344 source

      Not checked in the free run.

    • cites [209] Yang CK Kim JK Patel SR Lee JH Age-related changes in sleep/wake patterns among Korean teenagers Pediatrics 2005 115 250 260 15866859 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Over 45% of adolescents in the United States report obtaining less than 8 hours of sleep on school nights.

    “Despite this fact, over 45% of adolescents in the United States report obtaining less than 8 hours of sleep on school nights [137].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [137] Neuman A Gothilf Y Haim A Ben-Aharon G Zisapel N Nocturnal patterns and up-regulated excretion of the melatonin metabolite 6-sulfatoxymelatonin in the diurnal rodent Psammomys obesus post-weaning under a short photoperiod Comp Biochem Physiol 2005 A 142 297 307 16172010 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    15-52% of adolescents have problems with excessive sleepiness, including oversleeping, inadvertent napping, and sleeping during class.

    “Other surveys indicate that 15-52% of adolescents have problems with excessive sleepiness, including oversleeping, inadvertent napping, and sleeping during class [62].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [62] Gradisar M Gardner G Dohnt H Recent worldwide sleep patterns and problems during adolesence: A review and meta-analysis of age, region, and sleep Sleep Med 2011 12 110 118 21257344 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In other cultures, similar developmental timing is observed, although the peak delay may occur as early as 15-16 years of age.

    “In other cultures, similar developmental timing is observed, although the peak delay may occur as early as 15-16 years of age [45, 163, 188, 209].”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [45] Crowley SJ Acebo C Carskadon MA Sleep, circadian rhythms, and delayed phase in adolescence Sleep Med 2007 8 602 612 17383934 source

      Not checked in the free run.

    • cites [163] Russo PM Bruni O Lucidi F Ferri R Violani C Sleep Habits and Circadian Preference in Italian Children and Adolescents J Sleep Res 2007 16 163 169 17542946 source

      Not checked in the free run.

    • cites [188] Thorleifsdottir B Bjornsson JK Benediktsdottir B Gislason TH Kristbjarnarson H Sleep and sleep habits from childhood to young adulthood over a 10-year period J Psychosom Res 2002 53 529 537 12127168 source

      Not checked in the free run.

    • cites [209] Yang CK Kim JK Patel SR Lee JH Age-related changes in sleep/wake patterns among Korean teenagers Pediatrics 2005 115 250 260 15866859 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Weekend bedtimes delayed by ~2.75 hrs between the ages of 11-18, even though overall bedtimes and wake times varied by culture.

    “A recent metanalysis of 13 studies from 9 countries indicated that weekend bedtimes delayed by ~2.75 hrs between the ages of 11-18, even though overall bedtimes and wake times varied by culture [62].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [62] Gradisar M Gardner G Dohnt H Recent worldwide sleep patterns and problems during adolesence: A review and meta-analysis of age, region, and sleep Sleep Med 2011 12 110 118 21257344 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Girls show maximum delay at the age of 19.5 years, and boys show maximum delay later at 20.9 years.

    “Similarly, girls show maximum delay at the age of 19.5 years, and boys show maximum delay later at 20.9 years [160].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [160] Roenneberg T Kuehnle T Pramstaller PP Ricken J Havel M Guth A Merrow M A marker for the end of adolescence Curr Biol 2004 14 R1038 R1039 15620633 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisenone given

    The timing of sleep derives from three primary components: an internal circadian timekeeping system, a homeostatic drive for sleep, and external constraints (masking).

    “Traditionally, the timing of sleep is thought to derive from three primary components: an internal (endogenous) daily circadian timekeeping system, a homeostatic drive for sleep (“sleep pressure”) that builds up over the course of being awake and decreases during sleep, and other external constraints (which are often referred to as “masking”).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The SCN sends a daily signal to GnRH neurons; when estrogen levels are high, this signal helps drive the GnRH/LH surge that leads to ovulation.

    “Further investigation revealed that the SCN sends a signal daily to GnRH neurons. When estrogen levels are high, this signal helps drive the GnRH/LH surge that leads to ovulation [39].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [39] Chappell PE Clocks and the Black Box: Circadian influences on gonadotropin releasing hormone secretion J Neuroendocrinol 2005 17 119 130 15796763 source

      Not checked in the free run.

  • May combine two claims.

    Premisenone given

    Gonadal hormones can transiently affect activity and permanently organize the circadian system.

    “Gonadal hormones can transiently affect activity and permanently organize the circadian system.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Scientifically, the terms puberty and adolescence refer to separate concepts.

    “Although colloquially the terms “puberty” and “adolescence” are used interchangeably, scientifically they refer to separate concepts [179].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [179] Sisk C Zehr J Pubertal hormones organize the adolescent brain and behavior Front Neuroendocrinol 2005 26 163 174 16309736

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Physiological correlates of sexual maturation include development of the HPG axis, increases in circulating gonadal hormones, and maturation of the testes, ovaries, uterus, and external genitalia.

    “Therefore, most researchers measure the physiological correlates of sexual maturation – the development of the HPG axis, increases in circulating gonadal hormones (e.g., testosterone, estrogen), and the maturation of the testes, ovaries, uterus, and external genitalia [158].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [158] Richardson GS Tate BA Carskadon MA Endocrine changes associated with puberty and adolescence Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 27 39 Cambridge University Press

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation

    PER2 rhythms are phase-advanced by gonadectomy in males and by early pregnancy in females, but not by the estrous cycle.

    “Rhythms for the clock protein, PER2, are phase-advanced by gonadectomy in males [147], and by early pregnancy in females [169], but not by the estrous cycle [147].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [147] Perrin JS Segall LA Harbour VL Woodside B Amir S The expression of the clock protein PER2 in the limbic forebrain is modulated by the estrous cycle Proc Natl Acad Sci U.S.A 2006 103 5591 5596 16554373 PMC1459398 source

      Not checked in the free run.

    • cites [169] Schrader JA Nunez AA Smale L Changes in and dorsal to the rat suprachiasmatic nucleus during early pregnancy Neuroscience 2010 171 513 523 20807562 PMC2975742 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The effects of gonadal hormones on circadian physiology are diverse, and likely to be dependent on the nature and duration of hormone exposure, the surrounding hormonal milieu, and the sex of the individual.

    “Thus, it seems that the effects of gonadal hormones on circadian physiology are diverse, and likely to be dependent on the nature and duration of hormone exposure, the surrounding hormonal milieu, and the sex of the individual, suggesting that the function of gonadal effects on the circadian system may be similarly diverse.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationreasoning

    Since reproductive hormones alter circadian rhythms and circadian physiology during early development and adulthood, puberty should also be a time of circadian rhythm development.

    “Since reproductive hormones alter circadian rhythms and circadian physiology during early development and adulthood, we expect that puberty should also be a time of circadian rhythm development.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Premisecitation

    Puberty is defined as the process leading to the attainment of sexual maturation, beginning with the activation of the HPG axis and ending with reproductive competency.

    “Traditionally, puberty is defined as the process leading to the attainment of sexual maturation [181], beginning with the activation of the HPG axis, and ending with reproductive competency [153, 178].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [181] Spear LP The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 2000 24 417 463 10817843 source

      Not checked in the free run.

    • cites [153] Plant TM Knobil E Neill JD Puberty in primates The Physiology of Reproduction 1994 453 485 Raven

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [178] Sisk CL Foster DL The neural basis of puberty and adolescence Nat Neurosci 2004 7 1040 1047 15452575 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Ovariectomy causes an 8 hour delay in the VIP transcript rhythm in the SCN, so that its phasing resembles that of intact males.

    “In the case of VIP, which is a neurotransmitter that is important for oscillator coupling, ovariectomy causes a remarkable 8 hour delay, so that the phasing of the transcript rhythm resembles that of intact males [97, 107].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [97] Krajnak K Kashon ML Rosewell KL Wise PM Sex differences in the daily rhythm of vasoactive intestinal polypeptide but not arginine vasopressin messenger ribonucleic acid in the suprachiasmatic nuclei Endocrinology 1998 139 4189 4196 9751499 source

      Not checked in the free run.

    • cites [107] Mahoney MM Ramanathan C Hagenauer MH Lee TM Smale L Daily Rhythms and sex differences in vasoactive intestinal polypeptide, VIPR2 receptor and arginine vasopressin mRNA in the suprachiasmatic nucleus of a diurnal rodent, Arvicanthis niloticus Eur J Neurosci 2009 30 1537 1543 19811536 PMC2775094 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Estrogen enhances electrical intercellular coupling by increasing the number of gap junctions in the SCN, in a manner opposed by progesterone.

    “Estrogen enhances electrical intercellular coupling by increasing the number of gap junctions in the SCN, [175, 176] in a manner that is opposed by progesterone [176].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [175] Shinohara K Funabashi T Mitushima D Kimura F Effects of estrogen on the expression of connexin32 and connexin43 mRNAs in the suprachiasmatic nucleus of female rats Neurosci Lett 2000 286 107 110 10825648 source

      Not checked in the free run.

    • cites [176] Shinohara K Funabashi T Nakamura TJ Kimura F Effects of estrogen and progesterone on the expression of connexin-36 mRNA in the suprachiasmatic nucleus of female rats Neurosci Lett 2001 309 37 40 11489541 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Puberty is a time of intense hormonal change.

    “Puberty is a time of intense hormonal change.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Some sex differences in circadian parameters are activated by the different hormonal milieu of adult males and females, and some arise organizationally during development.

    “Although some of these sex differences are activated by the different hormonal milieu of adult males and females, some sex differences also arise organizationally during development [23].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Brockman R Bunick D Mahoney MM Estradiol deficiency during development modulates the expression of circadian and daily rhythms in male and female aromatase knockout mice Horm Behav 2011 60 439 447 21816154 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Pubertal changes in the distribution of activity were internally-generated and not a change in the passive response of the animals to the light cycle.

    “These data suggested that pubertal changes in the distribution of activity were internally-generated and not a change in the passive response of the animals to the light cycle [66].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [66] Hagenauer MH King AF Possidente B McGinnis MY Lumia AR Peckham EM Lee TM Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency Horm Behav 2011 60 46 57 21397604 PMC3112245 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    In degus, it is unlikely that the hormonal effects on chronotype are purely activational, but may instead represent a permanent, organizational change to the sensitive pubertal brain.

    “Thus, in this species it is unlikely that the hormonal effects on chronotype are purely activational, but may instead represent a permanent, organizational change to the sensitive pubertal brain (e.g., [75]).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [75] Hummer DL Jechura TJ Mahoney MM Lee TM Gonadal hormone effects on entrained and free-running rhythms in the developing diurnal rodent, Octodon degus Am J Physiol Regul Integr Comp Physiol 2007 292 R586 R597 16917014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Ovariectomized adult female rodents lost the phase advance and increase in wheel running activity that typically accompanies estrus, and in general exhibited a more dispersed activity distribution and delayed activity rhythm phase.

    “This was also true of ovariectomized adult female rodents: they lost the phase advance and increase in wheel running activity that typically accompanies estrus [49, 78, 100, 129], and in general exhibited a more dispersed activity distribution and delayed activity rhythm phase [187, 203, although see 23].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [49] Davis FC Darrow JM Menaker M Sex differences in the circadian control of hamster wheel-running activity Am J Physiol 1983 244 R93 R105 6849422

      Not checked in the free run.

    • cites [78] Iwahana E Karatsoreos I Shibata S Silver R Gonadectomy reveals sex differences in circadian rhythms and suprachiasmatic nucleus androgen receptors in mice Horm Behav 2008 53 422 430 18164002 PMC3266066 source

      Not checked in the free run.

    • cites [100] Labyak SE Lee TM Estrus- and steroid-induced changes in circadian rhythms in a diurnal rodent, Octodon degus Physiol Behav 1995 58 573 585 8587967 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The presence of sex differences suggested that pubertal hormones might drive the chronotype shift.

    “The presence of sex differences suggested that pubertal hormones might drive the chronotype shift.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Administration of testosterone or dihydrotestosterone to castrated adult males restored normal circadian activity patterns, and estrogen treatment reconsolidated rhythms in ovariectomized rats.

    “In these previous studies, the administration of testosterone or dihydrotestosterone to castrated adult males was able to restore the normal circadian activity patterns [47, 78, 90, 128] and estrogen treatment was able to reconsolidate rhythms in ovariectomized rats [187, 203].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [47] Daan S Damassa D Pittendrigh CS Smith ER An effect of castration and testosterone replacement on the circadian pacemaker in mice Proc Natl Acad Sci U.S.A 1975 72 3744 3747 1059163 PMC433074 source

      Not checked in the free run.

    • cites [78] Iwahana E Karatsoreos I Shibata S Silver R Gonadectomy reveals sex differences in circadian rhythms and suprachiasmatic nucleus androgen receptors in mice Horm Behav 2008 53 422 430 18164002 PMC3266066 source

      Not checked in the free run.

    • cites [90] Karatsoreos IN Wang A Sasanian J Silver R A role for androgens in regulating circadian behavior and the suprachiasmatic nucleus Endocrinology 2007 148 5487 5495 17702841 PMC3281763 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    In humans, there is moderate support for the hypothesis that the circadian system is especially sensitive to evening light in adolescents, and less sensitive to morning light.

    “In humans, there is moderate support for the hypothesis that the circadian system is especially sensitive to evening light in adolescents, and less sensitive to morning light.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    These changes in free-running period do not predict the pubertal change in chronotype, which takes the form of a phase-advance in both sexes.

    “Thus, these changes in free-running period do not predict the pubertal change in chronotype, which takes the form of a phase-advance in both sexes [66].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [66] Hagenauer MH King AF Possidente B McGinnis MY Lumia AR Peckham EM Lee TM Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency Horm Behav 2011 60 46 57 21397604 PMC3112245 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    An intervention that increased exposure of adolescents (ages 15-17 years) to bright, short-wavelength light in the morning on weekends had little effect, implying that the circadian systems of the adolescents were relatively insensitive to morning light.

    “To their surprise, these interventions had little effect, implying that the circadian systems of the adolescents were relatively insensitive to morning light [46].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [46] Crowley SJ Carskadon MA Modifications to weekend recovery sleep delay circadian phase in older adolescents Chronobiol Int 2010 27 1669 1492 PMC3415304 20795887 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Human adolescents have an endogenous period of 24.27 h, significantly longer than the period length found in adults (24.12 h) using similar protocols.

    “They found that human adolescents have an endogenous period of 24.27 h, significantly longer than the period length found in adults (24.12 h) using similar protocols [28, 34].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [28] Carskadon MA Marcus CL Carroll JL Donnelly DF Loughlin GM Maturation of processes regulating sleep in adolescents Sleep in Children: Developmental Changes in Sleep Patterns 2008 95 109 Informa Healthcare ed 2

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [34] Carskadon MA Labyak SE Acebo C Seifer R Intrinsic circadian period of adolescent humans measured in conditions of forced desynchrony Neurosci Lett 1999 260 129 132 10025716 source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationreasoning

    A lengthening of free-running period during adolescence, as seen in human adolescents, would be expected to cause a delay in circadian chronotype, whereas a shortening of free-running period, as seen in young male degus, would be expected to produce an advance in chronotype.

    “In that case, a lengthening of free-running period during adolescence, as is seen in human adolescents, would be expected to cause a delay in circadian chronotype, whereas a shortening of free-running period, as is seen in young male degus, would be expected to produce an advance in chronotype.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductreasoning

    Both of these studies lacked a child or older adult control group, and thus it is unclear whether morning light treatment under these particular conditions advances circadian phase in individuals of any age.

    “However, it should be noted that both of these studies lacked a child or older adult control group, and thus it is unclear whether morning light treatment under these particular conditions advances circadian phase in individuals of any age.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    A change in free-running period could cause an adolescent change in chronotype or entrained phase, because it would alter the amount of daily resetting necessary for circadian rhythms to entrain to a normal 24 hr day.

    “A change in free-running period could also cause an adolescent change in chronotype or entrained phase, because it would alter the amount of daily resetting that is necessary for circadian rhythms to entrain to a normal 24 hr day.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    During the transition from winter to spring, adolescents became more evening type, and this change in chronotype correlated with increased light exposure in the evening but not the morning.

    “Another study found that during the transition from winter to spring, adolescents became more evening type, and this change in chronotype correlated with increased light exposure in the evening but not the morning [55].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [55] Figueiro MG Rea MS Evening daylight may cause adolescents to sleep less in spring thatn in winter Chronobiol Int 2010 27 1242 1258 20653452 PMC3349220 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    A recent study by Randler et al. suggests a positive correlation between evening chronotype and circulating testosterone levels in adult men (ages 19-37).

    “As mentioned earlier, a recent study by Randler et al. [156] suggests that there is a positive correlation between evening chronotype and circulating testosterone levels in adult men (ages 19-37).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [156] Randler C Ebenhöh N Fischer A Hoechel S Schroff C Stoll JC Vollmer C Chronotype but not to sleep length is related to salivary testosterone in young adult men Psychoneuroendocrinology in press 22425131 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Sex differences in the range of entrainment of the circadian system in hamsters seemed to depend on gonadal hormone exposure during puberty.

    “One study observed that sex differences in the range of entrainment of the circadian system in hamsters seemed to depend on gonadal hormone exposure during puberty [49].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [49] Davis FC Darrow JM Menaker M Sex differences in the circadian control of hamster wheel-running activity Am J Physiol 1983 244 R93 R105 6849422

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The timing of adolescent phase changes in humans displays sex differences and human males show larger phase changes than females.

    “Since the timing of adolescent phase changes in humans also displays sex differences and human males show larger phase changes than females [160]”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [160] Roenneberg T Kuehnle T Pramstaller PP Ricken J Havel M Guth A Merrow M A marker for the end of adolescence Curr Biol 2004 14 R1038 R1039 15620633 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Gonadal hormones can alter properties of the suprachiasmatic nucleus related to oscillator coupling (e.g., the number of electrical gap junctions connecting cells, glial cell proliferation, VIP signaling).

    “Similarly, we know that gonadal hormones can alter properties of the suprachiasmatic nucleus related to oscillator coupling (e.g., the number of electrical gap junctions connecting cells, glial cell proliferation, VIP signaling).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationreasoning

    To alter chronotype, each of these changes would need to alter the phasing of SCN rhythms.

    “However, to alter chronotype, we believe that each of these changes would need to alter the phasing of SCN rhythms.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The correlation between these anatomical changes, secondary sex development and pubertal hormones has not been explicitly tested.

    “However, the correlation between these anatomical changes, secondary sex development and pubertal hormones has not been explicitly tested.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    Gonadal hormones can affect everything from the sensitivity of the circadian system to time cues, to the phasing and coupling of oscillators within the SCN, as well as the strength of SCN output and phasing of downstream oscillators.

    “As discussed earlier, we know that gonadal hormones can affect everything from the sensitivity of the circadian system to time cues, to the phasing and coupling of oscillators within the SCN, as well as the strength of SCN output and phasing of downstream oscillators.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Adolescents in Brazil who did not have electrical lighting at home had significantly earlier sleep onsets and less sleep deprivation than their peers.

    “Indeed, a recent study found that adolescents in Brazil who did not have electrical lighting at home had significantly earlier sleep onsets and less sleep deprivation than their peers [146].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [146] Peixoto CAT da Silva AGT Carskadon MA Louzada FM Adolescents living in homes without electrical lighting have earlier sleep times Behav Sleep Med 2009 7 73 80 19330580 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    It is likely that multiple aspects of the circadian timekeeping system are affected by pubertal hormones, suggesting that adolescent changes in chronotype may derive from the effects of hormones on the circadian timekeeping system.

    “We conclude that it is likely that multiple aspects of the circadian timekeeping system are affected by pubertal hormones, suggesting that adolescent changes in chronotype may derive from the effects of hormones on the circadian timekeeping system.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    There are pronounced species differences in the degree of circadian regulation of the hypothalamic pituitary gonadal axis, so it makes sense that gonadal hormone feedback should be similarly diverse.

    “Indeed, since there are pronounced species differences in the degree of circadian regulation of the hypothalamic pituitary gonadal axis [39], it makes sense that gonadal hormone feedback should be similarly diverse.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [39] Chappell PE Clocks and the Black Box: Circadian influences on gonadotropin releasing hormone secretion J Neuroendocrinol 2005 17 119 130 15796763 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The relationship between phase changes and pubertal timing in each species, as well as the dependency on pubertal hormones, suggests that the comparison to the phase delay between pre-puberty and sexual maturity in humans and macaques may be more appropriate, although the direction of phase change during puberty clearly differs between these species.

    “The relationship between phase changes and pubertal timing in each species, as well as the dependency on pubertal hormones, suggests that the latter comparison may be more appropriate, although the direction of phase change during puberty clearly differs between these species.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [60] Golub MS Takeuchi PT Hoban-Higgins TM Carskadon MA Nutrition and circadian activity offset in adolescent rhesus monkeys Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 50 68 Cambridge University Press source

      Not checked in the free run.

    • cites [160] Roenneberg T Kuehnle T Pramstaller PP Ricken J Havel M Guth A Merrow M A marker for the end of adolescence Curr Biol 2004 14 R1038 R1039 15620633 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The dam nurses predominantly during the day, and this nursing pattern has a large influence on the phasing of activity rhythms in the pups.

    “The dam nurses predominantly during the day, and this nursing pattern has a large influence on the phasing of activity rhythms in the pups [174, 182, 186].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [174] Shimoda K Hanada K Yamada N Takahashi K Takahashi S Periodic exposure to mother is potent zeitgeber of rat pups’ rhythm Physiol. Behav 1985 36 723 730 3714847 source

      Not checked in the free run.

    • cites [182] Sugishita M Takashima M Takeuchi Y Kato Y Yamauchi T Takahashi K Periodic mother deprivation during the light period reversed the phase of serotonin N-acetyltransferase activity rhythm of the pineal gland in rat pups Pharmacol Biochem Behav 1993 46 609 615 8278438 source

      Not checked in the free run.

    • cites [186] Thiels E Alberts JR Cramer CP Weaning in rats: II pup behavior patterns Dev Psychobiol 1990 23 495 510 2272406 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The pups will exhibit a diurnal activity pattern until around age P18 when they begin to consume significant amounts of solid food.

    “The pups will exhibit a diurnal activity pattern until around age P18 when they begin to consume significant amounts of solid food [21, 186].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [21] Bolles RC Woods PJ The ontogeny of behavior in the albino rat Anim Behav 1964 12 427 441 source

      Not checked in the free run.

    • cites [186] Thiels E Alberts JR Cramer CP Weaning in rats: II pup behavior patterns Dev Psychobiol 1990 23 495 510 2272406 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Pubertal hormones may have different effects on the circadian system of primates and rodents.

    “Therefore, alternatively, it could simply be that pubertal hormones have different effects on the circadian system of primates and rodents.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The causal mechanisms of the phenomenon, as suggested by the relationship between circadian changes and pubertal timing, sex, and gonadal dependence, indicate that the phenomenon that we are observing is analogous between species, whereas the formal characteristics may differ.

    “The causal mechanisms of the phenomenon, as suggested by the relationship between circadian changes and pubertal timing, sex, and gonadal dependence, indicate that the phenomenon that we are observing is analogous between species, whereas the formal characteristics may differ in the ways discussed above.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [20] Beach FA Potter R Whelan J Animal models for human sexuality Sex, Hormones and Behavior 113 143 Ciba Foundation Symposium 62, Excerpta Medica Amsterdam 1979 256826

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Puberty in primates is characterized by several years of preceding gonadal quiescence, whereas puberty in rodents follows low-level steroidogenesis throughout the infantile and juvenile periods.

    “Likewise, as discussed in the introduction, puberty in primates is characterized by several years of preceding gonadal quiescence [153], whereas puberty in rodents follows low-level steroidogenesis throughout the infantile and juvenile periods [139].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [153] Plant TM Knobil E Neill JD Puberty in primates The Physiology of Reproduction 1994 453 485 Raven

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [139] Ojeda SR Urbanski HF Knobil E Neill JD Puberty in the rat The Physiology of Reproduction 1994 363 409 Raven

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisereasoning

    Amongst toad species, it is extremely common for younger toads (metamorphlings) to be diurnal, whereas juveniles are crepuscular, and adults are active early in the night.

    “Amongst toad species, it is extremely common for younger toads (metamorphlings) to be diurnal, whereas juveniles are crepuscular, and adults are active early in the night.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    On weekends, there is a secondary peak in sexual activity that develops in the morning, which occurs around the time that testosterone peaks in men, again suggesting that the weekday evening peak may be an artifact of modern conditions.

    “On weekends, there is a secondary peak in sexual activity that develops in the morning [142], which occurs around the time that testosterone peaks in men [190], again suggesting that the weekday evening peak may be an artifact of modern conditions.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [142] Palmer JD Udry JR Morris NM Diurnal and weekly but no lunar rhythms in human copulation Hum Biol 1982 54 111 121 7200945

      Not checked in the free run.

    • cites [190] Turek FW Van Cauter E Knobil E Neill JD Rhythms in Reproduction The Physiolog of Reproduction 1994 487 540 Raven

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Interpretationcitation

    The reason for the toad chronotype shift appears to be related to the risk of predation for the young toads as well as the need to avoid dehydration.

    “The reason for this chronotype shift appears to be related to the risk of predation for the young toads as well as the need to avoid dehydration.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [57] Freeland WJ Kerin SH Ontogenetic alteration of activity and habitat selection by Bufo marinus Wildl Res 1991 18 431 437 source

      Not checked in the free run.

    • cites [152] Pizatto L Child T Shine R Why be Diurnal? Shifts in activity time enable young cane toads to evade cannibalistic conspecifics Behav Ecol 2008 19 990 997

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    College freshman are commonly the subject of human psychological studies, but current evidence suggests that they exhibit rhythms atypical of the rest of the population and exist in a perpetual state of sleep deprivation.

    “Likewise, college freshman are commonly the subject of human psychological studies, but current evidence suggests that they exhibit rhythms atypical of the rest of the population and exist in a perpetual state of sleep deprivation.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    The most important conclusion of our review is that hormonally-driven changes in circadian activity during puberty are common across mammalian species, and therefore likely to be found in humans as well.

    “The most important conclusion of our review is that hormonally-driven changes in circadian activity during puberty are common across mammalian species, and therefore likely to be found in humans as well.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Testosterone levels are lower in individuals that are frequent recipients of aggressive behavior, and higher in individuals that are frequent initiators (chimpanzees).

    “For example, testosterone levels are lower in individuals that are frequent recipients of aggressive behavior, and higher in individuals that are frequent initiators (chimpanzees: [12]).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [12] Anestis SF Testosterone in juvenile and adolescent male chimpanzees (Pan troglodytes): Effects of dominance, rank, aggression, and behavioral style Am J Phys Anthropol 2006 130 536 545 16425194 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Juvenile chubs are diurnal, whereas adult chubs are nocturnal.

    “For example, juvenile chubs (a variety of fish) are diurnal, whereas adult chubs are nocturnal.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [106] Magnan P FitzGerald GJ Ontogenetic changes in diel activity, food habits, and spatial distribution of juvenile and adult creek chub Env Biol Fish 1984 11 301 307 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The circadian timekeeping system is sensitive to gonadal hormones because it plays an integral role in the HPG axis.

    “According to the gonadal hormone “feedback” theory, the circadian timekeeping system is sensitive to gonadal hormones because it plays an integral role in the HPG axis (as reviewed earlier; [89]).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [89] Karatsoreos IN Silver R Minireview: The Neuroendocrinology of the Suprachiasmatic Nucleus as a Conductor of Body Time in Mammals Endocrinology 2007 148 5640 5647 17901227 PMC3423957 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    There is a tendency for humans to be more sexually active in the evening, which could provide incentive for individuals to stay up later.

    “There is a tendency for humans to be more sexually active in the evening, which could provide incentive for individuals to stay up later.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Pubertal animals also start to be treated competitively by adults, and aggressive interactions can peak during the pubertal period in some species.

    “Pubertal animals also start to be treated competitively by adults, and aggressive interactions can peak during the pubertal period in some species [181].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [181] Spear LP The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 2000 24 417 463 10817843 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The effects of sleep deprivation on grades, car accident risk, and mood are indisputable.

    “The effects of sleep deprivation on grades, car accident risk, and mood are indisputable [27, 201, 202].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [27] Carskadon MA Carskadon MA Risks of driving while sleepy in adolescents and young adults Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 148 158 Cambridge University Press

      Not checked in the free run.

    • cites [201] Wolfson AR Carskadon MA Sleep Schedules and Daytime Functioning in Adolescents Child Dev 1998 69 875 887 9768476 source

      Not checked in the free run.

    • cites [202] Wolfson AR Carskadon MA Understanding Adolescent Sleep Patterns and School Performance: A Critical Appraisal Sleep Med Rev 2003 7 491 506 15018092 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    These chronotype differences in chubs are likely to be related to either risk of predation or optimal hunting time, since juvenile chubs have smaller mouths and consume different prey.

    “These chronotype differences are likely to be related to either risk of predation or optimal hunting time, since juvenile chubs have smaller mouths and consume different prey [106].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [106] Magnan P FitzGerald GJ Ontogenetic changes in diel activity, food habits, and spatial distribution of juvenile and adult creek chub Env Biol Fish 1984 11 301 307 source

      Not checked in the free run.

  • May combine two claims.

    Premisenone given

    During puberty in primates, individuals become increasingly more involved in the adult social hierarchy, engaging in more affiliative behaviors and associating with same sex adults.

    “During puberty in primates, individuals become increasingly more involved in the adult social hierarchy, engaging in more affiliative behaviors and associating with same sex adults.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Gonadal hormones correlate with competitive status during adulthood in many species as well as during puberty.

    “Gonadal hormones correlate with competitive status during adulthood in many species [73] as well as during puberty [12].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [73] Hirshenhauser K Oliveira RF Social modulation of androgens in male vertebrates: meta analysis of the challenge hypothesis Anim Behav 2006 71 265 277 source

      Not checked in the free run.

    • cites [12] Anestis SF Testosterone in juvenile and adolescent male chimpanzees (Pan troglodytes): Effects of dominance, rank, aggression, and behavioral style Am J Phys Anthropol 2006 130 536 545 16425194 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisereasoning

    Individuals that are regularly up early, and expose themselves to morning light, can shift their phase earlier.

    “Likewise, individuals that are regularly up early, and expose themselves to morning light, can shift their phase earlier.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    There is also increased sexual activity on weekends, which suggests that the daily rhythm in sexual activity is an artifact of the modern work week.

    “However, there is also increased sexual activity on weekends, which suggests that the daily rhythm in sexual activity is an artifact of the modern work week [142].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [142] Palmer JD Udry JR Morris NM Diurnal and weekly but no lunar rhythms in human copulation Hum Biol 1982 54 111 121 7200945

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Amongst rodent species, puberty overlaps with a play period, but late puberty is also a time of intense competition, as many individuals are eventually evicted or emigrate from the colony or living group (especially males).

    “Amongst rodent species, puberty overlaps with a play period [21, 181], but late puberty is also a time of intense competition [21], as many individuals are eventually evicted or emigrate from the colony or living group (especially males, [53]).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [21] Bolles RC Woods PJ The ontogeny of behavior in the albino rat Anim Behav 1964 12 427 441 source

      Not checked in the free run.

    • cites [181] Spear LP The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 2000 24 417 463 10817843 source

      Not checked in the free run.

    • cites [53] Ebensperger LA Chesh AS Castro RA Tolhuysen LO Quirici V Burger JR Hayes LD Instability rules social groups in the communal breeder rodent Octodon degus Ethol 2009 115 540 554 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Even the adolescents with earliest parental-set bedtimes only received 8 hrs 10 min of sleep per night, on average, far less than the recommended 9-10 hours.

    “However, even the adolescents with earliest parental-set bedtimes only received 8 hrs 10 min of sleep per night, on average [58], far less than the recommended 9-10 hours [33, 29].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [58] Gangwisch JE Babiss LA Malaspina D Turner JB Zammit GK Posner K Earlier parental set bedtimes as a protective factor against depression and suicidal ideation Sleep 2010 33 97 106 20120626 PMC2802254 source

      Not checked in the free run.

    • cites [33] Carskadon MA Harvey K Duke P Anders TF Litt IF Dement WC Pubertal changes in daytime sleepiness Sleep 1980 2 453 460 7403744 source

      Not checked in the free run.

    • cites [29] Carskadon MA Sleep in adolescents: The perfect storm Pediatr Clin N Amer 2011 58 637 647 PMC3130594 21600346 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Moving school start times modestly later (30 min-1 hr) was found to increase total sleep time on weekdays by 15-45 minutes, leading to a 20-30% decrease in the number of students reporting daytime sleepiness, difficulty staying awake during class, and tiredness that interfered with completing homework.

    “Moving school start times modestly later (30 min-1 hr) was found to increase total sleep time on weekdays by 15-45 minutes [48, 141], leading to a 20-30% decrease in the number of students reporting daytime sleepiness, difficulty staying awake during class, and tiredness that interfered with completing homework.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [48] Danner F Phillips B Adolescent sleep, school start times, and teen motor vehicle crashes J Clin Sleep Med 2008 4 533 535 19110880 PMC2603528 source

      Not checked in the free run.

    • cites [141] Owens JA Belon K Moss P Impact of delaying school start time on adolescent sleep, mood, and behavior Arch Pediatr Adolesc Med 2010 164 608 614 20603459

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In high or low latitudes, daylight exposure can also produce the added benefit of reducing seasonal affective disorder (SAD), a mood disorder that affects more adolescents than any other age group.

    “In high or low latitudes, daylight exposure can also produce the added benefit of reducing seasonal affective disorder (SAD), a mood disorder that affects more adolescents than any other age group [77, 189].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [77] Imai M Kayukawa Y Ohta T Li L Nakagawa T Cross-regional survey of seasonal affective disorders in adults and high school students in Japan J Affect Disord 2003 77 127 133 14607389 source

      Not checked in the free run.

    • cites [189] Tonetti L Barbato G Fabbri M Adan A Natale V Mood seasonality: A crosssectional study of subjects aged between 10-25 years J Affect Dis 2007 97 155 160 16860875 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Later school start times were associated with better academic performance, including decreased truancy, tardiness, and drop-out rate, and better grades in first hour classes.

    “Overall, later school start times were associated with better academic performance, including decreased truancy, tardiness, and drop-out rate, and better grades in first hour classes [141, 194].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [141] Owens JA Belon K Moss P Impact of delaying school start time on adolescent sleep, mood, and behavior Arch Pediatr Adolesc Med 2010 164 608 614 20603459

      Not checked in the free run.

    • cites [194] Wahlstrom KL Carskadon MA Accommodating the Sleep Patterns of Adolescents within Current Educational Structures: An Uncharted Path Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002 172 197 Cambridge University Press source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Two recent studies indicate that earlier parent-set bedtimes can help teenagers adjust to early school start times, leading to greater total sleep time, improved daytime wakefulness, reduced fatigue, and better emotional health.

    “Two recent studies indicate that earlier parent-set bedtimes can help teenagers adjust to early school start times, leading to greater total sleep time, improved daytime wakefulness, reduced fatigue, and better emotional health [58, 177].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [58] Gangwisch JE Babiss LA Malaspina D Turner JB Zammit GK Posner K Earlier parental set bedtimes as a protective factor against depression and suicidal ideation Sleep 2010 33 97 106 20120626 PMC2802254 source

      Not checked in the free run.

    • cites [177] Short MA Gradisar M Wright H Lack LC Dohnt H Carskadon MA Time for bed: Parent-set bedtimes associated with improved sleep and daytime functioning in adolescents Sleep 2011 34 797 800 21629368 PMC3098947 source

      Not checked in the free run.

84 of 84

  • The authors state this as an assumption.

    Teenagers attending the same grade in school are exposed to a similar social environment.

    “If we assume that teenagers attending the same grade in school are exposed to a similar social environment, this evidence suggests that a biological component drives adolescent sleep patterns.”

  • The paper relies on this without support.

    The timing of rest and activity rhythms derives from three primary components: an endogenous daily circadian timekeeping system, a homeostatic drive for sleep, and other external constraints (masking).

    “As discussed earlier, the timing of rest and activity rhythms is thought to derive from three primary components: an endogenous daily circadian timekeeping system, a homeostatic drive for sleep, and other external constraints (which are often referred to as “masking”).”

  • The paper relies on this without support.

    Animal models can be used to address fundamental questions regarding the delayed sleep patterns of human adolescents.

    “This review began with the concept that we could use animal models to address fundamental questions regarding the delayed sleep patterns of human adolescents, while avoiding the technical and ethical issues associated with using human subjects.”

  • The paper relies on this without support.

    The risks, needs, and social interactions of mammalian species, including humans, change during adolescent development.

    “Although, clearly, most human teenagers are not at high risk of being consumed by their parents, there is an argument to be made that the risks, needs, and social interactions of mammalian species, including humans, change during adolescent development.”
4 of 4

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • At the onset of puberty, sleep-wake cycles and melatonin rhythms start to phase delay, a shift that is dependent on the presence of gonadal hormones and coincides with sexual maturity.

    “At the onset of puberty, sleep–wake cycles and melatonin rhythms start to phase delay141 — a shift that is dependent on the presence of gonadal hormones, and that coincides with sexual maturity142,143.”

    From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [142]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Adolescent sleep statistic cites a sand-rat study

    Minor

    The cited reference [137] is listed as a study of melatonin excretion in the sand rat, not a study of US adolescents' reported sleep duration.

  • Gerbil VIP claim cites a GnRH cell-line study

    Minor

    The statement attributes findings about male gerbils' SCN VIP levels to [40], but the listed reference describes circadian gene expression in a hypothalamic GnRH-secreting cell line.

2 of 2

Cites

Flagged first, then by citations

Research works printed but not linked: 6

  1. Carskadon, 1989, Impact of part-time employment on adolescent sleep patterns, Sleep Res., 18, 114
  2. Carskadon, 2002, Failure to identify pubertally-mediated melatonin sensitivity to light in adolescents, Sleep, 25, A191
  3. Gritton, H., 2011. Bi-Directional Interactions between Cognition and Biological Rhythms. Dissertation in Fulfillment of a Doctor of Philosophy in Neuroscience. University of Michigan, Ann Arbor.
  4. Pinto, 1999, Neuroactive steroids alter the circadian system of the Syrian hamster in a phase-dependent manner, Life Sci., 65, 2497, 10.1016/S0024-3205(99)00516-0 · DOI · Paper page
  5. National Sleep Foundation Sleep and Teens Task Force, 2000. Adolescent Sleep Needs and Patterns: Research Report and Resource Guide. National Sleep Foundation, Washington, DC, pp. 1–26. <http://www.sleepfoundation.org/atf/cf/%7BF6BF2668-A1B4-4FE8-8D1A-A5D39340D9CB%7D/sleep_and_teens_report1.pdf>.
  6. Weinert, 1998, Light induced phase and period responses of circadian activity rhythms in laboratory mice of different age, Zoology, 101, 45

Cited by

Sorted by citations

Related

Authors
Hagenauer, M. H., & Lee, T. M.
Affiliations
University of Michigan (US)
ORCID
Venue
Frontiers in Neuroendocrinology
Publisher
Elsevier BV
Published
2012-08
Volume
33
Issue
3
Pages
211-229
ISSN
0091-3022 (ISSN-L)
DOI
10.1016/j.yfrne.2012.04.003
PMC
PMC4762453
OpenAlex
W2023562973
Semantic Scholar
aaa640668f3cfcefc43f84b815211e99075259cb
Cited by
143
References
208
Citations by year
2026: 10 · 2025: 22 · 2024: 12 · 2023: 14 · 2022: 13 · 2021: 14 · 2020: 10 · 2019: 7 · 2018: 6 · 2017: 9 · 2016: 6 · 2015: 6 · 2014: 7 · 2013: 7
FWCI
0.72
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Frontiers in Neuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Diabetes and Digestive and Kidney Diseases (T32DK071212)
Topics
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
evening chronotype, sleep onset delay, puberty, circadian clock, reproductive hormones, sex differences, adolescent sleep
MeSH terms
Adolescent, Adolescent Behavior, Animals, Circadian Rhythm, Female, Humans, Male, Neurosecretory Systems, Puberty, Reproduction, Sleep, Sleep Deprivation, Social Dominance, Suprachiasmatic Nucleus, Photoperiod, Estrous Cycle, Gonadal Hormones, Mice, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review