Adolescent sleep patterns in humans and laboratory animals

Hormones and Behavior

Volumn 64, Issue 2, 2013, Pages 270-279

  Hagenauer, Megan Hastings ^a,b   Lee, Theresa M ^a,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Adolescent; Chronotype; Circadian; Development; Homeostasis; Hormone; Puberty; Rodent; Sleep; Two process model

Indexed keywords

ADOLESCENCE; ALPHA RHYTHM; BETA RHYTHM; CIRCADIAN RHYTHM; DAYTIME SOMNOLENCE; DELTA RHYTHM; HUMAN; LIGHT EXPOSURE; NONHUMAN; NONREM SLEEP; PRIMATE; PRIORITY JOURNAL; PUBERTY; REM SLEEP; REVIEW; RODENT; SLEEP PATTERN; SLEEP TIME; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; SPECIES COMPARISON; THETA RHYTHM; WAKEFULNESS;

ADOLESCENT; CHRONOTYPE; CIRCADIAN; DEVELOPMENT; HOMEOSTASIS; HORMONE; PUBERTY; RODENT; SLEEP; TWO-PROCESS MODEL;

ADOLESCENT; ADOLESCENT PSYCHOLOGY; ANIMALS; ANIMALS, LABORATORY; HOMEOSTASIS; HUMANS; PUBERTY; SEXUAL MATURATION; SLEEP;

EID: 84883385321     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.01.013     Document Type: Review

References (111)

1. Ahnaou A., Nayak S., Heylen A., Ashton D., Drinkenburg W.H.I.M. Sleep and EEG profile in neonatal hippocampal lesion model of schizophrenia. Physiol. Behav. 2007, 92:461-467.
2. Alfoldi P., Tobler I., Borbely A.A. Sleep regulation in rats during early development. Am. J. Physiol. 1990, 258:R634-R644.
3. Andrade M., Menna-Barreto L. 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. M.A. Carskadon (Ed.).
4. Aserinsky E., Kleitman N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 1953, 118(3062):273-274.
5. Baker F.C., Turlington S.R., Colrain I. Developmental changes in the sleep electroencephalogram of adolescent boys and girls. J. Sleep Res. 2012, 21:59-67.
6. Bock J., Murmu R.P., Ferdman N., Leshem M., Braun K. Refinement of dendritic and synaptic networks in the rodent anterior cingulate and orbitofrontal cortex: critical impact of early and late social experience. Dev. Neurobiol. 2008, 68:685-695.
7. Borbely A.A., Baumann F., Brandeis D., Strauch I., Lehmann D. Sleep deprivation: effect on sleep stages and EEG power density in man. EEG Clin. Neurophysiol. 1981, 51:483-493.
8. Borisenkov M.F. The pattern of entrainment of the human sleep-wake rhythm by the natural photoperiod of the north. Chronobiol. Int. 2011, 28:921-929.
9. Bronzino J.D., Siok C.J., Austin K., Austin-Lafrance R.J., Morgane P.J. Spectral analysis of the electroencephalogram in the developing rat. Brain Res. Dev. Brain Res. 1987, 35:257-267.
10. Buchmann A., Ringli M., Kurth S., Schaerer M., Geiger A., Jenni O.G., Huber R. EEG sleep slow-wave activity as a mirror of cortical maturation. Cereb. Cortex 2011, 21:607-615.
11. Cain N., Gradisar M. Electronic media use and sleep in school-aged children and adolescents: a review. Sleep Med. 2010, 11:735-742.
12. Cambras T., Diez-Noguera A. Changes in motor activity during the development of the circadian rhythm in the rat. J. Interdiscip. Cycle Res. 1988, 19:65-74.
13. Campbell B. Adrenarche and the evolution of human life history. Am. J. Hum. Biol. 2006, 18:569-589.
14. Campbell B. Adrenarche in comparative perspective. Am. J. Hum. Biol. 2011, 23:44-52.
15. Campbell I.G., Feinberg I. Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. PNAS 2009, 106(13):5177-5180.
16. Campbell I.G., Darchia N., Higgins L.M., Dykan I.V., Davis N.M., de Bie E., Feinberg I. Adolescent changes in the homeostatic regulation of EEG activity in the delta and theta frequency bands during NREM sleep. Sleep 2011, 34(1):83-91.
17. Campbell I.G., Grimm K.J., de Bie E., Feinberg I. Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation. PNAS 2012, 109(15):5740-5743.
18. Carskadon M.A. Maturation of processes regulating sleep in adolescents. Sleep in Children: Developmental Changes in Sleep Patterns 2008, 95-109. Informa Healthcare. 2nd ed. C.L. Marcus, J.L. Carroll, D.F. Donnelly, G.M. Loughlin (Eds.).
19. Carskadon M.A. Sleep in adolescents: the perfect storm. Pediatr. Clin. North Am. 2011, 58:637-647.
20. Carskadon M.A., Acebo C. Regulation of sleepiness in adolescents: update, insights, and speculation. Sleep 2002, 25(6):606-614.
21. Carskadon M.A., Harvey K., Duke P., Anders T.F., Litt I.F., Dement W.C. Pubertal changes in daytime sleepiness. Sleep 1980, 2(4):453-460.
22. Carskadon M.A., Mancuso J., Rosekind M.R. Impact of part-time employment on adolescent sleep patterns. Sleep Res. 1989, 18:114.
23. Carskadon M.A., Vieira C., Acebo C. Association between puberty and delayed phase preference. Sleep 1993, 16:258-262.
24. Carskadon M.A., Acebo C., Richardson G.S., Tate B.A., Seifer R. An approach to studying circadian rhythms in adolescent humans. J. Biol. Rhythms 1997, 12(3):278-289.
25. Carskadon M.A., Wolfson A.R., Acebo C., Tzischinsky O., Seifer R. Adolescent sleep patterns, circadian timing, and sleepiness at a transition to early school days. Sleep 1998, 21:871-881.
26. Carskadon M.A., Labyak S.E., Acebo C., Seifer R. Intrinsic circadian period of adolescent humans measured in conditions of forced desynchrony. Neurosci. Lett. 1999, 260:129-132.
27. Carskadon M.A., Acebo C., Jenni O.G. Regulation of adolescent sleep: implications for behavior. Ann. N.Y. Acad. Sci. 2004, 1021:276-291.
28. Castro E.C.V., Andrade M.M.M. Longitudinal study of the spectral composition of behavioral rhythms in the rat. Biol. Rhythm. Res. 2005, 36:131-140.
29. Colrain I.M., Baker F.C. Changes in sleep as a function of adolescent development. Neuropsychol. Rev. 2011, 21:5-21.
30. Crowley S.J., Carskadon M.A. Modifications to weekend recovery sleep delay circadian phase in older adolescents. Chronobiol. Int. 2010, 27:1469-1492.
31. Crowley S.J., Acebo C., Carskadon M.A. Sleep, circadian rhythms, and delayed phase in adolescence. Sleep Med. 2007, 8:602-612.
32. Daan S., Beersma D.G.M., Borbely A.A. Timing of human sleep: recovery process gated by a circadian pacemaker. Am. J. Physiol. 1984, 246:R161-R178.
33. Dahl R.E. The development and disorders of sleep. Adv. Pediatr. 1998, 45:73-90.
34. Dement W., Kleitman N. Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. EEG Clin. Neurophysiol. 1957, 9:673-690.
35. Diez-Noguera A., Cambras T. Sex differences in the development of the motor activity circadian rhythm in rats under constant light. Physiol. Behav. 1990, 47:889-894.
36. Dijk D.J., Czeisler C.A. Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans. Neurosci. Lett. 1994, 166:63-68.
37. Edgar D.M., Dement W.C., Fuller C.A. Effect of SCN lesions on sleep in squirrel monkeys - evidence for opponent processes in sleep wake regulation. J. Neurosci. 1993, 13(3):1065-1079.
38. Feinberg I., Campbell I.G. Sleep EEG changes during adolescence: an index of fundamental brain reorganization. Brain Cogn. 2010, 72:56-65.
39. Feinberg I., Thode H.C., Chugani H.T., March J.D. Gamma distribution model describes maturational curves for delta wave amplitude, cerebral metabolic rate and synaptic density. J. Theor. Biol. 1990, 142:149-161.
40. Feinberg I., Davis N.M., de Bie E., Grimm K.J., Campbell I.G. The maturational trajectories of NREM and REM sleep durations differ across adolescence on both school night and extended sleep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 302:R533-R540.
41. Fleshner M., Booth V., Forger D.B., Diniz Behn C.G. Circadian regulation of sleep-wake behavior in nocturnal rats requires multiple signals from suprachiasmatic nucleus. Philos. Trans. R. Soc. Lond. A 2011, 369:3855-3883.
42. Frank M.G., Heller H.C. Development of diurnal organization of EEG slow-wave activity and slow-wave sleep in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1997, 273:R472-R478.
43. Franken P., Tobler I., Borbely A.A. Sleep homeostasis in the rat: simulation of the time course of EEG slow-wave activity. Neurosci. Lett. 1991, 130:141-144.
44. Gaudreau H., Carrier J., Montplaisir J. Age-related modifications of NREM sleep EEG: from childhood to middle age. J. Sleep Res. 2001, 10:165-172.
45. Giannotti F., Cortesi F. 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. M.A. Carskadon (Ed.).
46. Giedd J.N., Raznahan A., Mills K.L., Lenroot R.K. Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biol. Sex Differ. 2012, 3(19):1-9.
47. Golub M.S., Takeuchi P.T., Hendrickx C.L., Gershwin A.G. Activity and attention in zinc-deprived adolescent monkeys. Am. J. Clin. Nutr. 1996, 64(6):908-915.
48. Golub M.S., Takeuchi P.T., Hoban-Higgins T.M. Nutrition and circadian activity offset in adolescent rhesus monkeys. Adolescent Sleep Patterns: Biological, Social, and Psychological Influences 2002, 50-68. Cambridge University Press. M.A. Carskadon (Ed.).
49. Gradisar M., Gardner G., Dohnt H. Recent worldwide sleep patterns and problems during adolescence: a review and meta-analysis of age, region, and sleep. Sleep Med. 2011, 12:110-118.
50. Gvilia I., Suntsova N., Angara B., McGinty D., Szymusiak R. Maturation of sleep homeostasis in developing rats: a role for preoptic area neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R885-R894.
51. Hagenauer M.H., Lee T.M. The neuroendocrine control of the circadian system: Adolescent chronotype. Front. Neuroendocrinol. 2012, 33:211-229.
52. Hagenauer M.H., Perryman J.I., Lee T.M., Carskadon M.A. Adolescent changes in the homeostatic and circadian regulation of sleep. Dev. Neurosci. 2009, 31:276-284.
53. Hagenauer M.H., King A.F., Possidente B., McGinnis M.Y., Lumia A.R., Peckham E.M., Lee T.M. Changes in circadian rhythms during puberty in Rattus norvegicus: developmental time course and gonadal dependency. Horm. Behav. 2011, 60:46-57.
54. Hagenauer M.H., Ku J.H., Lee T.M. Chronotype changes during puberty depend on gonadal hormones in the slow-developing rodent, Octodon degus. Horm. Behav. 2011, 60:37-45.
55. Hummer D.L. Development and Sexual Differentiation of the Circadian System of Octodon Degus. Dissertation in Fulfillment of a Doctor of Philosophy in Psychology 2006, University of Michigan, Ann Arbor.
56. Hummer D.L., Jechura T.J., Mahoney M.M., Lee T.M. 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.
57. Ibuka N. Ontogenesis of circadian sleep-wakefulness rhythms and developmental changes of sleep in the altricial rat and in the precocial guinea pig. Behav. Brain Res. 1984, 11:185-196.
58. Jenni O.G., Carskadon M.A. Spectral analysis of the sleep electroencephalogram during adolescence. Sleep 2004, 27(4):774-783.
59. Jenni O.G., Carskadon M.A. Sleep behavior and sleep regulation from infancy through adolescence: normative aspects. Sleep Med. Clin. 2007, 2:321-329.
60. Jenni O.G., Achermann P., Carskadon M.A. Homeostatic sleep regulation in adolescents. Sleep 2005, 28(11):1446-1454.
61. Johnson C.H. Phase response curves: what can they tell us about circadian clocks?. Circadian Clocks from Cell to Human 1992, 209-246. Hokkaido University Press, Sapporo. T. Hiroshige, K. Honma (Eds.).
62. Joutsiniemi S.L., Leinonen L., Laakso M.L. Continuous recording of locomotor activity in groups of rats: postweaning maturation. Physiol. Behav. 1991, 50:649-654.
63. Jouvet-Mounier D., Astic L., Lacote D. Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev. Psychobiol. 1970, 2(4):216-239.
64. Karatsoreos I.N., Silver R. Minireview: the neuroendocrinology of the suprachiasmatic nucleus as a conductor of body time in mammals. Endocrinology 2007, 148:5640-5647.
65. Kas M.J.H., Edgar D.M. Circadian timed wakefulness at dawn opposes compensatory sleep responses after sleep deprivation in Octodon degus. Sleep 1999, 22(8):1045-1053.
66. Kennaway D.J. The role of circadian rhythmicity in reproduction. Hum. Reprod. Update 2005, 11:91-101.
67. Kurth S., Jenni O.G., Riedner B.A., Tononi G., Carskadon M.A., Huber R. Characteristics of sleep slow waves in children and adolescents. Sleep 2010, 33(4):475-480.
68. Kurth S., Ringli M., Geiger A., LeBourgeois M., Jenni O.G., Huber R. Mapping of cortical activity in the first two decades of life: a high-density sleep electroencephalographic study. J. Neurosci. 2010, 30(40):13211-13219.
69. Lewy A.J., Sack R.L. The dim light melatonin onset as a marker for circadian phase position. Chronobiol. Int. 1989, 93-102.
70. McGinnis M.Y., Lumia A.R., Tetel M.J., Molenda-Figueira H.A., 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.
71. Melo P.R., Belisio A.S., Menezes A.A.L., Azevedo C.V.M. Influence of seasonality on circadian motor activity rhythm in common marmosets during puberty. Chronobiol. Int. 2010, 27(7):1420-1437.
72. Mirmiran M., Van den dungen H., Uylings H.B.M. Sleep patterns during rearing under different environmental conditions in juvenile rats. Brain Res. 1982, 233:287-298.
73. Mistlberger R.E. Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res. Rev. 2005, 49:429-454.
74. Mong J.A., Baker F.C., Mahoney M.M., Paul K.N., Schwartz M.D., Semba K., Silver R. Sleep, rhythms, and the endocrine brain: influence of sex and gonadal hormones. J. Neurosci. 2011, 31:16107-16116.
75. Moser D., Anderer P., Gruber G., Parapatics S., Loretz E., Boeck M., Kloesch G., Heller E., Schmidt A., Danker-Hopfe H., Saletu B., Zeitlhofer J., Dorffner G. Sleep classification according to AASM and Rechtshaffen & Kales: effects on sleep scoring parameters. Sleep 2009, 32(2):139-149.
76. National Sleep Foundation Sleep and Teens Task Force Adolescent Sleep Needs and Patterns: Research Report and Resource Guide 2000, 1-26. National Sleep Foundation, Washington D.C.
77. Ojeda S.R., Urbanski H.F. Puberty in the rat. The Physiology of Reproduction. Raven 1994, 363-409. E. Knobil, J.D. Neill (Eds.).
78. Peixoto C.A.T., da Silva A.G.T., Carskadon M.A., Louzada F.M. Adolescents living in homes without electrical lighting have earlier sleep times. Behav. Sleep Med. 2009, 7:73-80.
79. Perryman J.I. Circadian and Homeostatic Components of Sleep Across Sex and Development in a Diurnal Rodent, Octodon Degus. Dissertation in Fulfillment of a Doctor of Philosophy in Neuroscience 2010, University of Michigan, Ann Arbor.
80. Phillips A.J.K., Robinson P.A., Kedziora D.J., Abeysuriya R.G. Mammalian sleep dynamics: how diverse features arise from a common physiological framework. PLOS Comput. Biol. 2010, 6(6, e1000826):1-9.
81. Plant T.M. Puberty in primates. The Physiology of Reproduction. Raven 1994, 453-485. E. Knobil, J.D. Neill (Eds.).
82. Randler C. Gender differences in Morningness-Eveningness during adolescence. J. Genet. Psychol. 2011, 172(3):302-303.
83. Raznahan A., Lee Y., Stidd R., Long R., Greenstein D., Clasen L., Addington A., Gogtay N., Rapoport J.L., Giedd J.N. Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. PNAS 2010, 107(39):16988-16993.
84. Roenneberg T., Daan S., Merrow M. The art of entrainment. J. Biol. Rhythms 2003, 18:183-194.
85. Roenneberg T., Kuehnle T., Pramstaller P.P., Ricken J., Havel M., Guth A., Merrow M. A marker for the end of adolescence. Curr. Biol. 2004, 14:R1038-R1039.
86. Russo P.M., 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.
87. Sadeh A., Dahl R.E., Shahar G., Rosenblat-Stein S. Sleep and the transition to adolescence: a longitudinal study. Sleep 2009, 32:1602-1609.
88. Sellix M.T., Menaker M. Circadian clocks in the ovary. Trends Endocrinol. Metab. 2010, 21:628-636.
89. Shaffery J.P., Lopez J., Bissette G., Roffwarg H.P. Rapid eye movement sleep deprivation in post-critical period, adolescent rats alters the balance between inhibitory and excitatory mechanisms in visual cortex. Neurosci. Lett. 2006, 393:131-135.
90. Sharkey K.M., Carskadon M.A., Figueiro M.G., Zhu Y., Rea M.S. Effects of an advanced sleep schedule and morning short wavelength light exposure on circadian phase in young adults with late sleep schedules. Sleep Med. 2011, 12:685-692.
91. Sieck G.C., Ramaley J.A., Harper R.M., Taylor A.N. Sleep-wakefulness changes at the time of puberty in the female rat. Brain Res. 1976, 116:346-352.
92. Sieck G.C., Ramaley J.A., Harper R.M., Taylor A.N. Puberty-related alterations in the organization of sleep-wakefulness states: differences between spontaneous and induced pubertal conditions. Exp. Neurol. 1978, 61:407-420.
93. Sisk C.L., Foster D.L. The neural basis of puberty and adolescence. Nat. Neurosci. 2004, 7:1040-1047.
94. Sisk C., Zehr J. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 2005, 26:163-174.
95. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 24:417-463.
96. Tarokh L., Carskadon M.A., Achermann P. Dissipation of sleep pressure is stable across adolescence. Neuroscience 2012, 216:167-177.
97. Taylor D.J., Jenni O.G., Acebo C., Carskadon M.A. Sleep tendency during extended wakefulness: insights into adolescent sleep regulation and behavior. J. Sleep Res. 2005, 14:239-244.
98. Terman L.M., Hocking A. The sleep of school age children: its distribution according to age and its relation to physical and mental efficiency. Part 1: the distribution of sleep according to age. J. Educ. Psychol. 1913, 4:138-147.
99. Terman L.M., Hocking A. The sleep of school age children: its distribution according to age and its relation to physical and mental efficiency. Part 3: the conditions of children's sleep. J. Educ. Psychol. 1913, 4(5):269-282.
100. Thorleifsdottir B., Bjornsson J.K., Benediktsdottir B., Gislason T.H., Kristbjarnarson H. Sleep and sleep habits from childhood to young adulthood over a 10-year period. J. Psychosom. Res. 2002, 53:529-537.
101. Tobler I., Borbeley A.A. Sleep EEG in the rat as a function of prior waking. Electroencephalogr. Clin. Neurophysiol. 1986, 64:74-76.
102. Tobler I., Franken P., Trachsel L., Borbeley A.A. Models of sleep regulation in mammals. J. Sleep Res. 1992, 1:125-127.
103. Turek F.W., Van Cauter E. Rhythms in reproduction. The Physiology of Reproduction. Raven 1994, 487-540. E. Knobil, J.D. Neill (Eds.).
104. Van den Bulck J. Television viewing, computer game playing, and internet use and self-reported time to bed and time out of bed in secondary school children. Sleep 2004, 27:101-104.
105. Van Eden C.G., Uylings H.B.M. Postnatal volumetric development of the prefrontal cortex in the rat. J. Comp. Neurol. 1985, 241:268-274.
106. Vollmer C., Michel U., Randler C. Outdoor light at night (LAN) is correlated with eveningness in adolescents. Chronobiol. Int. 2012, 29(4):502-508.
107. 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.
108. Weinert D., Waterhouse J. Daily activity and temperature rhythms do not change spontaneously with age in laboratory mice. Physiol. Behav. 1999, 66:605-612.
109. Weinert D., Eimert H., Erkert H.G., Schneyer U. Resynchronization of the circadian corticosterone rhythm after a light/dark shift in juvenile and adult mice. Chronobiol. Int. 1994, 11:222-231.
110. Yang C.K., Kim J.K., Patel S.R., Lee J.H. Age-related changes in sleep/wake patterns among Korean teenagers. Pediatrics 2005, 115:250-260.
111. Yasenkov R., Deboer T. Circadian regulation of sleep and the sleep EEG under constant sleep pressure in the rat. Sleep 2010, 33(5):631-641.