Weekly, seasonal, and chronotype-dependent variation of dim-light melatonin onset.


Journal

Journal of pineal research
ISSN: 1600-079X
Titre abrégé: J Pineal Res
Pays: England
ID NLM: 8504412

Informations de publication

Date de publication:
Apr 2021
Historique:
revised: 11 02 2021
received: 20 01 2021
accepted: 16 02 2021
pubmed: 21 2 2021
medline: 11 11 2021
entrez: 20 2 2021
Statut: ppublish

Résumé

In humans, the most important zeitgeber for entrainment is light. Laboratory studies have shown that meaningful changes in light exposure lead to phase shifts in markers of the circadian clock. In natural settings, light is a complex signal varying with external conditions and individual behaviors; nonetheless, phase of entrainment is assumed to be fairly stable. Here, we investigated the influence of season and weekly schedule (as indicators of variation in light landscapes) on phase of entrainment. Using a within-subjects design (N = 33), we assessed dim-light melatonin onset (DLMO) as a circadian phase marker in humans, on workdays and work-free days, in summer (under daylight saving time) and in winter, while also estimating sleep times from actimetry. Our mixed-model regressions show that both season and weekly structure are linked with changes in phase of entrainment and sleep. In summer, both DLMO and sleep times were about 1 hour earlier compared to winter, and sleep duration was shorter. On work-free days, DLMO and sleep times were later, and their phase relationship differed more relative to workdays. All these effects were stronger in later chronotypes (those who habitually sleep late). Our results confirm that phase of entrainment is earlier when stronger zeitgebers are present (summer) and show that it relates to midday or midnight rather than sunrise or sunset. Additionally, they suggest that late chronotypes are capable of rapid phase shifts each week as they move between workdays and work-free days, stimulating interesting questions about the stability of circadian phase under natural conditions.

Identifiants

pubmed: 33608951
doi: 10.1111/jpi.12723
doi:

Substances chimiques

Biomarkers 0
Melatonin JL5DK93RCL

Types de publication

Comparative Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e12723

Subventions

Organisme : Stichting voor de Technische Wetenschappen

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021 The Authors. Journal of Pineal Research published by John Wiley & Sons Ltd.

Références

Aschoff J. Circadian Clocks: Proceedings. Amsterdam, The Netherlands: North-Holland Publishing Company; 1965.
Duffy JF, Wright KP Jr. Entrainment of the human circadian system by light. J Biol Rhythms. 2005;20(4):326-338.
Roenneberg T, Foster RG. Twilight times: light and the circadian system. Photochem Photobiol. 1997;66(5):549-561.
Roenneberg T, Kantermann T, Juda M, Vetter C, Allebrandt KV. Light and the human circadian clock. Handb Exp Pharmacol. 2013;217:311-331.
Roenneberg T, Kumar CJ, Merrow M. The human circadian clock entrains to sun time. Curr Biol. 2007;17(2):R44-R45.
Shochat T, Santhi N, Herer P, Flavell SA, Skeldon AC, Dijk DJ. Sleep timing in late autumn and late spring associates with light exposure rather than sun time in college students. Front Neurosci. 2019;13:882.
Crowley SJ, Molina TA, Burgess HJ. A week in the life of full-time office workers: work day and weekend light exposure in summer and winter. Appl Ergon. 2015;46 (Pt A):193-200.
Refinetti R. Chronotype variability and patterns of light exposure of a large cohort of United States residents. Yale J Biol Med. 2019;92(2):179-186.
Thorne HC, Jones KH, Peters SP, Archer SN, Dijk DJ. Daily and seasonal variation in the spectral composition of light exposure in humans. Chronobiol Int. 2009;26(5):854-866.
Sletten TL, Vincenzi S, Redman JR, Lockley SW, Rajaratnam SM. Timing of sleep and its relationship with the endogenous melatonin rhythm. Front Neurol. 2010;1:137.
Burgess HJ, Eastman CI. The dim light melatonin onset following fixed and free sleep schedules. J Sleep Res. 2005;14(3):229-237.
Mongrain V, Lavoie S, Selmaoui B, Paquet J, Dumont M. Phase relationships between sleep-wake cycle and underlying circadian rhythms in Morningness-Eveningness. J Biol Rhythms. 2004;19(3):248-257.
Lewy AJ, Wehr TA, Goodwin FK, Newsome DA, Markey SP. Light suppresses melatonin secretion in humans. Science. 1980;210(4475):1267-1269.
Khalsa SB, Jewett ME, Cajochen C, Czeisler CA. A phase response curve to single bright light pulses in human subjects. J Physiol. 2003;549(Pt 3):945-952.
Honma K, Honma S, Kohsaka M, Fukuda N. Seasonal variation in the human circadian rhythm: dissociation between sleep and temperature rhythm. Am J Physiol. 1992;262(5 Pt 2):R885-R891.
Illnerová H, Zvolsky P, Vaněček J. The circadian rhythm in plasma melatonin concentration of the urbanized man: the effect of summer and winter time. Brain Res. 1985;328(1):186-189.
Kennaway DJ, Royles P. Circadian rhythms of 6-sulphatoxy melatonin, cortisol and electrolyte excretion at the summer and winter solstices in normal men and women. Acta Endocrinol (Copenh). 1986;113(3):450-456.
Arendt J, Middleton B. Human seasonal and circadian studies in Antarctica (Halley, 75 degrees S). Gen Comp Endocrinol. 2018;258:250-258.
Stothard ER, McHill AW, Depner CM, et al. Circadian entrainment to the natural light-dark cycle across seasons and the weekend. Curr Biol. 2017;27(4):508-513.
Kantermann T, Juda M, Merrow M, Roenneberg T. The human circadian clock's seasonal adjustment is disrupted by daylight saving time. Curr Biol. 2007;17(22):1996-2000.
Burgess HJ, Eastman CI. A late wake time phase delays the human dim light melatonin rhythm. Neurosci Lett. 2006;395(3):191-195.
Jelı́nková-Vondrašová D, Hájek I, Illnerová H. Adjustment of the human circadian system to changes of the sleep schedule under dim light at home. Neurosci Lett. 1999;265(2):111-114
Taylor A, Wright HR, Lack LC. Sleeping-in on the weekend delays circadian phase and increases sleepiness the following week. Sleep Biol Rhythms. 2008;6(3):172-179.
Yang CM, Spielman AJ, D'Ambrosio P, Serizawa S, Nunes J, Birnbaum J. A single dose of melatonin prevents the phase delay associated with a delayed weekend sleep pattern. Sleep. 2001;24(3):272-281.
Roenneberg T, Wirz-Justice A, Merrow M. Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms. 2003;18(1):80-90.
Barron ML. Light exposure, melatonin secretion, and menstrual cycle parameters: an integrative review. Biol Res Nurs. 2007;9(1):49-69.
Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation; 1996;1:82.
Buysse DJ, Reynolds CF III, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193-213.
Roenneberg T, Keller LK, Fischer D, Matera JL, Vetter C, Winnebeck EC. Human activity and rest in situ. Methods Enzymol. 2015;552:257-283.
R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:14065823; 2014.
Kuznetsova A, Brockhoff PB, Christensen RH. lmerTest package: tests in linear mixed effects models. J Stat Softw. 2017;82(13):1-26.
Champely S, Champely MS. Package ‘PairedData’; 2018.
Wickham H. ggplot2: Elegant Graphics for Data Analysis. Cham, Switzerland: Springer; 2016.
Wittmann M, Dinich J, Merrow M, Roenneberg T. Social jetlag: misalignment of biological and social time. Chronobiol Int. 2006;23(1-2):497-509.
Arendt J. Melatonin and human rhythms. Chronobiol Int. 2006;23(1-2):21-37.
Klerman EB, Gershengorn HB, Duffy JF, Kronauer RE. Comparisons of the variability of three markers of the human circadian pacemaker. J Biol Rhythms. 2002;17(2):181-193.
Lewy AJ. The dim light melatonin onset, melatonin assays and biological rhythm research in humans. Biol Signals Recept. 1999;8(1-2):79-83.
Lockley SW. Journal of pineal research guideline for authors: measuring melatonin in humans. J Pineal Res. 2020;69(2):e12664.
Roenneberg T, Kuehnle T, Pramstaller PP, et al. A marker for the end of adolescence. Curr Biol. 2004;14(24):R1038-R1039.
Roenneberg T, Kuehnle T, Juda M, et al. Epidemiology of the human circadian clock. Sleep Med Rev. 2007;11(6):429-438.
Duffy JF, Dijk DJ, Hall EF, Czeisler CA. Relationship of endogenous circadian melatonin and temperature rhythms to self-reported preference for morning or evening activity in young and older people. J Investig Med. 1999;47(3):141-150.
Benloucif S, Green K, L'Hermite-Baleriaux M, Weintraub S, Wolfe LF, Zee PC. Responsiveness of the aging circadian clock to light. Neurobiol Aging. 2006;27(12):1870-1879.
Sletten TL, Revell VL, Middleton B, Lederle KA, Skene DJ. Age-related changes in acute and phase-advancing responses to monochromatic light. J Biol Rhythms. 2009;24(1):73-84.
Olbrich D, Dittmar M. Older poor-sleeping women display a smaller evening increase in melatonin secretion and lower values of melatonin and core body temperature than good sleepers. Chronobiol Int. 2011;28(8):681-689.
Cain SW, Dennison CF, Zeitzer JM, et al. Sex differences in phase angle of entrainment and melatonin amplitude in humans. J Biol Rhythms. 2010;25(4):288-296.
Ruiz FS, Beijamini F, Beale AD, et al. Early chronotype with advanced activity rhythms and dim light melatonin onset in a rural population. J Pineal Res. 2020;69:e12675.
Duffy JF, Cain SW, Chang A-M, et al. Sex difference in the near-24-hour intrinsic period of the human circadian timing system. Proc Natl Acad Sci USA. 2011;108(Suppl 3):15602-15608.
Wright KP Jr, Gronfier C, Duffy JF, Czeisler CA. Intrinsic period and light intensity determine the phase relationship between melatonin and sleep in humans. J Biol Rhythms. 2005;20(2):168-177.
Lewy AJ. Circadian misalignment in mood disturbances. Curr Psychiatry Rep. 2009;11(6):459-465.
Kim SJ, Lim YC, Suh IB, Lee JH. Disrupted sleep maintenance is associated with altered circadian phase and phase angle in community-dwelling adults. Sleep Med. 2020;73:250-256.
Flynn-Evans EE, Shekleton JA, Miller B, et al. Circadian Phase and Phase Angle Disorders in Primary Insomnia. Sleep. 2017;40(12):zsx163.
Roenneberg T, Hut R, Daan S, Merrow M. Entrainment concepts revisited. J Biol Rhythms. 2010;25(5):329-339.
Wehr TA, Giesen HA, Moul DE, Turner EH, Schwartz PJ. Suppression of men's responses to seasonal changes in day length by modern artificial lighting. Am J Physiol. 1995;269(1 Pt 2):R173-R178.
Roenneberg T, Merrow M. Entrainment of the human circadian clock. Cold Spring Harb Symp Quant Biol. 2007;72:293-299.
Wright KP Jr, McHill AW, Birks BR, Griffin BR, Rusterholz T, Chinoy ED. Entrainment of the human circadian clock to the natural light-dark cycle. Curr Biol. 2013;23(16):1554-1558.
Yetish G, Kaplan H, Gurven M, et al. Natural sleep and its seasonal variations in three pre-industrial societies. Curr Biol. 2015;25(21):2862-2868.
Hashizaki M, Nakajima H, Shiga T, Tsutsumi M, Kume K. A longitudinal large-scale objective sleep data analysis revealed a seasonal sleep variation in the Japanese population. Chronobiol Int. 2018;35(7):933-945.
Roenneberg T, Winnebeck EC, Klerman EB. Daylight saving time and artificial time zones - a battle between biological and social times. Front Physiol. 2019;10:944.
Paine SJ, Gander PH. Differences in circadian phase and weekday/weekend sleep patterns in a sample of middle-aged morning types and evening types. Chronobiol Int. 2016;33(8):1009-1017.
Goulet G, Mongrain V, Desrosiers C, Paquet J, Dumont M. Daily light exposure in morning-type and evening-type individuals. J Biol Rhythms. 2007;22(2):151-158.
Hebert M, Martin SK, Lee C, Eastman CI. The effects of prior light history on the suppression of melatonin by light in humans. J Pineal Res. 2002;33(4):198-203.
https://gynopedia.org/Netherlands
Wright KP Jr, Badia P. Effects of menstrual cycle phase and oral contraceptives on alertness, cognitive performance, and circadian rhythms during sleep deprivation. Behav Brain Res. 1999;103(2):185-194.
Dijk DJ, Duffy JF, Silva EJ, Shanahan TL, Boivin DB, Czeisler CA. Amplitude reduction and phase shifts of melatonin, cortisol and other circadian rhythms after a gradual advance of sleep and light exposure in humans. PLoS One. 2012;7(2):e30037.

Auteurs

Giulia Zerbini (G)

Institute of Medical Psychology, Faculty of Medicine, LMU Munich, Munich, Germany.
Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.
Department of Medical Psychology and Sociology, Faculty of Medicine, University of Augsburg, Augsburg, Germany.

Eva C Winnebeck (EC)

Institute of Medical Psychology, Faculty of Medicine, LMU Munich, Munich, Germany.

Martha Merrow (M)

Institute of Medical Psychology, Faculty of Medicine, LMU Munich, Munich, Germany.

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