Phase delaying the human circadian clock with a single light pulse and moderate delay of the sleep/dark episode: no influence of iris color

Jillian L Canton, Mark R Smith, Ho-Sun Choi, Charmane I Eastman, Jillian L Canton, Mark R Smith, Ho-Sun Choi, Charmane I Eastman

Abstract

Background: Light exposure in the late evening and nighttime and a delay of the sleep/dark episode can phase delay the circadian clock. This study assessed the size of the phase delay produced by a single light pulse combined with a moderate delay of the sleep/dark episode for one day. Because iris color or race has been reported to influence light-induced melatonin suppression, and we have recently reported racial differences in free-running circadian period and circadian phase shifting in response to light pulses, we also tested for differences in the magnitude of the phase delay in subjects with blue and brown irises.

Methods: Subjects (blue-eyed n = 7; brown eyed n = 6) maintained a regular sleep schedule for 1 week before coming to the laboratory for a baseline phase assessment, during which saliva was collected every 30 minutes to determine the time of the dim light melatonin onset (DLMO). Immediately following the baseline phase assessment, which ended 2 hours after baseline bedtime, subjects received a 2-hour bright light pulse (~4,000 lux). An 8-hour sleep episode followed the light pulse (i.e. was delayed 4 hours from baseline). A final phase assessment was conducted the subsequent night to determine the phase shift of the DLMO from the baseline to final phase assessment.Phase delays of the DLMO were compared in subjects with blue and brown irises. Iris color was also quantified from photographs using the three dimensions of red-green-blue color axes, as well as a lightness scale. These variables were correlated with phase shift of the DLMO, with the hypothesis that subjects with lighter irises would have larger phase delays.

Results: The average phase delay of the DLMO was -1.3 +/- 0.6 h, with a maximum delay of ~2 hours, and was similar for subjects with blue and brown irises. There were no significant correlations between any of the iris color variables and the magnitude of the phase delay.

Conclusion: A single 2-hour bright light pulse combined with a moderate delay of the sleep/dark episode delayed the circadian clock an average of ~1.5 hours. There was no evidence that iris color influenced the magnitude of the phase shift. Future studies are needed to replicate our findings that iris color does not impact the magnitude of light-induced circadian phase shifts, and that the previously reported differences may be due to race.

Figures

Figure 1
Figure 1
Protocol diagram. This protocol is for a subject sleeping from 23:00–7:00 at baseline (days 1–7). Shaded rectangle with L inside shows time of bright light exposure (2 h, ~4000 lux).
Figure 2
Figure 2
Circadian rhythm phase delays with a single bright light pulse and delayed sleep/dark episode. The horizontal lines represent the median phase delays.

References

    1. Czeisler CA, Kronauer RE, Allan JS, Duffy JF, Jewett ME, Brown EN, Ronda JM. Bright light induction of strong (type 0) resetting of the human circadian pacemaker. Science. 1989;244:1328–1333. doi: 10.1126/science.2734611.
    1. Honma K, Honma S. A human phase response curve for bright light pulses. The Japanese Journal of Psychiatry and Neurology. 1988;42:167–168.
    1. Minors DS, Waterhouse JM, Wirz-Justice A. A human phase-response curve to light. Neurosci Lett. 1991;133:36–40. doi: 10.1016/0304-3940(91)90051-T.
    1. Revell VL, Eastman CI. How to trick mother nature into letting you fly around or stay up all night. J Biol Rhythms. 2005;20:353–365. doi: 10.1177/0748730405277233.
    1. Wright HR, Lack LC. Effect of light wavelength on suppression and phase delay of the melatonin rhythm. Chronobiol Int. 2001;18:801–808. doi: 10.1081/CBI-100107515.
    1. Wright HR, Lack LC, Kennaway DJ. Differential effects of light wavelength in phase advancing the melatonin rhythm. J Pineal Res. 2004;36:140–144. doi: 10.1046/j.1600-079X.2003.00108.x.
    1. Warman VL, Dijk DJ, Warman GR, Arendt J, Skene DJ. Phase advancing human circadian rhythms with short wavelength light. Neurosci Lett. 2003;342:37–40. doi: 10.1016/S0304-3940(03)00223-4.
    1. Lockley SW, Brainard GC, Czeisler CA. High sensitivity of the human circadian melatonin rhythm to resetting by short wavelength light. J Clin Endocrinol Metab. 2003;88:4502–4505. doi: 10.1210/jc.2003-030570.
    1. Zeitzer JM, Dijk DJ, Kronauer RE, Brown EN, Czeisler CA. Sensitivity of the human circadian pacemaker to nocturnal light: melatonin phase resetting and suppression. J Physiol . 2000;526 Pt 3:695–702.
    1. Boivin DB, Duffy JF, Kronauer RE, Czeisler CA. Dose-response relationships for resetting of human circadian clock by light. Nature. 1996;379:540–542. doi: 10.1038/379540a0.
    1. Rimmer DW, Boivin DB, Shanahan TL, Kronauer RE, Duffy JF, Czeisler CA. Dynamic resetting of the human circadian pacemaker by intermittent bright light. Am J Physiol Regul Integr Comp Physiol . 2000;279:R1574–R1579.
    1. Gronfier C, Wright KP, Kronauer RE, Jewett ME, Czeisler CA. Efficacy of a single sequence of intermittent bright light pulses for delaying circadian phase in humans. Am J Physiol Endocrinol Metab . 2004;287:E174–E181. doi: 10.1152/ajpendo.00385.2003.
    1. Burgess HJ, Crowley SJ, Gazda CJ, Fogg LF, Eastman CI. Preflight adjustment to eastward travel: 3 days of advancing sleep with and without morning bright light. J Biol Rhythms. 2003;18:318–328. doi: 10.1177/0748730403253585.
    1. Benloucif S, Guico MJ, Wolfe LF, L'Hermite-Baleriaux M, Zee PC. Effect of increasing light intensity vs. increasing light duration on phase shifts of the circadian clock of humans. Sleep. 2003;26:A103.
    1. Mitchell PJ, Hoese EK, Liu L, Fogg LF, Eastman CI. Conflicting bright light exposure during night shifts impedes circadian adaptation. J Biol Rhythms. 1997;12:5–15. doi: 10.1177/074873049701200103.
    1. 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;24:272–281.
    1. Taylor A, Wright HR, Lack LC. Sleeping-in on the weekend delays circadian phase and increases sleepiness the following week. Sleep and Biological Rhythms. 2008;6:172–179. doi: 10.1111/j.1479-8425.2008.00356.x.
    1. Burgess HJ, Eastman CI. A late wake time phase delays the human dim light melatonin rhythm. Neurosci Lett. 2006;395:191–195. doi: 10.1016/j.neulet.2005.10.082.
    1. Burgess HJ, Eastman CI. Early versus late bedtimes phase shift the human dim light melatonin rhythm despite a fixed morning lights on time. Neurosci Lett. 2004;356:115–118. doi: 10.1016/j.neulet.2003.11.032.
    1. Dawson D, Encel N, Lushington K. Improving adaptation to simulated night shift: Timed exposure to bright light versus daytime melatonin administration. Sleep. 1995;18:11–21.
    1. Campbell SS. Effects of times bright-light exposure on shift-work adaptation in middle-aged subjects. Sleep. 1995;18:408–416.
    1. Burgess HJ, Eastman CI. Short nights reduce light-induced circadian phase delays in humans. Sleep. 2006;29:25–30.
    1. Smith M, Fogg L, Eastman C. Practical interventions to promote circadian adaptation to permanent night shift work: Study 4. J Biol Rhythms. 2009;24:161–172. doi: 10.1177/0748730409332068.
    1. Youngstedt SD, Kripke DF, Elliott JA. Circadian phase-delaying effects of bright light alone and combined with exercise in humans. Am J Physiol Regul Integr Comp Physiol. 2002;282:R259–R266.
    1. Kennaway DJ, Earl CR, Shaw PF, Royles P, Carbone F, Webb H. Phase delay of the rhythm of 6-sulphatoxy melatonin excretion by artifical light. J Pineal Res. 1987;4:315–320. doi: 10.1111/j.1600-079X.1987.tb00869.x.
    1. Laakso ML, Hatonen T, Stenberg D, Alila A, Smith S. One-hour exposure to moderate illuminance (500lux) shifts the human melatonin rhythm. J Pineal Res. 1993;15:21–26. doi: 10.1111/j.1600-079X.1993.tb00505.x.
    1. Duffy JF, Zeitzer JM, Czeisler CA. Decreased sensitivity to phase-delaying effects of moderate intensity light in older subjects. Neurobiol Aging. 2007;28:799–807. doi: 10.1016/j.neurobiolaging.2006.03.005.
    1. Khalsa SB, Jewett ME, Cajochen C, Czeisler CA. A phase response curve to single bright light pulses in human subjects. J Physiol . 2003;549 :945–952. doi: 10.1113/jphysiol.2003.040477.
    1. Eastman C, Burgess H. How to travel the world without jet lag. Sleep Medicine Clinics. 2009;4:241–255. doi: 10.1016/j.jsmc.2009.02.006.
    1. Eastman CI, Martin SK. How to use light and dark to produce circadian adaptation to night shift work. Ann Med. 1999;31:87–98. doi: 10.3109/07853899908998783.
    1. Revell VL, Burgess HJ, Gazda CJ, Smith MR, Fogg LF, Eastman CI. Advancing human circadian rhythms with afternoon melatonin and morning intermittent bright light. J Clin Endocrinol Metab. 2006;91:54–59. doi: 10.1210/jc.2005-1009.
    1. Smith MR, Eastman CI. Phase delaying the human circadian clock with blue-enriched polychromatic light. Chronobiol Int. 2009;26:709–275. doi: 10.1080/07420520902927742.
    1. 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;33:198–203. doi: 10.1034/j.1600-079X.2002.01885.x.
    1. Smith KA, Schoen MW, Czeisler CA. Adaptation of human pineal melatonin suppression by recent photic history. J Clin Endocrinol Metab. 2004;89:3610–3614. doi: 10.1210/jc.2003-032100.
    1. Chang A, Scheer FA, Czeisler CA. Adaptation of the human circadian system by prior light history. Sleep. 2008. p. A45.
    1. White TM, Terman M. Effect of Iris pigmentation and latitude on chronotype and sleep timing. Chronobiol Int. 2003;20:1193–1195.
    1. Higuchi S, Motohashi Y, Ishibashi K, Maeda T. Influence of eye colors of Caucasians and Asians on suppression of melatonin secretion by light. Am J Physiol Regul Integr Comp Physiol. 2007;292:R2352–2356.
    1. Ijspeert JK, de Waard PW, van den Berg TJ, de Jong PT. The intraocular straylight function in 129 healthy volunteers; dependence on angle, age and pigmentation. Vision Res. 1990;30:699–707. doi: 10.1016/0042-6989(90)90096-4.
    1. van den Berg TJ, Ijspeert JK, de Waard PW. Dependence of intraocular straylight on pigmentation and light transmission through the ocular wall. Vision Res. 1991;31:1361–1367. doi: 10.1016/0042-6989(91)90057-C.
    1. Smith MR, Burgess HJ, Fogg LF, Eastman CI. Racial Differences in the Human Endogenous Circadian Period. Plos One. 2009;4:e6014. doi: 10.1371/journal.pone.0006014.
    1. Horne JA, Ostberg O. Self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4:97–110.
    1. Smith MR, Revell VL, Eastman CI. Phase advancing the human circadian clock with blue-enriched polychromatic light. Sleep Medicine. 2009;10:287–294. doi: 10.1016/j.sleep.2008.05.005.
    1. Lee C, Smith M, Eastman C. A compromise phase position for permanent night shift workers: circadian phase after two night shifts with scheduled sleep and light/dark exposure. Chronobiol Int. 2006;23:859–875. doi: 10.1080/07420520600827160.
    1. Voultsios A, Kennaway DJ, Dawson D. Salivary melatonin as a circadian phase marker: validation and comparison to plasma melatonin. J Biol Rhythms. 1997;12:457–466.
    1. Silvar SD, Pollack RH. Racial differences in pigmentation of the fundus oculi. Pyschonomic Science. 1967;7:159–160.
    1. Brown JM. Fundus pigmentation and equiluminant moving phantoms. Percept Mot Skills. 2000;90:963–973. doi: 10.2466/PMS.90.3.963-973.
    1. Weiter JJ, Delori FC, Wing GL, Fitch KA. Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes. Invest Ophthalmol Vis Sci. 1986;27:145–152.
    1. Gamlin PD, McDougal DH, Pokorny J, Smith VC, Yau KW, Dacey DM. Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res. 2007;47:946–954. doi: 10.1016/j.visres.2006.12.015.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe