Optimizing Light Flash Sequence Duration to Shift Human Circadian Phase
Daniel S Joyce, Manuel Spitschan, Jamie M Zeitzer, Daniel S Joyce, Manuel Spitschan, Jamie M Zeitzer
Abstract
Unlike light input for forming images, non-image-forming retinal pathways are optimized to convey information about the total light environment, integrating this information over time and space. In a variety of species, discontinuous light sequences (flashes) can be effective stimuli, notably impacting circadian entrainment. In this study, we examined the extent to which this temporal integration can occur. A group of healthy, young (n = 20) individuals took part in a series of 16-day protocols in which we examined the impact of different lengths of light flash sequences on circadian timing. We find a significant phase change of -0.70 h in response to flashes that did not differ by duration; a 15-min sequence could engender as much change in circadian timing as 3.5-h sequences. Acute suppression of melatonin was also observed during short (15-min) exposures, but not in exposures over one hour in length. Our data are consistent with the theory that responses to light flashes are mediated by the extrinsic, rod/cone pathway, and saturate the response of this pathway within 15 min. Further excitation leads to no greater change in circadian timing and an inability to acutely suppress melatonin, indicating that this pathway may be in a refractory state following this brief light stimulation.
Keywords: circadian rhythm; dim light melatonin onset; flash; light; melatonin; sleep.
Conflict of interest statement
The authors declare no conflict of interest.
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References
- Gamlin P.D.R., McDougal D.H., Pokorny J., Smith V.C., Yau K.W., Dacey D.M. 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.
- Allen A.E., Storchi R., Martial F.P., Petersen R.S., Montemurro M.A., Brown T.M., Lucas R.J. Melanopsin-driven light adaptation in mouse vision. Curr. Biol. 2014;24:2481–2490. doi: 10.1016/j.cub.2014.09.015.
- Milosavljevic N., Storchi R., Eleftheriou C.G., Colins A., Petersen R.S., Lucas R.J. Photoreceptive retinal ganglion cells control the information rate of the optic nerve. Proc. Natl. Acad. Sci. USA. 2018;115:E11817–E11826. doi: 10.1073/pnas.1810701115.
- Joyce D.S., Feigl B., Cao D., Zele A.J. Temporal characteristics of melanopsin inputs to the human pupil light reflex. Vision Res. 2015;107:58–66. doi: 10.1016/j.visres.2014.12.001.
- Joyce D.S., Feigl B., Zele A.J. Melanopsin-mediated post-illumination pupil response in the peripheral retina. J. Vis. 2016;16:5. doi: 10.1167/16.8.5.
- Spitschan M., Lucas R.J., Brown T.M. Chromatic clocks: Color opponency in non-image-forming visual function. Neurosci. Biobehav. Rev. 2017;78:24–33. doi: 10.1016/j.neubiorev.2017.04.016.
- Berson D.M., Dunn F.A., Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295:1070–1073. doi: 10.1126/science.1067262.
- Zeitzer J.M., Ruby N.F., Fisicaro R.A., Heller H.C. Response of the human circadian system to millisecond flashes of light. PLoS ONE. 2011;6:e22078. doi: 10.1371/journal.pone.0022078.
- Zeitzer J.M., Dijk D.-J., Kronauer R.E., Brown E.N., Czeisler C.A. Sensitivity of the human circadian pacemaker to nocturnal light: Melatonin phase resetting and suppression. J. Physiol. 2000;526:695–702. doi: 10.1111/j.1469-7793.2000.00695.x.
- Najjar R.P., Zeitzer J.M. Temporal integration of light flashes by the human circadian system. J. Clin. Investig. 2016;126:938–947. doi: 10.1172/JCI82306.
- Chang A.-M., Santhi N., St Hilaire M., Gronfier C., Bradstreet D.S., Duffy J.F., Lockley S.W., Kronauer R.E., Czeisler C.A. Human responses to bright light of different durations. J. Physiol. 2012;590:3103–3112. doi: 10.1113/jphysiol.2011.226555.
- Rahman S.A., Hilaire M.A.S., Chang A.-M., Santhi N., Duffy J.F., Kronauer R.E., Czeisler C.A., Lockley S.W., Klerman E.B. Circadian phase resetting by a single short-duration light exposure. JCI Insight. 2017;2:e89494. doi: 10.1172/jci.insight.89494.
- Buysse D.J., Reynolds III C.F., Monk T.H., Berman S.R., Kupfer D.J. The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Res. 1989;28:193–213. doi: 10.1016/0165-1781(89)90047-4.
- Babor T.F., de la Fuente J.R., Saunders J., Grant M. The Alcohol Use Disorders Identification Test: Guidelines for Use in Primary Care. World Health Organization: Department of Mental Health and Substance Dependence; Geneva, Switzerland: 2001.
- Radloff L.S. The CES-D Scale: A self-report depression scale for research in the general population. Appl. Psychol. Meas. 1977;1:385–401. doi: 10.1177/014662167700100306.
- Adan A., Almirall H. Horne & Östberg morningness-eveningness questionnaire: A reduced scale. Pers. Individ. Dif. 1991;12:241–253. doi: 10.1016/0191-8869(91)90110-W.
- Ishihara S. Ishihara’s Tests for Colour Deficiency. Kanehara Trading Inc.; Tokyo, Japan: 2007.
- Moher D., Schulz K.F., Altman D. The CONSORT statement: Revised recommendations for improving the quality of reports of parallel-group randomized trials. JAMA. 2001;285:1987–1991. doi: 10.1001/jama.285.15.1987.
- Carney C.E., Buysse D.J., Ancoli-Israel S., Edinger J.D., Krystal A.D., Lichstein K.L., Morin C.M. The Consensus Sleep Diary: Standardizing prospective sleep self-monitoring. Sleep. 2012;35:287–302. doi: 10.5665/sleep.1642.
- Duffy J.F., Dijk D.-J. Getting through to circadian oscillators: Why use constant routines? J. Biol. Rhythms. 2002;17:4–13. doi: 10.1177/074873002129002294.
- Mifflin M.D., St Jeor S.T., Hill L.A., Scott B.J., Daugherty S.A., Koh Y.O. A new predictive equation for resting energy expenditure in healthy individuals. Am. J. Clin. Nutr. 1990;51:241–247. doi: 10.1093/ajcn/51.2.241.
- Joyce D.S., Spitschan M., Zeitzer J.M. Duration invariance and intensity dependence of the human circadian system phase shifting response to brief light flashes. Proc. Biol. Sci. 2022;289:20211943. doi: 10.1098/rspb.2021.1943.
- St Hilaire M.A., Gooley J.J., Khalsa S.B.S., Kronauer R.E., Czeisler C.A., Lockley S.W. Human phase response curve to a 1 h pulse of bright white light. J. Physiol. 2012;590:3035–3045. doi: 10.1113/jphysiol.2012.227892.
- Voultsios A., Kennaway D.J., Dawson D. Salivary Melatonin as a Circadian Phase Marker: Validation and Comparison to Plasma Melatonin. J. Biol. Rhythms. 1997;12:457–466. doi: 10.1177/074873049701200507.
- Hoddes E., Zarcone V., Smythe H., Phillips R., Dement W.C. Quantification of sleepiness: A new approach. Psychophysiology. 1973;10:431–437. doi: 10.1111/j.1469-8986.1973.tb00801.x.
- Dinges D.F., Powell J.W. Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav. Res. Methods Instrum. Comput. 1985;17:652–655. doi: 10.3758/BF03200977.
- Gabel V., Kass M., Joyce D.S., Spitschan M., Zeitzer J.M. Auditory psychomotor vigilance testing in older and young adults: A revised threshold setting procedure. Sleep Breath. 2019;23:1021–1025. doi: 10.1007/s11325-019-01859-7.
- Basner M., Mollicone D., Dinges D.F. Validity and sensitivity of a brief psychomotor vigilance test (PVT-B) to total and partial sleep deprivation. Acta Astronaut. 2011;69:949–959. doi: 10.1016/j.actaastro.2011.07.015.
- Dacey D.M., Liao H.-W., Peterson B.B., Robinson F.R., Smith V.C., Pokorny J., Yau K.-W., Gamlin P.D. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005;433:749–754. doi: 10.1038/nature03387.
- Wong K.Y., Fernandez F.-X. Circadian responses to light-flash exposure: Conceptualization and new data guiding future directions. Front. Neurol. 2021;12:627550. doi: 10.3389/fneur.2021.627550.
- Gooley J.J., Rajaratnam S.M., Brainard G.C., Kronauer R.E., Czeisler C.A., Lockley S.W. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci. Transl. Med. 2010;2:31ra33. doi: 10.1126/scitranslmed.3000741.
- Ruby N.F., Brennan T.J., Xie X., Cao V., Franken P., Heller H.C., O’Hara B.F. Role of melanopsin in circadian responses to light. Science. 2002;298:2211–2213. doi: 10.1126/science.1076701.
- Brown T.M. Melanopic illuminance defines the magnitude of human circadian light responses under a wide range of conditions. J. Pineal Res. 2020;69:e12655. doi: 10.1111/jpi.12655.
- Kaladchibachi S., Negelspach D.C., Zeitzer J.M., Fernandez F. Optimization of circadian responses with shorter and shorter millisecond flashes. Biol. Lett. 2019;15:20190371. doi: 10.1098/rsbl.2019.0371.
- Muindi F., Colas D., Ikeme J., Ruby N.F., Heller H.C. Loss of Melanopsin Photoreception and Antagonism of the Histamine H3 Receptor by Ciproxifan Inhibit Light-Induced Sleep in Mice. PLoS ONE. 2015;10:e0128175. doi: 10.1371/journal.pone.0128175.
- Lucas R.J., Peirson S.N., Berson D.M., Brown T.M., Cooper H.M., Czeisler C.A., Figueiro M.G., Gamlin P.D., Lockley S.W., O’Hagan J.B., et al. Measuring and using light in the melanopsin age. Trends Neurosci. 2014;37:1–9. doi: 10.1016/j.tins.2013.10.004.
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