Nonphotic Entrainment in Humans?

Mistlberger, Ralph E.; Skene, Debra J.

doi:10.1177/0748730405277982

Cited by 267Circadian rhythm and melatoninSleep and Work-Related FatigueSleep and Wakefulness Research

Nonphotic Entrainment in Humans?

Mistlberger, Ralph E., Skene, Debra J.·2005·Journal of Biological Rhythms

DOI 10.1177/0748730405277982

Open this paper in CoChat — free account

Abstract

Although light is accepted as the dominant zeitgeber for entrainment of the human circadian system, there is evidence that nonphotic stimuli may play a role. This review critically assesses the current evidence in support of nonphotic entrainment in humans. Studies involving manipulations of sleep-wake schedules, exercise, mealtimes, and social stimuli are re-examined, bearing in mind the fact that the human circadian clock is sensitive to very dim light and has a free-running period very close to 24 h. Because of light confounds, the study of totally blind subjects with free-running circadian rhythms represents the ideal model to investigate the effects of nonphotic stimuli on circadian phase and period. Strong support for nonphotic entrainment in humans has already come from the study of a few blind subjects with entrained circadian rhythms. However, in these studies the nonphotic stimulus(i) responsible was not identified. The effect of appropriately timed exercise or exogenous melatonin represents the best proof to date of an effect of nonphotic stimuli on human circadian timing. Phase-response curves for both exercise and melatonin have been constructed. Given the powerful effect of feeding as a circadian zeitgeber in various nonhuman species, studies of meal timing are recommended. In conclusion, the available evidence indicates that it remains worthwhile to continue to study nonphotic effects on human circadian timing to identify treatment strategies for shift workers and transmeridian travelers as well as for the blind and possibly the elderly.

Integrity signals

Registry

Crossref · 10.1177/0748730405277982

Cites

116 of 116 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Exercise may act as a zeitgeber, entraining the circadian rhythm by producing either phase advances or phase delays depending on the timing.
“Exercise may also act as a zeitgeber, i.e., it can entrain the circadian rhythm by producing either phase advances or phase delays depending on the timing [102, 103].”
From Homeostatic and Circadian Control of Food Intake: Clinical Strategies to Prevent Overconsumption (2013) · cites this paper as [103]

Aviat space environ med
(1992) · Applied Ergonomics · doi:10.1016/0003-6870(92)90338-v · Cited by 7,153 · see citing works
Principles and Practice of Sleep Medicine
Kryger, M. H., Roth, T. G., & Dement, W. C. (2011) · Elsevier eBooks · doi:10.1016/c2009-0-59875-3 · Cited by 5,118 · see citing works
Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus
Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000) · Genes & Development · doi:10.1101/gad.183500 · Cited by 2,394 · see citing works
Action Spectrum for Melatonin Regulation in Humans: Evidence for a Novel Circadian Photoreceptor
Brainard, G. C., Hanifin, J. P., Greeson, J. M., Byrne, B., Glickman, G., Gerner, E., & Rollag, M. D. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06405.2001 · Cited by 1,930 · see citing works
Entrainment of the circadian clock in the liver by feeding
Stokkan, K.-A., Yamazaki, S., Tei, H., Sakaki, Y., & Menaker, M. (2001) · Science · doi:10.1126/science.291.5503.490 · Cited by 1,800 · see citing works
Stability, precision, and near-24-hour period of the human circadian pacemaker
Czeisler, C. A., Duffy, J. F., Shanahan, T. L., Brown, E. N., Mitchell, J. F., Rimmer, D. W., Ronda, J. M., Silva, E. J., Allan, J. S., Emens, J. S., et al. (1999) · Science · doi:10.1126/science.284.5423.2177 · Cited by 1,705 · see citing works
An action spectrum for melatonin suppression: evidence for a novel non‐rod, non‐cone photoreceptor system in humans
Thapan, K., Arendt, J., & Skene, D. J. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-1-00261.x · Cited by 1,320 · see citing works
Self-citation
Sensitivity of the human circadian pacemaker to nocturnal light: melatonin phase resetting and suppression
Zeitzer, J. M., Dijk, D., Kronauer, R. E., Brown, E. N., & Czeisler, C. A. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00695.x · Cited by 1,175 · see citing works
Bright Light Induction of Strong (Type 0) Resetting of the Human Circadian Pacemaker
Czeisler, C. A., Kronauer, R. E., Allan, J. S., Duffy, J. F., Jewett, M. E., Brown, E. N., & Ronda, J. M. (1989) · Science · doi:10.1126/science.2734611 · Cited by 946 · see citing works
Circadian food-anticipatory activity: Formal models and physiological mechanisms
Mistlberger, R. E. (1994) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)90023-x · Cited by 857 · see citing works
Self-citation
Regulation of adolescent sleep: Implications for behavior
CARSKADON, M. A., ACEBO, C., & JENNI, O. G. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.032 · Cited by 792 · see citing works
High Sensitivity of the Human Circadian Melatonin Rhythm to Resetting by Short Wavelength Light
Lockley, S. W., Brainard, G. C., & Czeisler, C. A. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030570 · Cited by 782 · see citing works
Bright light resets the human circadian pacemaker independent of the timing of the sleep-wake cycle
Czeisler, C. A., Allan, J. S., Strogatz, S. H., Ronda, J. M., Sánchez, R., Ríos, C. D., Freitag, W. O., Richardson, G. S., & Kronauer, R. E. (1986) · Science · doi:10.1126/science.3726555 · Cited by 770 · see citing works
Molecular Dissection of Two Distinct Actions of Melatonin on the Suprachiasmatic Circadian Clock
Liu, C., Weaver, D. R., Jin, X., Shearman, L. P., Pieschl, R. L., Gribkoff, V. K., & Reppert, S. M. (1997) · Neuron · doi:10.1016/s0896-6273(00)80350-5 · Cited by 723 · see citing works
The “other” circadian system: food as a Zeitgeber
Stephan, F. K. (2002) · Journal of Biological Rhythms · doi:10.1177/074873002129002591 · Cited by 672 · see citing works
Suppression of Melatonin Secretion in Some Blind Patients by Exposure to Bright Light
Czeisler, C. A., Shanahan, T. L., Klerman, E. B., Martens, H., Brotman, D. J., Emens, J. S., Klein, T., & Rizzo, J. F. (1995) · New England Journal of Medicine · doi:10.1056/nejm199501053320102 · Cited by 654 · see citing works
Melatonin as a chronobiotic
Arendt, J., & Skene, D. J. (2005) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2004.05.002 · Cited by 629 · see citing works
Self-citation
The Circadian System of Man
Wever, R. (1979) · Topics in environmental physiology and medicine · doi:10.1007/978-1-4612-6142-1 · Cited by 623 · see citing works
Dose-response relationships for resetting of human circadian clock by light
Boivin, D. B., Duffy, J. F., Kronauer, R. E., & Czeisler, C. A. (1996) · Nature · doi:10.1038/379540a0 · Cited by 559 · see citing works
Peripheral Circadian Oscillators in Mammals: Time and Food
Schibler, U., Ripperger, J. A., & Brown, S. A. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403018003007 · Cited by 525 · see citing works
The circadian system of man—Results of experiments under temporal isolation
(1980) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/s0300-9629(80)80040-5 · Cited by 515 · see citing works
Entrainment of free-running circadian rhythms by melatonin in blind people
Sack, R. L., Brandes, R. W., Kendall, A. R., & Lewy, A. J. (2000) · New England Journal of Medicine · doi:10.1056/nejm200010123431503 · Cited by 490 · see citing works
The effects of prior light history on the suppression of melatonin by light in humans
Hébert, M., Martin, S. K., Lee, C., & Eastman, C. I. (2002) · Journal of Pineal Research · doi:10.1034/j.1600-079x.2002.01885.x · Cited by 413 · cited 3× · see citing works
“, 2001), and sensitivity may be enhanced by prolonged exposure to dim light (Hebert et al., 2002; Smith et al., 2004).”
Background
LOCOMOTOR ACTIVITY AND NON‐PHOTIC INFLUENCES ON CIRCADIAN CLOCKS
Mrosovsky, N. (1996) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1996.tb01278.x · Cited by 412 · see citing works
Circadian rhythm abnormalities in totally blind people: incidence and clinical significance
Sack, R. L., Lewy, A. J., Blood, M. L., KEITH, L. D., & Nakagawa, H. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.75.1.1619000 · Cited by 408 · see citing works
Social influences on mammalian circadian rhythms: animal and human studies
Mistlberger, R. E., & Skene, D. J. (2004) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793103006353 · Cited by 402 · see citing works
Self-citation
Selective MT 2 melatonin receptor antagonists block melatonin‐mediated phase advances of circadian rhythms
Dubocovich, M. L., Yun, K., Al‐Ghoul, W. M., Benloucif, S., & Masana, M. I. (1998) · The FASEB Journal · doi:10.1096/fasebj.12.12.1211 · Cited by 364 · see citing works
Re-entrainment of circadian rhythms after phase-shifts of the Zeitgeber.
Aschoff, J., Hoffmann, K. H., Pohl, H. H., & Wever, R. A. (1975) · PubMed · Cited by 352 · see citing works
Human Circadian Rhythms in Continuous Darkness: Entrainment by Social Cues
Aschoff, J., Fatranská, M., Giedke, H., Doerr, P., Stamm, D., & Wisser, H. (1971) · Science · doi:10.1126/science.171.3967.213 · Cited by 348 · see citing works
Exercise elicits phase shifts and acute alterations of melatonin that vary with circadian phase
Buxton, O. M., Lee, C. W., L’Hermite‐Balériaux, M., Turek, F. W., & Cauter, E. V. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00355.2002 · Cited by 327 · see citing works
Sleep states alter activity of suprachiasmatic nucleus neurons
Deboer, T., Vansteensel, M. J., Détári, L., & Meijer, J. H. (2003) · Nature Neuroscience · doi:10.1038/nn1122 · Cited by 324 · see citing works
Relationship between Melatonin Rhythms and Visual Loss in the Blind
Lockley, S. W., Skene, D. J., Arendt, J., Tabandeh, H., Bird, A. C., & Defrance, R. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.11.4355 · Cited by 312 · see citing works
Self-citation
TEMPERATURE EFFECT ON ENTRAINMENT, PHASE SHIFTING, AND AMPLITUDE OF CIRCADIAN CLOCKS AND ITS MOLECULAR BASES
Rensing, L., & Ruoff, P. (2002) · Chronobiology International · doi:10.1081/cbi-120014569 · Cited by 306 · see citing works
Melatonin administration can entrain the free-running circadian system of blind subjects
Lockley, S. W., Skene, D. J., James, K., Thapan, K., Wright, J., & Arendt, J. (2000) · Journal of Endocrinology · doi:10.1677/joe.0.164r001 · Cited by 284 · see citing works
Self-citation
Activation of MT2melatonin receptors in rat suprachiasmatic nucleus phase advances the circadian clock
Hunt, A. E., Al‐Ghoul, W. M., Gillette, M. U., & Dubocovich, M. L. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.280.1.c110 · Cited by 266 · see citing works
Adaptation of Human Pineal Melatonin Suppression by Recent Photic History
Smith, K. A., Schoen, M. W., & Czeisler, C. A. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032100 · Cited by 256 · see citing works
Intrinsic near-24-h pacemaker period determines limits of circadian entrainment to a weak synchronizer in humans
Wright, K. P., Hughes, R. J., Kronauer, R. E., Dijk, D., & Czeisler, C. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.201530198 · Cited by 254 · see citing works
Rapid down-regulation of mammalian Period genes during behavioral resetting of the circadian clock
Maywood, E. S., Mrosovsky, N., Field, M. D., & Hastings, M. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.15211 · Cited by 248 · see citing works
A benzodiazepine used in the treatment of insomnia phase-shifts the mammalian circadian clock
Turek, F. W., & Losee-Olson, S. H. (1986) · Nature · doi:10.1038/321167a0 · Cited by 246 · see citing works
Physiological and Chronobiological Changes during Ramadan Intermittent Fasting
Roky, R., Houti, I. E., Moussamih, S., Qotbi, S., & Aadil, N. (2004) · Annals of Nutrition and Metabolism · doi:10.1159/000081076 · Cited by 245 · see citing works
A behavioural method for accelerating re-entrainment of rhythms to new light—dark cycles
Mrosovsky, N., & Salmon, P. A. (1987) · Nature · doi:10.1038/330372a0 · Cited by 241 · see citing works
Phase‐shifting human circadian rhythms: influence of sleep timing, social contact and light exposure.
Duffy, J. F., Kronauer, R. E., & Czeisler, C. A. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021593 · Cited by 234 · see citing works
Suppression of Nocturnal Plasma Melatonin and 6-Sulphatoxymelatonin by Bright and Dim Light in Man
Bojkowski, C. J., Aldhous, M. E., English, J., Franey, C. S., Poulton, A. L., Skene, D. J., & Arendt, J. (1987) · Hormone and Metabolic Research · doi:10.1055/s-2007-1011846 · Cited by 233 · see citing works
Self-citation
Nocturnal exercise phase delays circadian rhythms of melatonin and thyrotropin secretion in normal men
Reeth, O. V., Sturis, J., Byrne, M. M., Blackman, J. D., L’Hermite‐Balériaux, M., Leproult, R., Oliner, C. M., Refetoff, S., Turek, F. W., & Cauter, E. V. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.266.6.e964 · Cited by 231 · see citing works
Circadian Clock Resetting by Sleep Deprivation without Exercise in the Syrian Hamster
Antle, M. C., & Mistlberger, R. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09326.2000 · Cited by 229 · see citing works
Self-citation
A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock
Ding, J., Buchanan, G. F., Tischkau, S. A., Chen, D., Kuriashkina, L. R., Faiman, L. E., Alster, J. M., McPherson, P. S., Campbell, K. P., & Gillette, M. U. (1998) · Nature · doi:10.1038/28639 · Cited by 227 · see citing works
Ramadan fasting alters endocrine and neuroendocrine circadian patterns. Meal–time as a synchronizer in humans?
Bogdan, A., Bouchareb, B., & Touitou, Y. (2001) · Life Sciences · doi:10.1016/s0024-3205(01)00966-3 · Cited by 225 · see citing works
Daily exercise facilitates phase delays of circadian melatonin rhythm in very dim light
Barger, L. K., Wright, K. P., Hughes, R. J., & Czeisler, C. A. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00397.2003 · Cited by 218 · see citing works
Nonphotic entrainment of the human circadian pacemaker
Klerman, E. B., Rimmer, D. W., Dijk, D., Kronauer, R. E., Rizzo, J. F., & Czeisler, C. A. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.274.4.r991 · Cited by 217 · see citing works
Photic Regulation of Melatonin in Humans: Ocular and Neural Signal Transduction
Brainard, G. C., Rollag, M. D., & Hanifin, J. P. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200608 · Cited by 217 · see citing works
Different Types of Melatonin Circadian Secretory Rhythms in Some Blind Subjects
Lewy, A. J., & Newsome, D. A. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-56-6-1103 · Cited by 205 · see citing works
Phase advancing human circadian rhythms with short wavelength light
Warman, V. L., Dijk, D., Warman, G. R., Arendt, J., & Skene, D. J. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00223-4 · Cited by 192 · see citing works
Self-citation
Quantifying Human Circadian Pacemaker Response to Brief, Extended, and Repeated Light Stimuli over the Phototopic Range
Kronauer, R. E., Forger, D. B., & Jewett, M. E. (1999) · Journal of Biological Rhythms · doi:10.1177/074873099129001073 · Cited by 187 · see citing works
Posture influences melatonin concentrations in plasma and saliva in humans
Deacon, S., & Arendt, J. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)91059-6 · Cited by 185 · see citing works
How to use light and dark to produce circadian adaptation to night shift work
Eastman, C. I., & Martin, S. K. (1999) · Annals of Medicine · doi:10.3109/07853899908998783 · Cited by 180 · see citing works
Phase-advance shifts of human circadian pacemaker are accelerated by daytime physical exercise
Miyazaki, T., Hashimoto, S., Masubuchi, S., Honma, S., & Honma, K. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.1.r197 · Cited by 178 · see citing works
The Effect of Light on the Human Circadian Pacemaker
Czeisler, C. A. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514597.ch14 · Cited by 166 · see citing works
The Effects of Low-Dose 0.5-mg Melatonin on the Free-Running Circadian Rhythms of Blind Subjects
Hack, L. M., Lockley, S. W., Arendt, J., & Skene, D. J. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403256796 · Cited by 162 · see citing works
Self-citation
Synchronization of the Molecular Clockwork by Light- and Food-Related Cues in Mammals
Challet, É., Caldelas, I., Graff, C., & Pévet, P. (2003) · Biological Chemistry · doi:10.1515/bc.2003.079 · Cited by 158 · see citing works
Alteration of Internal Circadian Phase Relationships after Morning versus Evening Carbohydrate-Rich Meals in Humans
Kräuchi, K., Cajochen, C., Werth, E., & Wirz‐Justice, A. (2002) · Journal of Biological Rhythms · doi:10.1177/074873040201700409 · Cited by 146 · see citing works
Circadian phase-shifting effects of nocturnal exercise in older compared with young adults
Baehr, E. K., Eastman, C. I., Revelle, W., Olson, S. H. L., Wolfe, L. F., & Zee, P. C. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00761.2002 · Cited by 141 · see citing works
Entrainment of the master circadian clock by scheduled feeding
Castillo, M. R., Hochstetler, K. J., Tavernier, R. J., Greene, D. M., & Bult‐Ito, A. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00247.2004 · Cited by 141 · see citing works
Phase-shifting human circadian rhythms with exercise during the night shift
Eastman, C. I. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)02031-4 · Cited by 140 · see citing works
Acute and Delayed Effects of Exercise on Human Melatonin Secretion
Buxton, O. M., L’Hermite‐Balériaux, M., Hirschfeld, U., & Cauter, E. V. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200611 · Cited by 133 · see citing works
Efficacy of bright light and sleep/darkness scheduling in alleviating circadian maladaptation to night work
Horowitz, T. S., Cade, B. E., Wolfe, J. M., & Czeisler, C. A. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.2.e384 · Cited by 133 · see citing works
Photic Resetting of the Human Circadian Pacemaker in the Absence of Conscious Vision
Klerman, E., Shanahan, T. L., Brotman, D. J., Rimmer, D. W., Emens, J. S., Rizzo, J. F., & Czeisler, C. A. (2002) · Journal of Biological Rhythms · doi:10.1177/0748730402238237 · Cited by 132 · see citing works
Circadian Aspects of Postprandial Metabolism
Morgan, L., Hampton, S. M., Gibbs, M. A., & Arendt, J. (2003) · Chronobiology International · doi:10.1081/cbi-120024218 · Cited by 129 · see citing works
Entrainment of the Circadian System of Mammals by Nonphotic Cues
Hastings, M. H., Duffield, G. E., Smith, E. J. D., Maywood, E. S., & Ebling, F. J. P. (1998) · Chronobiology International · doi:10.3109/07420529808998700 · Cited by 123 · see citing works
Simulations of light effects on the human circadian pacemaker: implications for assessment of intrinsic period
Klerman, E., Dijk, D., Kronauer, R. E., & Czeisler, C. A. (1996) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1996.270.1.r271 · Cited by 120 · see citing works
Capturing the circadian rhythms of free-running blind people with 0.5 mg melatonin
Lewy, A. J., Bauer, V. K., Hasler, B. P., Kendall, A. R., Pires, M. L. N., & Sack, R. L. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02964-x · Cited by 120 · see citing works
Regulation of endothelial nitric oxide synthase by the actin cytoskeleton
Su, Y., Edwards-Bennett, S. M., Bubb, M., & Block, E. R. (2003) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00248.2002 · Cited by 120 · see citing works
Phase-Advance Shifts of Human Circadian Pacemaker are Accelerated by Daytime Physical Exercise
宮崎, 俊. (2001) · Medical Entomology and Zoology · Cited by 119 · see citing works
Effects of Daily Schedules of Forced Activity on Free-Running Rhythms in the Rat
Mistlberger, R. E. (1991) · Journal of Biological Rhythms · doi:10.1177/074873049100600108 · Cited by 117 · see citing works
Self-citation
Human circadian rhythms in constant dim light (8 lux) with knowledge of clock time
Middleton, B., Arendt, J., & Stone, B. M. (1996) · Journal of Sleep Research · doi:10.1046/j.1365-2869.1996.d01-67.x · Cited by 116 · see citing works
Intermittent bright light and exercise to entrain human circadian rhythms to night work
Baehr, E. K., Fogg, L., & Eastman, C. I. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.6.r1598 · Cited by 110 · see citing works
Endogenous and exogenous components in the circadian variation of core body temperature in humans
Hiddinga, A. E., BEERSMA, & van den Hoofdakker, R. H. (1997) · Journal of Sleep Research · doi:10.1046/j.1365-2869.1997.00047.x · Cited by 105 · see citing works
Let there be “more” light: enhancement of light actions on the circadian system through non-photic pathways
Yannielli, P. C., & Harrington, M. E. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.06.001 · Cited by 105 · see citing works
Resetting of the circadian clock by a conditioned stimulus
Amir, S., & Stewart, J. (1996) · Nature · doi:10.1038/379542a0 · Cited by 92 · see citing works
Is Sleep per se a Zeitgeber in Humans?
Danilenko, K. V., Cajochen, C., & Wirz‐Justice, A. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403251732 · Cited by 92 · see citing works
Daytime naps in darkness phase shift the human circadian rhythms of melatonin and thyrotropin secretion
Buxton, O. M., L’Hermite‐Balériaux, M., Turek, F. W., & Cauter, E. V. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.2.r373 · Cited by 91 · see citing works
Sensitivity of the Human Circadian Pacemaker to Moderately Bright Light
Boivin, D. B., Duffy, J. F., Kronauer, R. E., & Czeisler, C. A. (1994) · Journal of Biological Rhythms · doi:10.1177/074873049400900311 · Cited by 91 · see citing works
Early versus late bedtimes phase shift the human dim light melatonin rhythm despite a fixed morning lights on time
Burgess, H. J., & Eastman, C. I. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2003.11.032 · Cited by 88 · see citing works
Effects of light on human circadian rhythms
Skene, D. J., Lockley, S. W., Thapan, K., & Arendt, J. (1999) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19990302 · Cited by 88 · see citing works
Self-citation
Zur Zeitgeber-St�rke eines Licht-Dunkel-Wechsels f�r die circadiane Periodik des Menschen
Wever, R. A. (1970) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00586368 · Cited by 87 · see citing works
Stress-Induced Changes in Circadian Rhythms of Body Temperature and Activity in Rats Are not Caused by Pacemaker Changes
Meerlo, P., van den Hoofdakker, R. H., Koolhaas, J. M., & Daan, S. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200109 · Cited by 86 · see citing works
Adenosine and caffeine modulate circadian rhythms in the Syrian hamster
Antle, M. C., Steen, N. M., & Mistlberger, R. E. (2001) · Neuroreport · doi:10.1097/00001756-200109170-00029 · Cited by 74 · see citing works
Self-citation
Adenosine Modulation of Calcium Currents and Presynaptic Inhibition of GABA Release in Suprachiasmatic and Arcuate Nucleus Neurons
Chen, G., & van den Pol, A. N. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3035 · Cited by 72 · see citing works
Differential effects of bright light and social cues on reentrainment of human circadian rhythms
Honma, K., Honma, S., Nakamura, K., Sasaki, M., Endo, T., & Takahashi, T. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.268.2.r528 · Cited by 72 · see citing works
Circadian phase-delaying effects of bright light alone and combined with exercise in humans
Youngstedt, S. D., Kripke, D. F., & Elliott, J. A. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00473.2001 · Cited by 69 · see citing works
Sleep deprivation can attenuate light-induced phase shifts of circadian rhythms in hamsters
Mistlberger, R. E., Landry, G. J., & Marchant, E. G. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00815-x · Cited by 69 · see citing works
Self-citation
Circadian Rhythms in Mammals: Formal Properties and Environmental Influences
Mistlberger, R. E., & Rusak, B. (2005) · Elsevier eBooks · doi:10.1016/b0-72-160797-7/50034-3 · Cited by 63 · see citing works
Self-citation
Timing of single daily meal influences relations among human circadian rhythms in urinary cyclic AMP and hemic glucagon, insulin and iron
Goetz, F. C., Bishop, J., Franz Halberg, A., Sothern, R. B., Brunning, R. D., Senske, B., Greenberg, B. Z., Minors, D. S., Stoney, P., Smith, I., et al. (1976) · Cellular and Molecular Life Sciences · doi:10.1007/bf01933983 · Cited by 58 · see citing works
Correlation between urinary cortisol and 6‐sulphatoxymelatonin rhythms in field studies of blind subjects
Skene, D. J., Lockley, S. W., James, & Arendt (1999) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1999.00714.x · Cited by 58 · see citing works
Self-citation
A Benzodiazepine Hypnotic Facilitates Adaptation of Circadian Rhythms and Sleep-Wake Homeostasis to an Eight Hour Delay Shift Simulating Westward Jet Lag
Buxton, O. M., Copinschi, G., Onderbergen, A. V., Karrison, T. G., & Cauter, E. V. (2000) · SLEEP · doi:10.1093/sleep/23.7.1g · Cited by 57 · see citing works
Human circadian phase in 12:12 h, 200:<8 lux and 1000:<8 lux light-dark cycles, without scheduled sleep or activity
Middleton, B., Stone, B. M., & Arendt, J. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00574-8 · Cited by 52 · see citing works
Effect of meal timing on diurnal rhythm of human cholesterol synthesis
Cella, L. K., Cauter, E. V., & Schoeller, D. A. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.269.5.e878 · Cited by 47 · see citing works
The effects of electric fields on circadian rhythmicity in men.
Wever, R. (1970) · PubMed · Cited by 46 · see citing works
Short‐term exposure to constant light promotes strong circadian phase‐resetting responses to nonphotic stimuli in Syrian hamsters
Knoch, M. E., Gobes, S. M. H., Pavlovska, I., Su, C., Mistlberger, R. E., & Glass, J. D. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03371.x · Cited by 45 · see citing works
Self-citation
Late-night presentation of an auditory stimulus phase delays human circadian rhythms
Goel, N. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00754.2004 · Cited by 44 · see citing works
GABAA/benzodiazepine receptor localization in the circadian timing system
Michels, K. M., Morin, L. P., & Moore, R. Y. (1990) · Brain Research · doi:10.1016/0006-8993(90)90753-x · Cited by 43 · see citing works
Rapid phase advance of the 24-h melatonin profile in response to afternoon dark exposure
Cauter, E. V., Moreno‐Reyes, R., Akseki, E., L’Hermite‐Balériaux, M., Hirschfeld, U., Leproult, R., & Copinschi, G. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.275.1.e48 · Cited by 41 · see citing works
Circadian phase-shifts induced by chlordiazepoxide without increased locomotor activity
Biello, S. M., & Mrosovsky, N. (1993) · Brain Research · doi:10.1016/0006-8993(93)90801-s · Cited by 40 · see citing works
Circadian modulation of the ryanodine receptor type 2 in the SCN of rodents
Díaz‐Muñoz, M., Dent, M. A. R., Granados‐Fuentes, D., et al. (1999) · Neuroreport · doi:10.1097/00001756-199902250-00007 · Cited by 37 · see citing works
Impact of Meal Timing and Frequency on the Twenty-Four-Hour Leptin Rhythm
Fogteloo, A. J., Pijl, H., Roelfsema, F., Frölich, M. A., & Meinders, A. E. (2004) · Hormone Research in Paediatrics · doi:10.1159/000079326 · Cited by 35 · see citing works
Adaptation of circadian rhythmicity to shift in light-dark cycle accelerated by a benzodiazepine
Reeth, O. V., & Turek, F. W. (1987) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1987.253.1.r204 · Cited by 34 · see citing works
Effects of okadaic acid and intracellular Cl- on Na(+)-K(+)-Cl- cotransport
Altamirano, A. A., Breitwieser, G. E., & Russell, J. M. (1995) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1995.269.4.c878 · Cited by 34 · see citing works
Zeitgebers, Entrainment and Masking of the Circadian System
Honma, K., & Honma, S. (2001) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 34 · see citing works
Using outdoor exercise to decrease jet lag in airline crewmembers.
SHIOTA, M., Sudou, M., & Ohshima, M. (1996) · PubMed · Cited by 30 · see citing works
The benzodiazepine triazolam phase-shifts circadian activity rhythms in a diurnal primate, the squirrel monkey (Saimiri sciureus)
Mistlberger, R. E., Houpt, T. A., & Moore‐Ede, M. C. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90814-a · Cited by 27 · see citing works
Self-citation
No Impact of Physical Activity on the Period of the Orcadian Pacemaker in Humans
Beersma, D. G. M., & Hiddinga, A. E. (1998) · Chronobiology International · doi:10.3109/07420529808998669 · Cited by 25 · see citing works
Autonomous circadian rhythms in man
Wever, R. (1975) · Die Naturwissenschaften · doi:10.1007/bf00612105 · Cited by 25 · see citing works
Change of pupil size as a function of exercise.
Ishigaki, H., Miyao, M., & Ishihara, S. (1991) · PubMed · Cited by 23 · see citing works
Effects of low-level, low-frequency fields on human circadian rhythms.
Wever, R. (1977) · PubMed · Cited by 16 · see citing works
Responses of the Circadian System of Rats to Conditioned and Unconditioned Stimuli
de Groot, M. H. M., & Rusak, B. (2000) · Journal of Biological Rhythms · doi:10.1177/074873000129001369 · Cited by 12 · see citing works
[Non-photic entrainment of human circadian clock--effects of forced sleep-wake schedule on the circadian rhythm in plasma melatonin].
Nakamura, K. (1996) · PubMed · Cited by 12 · see citing works
Failure of triazolam to alter circadian reentrainment rates in squirrel monkeys
Boulos, Z., & Houpt, T. A. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90145-7 · Cited by 6 · see citing works

Flagged first, then by citations

Sorted by citations

Meal timing regulates the human circadian system
Wehrens, S. M. T., Christou, S., Isherwood, C., Middleton, B., Gibbs, M. A., Archer, S. N., Skene, D. J., & Johnston, J. D. (2017) · Current Biology · doi:10.1016/j.cub.2017.04.059 · Cited by 596 · see citing works
Self-citation
Entrainment of the human circadian system by light
Duffy, J. F., & Wright, K. P. (2005) · Journal of Biological Rhythms · doi:10.1177/0748730405277983 · Cited by 515 · see citing works
Circadian rhythms and disorders of the timing of sleep
Meyer, N., Harvey, A. G., Lockley, S. W., & Dijk, D.-J. (2022) · The Lancet · doi:10.1016/s0140-6736(22)00877-7 · Cited by 346 · see citing works
Entrainment of the Human Circadian Clock
Roenneberg, T., & Merrow, M. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.043 · Cited by 272 · see citing works
Food as a circadian time cue - evidence from human studies
Lewis, P., Oster, H., Korf, H. W., Foster, R. G., & Erren, T. C. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0318-z · Cited by 207 · see citing works
The chronotherapeutic treatment of bipolar disorders: A systematic review and practice recommendations from the ISBD task force on chronotherapy and chronobiology
Gottlieb, J. F., Benedetti, F., Geoffroy, P. A., Henriksen, T. E. G., Lam, R. W., Murray, G., Phelps, J., Sit, D., Swartz, H. A., Crowe, M., et al. (2019) · Bipolar Disorders · doi:10.1111/bdi.12847 · Cited by 196 · see citing works
Exercise as a synchroniser of human circadian rhythms: an update and discussion of the methodological problems
Atkinson, G., Edwards, B., Reilly, T., & Waterhouse, J. (2007) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0361-z · Cited by 167 · see citing works
Sleep, its regulation and possible mechanisms of sleep disturbances
Porkka‐Heiskanen, T., Zitting, K. ‐., & Wigren, H. ‐. (2013) · Acta Physiologica · doi:10.1111/apha.12134 · Cited by 157 · see citing works
Internal desynchronization in a model of night-work by forced activity in rats
Salgado-Delgado, R., Ángeles-Castellanos, M., Buijs, M. R., & Escobar, C. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.03.066 · Cited by 157 · see citing works
Sleep and circadian contributions to adolescent alcohol use disorder
Hasler, B. P., Soehner, A. M., & Clark, D. B. (2015) · Alcohol · doi:10.1016/j.alcohol.2014.06.010 · Cited by 123 · see citing works
Latitudinal cline of chronotype
Leocadio-Miguel, M. A., Louzada, F. M., Duarte, L. L., Areas, R. P., Alam, M., Freire, M. V., Fontenele-Araujo, J., Menna-Barreto, L., & Pedrazzoli, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-05797-w · Cited by 99 · see citing works
Time-of-day dependent effects of contractile activity on the phase of the skeletal muscle clock
Kemler, D., Wolff, C. A., & Esser, K. A. (2020) · The Journal of Physiology · doi:10.1113/jp279779 · Cited by 87 · see citing works
In sync with the family: children and partners influence the sleep-wake circadian rhythm and social habits of women
Leonhard, C., & Randler, C. (2009) · Chronobiology International · doi:10.1080/07420520902821101 · Cited by 87 · see citing works
Central and peripheral circadian clocks and their role in Alzheimer's disease
Chauhan, R., Chen, K.-F., Kent, B. A., & Crowther, D. C. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.030627 · Cited by 58 · see citing works
“Other zeitgebers include nonphotic stimuli, such as temperature, food availability, exercise and social interactions (Buhr et al., 2010; Carneiro and Araujo, 2012; Glaser and Stanewsky, 2007; Hastings et al., 1998; Levine et al., 2002a; Mistlberger and Skene, 2005; Simoni et al., 2014), which under certain circumstanc…”
Background
Mother–infant circadian rhythm: Development of individual patterns and dyadic synchrony
Thomas, K. A., Burr, R. L., Spieker, S., Lee, J., & Chen, J. (2014) · Early Human Development · doi:10.1016/j.earlhumdev.2014.09.005 · Cited by 55 · see citing works
Are Individual Differences in Sleep and Circadian Timing Amplified by Use of Artificial Light Sources?
Swaminathan, K., Klerman, E. B., & Phillips, A. J. K. (2017) · Journal of Biological Rhythms · doi:10.1177/0748730417699310 · Cited by 45 · see citing works
Delayed sleep-wake phase disorder and its related sleep behaviors in the young generation.
Futenma, K., Takaesu, Y., Komada, Y., Shimura, A., Okajima, I., Matsui, K., Tanioka, K., & Inoue, Y. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1174719 · Cited by 42 · see citing works
<i>Zeitgeber</i> -effects of exercise on human circadian rhythms: what are alternative approaches to investigating the existence of a phase-response curve to exercise?
Edwards, B. J., Reilly, T., & Waterhouse, J. (2009) · Biological Rhythm Research · doi:10.1080/09291010802067072 · Cited by 31 · see citing works
Homeostatic and Circadian Control of Food Intake: Clinical Strategies to Prevent Overconsumption
Drapeau, V., & Gallant, A. R. (2013) · Current Obesity Reports · doi:10.1007/s13679-012-0038-3 · Cited by 10 · see citing works

Clocks in the Wild: Entrainment to Natural Light
Schmal, C., Herzel, H., & Myung, J. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00272 · Cited by 53 · see citing works
Basic concepts and unique features of human circadian rhythms: implications for human health
Yamanaka, Y. (2020) · Nutrition Reviews · doi:10.1093/nutrit/nuaa072 · Cited by 32 · see citing works
Photic Entrainment of the Circadian System
Ashton, A., Foster, R., & Jagannath, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020729 · Cited by 106 · see citing works
Period Responses to Zeitgeber Signals Stabilize Circadian Clocks During Entrainment
Sharma, V. K. (2003) · Chronobiology International · doi:10.1081/cbi-120020422 · Cited by 17 · see citing works
Period and Phase Adjustments of Human Circadian Rhythms in the Real World
Honma, K., Hashimoto, S., Nakao, M., & Honma, S. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403018003008 · Cited by 45 · see citing works

Authors: Mistlberger, R. E., & Skene, D. J.
Affiliations: Simon Fraser University (CA)
University of Surrey (GB)
Corresponding author: Mistlberger, Ralph E.
Skene, Debra J.
ORCID: Mistlberger, Ralph E.
Skene, Debra J.
Venue: Journal of Biological Rhythms
Publisher: SAGE Publications
Published: 2005-08
Volume: 20
Issue: 4
Pages: 339-352
ISSN: 0748-7304 (ISSN-L)
1552-4531
DOI: 10.1177/0748730405277982
OpenAlex: W2028158092
Cited by: 267
References: 116
Citations by year: 2026: 10 · 2025: 11 · 2024: 14 · 2023: 20 · 2022: 15 · 2021: 12 · 2020: 13 · 2019: 14 · 2018: 11 · 2017: 15 · 2016: 9 · 2015: 8 · 2014: 11 · 2013: 15 · 2012: 13
FWCI: 4.77
Type: journal article
Language: en
Open access: closed
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Journal of Biological Rhythms (publishedVersion)
PubMed (publishedVersion)
Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
Funders: Wellcome Trust
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Keywords: non-photic entrainment, circadian rhythm, circadian clock, zeitgebers, blind subjects, free-running rhythm, physical activity, melatonin, meal timing, social stimuli, phase response curve, shift work, transmeridian travel, older adults
MeSH terms: Blindness, Circadian Rhythm, Humans, Light, Physical Stimulation, Sleep, Wakefulness

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.

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

Nonphotic Entrainment in Humans?

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks