FAILURE OF EXTRAOCULAR LIGHT TO FACILITATE CIRCADIAN RHYTHM REENTRAINMENT IN HUMANS

Although extraocular light can entrain the circadian rhythms of invertebrates and nonmammalian vertebrates, almost all studies show that the mammalian circadian system can only be affected by light to the eyes. The exception is a recent study by Campbell and Murphy that reported phase shifts in humans to bright light applied with fiber-optic pads behind the knees (popliteal region). We tested whether this extraocular light stimulus could accelerate the entrainment of circadian rhythms to a shift of the sleep schedule, as occurs in shift work or jet lag. In experiment 1, the sleep/dark episodes were delayed 8h from baseline for 2 days, and 3h light exposures were timed to occur before the temperature minimum to help delay circadian rhythms. There were three groups: (1) bright (about 13,000 lux) extraocular light from fiber-optic pads, (2) control (dim light, 10–20 lux), and (3) medium-intensity (about 1000 lux) ocular light from light boxes. In experiment 2, the sleep/dark episodes were inverted, and extraocular light was applied either before the temperature minimum to help delay circadian rhythms or after the temperature minimum to help advance rhythms. Circadian phase markers were the salivary dim light melatonin onset (DLMO) and the rectal temperature minimum. There was no evidence that the popliteal extraocular light had a phase-shifting effect in either experiment. Possible reasons for phase shifts in the Campbell and Murphy study and not the current study include the many differences between the protocols. In the current study, there was substantial sleep deprivation before the extraocular light was applied. There was a large shift in the sleep/dark schedule, rather than allowing subjects to sleep each day from midnight to noon, as in the Campbell and Murphy study. Also, when extraocular light was applied in the current protocol, subjects did not experience a change from sleeping to awake, a change in posture (from lying in bed to sitting in a chair), or a change in ocular light (from dark to dim light). Further research is necessary to determine the conditions under which extraocular light might produce phase shifts in human circadian rhythms. (Chronobiology International, 17(6), 807–826, 2000).

[1]  Lennart Wetterberg,et al.  Light and biological rhythms in man , 2014 .

[2]  W. Revelle,et al.  Individual differences in the phase and amplitude of the human circadian temperature rhythm: with an emphasis on morningness–eveningness , 2000, Journal of sleep research.

[3]  W. P. Hayes,et al.  A Novel Human Opsin in the Inner Retina , 2000, The Journal of Neuroscience.

[4]  A Yasui,et al.  Photic induction of mPer1 and mPer2 in cry-deficient mice lacking a biological clock. , 1999, Science.

[5]  C. Eastman,et al.  Intermittent bright light and exercise to entrain human circadian rhythms to night work. , 1999, The American journal of physiology.

[6]  C. Eastman,et al.  Nocturnal melatonin secretion is not suppressed by light exposure behind the knee in humans , 1999, Neuroscience Letters.

[7]  J. Meijer,et al.  Functional absence of extraocular photoreception in hamster circadian rhythm entrainment , 1999, Brain Research.

[8]  M. Menaker,et al.  No Evidence for Extraocular Photoreceptors in the Circadian System of the Syrian Hamster , 1999, Journal of biological rhythms.

[9]  J. Olcese,et al.  Pineal rhythms are synchronized to light–dark cycles in congenitally anophthalmic mutant rats , 1999, Brain Research.

[10]  R. Foster,et al.  Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[11]  R. Foster,et al.  Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. , 1999, Science.

[12]  R. Foster,et al.  Neither functional rod photoreceptors nor rod or cone outer segments are required for the photic inhibition of pineal melatonin. , 1999, Endocrinology.

[13]  R. Foster,et al.  Photoentrainment in Mammals: A Role for Cryptochrome? , 1999, Journal of biological rhythms.

[14]  D. S. Hsu,et al.  Role of mouse cryptochrome blue-light photoreceptor in circadian photoresponses. , 1998, Science.

[15]  S. Hampton,et al.  Extraocular light exposure does not suppress plasma melatonin in humans. , 1998, The Journal of clinical endocrinology and metabolism.

[16]  A. Sancar,et al.  Vitamin B2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Ottenweller,et al.  Daily Patterns of Running Wheel Activity in Male Anophthalmic Mice , 1998, Physiology & Behavior.

[18]  R. Foster Shedding Light on the Biological Clock , 1998, Neuron.

[19]  C. Eastman,et al.  Medium-intensity light produces circadian rhythm adaptation to simulated night-shift work. , 1998, Sleep.

[20]  S. Campbell,et al.  Extraocular circadian phototransduction in humans. , 1998, Science.

[21]  E. van Cauter,et al.  Acute and Delayed Effects of Exercise on Human Melatonin Secretion , 1997, Journal of biological rhythms.

[22]  R. Mistlberger,et al.  Sleep deprivation can attenuate light-induced phase shifts of circadian rhythms in hamsters , 1997, Neuroscience Letters.

[23]  S. Snyder,et al.  Developmental Expression Pattern of Phototransduction Components in Mammalian Pineal Implies a Light-Sensing Function , 1997, The Journal of Neuroscience.

[24]  A C Bird,et al.  Relationship between melatonin rhythms and visual loss in the blind. , 1997, The Journal of clinical endocrinology and metabolism.

[25]  Charmane I. Eastman,et al.  Conflicting Bright Light Exposure during Night Shifts Impedes Circadian Adaptation , 1997, Journal of biological rhythms.

[26]  D. Oren Humoral Phototransduction: Blood Is a Messenger , 1996 .

[27]  C. Eastman,et al.  Dark goggles and bright light improve circadian rhythm adaptation to night-shift work. , 1994, Sleep.

[28]  M. Byrne,et al.  Nocturnal exercise phase delays circadian rhythms of melatonin and thyrotropin secretion in normal men. , 1994, The American journal of physiology.

[29]  R. Foster Photoreceptors and Circadian Systems , 1993 .

[30]  A. Lewy,et al.  Circadian rhythm abnormalities in totally blind people: incidence and clinical significance. , 1992, The Journal of clinical endocrinology and metabolism.

[31]  N. Ibuka Circadian rhythms in sleep-wakefulness and wheel-running activity in a congenitally anophthalmic rat mutant , 1987, Physiology & Behavior.

[32]  D A Newsome,et al.  Light suppresses melatonin secretion in humans. , 1980, Science.

[33]  R. Moore,et al.  Suprachiasmatic nucleus, secondary synchronizing stimuli and the central neural control of circadian rhythms , 1980, Brain Research.

[34]  I. Zucker,et al.  Neural regulation of circadian rhythms. , 1979, Physiological reviews.

[35]  C. P. Richter Inborn nature of the rat's 24-hour clock. , 1971, Journal of comparative and physiological psychology.

[36]  W. B. Quay Physiological significance of the pineal during adaptation to shifts in photoperiod. , 1970, Physiology & behavior.

[37]  Izzo,et al.  SUPPRESSION OF MELATONIN SECRETION IN SOME BLIND PATIENTS BY EXPOSURE TO BRIGHT LIGHT , 2001 .

[38]  C. Eastman,et al.  How to use light and dark to produce circadian adaptation to night shift work. , 1999, Annals of medicine.

[39]  C. M. Singer,et al.  The human phase response curve (PRC) to melatonin is about 12 hours out of phase with the PRC to light. , 1998, Chronobiology international.

[40]  P. Diwan,et al.  A behavioral profile of bilateral anophthalmic mutant rats. , 1995, Experimental animals.

[41]  M. Menaker,et al.  Circadian Photoreception in Mammals and Other Vertebrates , 1993 .

[42]  I. Zucker,et al.  Absence of extraocular photoreception in diurnal and nocturnal rodents exposed to direct sunlight , 1981 .

[43]  C. P. Richter Discovery of fire by man--its effects on his 24-hour clock and intellectual and cultural evolution. , 1977, The Johns Hopkins medical journal.

[44]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.