Temporal integration of light flashes by the human circadian system

Journal of Clinical Investigation

Volumn 126, Issue 3, 2016, Pages 938-947

  Najjar, Raymond P ^a,b   Zeitzer, Jamie M ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MELATONIN;

ADULT; ALERTNESS; ARTICLE; CIRCADIAN RHYTHM; CLINICAL ARTICLE; CLINICAL ASSESSMENT; FEMALE; HUMAN; INTEGRATION; LIGHT; LIGHT EXPOSURE; MALE; PRIORITY JOURNAL; SOMNOLENCE; BLOOD; CLINICAL TRIAL; PHOTOSTIMULATION; RADIATION RESPONSE; VISION; WAKEFULNESS; YOUNG ADULT;

ADULT; CIRCADIAN RHYTHM; FEMALE; HUMANS; MALE; MELATONIN; PHOTIC STIMULATION; VISUAL PERCEPTION; WAKEFULNESS; YOUNG ADULT;

EID: 84959920978     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI82306     Document Type: Article

References (87)

1. Czeisler CA, Wright KP Jr. Influence of light on circadian rhythmicity in humans. In: Turek FW, Zee PC, eds. Regulation of Sleep and Circadian Rhythms. New York, New York, USA: Marcel Dekker; 1999:149-180.
2. Duffy JF, Kronauer RE, Czeisler CA. Phase-shifting human circadian rhythms: influence of sleep timing, social contact and light exposure. J Physiol. 1996;495(pt 1):289-297.
3. Skene DJ, Lockley SW, Thapan K, Arendt J. Effects of light on human circadian rhythms. Reprod Nutr Dev. 1999;39(3):295-304.
4. Dijk DJ, Czeisler CA. Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci. 1995;15(5 pt 1):3526-3538.
5. Spiegel K, Sheridan JF, Van Cauter E. Effect of sleep deprivation on response to immunization. JAMA. 2002;288(12):1471-1472.
6. Weibel L, Brandenberger G. Disturbances in hormonal profiles of night workers during their usual sleep and work times. J Biol Rhythms. 1998;13(3):202-208.
7. Wright KP Jr, Hull JT, Czeisler CA. Relationship between alertness, performance, and body temperature in humans. Am J Physiol. 2002;283(6):R1370-R1377.
8. Young ME, Bray MS. Potential role for peripheral circadian clock dyssynchrony in the pathogenesis of cardiovascular dysfunction. Sleep Med. 2007;8(6):656-667.
9. Roenneberg T, Allebrandt KV, Merrow M, Vetter C. Social jetlag and obesity. Curr Biol. 2012;22(10):939-943.
10. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295(5557):1070-1073.
11. Provencio I, et al. A novel human opsin in the inner retina. J Neurosci. 2000;20(2):600-605.
12. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. Melanopsin: An opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A. 1998;95(1):340-345.
13. Belenky MA, Smeraski CA, Provencio I, Sollars PJ, Pickard GE. Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J Comp Neurol. 2003;460(3):380-393.
14. Lucas RJ, et al. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science. 2003;299(5604):245-247.
15. Hattar S, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003;424(6944):76-81.
16. Hattar S, et al. Central projections of melanopsinexpressing retinal ganglion cells in the mouse. J Comp Neurol. 2006;497(3):326-349.
17. Panda S, et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002;298(5601):2213-2216.
18. Lewy AJ, Wehr TA, Goodwin FK, Newsome DA, Markey SP. Light suppresses melatonin secretion in humans. Science. 1980;210(4475):1267-1269.
19. Badia P, Myers B, Boecker M, Culpepper J, Harsh JR. Bright light effects on body temperature, alertness, EEG and behavior. Physiol Behav. 1991;50(3):583-588.
20. Cajochen C, Zeitzer JM, Czeisler CA, Dijk DJ. Dose-response relationship for light intensity and ocular and electroencephalographic correlates of human alertness. Behav Brain Res. 2000;115(1):75-83.
21. Altimus CM, et al. Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc Natl Acad Sci U S A. 2008;105(50):19998-20003.
22. Kripke DF. Light treatment for nonseasonal depression: speed, efficacy, and combined treatment. J Affect Disord. 1998;49(2):109-117.
23. Wirz-Justice A, van der Velde P, Bucher A, Nil R. Comparison of light treatment with citalopram in winter depression: a longitudinal single case study. Int Clin Psychopharmacol. 1992;7(2):109-116.
24. Noseda R, et al. A neural mechanism for exacerbation of headache by light. Nat Neurosci. 2010;13(2):239-245.
25. Anderson JL, Glod CA, Dai J, Cao Y, Lockley SW. Lux vs. wavelength in light treatment of Seasonal Affective Disorder. Acta Psychiatr Scand. 2009;120(3):203-212.
26. Eastman CI, Gazda CJ, Burgess HJ, Crowley SJ, Fogg LF. Advancing circadian rhythms before eastward flight: a strategy to prevent or reduce jet lag. Sleep. 2005;28(1):33-44.
27. Glickman G, Byrne B, Pineda C, Hauck WW, Brainard GC. Light therapy for seasonal affective disorder with blue narrow-band light-emitting diodes (LEDs). Biol Psychiatry. 2006;59(6):502-507.
28. Kripke DF, Mullaney DJ, Klauber MR, Risch SC, Gillin JC. Controlled trial of bright light for nonseasonal major depressive disorders. Biol Psychiatry. 1992;31(2):119-134.
29. Lack L, Wright H. The effect of evening bright light in delaying the circadian rhythms and lengthening the sleep of early morning awakening insomniacs. Sleep. 1993;16(5):436-443.
30. Parry BL, et al. Neuroendocrine effects of light therapy in late luteal phase dysphoric disorder. Biol Psychiatry. 1994;36(6):356-364.
31. Wirz-Justice A, et al. A randomized, double-blind, placebo-controlled study of light therapy for antepartum depression. J Clin Psychiatry. 2011;72(7):986-993.
32. Wright KP Jr, Hull JT, Hughes RJ, Ronda JM, Czeisler CA. Sleep and wakefulness out of phase with internal biological time impairs learning in humans. J Cogn Neurosci. 2006;18(4):508-521.
33. Gooley JJ, et al. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci Transl Med. 2010;2(31):31ra33.
34. Gooley JJ, et al. Melanopsin and rod-cone photoreceptors play different roles in mediating pupillary light responses during exposure to continuous light in humans. J Neurosci. 2012;32(41):14242-14253.
35. Bailes HJ, Lucas RJ. Human melanopsin forms a pigment maximally sensitive to blue light (max 479 nm) supporting activation of G(q/11) and G(i/o) signalling cascades. Proc Biol Sci. 2013;280(1759):20122987.
36. Brainard GC, et al. Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J Neurosci. 2001;21(16):6405-6412.
37. Najjar RP, et al. Aging of non-visual spectral sensitivity to light in humans: compensatory mechanisms? PLoS One. 2014;9(1):e85837.
38. Thapan K, Arendt J, Skene DJ. An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J Physiol. 2001;535(pt 1):261-267.
39. Zaidi FH, et al. Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Curr Biol. 2007;17(24):2122-2128.
40. Zeitzer JM, Dijk DJ, Kronauer R, Brown E, Czeisler CA. Sensitivity of the human circadian pacemaker to nocturnal light: melatonin phase resetting and suppression. J Physiol. 2000;526(pt 3):695-702.
41. Chang A-M, et al. Human responses to bright light of different durations. J Physiol. 2012;590(13):3103-3112.
42. Gronfier C, Wright KP Jr, 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. 2004;287(1):E174-E181.
43. Rimmer DW, et al. Dynamic resetting of the human circadian pacemaker by intermittent bright light. Am J Physiol. 2000;279(5):R1574-R1579.
44. Zeitzer JM, Ruby NF, Fisicaro RA, Heller HC. Response of the human circadian system to millisecond flashes of light. PLoS One. 2011;6(7):e22078.
45. Arvanitogiannis A, Amir S. Resetting the rat circadian clock by ultra-short light flashes. Neurosci Lett. 1999;261(3):159-162.
46. Nelson DE, Takahashi JS. Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). J Physiol. 1991;439:115-145.
47. Vidal L, Morin LP. Absence of normal photic integration in the circadian visual system: response to millisecond light flashes. J Neurosci. 2007;27(13):3375-3382.
48. Van Den Pol AN, Cao V, Heller HC. Circadian system of mice integrates brief light stimuli. Am J Physiol. 1998;275(2 pt 2):R654-R657.
49. St Hilaire MA, et al. Human phase response curve to a 1 h pulse of bright white light. J Physiol. 2012;590(13):3035-3045.
50. Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4(2):97-110.
51. Reite M, Weissberg MP, Ruddy J. Circadian rhythm-based sleep complaints. In: Clinical Manual for Evaluation and Treatment of Sleep Disorders. Washington, DC, USA: American Psychiatric Pub; 2008:97-121.
52. Buysse DJ, Reynolds CF 3rd, 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.
53. Hoddes E, Zarcone V, Smythe H, Phillips R, Dement WC. Quantification of sleepiness: a new approach. Psychophysiology. 1973;10(4):431-436.
54. Khalsa SBS, 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.
55. Gronfier C, Wright KP, Kronauer RE, Czeisler CA. Entrainment of the human circadian pacemaker to longer-than-24-h days. Proc Natl Acad Sci U S A. 2007;104(21):9081-9086.
56. Emanuel AJ, Do MTH. Melanopsin tristability for sustained and broadband phototransduction. Neuron. 2015;85(5):1043-1055.
57. Hollins M, Alpern M. Dark adaptation and visual pigment regeneration in human cones. J Gen Physiol. 1973;62(4):430-447.
58. Rushton WAH, Henry GH. Bleaching and regeneration of cone pigments in man. Vision Res. 1968;8(6):617-631.
59. Coolen ACC, van Norren D. Kinetics of human cone photopigments explained with a Rushton-Henry model. Biol Cybern. 1988;58(2):123-128.
60. Nelson DE, Takahashi JS. Integration and saturation within the circadian photic entrainment pathway of hamsters. Am J Physiol. 1999;277(5):R1351-R1361.
61. Groos GA, Mason R. The visual properties of rat and cat suprachiasmatic neurones. J Comp Physiol. 1980;135(4):349-356.
62. Drouyer E, Rieux C, Hut RA, Cooper HM. Responses of suprachiasmatic nucleus neurons to light and dark adaptation: relative contributions of melanopsin and rod-cone inputs. J Neurosci. 2007;27(36):9623-9631.
63. Hecht S, Shlaer S. Intermittent stimulation by light. J Gen Physiol. 1936;19(6):965-977.
64. Jarvis JR, Prescott NB, Wathes CM. A mechanistic inter-species comparison of flicker sensitivity. Vision Res. 2003;43(16):1723-1734.
65. Güler AD, et al. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature. 2008;453(7191):102-105.
66. Schmidt TM, Chen S-K, Hattar S. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci. 2011;34(11):572-580.
67. Zhao X, Stafford BK, Godin AL, King WM, Wong KY. Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells. J Physiol. 2014;592(7):1619-1636.
68. Levine JD, Weiss ML, Rosenwasser AM, Miselis RR. Retinohypothalamic tract in the female albino rat: a study using horseradish peroxidase conjugated to cholera toxin. J Comp Neurol. 1991;306(2):344-360.
69. Johnson RF, Morin LP, Moore RY. Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res. 1988;462(2):301-312.
70. Lu J, Shiromani P, Saper CB. Retinal input to the sleep-active ventrolateral preoptic nucleus in the rat. Neuroscience. 1999;93(1):209-214.
71. Robinson J, Bayliss SC, Fielder AR. Transmission of light across the adult and neonatal eyelid in vivo. Vision Res. 1991;31(10):1837-1840.
72. Zeitzer JM, Fisicaro RA, Ruby NF, Heller HC. Millisecond flashes of light phase delay the human circadian clock during sleep. J Biol Rhythms. 2014;29(5):370-376.
73. Feinberg R, Podolak E. Latency Of Pupillary Reflex To Light Stimulation And Its Relationship To Aging. Washington, DC, USA: Federal Aviation Agency, Office of Aviation Medicine, Georgetown Clinical Research Institute; 1965.
74. Strang CE, Renna JM, Amthor FR, Keyser KT. Muscarinic acetylcholine receptor localization and activation effects on ganglion response properties. Invest Ophthalmol Vis Sci. 2010;51(5):2778-2789.
75. Lam RW, et al. The Can-SAD study: a randomized controlled trial of the effectiveness of light therapy and fluoxetine in patients with winter seasonal affective disorder. Am J Psychiatry. 2006;163(5):805-812.
76. Najjar RP, et al. Chronic artificial blue-enriched white light is an effective countermeasure to delayed circadian phase and neurobehavioral decrements. PLoS One. 2014;9(7):e102827.
77. Vetter C, Juda M, Lang D, Wojtysiak A, Roenneberg T. Blue-enriched office light competes with natural light as a zeitgeber. Scand J Work Environ Health. 2011;37(5):437-445.
78. Viola AU, James LM, Schlangen LJM, Dijk DJ. Blue-enriched white light in the workplace improves self-reported alertness, performance and sleep quality. Scand J Work Environ Health. 2008;34(4):297-306.
79. Van Someren EJ, et al. Bright light therapy: improved sensitivity to its effects on rest-activity rhythms in Alzheimer patients by application of nonparametric methods. Chronobiol Int. 1999;16(4):505-518.
80. Revell VL, et al. Advancing human circadian rhythms with afternoon melatonin and morning intermittent bright light. J Clin Endocrinol Metab. 2006;91(1):54-59.
81. Babor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG. AUDIT: The Alcohol Use Disorders Identification Test: guidelines for use in primary health care. 2nd ed. Geneva, Switzerland: World Health Organization. Department of Mental Health and Substance Dependence; 2001.
82. Radloff LS. The CES-D scale a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1(3):385-401.
83. Carney CE, et al. The consensus sleep diary: standardizing prospective sleep self-monitoring. Sleep. 2012;35(2):287-302.
84. Duffy JF, Dijk D-J. Getting through to circadian oscillators: why use constant routines? J Biol Rhythms. 2002;17(1):4-13.
85. Mifflin MD, et al. A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr. 1990;51(2):241-247.
86. Voultsios A, Kennaway DJ, Dawson D. Salivary melatonin as a circadian phase marker: validation and comparison to plasma melatonin. J Biol Rhythms. 1997;12(5):457-466.
87. Dinges DF, Powell JW. Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav Res Methods Instrum Comput. 1985;17(6):652-655.