Photic sensitivity for circadian response to light varies with photoperiod

Journal of Biological Rhythms

Volumn 27, Issue 4, 2012, Pages 308-318

  Glickman, Gena ^a   Webb, Ian C ^b   Elliott, Jeffrey A ^a   Baltazar, Ricardo M ^c   Reale, Meghan E ^c   Lehman, Michael N ^b   Gorman, Michael R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c WESTERN UNIVERSITY   (Canada)

Author keywords

circadian; history; light; phase shift; photoperiod; sensitivity; winter

Indexed keywords

CIRCADIAN RHYTHM SIGNALING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C FOS;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; CIRCADIAN RHYTHM; HAMSTER; HUMAN; IMMUNOHISTOCHEMISTRY; LIGHT; MALE; METABOLISM; MOTOR ACTIVITY; PHOTOPERIODICITY; PHOTOSTIMULATION; PHYSIOLOGY; RADIATION EXPOSURE; SUPRACHIASMATIC NUCLEUS; SYRIAN HAMSTER; TIME;

ANALYSIS OF VARIANCE; ANIMALS; CIRCADIAN RHYTHM; CRICETINAE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNOHISTOCHEMISTRY; LIGHT; MALE; MESOCRICETUS; MOTOR ACTIVITY; PERIOD CIRCADIAN PROTEINS; PHOTIC STIMULATION; PHOTOPERIOD; PROTO-ONCOGENE PROTEINS C-FOS; SUPRACHIASMATIC NUCLEUS; TIME FACTORS;

ANIMALIA; CRICETINAE; MESOCRICETUS AURATUS;

EID: 84864606592     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730412450826     Document Type: Article

References (52)

1. Aggelopoulos NC, Meissl H. Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J Physiol. 2000 ; 523: 211-222 (Pubitemid 30135833)
2. Brainard GC, Hanifin JP, Greeson JM, Byrne B, Glickman G, Gerner E, Rollag MD. Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J Neurosci. 2001 ; 21: 6405-6412 (Pubitemid 32737772)
3. Burgess HJ, Eastman CI. Short nights reduce light-induced circadian phase delays in humans. Sleep. 2006 ; 29: 25-30 (Pubitemid 44019027)
4. Coogan AN, Piggins HD. Circadian and photic regulation of phosphorylation of ERK1/2 and Elk-1 in the suprachiasmatic nuclei of the Syrian hamster. J Neurosci. 2003 ; 23 (7). 3085-3093 (Pubitemid 36418644)
5. Cronly-Dillon J, Sharma SC. Effect of season and sex on the photopic spectral sensitivity of the three-spined stickleback. J Exp Biol. 1968 ; 49: 679-687
6. Dacey DM, Liao H-W, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau K-W, Gamlin PD. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005 ; 433: 749-754 (Pubitemid 40292984)
7. Evans JA, Elliott JA, Gorman MR. Photoperiod differentially modulates photic and nonphotic phase response curves of hamsters. Am J Physiol Regul Integr Comp Physiol. 2004 ; 286: R539 - R546
8. Evans JA, Elliott JA, Gorman MR. Circadian effects of light no brighter than moonlight. J Biol Rhythms. 2007 ; 22: 356
9. Field MD, Maywood ES, O'Brien JA, Weaver DR, Reppert SM, Hastings MH. Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of circadian mechanisms. Neuron. 2000 ; 25: 437-447
10. Goldman BD, Elliott JA Processing of Environmental Information in Vertebrates. Stetson M, ed. New York: Springer-Verlag ; 1988: 203-218.
11. Gooley JJ, Lu J, Fischer D, Saper CB. A broad role for melanopsin in nonvisual photoreception. J Neurosci. 2003 ; 23: 7093-7106 (Pubitemid 36975874)
12. Güler AD, Ecker JL, Lall GS, Haq S, Altimu CM, Liao H-W, Barnard AR, Cahill H, Badea TC, Zhao H, et al. Melanopsin cells are the principle conduits for rod-cone input to non-image-forming vision. Nature. 2008 ; 453: 102-105 (Pubitemid 351630322)
13. Hattar S, Liao H-W, Takao M, Berson DM, Yau K-W. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002 ; 295: 1065-1070 (Pubitemid 34132235)
14. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003 ; 424: 76-81 (Pubitemid 36834844)
15. Honrado GI, Johnson RS, Golombek DA, Spiegelman BM, Papaioannou VE, Ralph MR. The circadian system of c-fos deficient mice. J Comp Physiol A. 1996 ; 178 (4). 563-570
16. Lam RW, Levitan RD. Pathophysiology of seasonal affective disorder: a review. J Psychiatry Neurosci. 2000 ; 25: 469-480 (Pubitemid 32059916)
17. Lavoie MP, Lam RW, Bouchard G, Sasseville A, Charron MC, Gagne AM, Tremblay P, Filteau MJ, Hebert M. Evidence of a biological effect of light therapy on the retina of patients with seasonal affective disorder. Biol Psychiatry. 2009 ; 66 (3). 253-258
18. Mathes A, Engel L, Holthues H, Wolloscheck T, Spessert R. Daily profile in melanopsin transcripts depends on seasonal lighting conditions in the rat retina. J Neuroendocrinol. 2007 ; 19: 952-957 (Pubitemid 350131081)
19. Maywood ES, Mrosovsky N, Field MD, Hastings MH. Rapid down-regulation of mammalian Period genes during behavioral resetting of the circadian clock. Proc Natl Acad Sci U S A. 1999 ; 96: 15211-15216 (Pubitemid 30019791)
20. Moore RY, Weis R, Moga MM. Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol. 2000 ; 420: 398-418 (Pubitemid 30183767)
21. Morin LP, Blanchard JH. Forebrain connections of the hamster intergeniculate leaflet: Comparison with those of lateral geniculate nucleus and retina. Vis Neurosci. 1999 ; 16: 1037-1054 (Pubitemid 30028231)
22. Morin LP, Wood RI Stereotaxic Atlas of the Golden Hamster Brain. San Diego, CA: Academic Press ; 2001 :
23. Nelson DE, Takahashi JS. Comparison of visual sensitivity for suppression of pineal melatonin and circadian phase-shifting in the golden hamster. Brain Res. 1991 ; 554: 272-277
24. Nuesslein-Hildesheim B, O'Brien JA, Ebling FJP, Maywood ES, Hastings MH. The circadian cycle of mPER clock gene product in the suprachiasmatic nucleus of the Siberian hamster encodes both daily and seasonal time. Eur J Neurosci. 2000 ; 12: 2856-2864
25. Obrietan K, Impey S, Storm DR. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat Neurosci. 1998 ; 1: 693-700 (Pubitemid 128406380)
26. Owen J, Arendt J. Melatonin suppression in human subjects by bright and dim light in Antarctica: Time and season-dependent effects. Neurosci Lett. 1992 ; 137: 181-184
27. Pittendrigh CS Handbook of Behavioral Neurobiology: Biological Rhythms. Achoff J, ed. New York: Plenum ; 1981: 95-124.
28. Pittendrigh CS, Daan S. A functional analysis of circadian pacemakers in nocturnal rodents: IV. Entrainment: pacemaker as clock. J Comp Physiol. 1976 ; 106: 291-351
29. Pittendrigh CS, Elliott JA, Takamura T. The circadian component in photoperiodic induction. CIBA Foundation Symp. 1984 ; 104: 26-47
30. Reme C, Wirz-Justice A, Rhyner A, Hofmann S. Circadian rhythms in light response of retinal disk-shedding and autophagy. Brain Res. 1986 ; 369: 356-360 (Pubitemid 16047420)
31. Reppert SM, Weaver DR. Molecular analysis of mammalian circadian rhythms. Ann Rev Physiol. 2001 ; 63: 647-676 (Pubitemid 32304333)
32. Sekaran S, Foster RG, Lucas RJ, Hankins MW. Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol. 2003 ; 13: 1290-1298 (Pubitemid 36953301)
33. Shigeyoshi Y, Taguchi K, Yamamoto S, Takekida S, Yan L, Tei H, Moriya T, Shibata S, Loros J, Dunlap J, et al. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell. 1997 ; 91: 1043-1053 (Pubitemid 28027836)
34. Shimomura K, Menaker M. Light-induced phase shifts in tau mutant hamsters. J Biol Rhythms. 1994 ; 9: 97-110
35. Sollars PJ, Simpson AM, Ogilvie MD, Pickard GE. Light-induced Fos expression is attenuated in the suprachiasmatic nucleus of serotonin 1B receptor knockout mice. Neurosci Lett. 2006 ; 401: 209-213 (Pubitemid 43729520)
36. Sumová A, Jác M, Sládek M, Sauman I, Illnerová H. Clock gene daily profiles and their phase relationship in the rat suprachiasmatic nucleus are affected by photoperiod. J Biol Rhythms. 2003 ; 18: 134-144 (Pubitemid 37187298)
37. Sumová A, Travnickova Z, Peters R, Schwarts WJ, Illernova H. The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci U S A. 1995 ; 92: 7754-7758
38. Takahiko H, Yasuo T. Seasonal variation of spectral sensitivity in cray fish retinula cells. Comp Biochem Physiol 81A:. 1988 ;: 529-533
39. Tosini G, Menaker M. Circadian rhythms in cultured mammalian retina. Science. 1996 ; 272: 419-421 (Pubitemid 26138180)
40. Tournier BB, Menet JS, Dardente H, Poirel VJ, Malan A, Masson-Pevet M, Pevet P, Vuillez P. Photoperiod differentially regulates clock genes' expression in the suprachiasmatic nucleus of Syrian hamster. Neuroscience. 2003 ; 118: 317-322 (Pubitemid 36423247)
41. Travnicková Z, Sumová A, Peters R, Schwartz WJ, Illernová H. Photoperiod-dependent correlation between light-induced SCN c-Fos expression and resetting of circadian phase. Am J Physiol. 1996 ; 271: 825-831
42. vanderLeest HT, Houben T, Michel S, Deboer T, Albus H, Vansteensel MJ, Block GD, Meiier JH. Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol. 2007 ; 17: 468-473
43. vanderLeest HT, Rohling JHT, Michel S, Meijer JH. Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization. PLoS ONE. 2009 ; 4: e4976
44. von Gall C, Noton E, Lee C, Weaver DR. Light does not degrade the constitutively expressed BMAL1 protein in the suprachiasmatic nucleus. Eur J Neurosci. 2003 ; 18: 125-133 (Pubitemid 36920853)
45. Watanabe T, Naito E, Nakao N, Tei H, Yoshimura T, Ebihara S. Bimodal clock gene expression in mouse suprachiasmatic nucleus and peripheral tissues under a 7-hour light and 5-hour dark condition. J Biol Rhythms. 2007 ; 22: 58-68 (Pubitemid 46041613)
46. Watson RE, Wiegand SJ, Clough RW, Hoffman GE. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides. 1986 ; 7: 155-159 (Pubitemid 16082879)
47. Wehr TA, Moul DE, Barbato G, Giesen HA, Seidel JA, Barker C, Bender C. Conservation of photoperiod responsive mechanisms in humans. Am J Physiol. 1993 ; 265: R846 - R857
48. Wong KY, Dunn FA, Berson DM. Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron. 2005 ; 48: 1001-1010 (Pubitemid 41814703)
49. Yan L, Foley NC, Bobula JM, Kreigsfeld LJ, Silver R. Two antiphase oscillators occur in each suprachiasmatic nucleus of behaviorally split hamsters. J Neurosci. 2005 ; 25: 9017-9026 (Pubitemid 41384471)
50. Yan L, Silver R. Day-length encoding through tonic photic effects in the retinorecipient SCN region. Eur J Neurosci. 2008 ; 28: 2108-2115
51. Yan L, Silver R, Gorman MR. Reorganization of suprachiasmatic nucleus networks under 24-h LDLD conditions. J Biol Rhythms. 2010 ; 25: 19-27
52. Zawilska JB, Lorenc A, Berezinska M, Vivien-Roels B, Pevet P, Skene DJ. Photoperiod-dependent changes in melatonin synthesis in the turkey pineal gland and retina. Poult Sci. 2007 ; 86: 1397-1405 (Pubitemid 47580959)