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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2001 Nov 29;356(1415):1779–1789. doi: 10.1098/rstb.2001.0962

The regulation of circadian clocks by light in fruitflies and mice.

R G Foster 1, C Helfrich-Förster 1
PMCID: PMC1088554  PMID: 11710985

Abstract

A circadian clock has no survival value unless biological time is adjusted (entrained) to local time and, for most organisms, the profound changes in the light environment provide the local time signal (zeitgeber). Over 24 h, the amount of light, its spectral composition and its direction change in a systematic way. In theory, all of these features could be used for entrainment, but each would be subject to considerable variation or 'noise'. Despite this high degree of environmental noise, entrained organisms show remarkable precision in their daily activities. Thus, the photosensory task of entrainment is likely to be very complex, but fundamentally similar for all organisms. To test this hypothesis we compare the photoreceptors that mediate entrainment in both flies and mice, and assess their degree of convergence. Although superficially different, both organisms use specialized (employing novel photopigments) and complex (using multiple photopigments) photoreceptor mechanisms. We conclude that this multiplicity of photic inputs, in highly divergent organisms, must relate to the complex sensory task of using light as a zeitgeber.

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Selected References

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  1. Ahmad M., Cashmore A. R. Seeing blue: the discovery of cryptochrome. Plant Mol Biol. 1996 Mar;30(5):851–861. doi: 10.1007/BF00020798. [DOI] [PubMed] [Google Scholar]
  2. Cashmore A. R., Jarillo J. A., Wu Y. J., Liu D. Cryptochromes: blue light receptors for plants and animals. Science. 1999 Apr 30;284(5415):760–765. doi: 10.1126/science.284.5415.760. [DOI] [PubMed] [Google Scholar]
  3. Ceriani M. F., Darlington T. K., Staknis D., Más P., Petti A. A., Weitz C. J., Kay S. A. Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science. 1999 Jul 23;285(5427):553–556. doi: 10.1126/science.285.5427.553. [DOI] [PubMed] [Google Scholar]
  4. Cooper H. M., Herbin M., Nevo E. Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol. 1993 Feb 15;328(3):313–350. doi: 10.1002/cne.903280302. [DOI] [PubMed] [Google Scholar]
  5. Czeisler C. A., Shanahan T. L., Klerman E. B., Martens H., Brotman D. J., Emens J. S., Klein T., Rizzo J. F., 3rd Suppression of melatonin secretion in some blind patients by exposure to bright light. N Engl J Med. 1995 Jan 5;332(1):6–11. doi: 10.1056/NEJM199501053320102. [DOI] [PubMed] [Google Scholar]
  6. David-Gray Z. K., Cooper H. M., Janssen J. W., Nevo E., Foster R. G. Spectral tuning of a circadian photopigment in a subterranean 'blind' mammal (Spalax ehrenbergi). FEBS Lett. 1999 Nov 19;461(3):343–347. doi: 10.1016/s0014-5793(99)01455-6. [DOI] [PubMed] [Google Scholar]
  7. David-Gray Z. K., Janssen J. W., DeGrip W. J., Nevo E., Foster R. G. Light detection in a 'blind' mammal. Nat Neurosci. 1998 Dec;1(8):655–656. doi: 10.1038/3656. [DOI] [PubMed] [Google Scholar]
  8. Devlin P. F., Kay S. A. Cryptochromes--bringing the blues to circadian rhythms. Trends Cell Biol. 1999 Aug;9(8):295–298. doi: 10.1016/s0962-8924(99)01611-6. [DOI] [PubMed] [Google Scholar]
  9. Dushay M. S., Rosbash M., Hall J. C. The disconnected visual system mutations in Drosophila melanogaster drastically disrupt circadian rhythms. J Biol Rhythms. 1989 Spring;4(1):1–27. doi: 10.1177/074873048900400101. [DOI] [PubMed] [Google Scholar]
  10. Ebihara S., Tsuji K. Entrainment of the circadian activity rhythm to the light cycle: effective light intensity for a Zeitgeber in the retinal degenerate C3H mouse and the normal C57BL mouse. Physiol Behav. 1980 Mar;24(3):523–527. doi: 10.1016/0031-9384(80)90246-2. [DOI] [PubMed] [Google Scholar]
  11. Egan E. S., Franklin T. M., Hilderbrand-Chae M. J., McNeil G. P., Roberts M. A., Schroeder A. J., Zhang X., Jackson F. R. An extraretinally expressed insect cryptochrome with similarity to the blue light photoreceptors of mammals and plants. J Neurosci. 1999 May 15;19(10):3665–3673. doi: 10.1523/JNEUROSCI.19-10-03665.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Emery I. F., Noveral J. M., Jamison C. F., Siwicki K. K. Rhythms of Drosophila period gene expression in culture. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):4092–4096. doi: 10.1073/pnas.94.8.4092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Emery P., So W. V., Kaneko M., Hall J. C., Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell. 1998 Nov 25;95(5):669–679. doi: 10.1016/s0092-8674(00)81637-2. [DOI] [PubMed] [Google Scholar]
  14. Emery P., Stanewsky R., Hall J. C., Rosbash M. A unique circadian-rhythm photoreceptor. Nature. 2000 Mar 30;404(6777):456–457. doi: 10.1038/35006558. [DOI] [PubMed] [Google Scholar]
  15. Emery P., Stanewsky R., Helfrich-Förster C., Emery-Le M., Hall J. C., Rosbash M. Drosophila CRY is a deep brain circadian photoreceptor. Neuron. 2000 May;26(2):493–504. doi: 10.1016/s0896-6273(00)81181-2. [DOI] [PubMed] [Google Scholar]
  16. Engelmann W., Honegger H. W. Tagesperiodische Schlüpfrhythmik einer augenlosen Drosophila melanogaster-Mutante. Naturwissenschaften. 1966 Nov;53(22):588–588. doi: 10.1007/BF00600545. [DOI] [PubMed] [Google Scholar]
  17. Feiler R., Bjornson R., Kirschfeld K., Mismer D., Rubin G. M., Smith D. P., Socolich M., Zuker C. S. Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J Neurosci. 1992 Oct;12(10):3862–3868. doi: 10.1523/JNEUROSCI.12-10-03862.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Feiler R., Harris W. A., Kirschfeld K., Wehrhahn C., Zuker C. S. Targeted misexpression of a Drosophila opsin gene leads to altered visual function. Nature. 1988 Jun 23;333(6175):737–741. doi: 10.1038/333737a0. [DOI] [PubMed] [Google Scholar]
  19. Foster R. G., Provencio I., Hudson D., Fiske S., De Grip W., Menaker M. Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A. 1991 Jul;169(1):39–50. doi: 10.1007/BF00198171. [DOI] [PubMed] [Google Scholar]
  20. Frank K. D., Zimmerman W. F. Action spectra for phase shifts of a circadian rhythm in Drosophila. Science. 1969 Feb 14;163(3868):688–689. doi: 10.1126/science.163.3868.688. [DOI] [PubMed] [Google Scholar]
  21. Freedman M. S., Lucas R. J., Soni B., von Schantz M., Muñoz M., David-Gray Z., Foster R. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science. 1999 Apr 16;284(5413):502–504. doi: 10.1126/science.284.5413.502. [DOI] [PubMed] [Google Scholar]
  22. Giebultowicz J. M., Hege D. M. Circadian clock in Malpighian tubules. Nature. 1997 Apr 17;386(6626):664–664. doi: 10.1038/386664a0. [DOI] [PubMed] [Google Scholar]
  23. Giebultowicz J. M. Peripheral clocks and their role in circadian timing: insights from insects. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1791–1799. doi: 10.1098/rstb.2001.0960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Giebultowicz J. M., Stanewsky R., Hall J. C., Hege D. M. Transplanted Drosophila excretory tubules maintain circadian clock cycling out of phase with the host. Curr Biol. 2000 Jan 27;10(2):107–110. doi: 10.1016/s0960-9822(00)00299-2. [DOI] [PubMed] [Google Scholar]
  25. Goldman B. D., Goldman S. L., Riccio A. P., Terkel J. Circadian patterns of locomotor activity and body temperature in blind mole-rats, Spalax ehrenbergi. J Biol Rhythms. 1997 Aug;12(4):348–361. doi: 10.1177/074873049701200407. [DOI] [PubMed] [Google Scholar]
  26. Griffin E. A., Jr, Staknis D., Weitz C. J. Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science. 1999 Oct 22;286(5440):768–771. doi: 10.1126/science.286.5440.768. [DOI] [PubMed] [Google Scholar]
  27. Gwinner E., Brandstätter R. Complex bird clocks. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1801–1810. doi: 10.1098/rstb.2001.0959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Haim A., Heth G., Pratt H., Nevo E. Photoperiodic effects on thermoregulation in a 'blind' subterranean mammal. J Exp Biol. 1983 Nov;107:59–64. doi: 10.1242/jeb.107.1.59. [DOI] [PubMed] [Google Scholar]
  29. Hall J. C. Cryptochromes: sensory reception, transduction, and clock functions subserving circadian systems. Curr Opin Neurobiol. 2000 Aug;10(4):456–466. doi: 10.1016/s0959-4388(00)00117-3. [DOI] [PubMed] [Google Scholar]
  30. Hall J. C. Genetics of biological rhythms in drosophila. Adv Genet. 1998;38:135–184. doi: 10.1016/s0065-2660(08)60143-1. [DOI] [PubMed] [Google Scholar]
  31. Hall J. C. Molecular neurogenetics of biological rhythms. J Neurogenet. 1998 Sep;12(3):115–181. doi: 10.3109/01677069809108556. [DOI] [PubMed] [Google Scholar]
  32. Helfrich-Förster C. Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: a brain-behavioral study of disconnected mutants. J Comp Physiol A. 1998 Apr;182(4):435–453. doi: 10.1007/s003590050192. [DOI] [PubMed] [Google Scholar]
  33. Helfrich-Förster C. The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):612–616. doi: 10.1073/pnas.92.2.612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Helfrich-Förster C., Winter C., Hofbauer A., Hall J. C., Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron. 2001 Apr;30(1):249–261. doi: 10.1016/s0896-6273(01)00277-x. [DOI] [PubMed] [Google Scholar]
  35. Helfrich C. Role of the optic lobes in the regulation of the locomotor activity rhythm of Drosophila melanogaster: behavioral analysis of neural mutants. J Neurogenet. 1986 Nov;3(6):321–343. doi: 10.3109/01677068609106857. [DOI] [PubMed] [Google Scholar]
  36. Kaneko M., Hamblen M. J., Hall J. C. Involvement of the period gene in developmental time-memory: effect of the perShort mutation on phase shifts induced by light pulses delivered to Drosophila larvae. J Biol Rhythms. 2000 Feb;15(1):13–30. doi: 10.1177/074873040001500103. [DOI] [PubMed] [Google Scholar]
  37. Kaneko M., Helfrich-Förster C., Hall J. C. Spatial and temporal expression of the period and timeless genes in the developing nervous system of Drosophila: newly identified pacemaker candidates and novel features of clock gene product cycling. J Neurosci. 1997 Sep 1;17(17):6745–6760. doi: 10.1523/JNEUROSCI.17-17-06745.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kaneko M. Neural substrates of Drosophila rhythms revealed by mutants and molecular manipulations. Curr Opin Neurobiol. 1998 Oct;8(5):652–658. doi: 10.1016/s0959-4388(98)80095-0. [DOI] [PubMed] [Google Scholar]
  39. Konopka R. J., Pittendrigh C., Orr D. Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants. J Neurogenet. 1989 Sep;6(1):1–10. doi: 10.3109/01677068909107096. [DOI] [PubMed] [Google Scholar]
  40. Kume K., Zylka M. J., Sriram S., Shearman L. P., Weaver D. R., Jin X., Maywood E. S., Hastings M. H., Reppert S. M. mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell. 1999 Jul 23;98(2):193–205. doi: 10.1016/s0092-8674(00)81014-4. [DOI] [PubMed] [Google Scholar]
  41. Lin C., Robertson D. E., Ahmad M., Raibekas A. A., Jorns M. S., Dutton P. L., Cashmore A. R. Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1. Science. 1995 Aug 18;269(5226):968–970. doi: 10.1126/science.7638620. [DOI] [PubMed] [Google Scholar]
  42. Lockley S. W., Skene D. J., Arendt J., Tabandeh H., Bird A. C., Defrance R. Relationship between melatonin rhythms and visual loss in the blind. J Clin Endocrinol Metab. 1997 Nov;82(11):3763–3770. doi: 10.1210/jcem.82.11.4355. [DOI] [PubMed] [Google Scholar]
  43. Loukas A., Mullin N. P., Tetteh K. K., Moens L., Maizels R. M. A novel C-type lectin secreted by a tissue-dwelling parasitic nematode. 1999 Jul 29-Aug 12Curr Biol. 9(15):825–828. doi: 10.1016/s0960-9822(99)80366-2. [DOI] [PubMed] [Google Scholar]
  44. Lucas R. J., Douglas R. H., Foster R. G. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci. 2001 Jun;4(6):621–626. doi: 10.1038/88443. [DOI] [PubMed] [Google Scholar]
  45. Lucas R. J., Foster R. G. Photoentrainment in mammals: a role for cryptochrome? J Biol Rhythms. 1999 Feb;14(1):4–10. doi: 10.1177/074873099129000380. [DOI] [PubMed] [Google Scholar]
  46. Lucas R. J., Freedman M. S., Muñoz M., Garcia-Fernández J. M., Foster R. G. Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science. 1999 Apr 16;284(5413):505–507. doi: 10.1126/science.284.5413.505. [DOI] [PubMed] [Google Scholar]
  47. McCall M. A., Gregg R. G., Merriman K., Goto Y., Peachey N. S., Stanford L. R. Morphological and physiological consequences of the selective elimination of rod photoreceptors in transgenic mice. Exp Eye Res. 1996 Jul;63(1):35–50. doi: 10.1006/exer.1996.0089. [DOI] [PubMed] [Google Scholar]
  48. Miyamoto Y., Sancar A. Vitamin B2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6097–6102. doi: 10.1073/pnas.95.11.6097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Moore R. Y., Lenn N. J. A retinohypothalamic projection in the rat. J Comp Neurol. 1972 Sep;146(1):1–14. doi: 10.1002/cne.901460102. [DOI] [PubMed] [Google Scholar]
  50. Okamura H., Miyake S., Sumi Y., Yamaguchi S., Yasui A., Muijtjens M., Hoeijmakers J. H., van der Horst G. T. Photic induction of mPer1 and mPer2 in cry-deficient mice lacking a biological clock. Science. 1999 Dec 24;286(5449):2531–2534. doi: 10.1126/science.286.5449.2531. [DOI] [PubMed] [Google Scholar]
  51. Park J. H., Helfrich-Förster C., Lee G., Liu L., Rosbash M., Hall J. C. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3608–3613. doi: 10.1073/pnas.070036197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Philp A. R., Bellingham J., Garcia-Fernandez J., Foster R. G. A novel rod-like opsin isolated from the extra-retinal photoreceptors of teleost fish. FEBS Lett. 2000 Feb 25;468(2-3):181–188. doi: 10.1016/s0014-5793(00)01217-5. [DOI] [PubMed] [Google Scholar]
  53. Philp A. R., Garcia-Fernandez J. M., Soni B. G., Lucas R. J., Bellingham J., Foster R. G. Vertebrate ancient (VA) opsin and extraretinal photoreception in the Atlantic salmon (Salmo salar). J Exp Biol. 2000 Jun;203(Pt 12):1925–1936. doi: 10.1242/jeb.203.12.1925. [DOI] [PubMed] [Google Scholar]
  54. Plautz J. D., Kaneko M., Hall J. C., Kay S. A. Independent photoreceptive circadian clocks throughout Drosophila. Science. 1997 Nov 28;278(5343):1632–1635. doi: 10.1126/science.278.5343.1632. [DOI] [PubMed] [Google Scholar]
  55. Pollack I., Hofbauer A. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res. 1991 Nov;266(2):391–398. doi: 10.1007/BF00318195. [DOI] [PubMed] [Google Scholar]
  56. Provencio I., Cooper H. M., Foster R. G. Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentrainment. J Comp Neurol. 1998 Jun 15;395(4):417–439. doi: 10.1002/(sici)1096-9861(19980615)395:4<417::aid-cne1>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
  57. Provencio I., Foster R. G. Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics. Brain Res. 1995 Oct 2;694(1-2):183–190. doi: 10.1016/0006-8993(95)00694-l. [DOI] [PubMed] [Google Scholar]
  58. Provencio I., Rodriguez I. R., Jiang G., Hayes W. P., Moreira E. F., Rollag M. D. A novel human opsin in the inner retina. J Neurosci. 2000 Jan 15;20(2):600–605. doi: 10.1523/JNEUROSCI.20-02-00600.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Provencio I., Wong S., Lederman A. B., Argamaso S. M., Foster R. G. Visual and circadian responses to light in aged retinally degenerate mice. Vision Res. 1994 Jul;34(14):1799–1806. doi: 10.1016/0042-6989(94)90304-2. [DOI] [PubMed] [Google Scholar]
  60. Renn S. C., Park J. H., Rosbash M., Hall J. C., Taghert P. H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell. 1999 Dec 23;99(7):791–802. doi: 10.1016/s0092-8674(00)81676-1. [DOI] [PubMed] [Google Scholar]
  61. Roenneberg T., Foster R. G. Twilight times: light and the circadian system. Photochem Photobiol. 1997 Nov;66(5):549–561. doi: 10.1111/j.1751-1097.1997.tb03188.x. [DOI] [PubMed] [Google Scholar]
  62. Salcedo E., Huber A., Henrich S., Chadwell L. V., Chou W. H., Paulsen R., Britt S. G. Blue- and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J Neurosci. 1999 Dec 15;19(24):10716–10726. doi: 10.1523/JNEUROSCI.19-24-10716.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Scully A. L., Kay S. A. Time flies for Drosophila. Cell. 2000 Feb 4;100(3):297–300. doi: 10.1016/s0092-8674(00)80665-0. [DOI] [PubMed] [Google Scholar]
  64. Selby C. P., Sancar A. A third member of the photolyase/blue-light photoreceptor family in Drosophila: a putative circadian photoreceptor. Photochem Photobiol. 1999 Jan;69(1):105–107. [PubMed] [Google Scholar]
  65. Shearman L. P., Sriram S., Weaver D. R., Maywood E. S., Chaves I., Zheng B., Kume K., Lee C. C., van der Horst G. T., Hastings M. H. Interacting molecular loops in the mammalian circadian clock. Science. 2000 May 12;288(5468):1013–1019. doi: 10.1126/science.288.5468.1013. [DOI] [PubMed] [Google Scholar]
  66. Sigmund C. D. Viewpoint: are studies in genetically altered mice out of control? Arterioscler Thromb Vasc Biol. 2000 Jun;20(6):1425–1429. doi: 10.1161/01.atv.20.6.1425. [DOI] [PubMed] [Google Scholar]
  67. Simpson E. M., Linder C. C., Sargent E. E., Davisson M. T., Mobraaten L. E., Sharp J. J. Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat Genet. 1997 May;16(1):19–27. doi: 10.1038/ng0597-19. [DOI] [PubMed] [Google Scholar]
  68. Soni B. G., Philp A. R., Foster R. G., Knox B. E. Novel retinal photoreceptors. Nature. 1998 Jul 2;394(6688):27–28. doi: 10.1038/27794. [DOI] [PubMed] [Google Scholar]
  69. Stanewsky R., Kaneko M., Emery P., Beretta B., Wager-Smith K., Kay S. A., Rosbash M., Hall J. C. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell. 1998 Nov 25;95(5):681–692. doi: 10.1016/s0092-8674(00)81638-4. [DOI] [PubMed] [Google Scholar]
  70. Suri V., Qian Z., Hall J. C., Rosbash M. Evidence that the TIM light response is relevant to light-induced phase shifts in Drosophila melanogaster. Neuron. 1998 Jul;21(1):225–234. doi: 10.1016/s0896-6273(00)80529-2. [DOI] [PubMed] [Google Scholar]
  71. Thresher R. J., Vitaterna M. H., Miyamoto Y., Kazantsev A., Hsu D. S., Petit C., Selby C. P., Dawut L., Smithies O., Takahashi J. S. Role of mouse cryptochrome blue-light photoreceptor in circadian photoresponses. Science. 1998 Nov 20;282(5393):1490–1494. doi: 10.1126/science.282.5393.1490. [DOI] [PubMed] [Google Scholar]
  72. Vitaterna M. H., Selby C. P., Todo T., Niwa H., Thompson C., Fruechte E. M., Hitomi K., Thresher R. J., Ishikawa T., Miyazaki J. Differential regulation of mammalian period genes and circadian rhythmicity by cryptochromes 1 and 2. Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12114–12119. doi: 10.1073/pnas.96.21.12114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wheeler D. A., Hamblen-Coyle M. J., Dushay M. S., Hall J. C. Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J Biol Rhythms. 1993 Spring;8(1):67–94. doi: 10.1177/074873049300800106. [DOI] [PubMed] [Google Scholar]
  74. Whitmore D., Foulkes N. S., Sassone-Corsi P. Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature. 2000 Mar 2;404(6773):87–91. doi: 10.1038/35003589. [DOI] [PubMed] [Google Scholar]
  75. Yasuyama K., Meinertzhagen I. A. Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J Comp Neurol. 1999 Sep 20;412(2):193–202. doi: 10.1002/(sici)1096-9861(19990920)412:2<193::aid-cne1>3.0.co;2-0. [DOI] [PubMed] [Google Scholar]
  76. Yoshimura T., Ebihara S. Decline of circadian photosensitivity associated with retinal degeneration in CBA/J-rd/rd mice. Brain Res. 1998 Jan 1;779(1-2):188–193. doi: 10.1016/s0006-8993(97)01122-0. [DOI] [PubMed] [Google Scholar]
  77. Yoshimura T., Nishio M., Goto M., Ebihara S. Differences in circadian photosensitivity between retinally degenerate CBA/J mice (rd/rd) and normal CBA/N mice (+/+). J Biol Rhythms. 1994 Spring;9(1):51–60. doi: 10.1177/074873049400900105. [DOI] [PubMed] [Google Scholar]
  78. Zerr D. M., Hall J. C., Rosbash M., Siwicki K. K. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci. 1990 Aug;10(8):2749–2762. doi: 10.1523/JNEUROSCI.10-08-02749.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Zimmerman W. F., Goldsmith T. H. Photosensitivity of the circadian rhythm and of visual receptors in carotenoid-depleted Drosophila. Science. 1971 Mar 19;171(3976):1167–1169. doi: 10.1126/science.171.3976.1167. [DOI] [PubMed] [Google Scholar]
  80. van Swinderen B., Hall J. C. Analysis of conditioned courtship in dusky-Andante rhythm mutants of Drosophila. Learn Mem. 1995 Mar-Apr;2(2):49–61. doi: 10.1101/lm.2.2.49. [DOI] [PubMed] [Google Scholar]
  81. van der Horst G. T., Muijtjens M., Kobayashi K., Takano R., Kanno S., Takao M., de Wit J., Verkerk A., Eker A. P., van Leenen D. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature. 1999 Apr 15;398(6728):627–630. doi: 10.1038/19323. [DOI] [PubMed] [Google Scholar]
  82. von Schantz M., Argamaso-Hernan S. M., Szél A., Foster R. G. Photopigments and photoentrainment in the Syrian golden hamster. Brain Res. 1997 Oct 3;770(1-2):131–138. doi: 10.1016/s0006-8993(97)00791-9. [DOI] [PubMed] [Google Scholar]

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