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Nonimage Forming Photoreceptors

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The Circadian Clock

Part of the book series: Protein Reviews ((PRON,volume 12))

Abstract

The possession of a circadian system allows an organism to anticipate 24 h rhythmic phenomena, rather than passively responding to changes in the external environment. Physiology and behaviour can be fine-tuned in advance of the altered conditions and no time will be lost in the adjustment process. In mammals, the suprachiasmatic nuclei (SCN) of the hypothalamus are the site of a master circadian pacemaker, coordinating 24 h rhythms throughout the body including sleep/wake cycles. The primary regulatory input into the SCN is light. The light-dark cycle arising from the rotation of the Earth provides a robust 24 h signal enabling the internal and external cycles to be synchronised (entrained). The influence of light upon this central clock is mediated by photoreceptors within the eye, but until recently it remained unclear which ocular cells provided dawn/dusk information for photoentrainment. Research into the mechanisms of mammalian photoentrainment resulted in the identification of a third class of ocular photoreceptor, quite different from the rods and cones. This system is comprised of a subset of photosensitive retinal ganglion cells (pRGCs) expressing the photopigment melanopsin. Subsequent studies have shown that these cells not only regulate the circadian system but also mediate a broad range of other irradiance-detection tasks, including pineal melatonin suppression and pupil constriction.

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References

  1. Aschoff J (1984) Circadian timing. Ann N Y Acad Sci 423:442–468

    Article  CAS  PubMed  Google Scholar 

  2. Pittendrigh CS (1993) Temporal organisation: reflections of a Darwinian Clock-Watcher. Annu Rev Physiol 55:17–54

    Article  Google Scholar 

  3. Roenneberg T, Foster RG (1997) Twilight times: light and the circadian system. Photochem Photobiol 66:549–561

    Article  CAS  PubMed  Google Scholar 

  4. Moore R, Lenn N (1972) A retinohypothalamic projection in the rat. J Comp Neurol 146:1–14

    Article  CAS  PubMed  Google Scholar 

  5. Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201–206

    Article  CAS  PubMed  Google Scholar 

  6. Shand J, Foster RG (1999) The extraretinal photoreceptors of non-mammalian vertebrates. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Dordrecht, Netherlands, Kluwer Academic Publishers, pp 197–222

    Google Scholar 

  7. Campbell S, Murphy P (1998) Extraocular phototransduction in humans. Science 179:396–398

    Article  Google Scholar 

  8. Wright KP Jr, Czeisler CA (2002) Absence of circadian phase resetting in response to bright light behind the knees. Science 297:571

    Article  CAS  PubMed  Google Scholar 

  9. Nelson RJ, Zucker I (1981) Absence of extra-ocular photoreception in diurnal and nocturnal rodents exposed to direct sunlight. Comp Biochem Physiol 69A:145–148

    Article  Google Scholar 

  10. Rodieck RW (1998) The first steps in seeing. Sinauer Associates, INC., Sunderland, MA

    Google Scholar 

  11. Provencio I, Cooper HM, Foster RG (1998) Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentrainment. J Comp Neurol 395:417–439

    Article  CAS  PubMed  Google Scholar 

  12. Nelson DE, Takahashi JS (1991) Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). J Physiol 439:115–145

    CAS  PubMed  Google Scholar 

  13. Nelson DE, Takahashi JS (1991) Comparison of visual sensitivity for suppression of pineal melatonin and circadian phase-shifting in the golden hamster. Brain Res 554:272–277

    Article  CAS  PubMed  Google Scholar 

  14. Carter-Dawson LD, LaVail MM, Sidman RL (1978) Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci 17:489–498

    CAS  PubMed  Google Scholar 

  15. Provencio I, Wong S, Lederman AB, Argamaso SM, Foster RG (1994) Visual and circadian responses to light in aged retinally degenerate mice. Vision Res 34:1799–1806

    Article  CAS  PubMed  Google Scholar 

  16. Peirson SN, Thompson S, Hankins MW, Foster RG (2005) Mammalian photoentrainment: results, methods, and approaches. Methods Enzymol 393:697–726

    Article  CAS  PubMed  Google Scholar 

  17. Foster RG, Provencio I, Hudson D, Fiske S, De Grip W, Menaker M (1991) Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A 169:39–50

    Article  CAS  PubMed  Google Scholar 

  18. Provencio I, Foster RG (1995) Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics. Brain Res 694:183–190

    Article  CAS  PubMed  Google Scholar 

  19. Yoshimura T, Ebihara S (1996) Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+)mice. J Comp Physiol A 178:797–802

    Article  CAS  PubMed  Google Scholar 

  20. Foster RG, Argamaso S, Coleman S, Colwell CS, Lederman A, Provencio I (1993) Photoreceptors regulating circadian behavior: a mouse model. J Biol Rhythms 8(Suppl):17–23

    Google Scholar 

  21. Freedman MS, Lucas RJ, Soni B, von Schantz M, Munoz M, David-Gray Z, Foster R (1999) Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502–504

    Article  CAS  PubMed  Google Scholar 

  22. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073

    Article  CAS  PubMed  Google Scholar 

  23. Sekaran S, Foster RG, Lucas RJ, Hankins MW (2003) Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol 13:1290–1298

    Article  CAS  PubMed  Google Scholar 

  24. Tu DC, Zhang D, Demas J, Slutsky EB, Provencio I, Holy TE, Van Gelder RN (2005) Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48:987–999

    Article  CAS  PubMed  Google Scholar 

  25. Lucas R, Douglas R, Foster R (2001) Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 4:621–626

    Article  CAS  PubMed  Google Scholar 

  26. Jacobs GH, Neitz J, Deegan JFd (1991) Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353:655–657

    Article  CAS  PubMed  Google Scholar 

  27. Bridges CDB (1959) The visual pigments of some common laboratory animals. Nature 184:1727–1728

    Article  PubMed  Google Scholar 

  28. Sun H, Macke JP, Nathans J (1997) Mechanisms of spectral tuning in the mouse green cone pigment. Proc Natal Acad Sci U S A 94:8860–8865

    Article  CAS  Google Scholar 

  29. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG et al (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:75–81

    Article  Google Scholar 

  30. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95:340–345

    Article  CAS  PubMed  Google Scholar 

  31. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD (2000) A novel human opsin in the inner retina. J Neurosci 20:600–605

    CAS  PubMed  Google Scholar 

  32. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, Heller HC, O’Hara BF (2002) Role of melanopsin in circadian responses to light. Science 298:2211–2213

    Article  CAS  PubMed  Google Scholar 

  33. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, Hogenesch JB, Provencio I, Kay SA (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213–2216

    Article  CAS  PubMed  Google Scholar 

  34. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M et al (2003) Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:525–527

    Article  CAS  PubMed  Google Scholar 

  35. Foster R, Bellingham J (2002) Opsins and melanopsins. Curr Biol 12:R543–544

    Article  CAS  PubMed  Google Scholar 

  36. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW (2005) Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741–745

    Article  CAS  PubMed  Google Scholar 

  37. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM (2005) Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745–749

    Article  CAS  PubMed  Google Scholar 

  38. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T (2005) Illumination of the melanopsin signaling pathway. Science 307:600–604

    Article  CAS  PubMed  Google Scholar 

  39. Sekaran S, Lall GS, Ralphs KL, Wolstenholme AJ, Lucas RJ, Foster RG, Hankins MW (2007) 2-Aminoethoxydiphenylborane is an acute inhibitor of directly photosensitive retinal ganglion cell activity in vitro and in vivo. J Neurosci 27:3981–3986

    Article  CAS  PubMed  Google Scholar 

  40. Peirson SN, Oster H, Jones SL, Leitges M, Hankins MW, Foster RG (2007) Microarray ­analysis and functional genomics identify novel components of melanopsin signaling. Curr Biol 17:1363–1372

    Article  CAS  PubMed  Google Scholar 

  41. Hankins MW, Peirson SN, Foster RG (2008) Melanopsin: an exciting photopigment. Trends Neurosci 31:27–36

    Article  CAS  PubMed  Google Scholar 

  42. Lucas RJ, Freedman MS, Lupi D, Munoz M, David-Gray ZK, Foster RG (2001) Identifying the photoreceptive inputs to the mammalian circadian system using transgenic and retinally degenerate mice. Behav Brain Res 125:97–102

    Article  CAS  PubMed  Google Scholar 

  43. Mrosovsky N, Hattar S (2003) Impaired masking responses to light in melanopsin-knockout mice. Chronobiol Int 20:989–999

    Article  CAS  PubMed  Google Scholar 

  44. Thompson S, Foster RG, Stone EM, Sheffield VC, Mrosovsky N (2008) Classical and ­melanopsin photoreception in irradiance detection: negative masking of locomotor activity by light. Eur J Neurosci 27:1973–1979

    Article  PubMed  Google Scholar 

  45. Thompson S, Lupi D, Hankins MW, Peirson SN, Foster RG (2008) The effects of rod and cone loss on the photic regulation of locomotor activity and heart rate. Eur J Neurosci 28:724–729

    Article  PubMed  Google Scholar 

  46. Lupi D, Oster H, Thompson S, Foster RG (2008) The acute light-induction of sleep is mediated by OPN4-based photoreception. Nat Neurosci 11:1068–1073

    Google Scholar 

  47. Lucas RJ, Freedman MS, Munoz M, Garcia-Fernandez JM, Foster RG (1999) Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 284:505–507

    Article  CAS  PubMed  Google Scholar 

  48. Lucas RJ, Douglas RH, Foster RG (2001) Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 4:621–626

    Article  CAS  PubMed  Google Scholar 

  49. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau KW (2003) Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245–247

    Article  CAS  PubMed  Google Scholar 

  50. Mrosovsky N, Lucas R, Foster R (2001) Persistence of masking responses to light in mice lacking rods and cones. J Biol Rhythms 16:585–587

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Nuffield Laboratory of Ophthalmology, University of Oxford, Level 5 and 6 West Wing, The John Radcliffe Hospital, Headley Way, Headington, Oxford, OX3 9DU, UK

    Russell G. Foster

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  1. Stuart N. Peirson
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  2. Russell G. Foster
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Correspondence to Russell G. Foster .

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Editors and Affiliations

  1. Inst. Biochimie, Université de Fribourg, rue du Musee 5, Fribourg, 1700, Switzerland

    Urs Albrecht

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Peirson, S.N., Foster, R.G. (2010). Nonimage Forming Photoreceptors. In: Albrecht, U. (eds) The Circadian Clock. Protein Reviews, vol 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1262-6_4

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