Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance

Neuron

Volumn 66, Issue 3, 2010, Pages 417-428

  Lall, Gurprit S ^a   Revell, Victoria L ^a   Momiji, Hiroshi ^b   Al Enezi, Jazi ^a   Altimus, Cara M ^c   Güler, Ali D ^c   Aguilar, Carlos ^a   Cameron, Morven A ^a   Allender, Susan ^a   Hankins, Mark W ^d   Lucas, Robert J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

CELLBIO; SYSNEURO

Indexed keywords

MELANOPSIN; OPSIN;

ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FEMALE; LIGHT ADAPTATION; LIGHT EXPOSURE; LIGHT IRRADIANCE; MALE; MOUSE; NIGHT VISION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUPIL REFLEX; RETINA CONE; RETINA GANGLION CELL; RETINA ROD; SPECTRAL SENSITIVITY; VISUAL STIMULATION;

ANALYSIS OF VARIANCE; ANIMALS; CIRCADIAN RHYTHM; HUMANS; LIGHT; LIGHT SIGNAL TRANSDUCTION; MICE; MICE, TRANSGENIC; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; ROD OPSINS; TIME FACTORS; VISION, OCULAR;

EID: 77952689495     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.04.037     Document Type: Article

References (69)

1. Abd-El-Barr M.M., Pennesi M.E., Saszik S.M., Barrow A.J., Lem J., Bramblett D.E., Paul D.L., Frishman L.J., Wu S.M. Genetic Dissection of Rod and Cone Pathways in the Dark-Adapted Mouse Retina. J. Neurophysiol. 2009, 102:1945-1955.
2. Aggelopoulos N.C., Meissl H. Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J. Physiol. 2000, 523:211-222.
3. Alpern M. Rhodopsin kinetics in the human eye. J. Physiol. 1971, 217:447-471.
4. Altimus C.M., Güler A.D., Villa K.L., McNeill D.S., Legates T.A., Hattar S. Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc. Natl. Acad. Sci. USA 2008, 105:19998-20003.
5. Bachleitner W., Kempinger L., Wülbeck C., Rieger D., Helfrich-Förster C. Moonlight shifts the endogenous clock of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2007, 104:3538-3543.
6. Baver S.B., Pickard G.E., Sollars P.J., Pickard G.E. Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur. J. Neurosci. 2008, 27:1763-1770.
7. Belenky M.A., Smeraski C.A., Provencio I., Sollars P.J., Pickard G.E. Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J. Comp. Neurol. 2003, 460:380-393.
8. Berson D.M., Dunn F.A., Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 2002, 295:1070-1073.
9. Burkhardt D.A. Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. J. Neurosci. 1994, 14:1091-1105.
10. Calvert P.D., Krasnoperova N.V., Lyubarsky A.L., Isayama T., Nicoló M., Kosaras B., Wong G., Gannon K.S., Margolskee R.F., Sidman R.L., et al. Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha -subunit. Proc. Natl. Acad. Sci. USA 2000, 97:13913-13918.
11. Daan S., Pittendrigh C.S. A functional analysis of circadian pacemakers in nocturnal rodents. III Heavy water and constant light: Homeostasis of frequency?. J. Comp. Physiol. 1976, 106:267-290.
12. Dacey D.M., Liao H.W., Peterson B.B., Robinson F.R., Smith V.C., Pokorny J., Yau K.W., Gamlin P.D. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 2005, 433:749-754.
13. Deans M.R., Volgyi B., Goodenough D.A., Bloomfield S.A., Paul D.L. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 2002, 36:703-712.
14. Dkhissi-Benyahya O., Gronfier C., De Vanssay W., Flamant F., Cooper H.M. Modeling the role of mid-wavelength cones in circadian responses to light. Neuron 2007, 53:677-687.
15. Do M.T., Kang S.H., Xue T., Zhong H., Liao H.W., Bergles D.E., Yau K.W. Photon capture and signalling by melanopsin retinal ganglion cells. Nature 2009, 457:281-287.
16. Drouyer E., Rieux C., Hut R.A., Cooper H.M. Responses of suprachiasmatic nucleus neurons to light and dark adaptation: relative contributions of melanopsin and rod-cone inputs. J. Neurosci. 2007, 27:9623-9631.
17. Dumitrescu O.N., Pucci F.G., Wong K.Y., Berson D.M. Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells. J. Comp. Neurol. 2009, 517:226-244.
18. Evans J.A., Elliott J.A., Gorman M.R. Dim nighttime illumination accelerates adjustment to timezone travel in an animal model. Curr. Biol. 2009, 19:R156-R157.
19. Figueiro M.G., Bullough J.D., Parsons R.H., Rea M.S. Preliminary evidence for spectral opponency in the suppression of melatonin by light in humans. Neuroreport 2004, 15:313-316.
20. Freedman M.S., Lucas R.J., Soni B., von Schantz M., Muñoz M., David-Gray Z., Foster R.G. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 1999, 284:502-504.
21. Gamlin P.D., McDougal D.H., Pokorny J., Smith V.C., Yau K.W., Dacey D.M. Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res. 2007, 47:946-954.
22. Govardovskii V.I., Fyhrquist N., Reuter T., Kuzmin D.G., Donner K. In search of the visual pigment template. Vis. Neurosci. 2000, 17:509-528.
23. Göz D., Studholme K., Lappi D.A., Rollag M.D., Provencio I., Morin L.P. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLoS ONE 2008, 3:e3153.
24. Güler A.D., Ecker J.L., Lall G.S., Haq S., Altimus C.M., Liao H.W., Barnard A.R., Cahill H., Badea T.C., Zhao H., et al. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 2008, 453:102-105.
25. Hatori M., Le H., Vollmers C., Keding S.R., Tanaka N., Buch T., Waisman A., Schmedt C., Jegla T., Panda S. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS ONE 2008, 3:e2451.
26. Hattar S., Lucas R.J., Mrosovsky N., Thompson S., Douglas R.H., Hankins M.W., Lem J., Biel M., Hofmann F., Foster R.G., Yau K.W. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 2003, 424:76-81.
27. Haverkamp S., Wässle H., Duebel J., Kuner T., Augustine G.J., Feng G., Euler T. The primordial, blue-cone color system of the mouse retina. J. Neurosci. 2005, 25:5438-5445.
28. Hoshi H., Liu W.L., Massey S.C., Mills S.L. ON inputs to the OFF layer: bipolar cells that break the stratification rules of the retina. J. Neurosci. 2009, 29:8875-8883.
29. Jacobs G.H., Williams G.A., Cahill H., Nathans J. Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 2007, 315:1723-1725.
30. 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, 284:505-507.
31. Lucas R.J., Douglas R.H., Foster R.G. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat. Neurosci. 2001, 4:621-626.
32. Lucas R.J., Hattar S., Takao M., Berson D.M., Foster R.G., Yau K.W. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 2003, 299:245-247.
33. Lupi D., Oster H., Thompson S., Foster R.G. The acute light-induction of sleep is mediated by OPN4-based photoreception. Nat. Neurosci. 2008, 11:1068-1073.
34. Lyubarsky A.L., Daniele L.L., Pugh E.N. From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vision Res. 2004, 44:3235-3251.
35. McDougal D.H., Gamlin P.D. The influence of intrinsically-photosensitive retinal ganglion cells on the spectral sensitivity and response dynamics of the human pupillary light reflex. Vis. Res. 2010, 50:72-87.
36. Melyan Z., Tarttelin E.E., Bellingham J., Lucas R.J., Hankins M.W. Addition of human melanopsin renders mammalian cells photoresponsive. Nature 2005, 433:741-745.
37. Mrosovsky N. Contribution of classic photoreceptors to entrainment. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 2003, 189:69-73.
38. Mrosovsky N., Hattar S. Diurnal mice (Mus musculus) and other examples of temporal niche switching. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 2005, 191:1011-1024.
39. Nathan J., Reh R., Ankoudinova I., Ankoudinova G., Chang B., Heckenlively J., Hurley J.B. Scotopic and photopic visual thresholds and spatial and temporal discrimination evaluated by behavior of mice in a water maze. Photochem. Photobiol. 2006, 82:1489-1494.
40. Nelson D.E., Takahashi J.S. Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). J. Physiol. 1991, 439:115-145.
41. Nikonov S.S., Kholodenko R., Lem J., Pugh E.N. Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J. Gen. Physiol. 2006, 127:359-374.
42. Normann R.A., Perlman I. The effects of background illumination on the photoresponses of red and green cones. J. Physiol. 1979, 286:491-507.
43. Østergaard J., Hannibal J., Fahrenkrug J. Synaptic contact between melanopsin-containing retinal ganglion cells and rod bipolar cells. Invest. Ophthalmol. Vis. Sci. 2007, 48:3812-3820.
44. Panda S., Sato T.K., Castrucci A.M., Rollag M.D., DeGrip W.J., Hogenesch J.B., Provencio I., Kay S.A. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 2002, 298:2213-2216.
45. Panda S., Provencio I., Tu D.C., Pires S.S., Rollag M.D., Castrucci A.M., Pletcher M.T., Sato T.K., Wiltshire T., Andahazy M., et al. Melanopsin is required for non-image-forming photic responses in blind mice. Science 2003, 301:525-527.
46. Panda S., Nayak S.K., Campo B., Walker J.R., Hogenesch J.B., Jegla T. Illumination of the melanopsin signaling pathway. Science 2005, 307:600-604.
47. Pang J.J., Gao F., Wu S.M. Light-evoked current responses in rod bipolar cells, cone depolarizing bipolar cells and AII amacrine cells in dark-adapted mouse retina. J. Physiol. 2004, 558:897-912.
48. Pennesi M.E., Lyubarsky A.L., Pugh E.N. Extreme responsiveness of the pupil of the dark-adapted mouse to steady retinal illumination. Invest. Ophthalmol. Vis. Sci. 1998, 39:2148-2156.
49. Perez-Leon J.A., Warren E.J., Allen C.N., Robinson D.W., Lane Brown R. Synaptic inputs to retinal ganglion cells that set the circadian clock. Eur. J. Neurosci. 2006, 24:1117-1123.
50. Provencio I., Foster R.G. Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics. Brain Res. 1995, 694:183-190.
51. Qiu X., Kumbalasiri T., Carlson S.M., Wong K.Y., Krishna V., Provencio I., Berson D.M. Induction of photosensitivity by heterologous expression of melanopsin. Nature 2005, 433:745-749.
52. Riemersma-van der Lek R.F., Swaab D.F., Twisk J., Hol E.M., Hoogendijk W.J., Van Someren E.J. Effect of bright light and melatonin on cognitive and noncognitive function in elderly residents of group care facilities: a randomized controlled trial. JAMA 2008, 299:2642-2655.
53. Rollag M.D. Does melanopsin bistability have physiological consequences?. J. Biol. Rhythms 2008, 23:396-399.
54. Ruby N.F., Brennan T.J., Xie X., Cao V., Franken P., Heller H.C., O'Hara B.F. Role of melanopsin in circadian responses to light. Science 2002, 298:2211-2213.
55. Sampath A.P., Strissel K.J., Elias R., Arshavsky V.Y., McGinnis J.F., Chen J., Kawamura S., Rieke F., Hurley J.B. Recoverin improves rod-mediated vision by enhancing signal transmission in the mouse retina. Neuron 2005, 46:413-420.
56. Schmidt T.M., Taniguchi K., Kofuji P. Intrinsic and extrinsic light responses in melanopsin-expressing ganglion cells during mouse development. J. Neurophysiol. 2008, 100:371-384.
57. Smallwood P.M., Olveczky B.P., Williams G.L., Jacobs G.H., Reese B.E., Meister M., Nathans J. Genetically engineered mice with an additional class of cone photoreceptors: implications for the evolution of color vision. Proc. Natl. Acad. Sci. USA 2003, 100:11706-11711.
58. Takahashi J.S., DeCoursey P.J., Bauman L., Menaker M. Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms. Nature 1984, 308:186-188.
59. Tsai J.W., Hannibal J., Hagiwara G., Colas D., Ruppert E., Ruby N.F., Heller H.C., Franken P., Bourgin P. Melanopsin as a sleep modulator: circadian gating of the direct effects of light on sleep and altered sleep homeostasis in Opn4(-/-) mice. PLoS Biol. 2009, 7:e1000125.
60. Tsujimura S., Ukai K., Ohama D., Nuruki A., Yunokuchi K. Contribution of human melanopsin retinal ganglion cells to steady-state pupil responses. Proc. Royal Soc. B. 2010, in press. Published online April 7, 2010. 10.1098/rspb.2010.0330.
61. Valeton J.M., van Norren D. Light adaptation of primate cones: an analysis based on extracellular data. Vision Res. 1983, 23:1539-1547.
62. Van Gelder R.N., Wee R., Lee J.A., Tu D.C. Reduced pupillary light responses in mice lacking cryptochromes. Science 2003, 299:222.
63. Viney T.J., Balint K., Hillier D., Siegert S., Boldogkoi Z., Enquist L.W., Meister M., Cepko C.L., Roska B. Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Curr. Biol. 2007, 17:981-988.
64. Viola A.U., James L.M., Schlangen L.J., Dijk D.J. Blue-enriched white light in the workplace improves self-reported alertness, performance and sleep quality. Scand. J. Work Environ. Health 2008, 34:297-306.
65. Williams G.A., Daigle K.A., Jacobs G.H. Rod and cone function in coneless mice. Vis. Neurosci. 2005, 22:807-816.
66. Wong K.Y., Dunn F.A., Graham D.M., Berson D.M. Synaptic influences on rat ganglion-cell photoreceptors. J. Physiol. 2007, 582:279-296.
67. Yoshimura T., Ebihara S. 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] 1996, 178:797-802.
68. Young R.S., Kimura E. Pupillary correlates of light-evoked melanopsin activity in humans. Vision Res. 2008, 48:862-871.
69. Zhu Y., Tu D.C., Denner D., Shane T., Fitzgerald C.M., Van Gelder R.N. Melanopsin-dependent persistence and photopotentiation of murine pupillary light responses. Invest. Ophthalmol. Vis. Sci. 2007, 48:1268-1275.