Diverse types of ganglion cell photoreceptors in the mammalian retina

Progress in Retinal and Eye Research

Volumn 31, Issue 4, 2012, Pages 287-302

  Sand, Andrea ^a   Schmidt, Tiffany M ^b   Kofuji, Paulo ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Circadian entrainment; Melanopsin; Photoreceptors; Pupillary light reflex; Retina; Vision

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; MELANOPSIN; MELATONIN; OPSIN;

CELL FUNCTION; CELL STRUCTURE; CELL SUBPOPULATION; CELL TYPE; CIRCADIAN RHYTHM; DENDRITIC CELL; EVOKED VISUAL RESPONSE; HORMONE RELEASE; HYPOTHALAMUS; INTRINSICALLY PHOTOSENSITIVE RETINAL GANGLION CELL; LATERAL GENICULATE NUCLEUS; LIGHT IRRADIANCE; MELANOPHORE; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; PREOPTIC NUCLEUS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN STABILITY; PUPIL; PUPIL REFLEX; RETINA; RETINA NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; SLEEP; VISUAL SYSTEM;

ANIMALS; CIRCADIAN RHYTHM; HUMANS; PHOTORECEPTOR CELLS, VERTEBRATE; REFLEX, PUPILLARY; RETINAL GANGLION CELLS; RETINAL PHOTORECEPTOR CELL INNER SEGMENT; ROD OPSINS;

EID: 84861457735     PISSN: 13509462     EISSN: 18731635     Source Type: Journal    
DOI: 10.1016/j.preteyeres.2012.03.003     Document Type: Review

References (129)

1. Allen A.E., Cameron M.A., Brown T.M., Vugler A.A., Lucas R.J. Visual responses in mice lacking critical components of all known retinal phototransduction cascades. PloS One 2010, 5:e15063.
2. Altimus C.M., Guler 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. U S A 2008, 105:19998-20003.
3. Bailes H.J., Lucas R.J. Melanopsin and inner retinal photoreception. Cell. Mol. Life Sci.: CMLS 2010, 67:99-111.
4. Baver S.B., Pickard G.E., Sollars P.J. 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.
5. 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.
6. Berson D.M., Dunn F.A., Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 2002, 295:1070-1073.
7. Berson D.M., Castrucci A.M., Provencio I. Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J. Comp. Neurol. 2010, 518:2405-2422.
8. Borbely A.A. Effects of light on sleep and activity rhythms. Prog. Neurobiol. 1978, 10:1-31.
9. Brown T.M., Gias C., Hatori M., Keding S.R., Semo M., Coffey P.J., Gigg J., Piggins H.D., Panda S., Lucas R.J. Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. PLoS Biol. 2010, 8:e1000558.
10. Chen S.K., Badea T.C., Hattar S. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 2011, 476:92-95.
11. Cook J.E., Chalupa L.M. Retinal mosaics: new insights into an old concept. Trends Neurosci. 2000, 23:26-34.
12. Coombs J., van der List D., Wang G.Y., Chalupa L.M. Morphological properties of mouse retinal ganglion cells. Neuroscience 2006, 140:123-136.
13. Czeisler C.A., Shanahan T.L., Klerman E.B., Martens H., Brotman D.J., Emens J.S., Klein T., Rizzo J.F. Suppression of melatonin secretion in some blind patients by exposure to bright light. N. Engl. J. Med. 1995, 332:6-11.
14. Dacey D.M. The mosaic of midget ganglion cells in the human retina. J. Neurosci. 1993, 13:5334-5355.
15. 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.
16. Davies W.I., Zheng L., Hughes S., Tamai T.K., Turton M., Halford S., Foster R.G., Whitmore D., Hankins M.W. Functional diversity of melanopsins and their global expression in the teleost retina. Cell. Mol. Life Sci.: CMLS 2011, 68:4115-4132.
17. Do M.T., Yau K.W. Intrinsically photosensitive retinal ganglion cells. Physiol. Rev. 2010, 90:1547-1581.
18. 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.
19. Drager U.C., Olsen J.F. Origins of crossed and uncrossed retinal projections in pigmented and albino mice. J. Comp. Neurol. 1980, 191:383-412.
20. 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.
21. 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, 24:523-527.
22. Ecker J.L., Dumitrescu O.N., Wong K.Y., Alam N.M., Chen S.K., LeGates T., Renna J.M., Prusky G.T., Berson D.M., Hattar S. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 2010, 67:49-60.
23. Fain G.L., Hardie R., Laughlin S.B. Phototransduction and the evolution of photoreceptors. Curr. Biol. 2010, 20:R114-R124.
24. Famiglietti E.V., Kolb H. Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science 1976, 194:193-195.
25. 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, 169:39-50.
26. Freedman M.S., Lucas R.J., Soni B., von Schantz M., Munoz M., David-Gray Z., Foster R. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 1999, 284:502-504.
27. Fu Y., Zhong H., Wang M.H., Luo D.G., Liao H.W., Maeda H., Hattar S., Frishman L.J., Yau K.W. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proc. Natl. Acad. Sci. U S A 2005, 102:10339-10344.
28. Gan L., Xiang M., Zhou L., Wagner D.S., Klein W.H., Nathans J. POU domain factor Brn-3b is required for the development of a large set of retinal ganglion cells. Proc. Natl. Acad. Sci. U S A 1996, 93:3920-3925.
29. Gooley J.J., Lu J., Chou T.C., Scammell T.E., Saper C.B. Melanopsin in cells of origin of the retinohypothalamic tract. Nat. Neurosci. 2001, 4:1165.
30. Gooley J.J., Lu J., Fischer D., Saper C.B. A broad role for melanopsin in nonvisual photoreception. J. Neurosci. 2003, 23:7093-7106.
31. Goz 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.
32. Graham D.M., Wong K.Y., Shapiro P., Frederick C., Pattabiraman K., Berson D.M. Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. J. Neurophysiol. 2008, 99:2522-2532.
33. Guler A.D., Altimus C.M., Ecker J.L., Hattar S. Multiple photoreceptors contribute to nonimage-forming visual functions predominantly through melanopsin-containing retinal ganglion cells. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:509-515.
34. Guler 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., Hankins M.W., Berson D.M., Lucas R.J., Yau K.W., Hattar S. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 2008, 453:102-105.
35. Hankins M.W., Peirson S.N., Foster R.G. Melanopsin: an exciting photopigment. Trends Neurosci. 2008, 31:27-36.
36. Hannibal J. Roles of PACAP-containing retinal ganglion cells in circadian timing. Int. Rev. Cytol. 2006, 251:1-39.
37. Hannibal J., Hindersson P., Knudsen S.M., Georg B., Fahrenkrug J. The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J. Neurosci. 2002, 22:RC191.
38. Hannibal J., Hindersson P., Ostergaard J., Georg B., Heegaard S., Larsen P.J., Fahrenkrug J. Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Invest. Ophthalmol. Vis. Sci. 2004, 45:4202-4209.
39. Hardie R.C., Raghu P. Visual transduction in Drosophila. Nature 2001, 413:186-193.
40. Hartwick A.T., Bramley J.R., Yu J., Stevens K.T., Allen C.N., Baldridge W.H., Sollars P.J., Pickard G.E. Light-evoked calcium responses of isolated melanopsin-expressing retinal ganglion cells. J. Neurosci. 2007, 27:13468-13480.
41. Hatori M., Panda S. The emerging roles of melanopsin in behavioral adaptation to light. Trends Mol. Med. 2010, 16:435-446.
42. 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.
43. Hattar S., Liao H.W., Takao M., Berson D.M., Yau K.W. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 2002, 295:1065-1070.
44. 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.
45. Hattar S., Kumar M., Park A., Tong P., Tung J., Yau K.W., Berson D.M. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol. 2006, 497:326-349.
46. Hendrickson A.E. Electron microscopic distribution of axoplasmic transport. J. Comp. Neurol. 1972, 144:381-397.
47. Hillman P., Hochstein S., Minke B. Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol. Rev. 1983, 63:668-772.
48. 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.
49. Hughes S., Pothecary C.A., Jagannath A., Foster R.G., Hankins M.W., Peirson S.N. Profound defects in pupillary responses to light in TRPM-channel null mice: a role for TRPM channels in non-image-forming photoreception. Eur. J. Neurosci. 2012, 35:34-43.
50. Ingham E.S., Gunhan E., Fuller P.M., Fuller C.A. Immunotoxin-induced ablation of melanopsin retinal ganglion cells in a non-murine mammalian model. J. Comp. Neurol. 2009, 516:125-140.
51. Jain V., Ravindran E., Dhingra N.K. Differential expression of Brn3 transcription factors in intrinsically-photosensitive retinal ganglion cells in mouse. J. Comp. Neurol. 2011.
52. Johnson R.F., Moore R.Y., Morin L.P. Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract. Brain Res. 1988, 460:297-313.
53. Jusuf P.R., Lee S.C., Hannibal J., Grunert U. Characterization and synaptic connectivity of melanopsin-containing ganglion cells in the primate retina. Eur. J. Neurosci. 2007, 26:2906-2921.
54. Kay J.N., De la Huerta I., Kim I.J., Zhang Y., Yamagata M., Chu M.W., Meister M., Sanes J.R. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J. Neurosci. 2011, 31:7753-7762.
55. Keeler C.E. The inheritance of a retinal abnormality in white mice. Proc. Natl. Acad. Sci. U S A 1924, 10:329-333.
56. Keeler C.E. Iris movements in blind mice. Am. J. Physiol. 1927, 81:107-112.
57. Keeler C.E., Sutcliffe E., Chaffee E.L. Normal and "rodless" retinae of the house mouse with respect to the electromotive force generated through stimulation by light. Proc. Natl. Acad. Sci. U S A 1928, 14:477-484.
58. Koike C., Numata T., Ueda H., Mori Y., Furukawa T. TRPM1: a vertebrate TRP channel responsible for retinal ON bipolar function. Cell Calcium 2010, 48:95-101.
59. Koyanagi M., Kubokawa K., Tsukamoto H., Shichida Y., Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr. Biol. 2005, 15:1065-1069.
60. La Morgia C., Ross-Cisneros F.N., Hannibal J., Montagna P., Sadun A.A., Carelli V. Melanopsin-expressing retinal ganglion cells: implications for human diseases. Vision Res. 2011, 51:296-302.
61. Lall G.S., Revell V.L., Momiji H., Al Enezi J., Altimus C.M., Guler A.D., Aguilar C., Cameron M.A., Allender S., Hankins M.W., Lucas R.J. Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 2010, 66:417-428.
62. Lamb T.D., Pugh E.N. Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest. Ophthalmol. Vis. Sci. 2006, 47:5137-5152.
63. Lamb T.D., Collin S.P., Pugh E.N. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat. Rev. Neurosci. 2007, 8:960-976.
64. Lewy A.J., Wehr T.A., Goodwin F.K., Newsome D.A., Markey S.P. Light suppresses melatonin secretion in humans. Science 1980, 210:1267-1269.
65. Lin B., Koizumi A., Tanaka N., Panda S., Masland R.H. Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc. Natl. Acad. Sci. U S A 2008, 105:16009-16014.
66. Lucas R.J., Freedman M.S., Munoz M., Garcia-Fernandez J.M., Foster R.G. Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 1999, 284:505-507.
67. 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.
68. 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.
69. Masland R.H. Cell populations of the retina: the Proctor lecture. Invest. Ophthalmol. Vis. Sci. 2011, 52:4581-4591.
70. Mawad K., Van Gelder R.N. Absence of long-wavelength photic potentiation of murine intrinsically photosensitive retinal ganglion cell firing in vitro. J. Biol. Rhythms 2008, 23:387-391.
71. 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.
72. Moore R.Y., Lenn N.J. A retinohypothalamic projection in the rat. J. Comp. Neurol. 1972, 146:1-14.
73. Moore R.Y., Speh J.C., Card J.P. The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. J. Comp. Neurol. 1995, 352:351-366.
74. Morin L.P., Blanchard J.H., Provencio I. Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: bifurcation and melanopsin immunoreactivity. J. Comp. Neurol. 2003, 465:401-416.
75. Muller L.P., Do M.T., Yau K.W., He S., Baldridge W.H. Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina. J. Comp. Neurol. 2010, 518:4813-4824.
76. Mure L.S., Rieux C., Hattar S., Cooper H.M. Melanopsin-dependent nonvisual responses: evidence for photopigment bistability in vivo. J. Biol. Rhythms 2007, 22:411-424.
77. 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.
78. Nelson R.J., Zucker I. Absence of extraocular photoreception in diurnal and nocturnal rodents exposed to direct sunlight. Comp. Biochem. Physiol. [A] 1981, 69:145-148.
79. Neumann S., Haverkamp S., Auferkorte O.N. Intrinsically photosensitive ganglion cells of the primate retina express distinct combinations of inhibitory neurotransmitter receptors. Neuroscience 2011, 199:24-31.
80. Noseda R., Kainz V., Jakubowski M., Gooley J.J., Saper C.B., Digre K., Burstein R. A neural mechanism for exacerbation of headache by light. Nat. Neurosci. 2010, 13:239-245.
81. O'Brien B.J., Isayama T., Richardson R., Berson D.M. Intrinsic physiological properties of cat retinal ganglion cells. J. Physiol. 2002, 538:787-802.
82. Oshima N. Direct reception of light by chromatophores of lower vertebrates. Pigment Cell Res. 2001, 14:312-319.
83. Ostergaard 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.
84. Panda S., Hogenesch J.B., Kay S.A. Circadian rhythms from flies to human. Nature 2002, 417:329-335.
85. 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.
86. 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., Kay S.A., Van Gelder R.N., Hogenesch J.B. Melanopsin is required for non-image-forming photic responses in blind mice. Science 2003, 301:525-527.
87. 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.
88. Peirson S., Foster R.G. Melanopsin: another way of signaling light. Neuron 2006, 49:331-339.
89. Perez-Leighton C.E., Schmidt T.M., Abramowitz J., Birnbaumer L., Kofuji P. Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur. J. Neurosci. 2011, 33:856-867.
90. 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.
91. Pickard G.E., Silverman A.J. Direct retinal projections to the hypothalamus, piriform cortex, and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horseradish peroxidase technique. J. Comp. Neurol. 1981, 196:155-172.
92. Pickard G.E., Sollars P.J. Intrinsically photosensitive retinal ganglion cells. Science China. Life Sci. 2010, 53:58-67.
93. Pickard G.E., Sollars P.J. Intrinsically photosensitive retinal ganglion cells. Rev. Physiol. Biochem. Pharmacol. 2011.
94. Pires S.S., Hughes S., Turton M., Melyan Z., Peirson S.N., Zheng L., Kosmaoglou M., Bellingham J., Cheetham M.E., Lucas R.J., Foster R.G., Hankins M.W., Halford S. Differential expression of two distinct functional isoforms of melanopsin (Opn4) in the mammalian retina. J. Neurosci. 2009, 29:12332-12342.
95. Provencio I., Jiang G., De Grip W.J., Hayes W.P., Rollag M.D. Melanopsin: an opsin in melanophores, brain, and eye. Proc. Natl. Acad. Sci. U S A 1998, 95:340-345.
96. 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, 20:600-605.
97. Provencio I., Rollag M.D., Castrucci A.M. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 2002, 415:493.
98. 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.
99. Redlin U. Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity. Chronobiol. Int. 2001, 18:737-758.
100. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418:935-941.
101. Robinson G.A., Madison R.D. Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft. Vision Res. 2004, 44:2667-2674.
102. 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.
103. Saper C.B., Scammell T.E., Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437:1257-1263.
104. Schmidt T.M., Kofuji P. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J. Neurosci. 2009, 29:476-482.
105. Schmidt T.M., Kofuji P. Differential cone pathway influence on intrinsically photosensitive retinal ganglion cell subtypes. J. Neurosci. 2010, 30:16262-16271.
106. Schmidt T.M., Kofuji P. Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J. Comp. Neurol. 2011, 519:1492-1504.
107. 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.
108. Schmidt T.M., Chen S.K., Hattar S. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci. 2011.
109. Sekaran S., Foster R.G., Lucas R.J., Hankins M.W. Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr. Biol. 2003, 13:1290-1298.
110. Sekaran S., Lall G.S., Ralphs K.L., Wolstenholme A.J., Lucas R.J., Foster R.G., Hankins M.W. 2-Aminoethoxydiphenylborane is an acute inhibitor of directly photosensitive retinal ganglion cell activity in vitro and in vivo. J. Neurosci. 2007, 27:3981-3986.
111. Semo M., Munoz Llamosas M., Foster R.G., Jeffery G. Melanopsin (Opn4) positive cells in the cat retina are randomly distributed across the ganglion cell layer. Vis. Neurosci. 2005, 22:111-116.
112. Slaughter M.M., Miller R.F. 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 1981, 211:182-185.
113. Sollars P.J., Smeraski C.A., Kaufman J.D., Ogilvie M.D., Provencio I., Pickard G.E. Melanopsin and non-melanopsin expressing retinal ganglion cells innervate the hypothalamic suprachiasmatic nucleus. Vis. Neurosci. 2003, 20:601-610.
114. Takahashi J.S., Hong H.K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 2008, 9:764-775.
115. Tu D.C., Zhang D., Demas J., Slutsky E.B., Provencio I., Holy T.E., Van Gelder R.N. Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 2005, 48:987-999.
116. Van Hook M.J., Berson D.M. Hyperpolarization-activated current (I(h)) in ganglion-cell photoreceptors. PloS One 2010, 5:e15344.
117. Vaney D.I. Territorial organization of direction-selective ganglion cells in rabbit retina. J. Neurosci. 1994, 14:6301-6316.
118. 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.
119. Wang J.S., Kefalov V.J. The cone-specific visual cycle. Prog. Retin. Eye Res. 2011, 30:115-128.
120. Warren E.J., Allen C.N., Brown R.L., Robinson D.W. Intrinsic light responses of retinal ganglion cells projecting to the circadian system. Eur. J. Neurosci. 2003, 17:1727-1735.
121. Warren E.J., Allen C.N., Brown R.L., Robinson D.W. The light-activated signaling pathway in SCN-projecting rat retinal ganglion cells. Eur. J. Neurosci. 2006, 23:2477-2487.
122. Wassle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 2004, 5:747-757.
123. Wassle H., Riemann H.J. The mosaic of nerve cells in the mammalian retina. Proc. R. Soc. Lond. B Biol. Sci. 1978, 200:441-461.
124. Witkovsky P. Dopamine and retinal function. Documenta Ophthalmologica. Adv. Ophthalmol. 2004, 108:17-40.
125. 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.
126. Wurtman R.J., Axelrod J., Phillips L.S. Melatonin synthesis in the pineal Gland: control by light. Science 1963, 142:1071-1073.
127. Xue T., Do M.T., Riccio A., Jiang Z., Hsieh J., Wang H.C., Merbs S.L., Welsbie D.S., Yoshioka T., Weissgerber P., Stolz S., Flockerzi V., Freichel M., Simon M.I., Clapham D.E., Yau K.W. Melanopsin signalling in mammalian iris and retina. Nature 2011, 479:67-73.
128. Yau K.W., Hardie R.C. Phototransduction motifs and variations. Cell 2009, 139:246-264.
129. Zhang D.Q., Wong K.Y., Sollars P.J., Berson D.M., Pickard G.E., McMahon D.G. Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc. Natl. Acad. Sci. U S A 2008, 105:14181-14186.