The rat retina has five types of ganglion-cell photoreceptors

Experimental Eye Research

Volumn 130, Issue , 2015, Pages 17-28

  Reifler, Aaron N ^a   Chervenak, Andrew P ^a   Dolikian, Michael E ^a   Benenati, Brian A ^a   Meyers, Benjamin S ^a   Demertzis, Zachary D ^a   Lynch, Andrew M ^a   Li, Benjamin Y ^a   Wachter, Rebecca D ^a   Abufarha, Fady S ^a   Dulka, Eden A ^a   Pack, Weston ^a   Zhao, Xiwu ^a   Wong, Kwoon Y ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

ChAT; Circadian photoentrainment; D AP5; DNQX; GCL; GFP; Intrinsically photosensitive retinal ganglion cell; IPL; IpRGC; L AP4; LGN; Light response; MEA; Melanopsin; ND; PACAP; PBS; Photoreceptors; RBPMS; RGC; SCN; Synaptic transmission; Whole cell recording

Indexed keywords

MELANOPSIN; SCOTOPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STRUCTURE; CELL TYPE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; INTRINSICALLY PHOTOSENSITIVE RETINAL GANGLION CELL; MALE; MEMBRANE STEADY POTENTIAL; MOUSE; NONHUMAN; PHOTORECEPTOR; PHOTOSENSITIVITY; PHOTOSTIMULATION; RAT; RETINA GANGLION CELL; SPECIES COMPARISON; SPECIES DIFFERENCE; SPIKE; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP; ANIMAL; AXON; COMPARATIVE STUDY; CYTOLOGY; ELECTROPHYSIOLOGY; LIGHT; MEMBRANE POTENTIAL; METABOLISM; NEWBORN; PHYSIOLOGY; PUPIL REFLEX; RADIATION RESPONSE; SPRAGUE DAWLEY RAT; VISION;

ANIMALS; ANIMALS, NEWBORN; AXONS; CIRCADIAN RHYTHM; ELECTROPHYSIOLOGY; LIGHT; MEMBRANE POTENTIALS; MICE; PHOTIC STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; REFLEX, PUPILLARY; RETINAL GANGLION CELLS; ROD OPSINS; VISION, OCULAR;

EID: 84911937722     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.11.010     Document Type: Article

References (71)

1. Altimus C.M., Guler A.D., Alam N.M., Arman A.C., Prusky G.T., Sampath A.P., Hattar S. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat. Neurosci. 2010, 13:1107-1112.
2. Bailes H.J., Lucas R.J. Human melanopsin forms a pigment maximally sensitive to blue light (lambdamax approximately 479nm) supporting activation of G(q/11) and G(i/o) signalling cascades. Proc. Biol. Sci. 2013, 280:20122987.
3. 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.
4. 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.
5. Berson D.M., Dunn F.A., Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 2002, 295:1070-1073.
6. Boudard D.L., Mendoza J., Hicks D. Loss of photic entrainment at low illuminances in rats with acute photoreceptor degeneration. Eur. J. Neurosci. 2009, 30:1527-1536.
7. Brainard G.C., Hanifin J.P., Greeson J.M., Byrne B., Glickman G., Gerner E., Rollag M.D. Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J.Neurosci. 2001, 21:6405-6412.
8. 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.
9. Butler M.P., Silver R. Divergent photic thresholds in the non-image-forming visual system: entrainment, masking and pupillary light reflex. Proc. Biol. Sci. 2011, 278:745-750.
10. 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.
11. 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.
12. 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.
13. 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.
14. Engelund A., Fahrenkrug J., Harrison A., Hannibal J. Vesicular glutamate transporter 2 (VGLUT2) is co-stored with PACAP in projections from the rat melanopsin-containing retinal ganglion cells. Cell. Tissue Res. 2010, 340:243-255.
15. Esquiva G., Lax P., Cuenca N. Impairment of intrinsically photosensitive retinal ganglion cells associated with late stages of retinal degeneration. Invest Ophthalmol. Vis. Sci. 2013, 54:4605-4618.
16. Estevez M.E., Fogerson P.M., Ilardi M.C., Borghuis B.G., Chan E., Weng S., Auferkorte O.N., Demb J.B., Berson D.M. Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. J.Neurosci. 2012, 32:13608-13620.
17. Gooley J.J., Rajaratnam S.M., Brainard G.C., Kronauer R.E., Czeisler C.A., Lockley S.W. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci. Transl. Med. 2010, 2:31ra33.
18. 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.
19. Hannibal J., Georg B., Fahrenkrug J. Differential expression of melanopsin mRNA and protein in Brown Norwegian rats. Exp. Eye Res. 2013, 106:55-63.
20. Hannibal J., Kankipati L., Strang C.E., Peterson B.B., Dacey D., Gamlin P.D. Central projections of intrinsically photosensitive retinal ganglion cells in the macaque monkey. J.Comp. Neurol. 2014, 522:2231-2248.
21. 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.
22. 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.
23. 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.
24. Hu C., Hill D.D., Wong K.Y. Intrinsic physiological properties of the five types of mouse ganglion-cell photoreceptors. J.Neurophysiol. 2013, 109:1876-1889.
25. Hut R.A., Oklejewicz M., Rieux C., Cooper H.M. Photic sensitivity ranges of hamster pupillary and circadian phase responses do not overlap. J.Biol. Rhythms 2008, 23:37-48.
26. 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.
27. 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.
28. Karnas D., Hicks D., Mordel J., Pevet P., Meissl H. Intrinsic photosensitive retinal ganglion cells in the diurnal rodent, arvicanthis ansorgei. PLoS One 2013, 8:e73343.
29. 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.
30. Lamb T.D. Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vis. Res. 1995, 35:3083-3091.
31. Li R.S., Chen B.Y., Tay D.K., Chan H.H., Pu M.L., So K.F. Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol. Vis. Sci. 2006, 47:2951-2958.
32. Luan L., Ren C., Lau B.W., Yang J., Pickard G.E., So K.F., Pu M. Y-like retinal ganglion cells innervate the dorsal raphe nucleus in the Mongolian gerbil (Meriones unguiculatus). PLoS One 2011, 6:e18938.
33. Masland R.H. The fundamental plan of the retina. Nat. Neurosci. 2001, 4:877-886.
34. McGuire R.A., Rand W.M., Wurtman R.J. Entrainment of the body temperature rhythm in rats: effect of color and intensity of environmental light. Science 1973, 181:956-957.
35. 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.
36. Morin L.P., Studholme K.M. Separation of function for classical and ganglion cell photoreceptors with respect to circadian rhythm entrainment and induction of photosomnolence. Neuroscience 2011, 199:213-224.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. Perez-Leon J.A., Warren E.J., Allen C.N., Robinson D.W., Brown R.L. Synaptic inputs to retinal ganglion cells that set the circadian clock. Eur. J. Neurosci. 2006, 24:1117-1123.
43. Pires S.S., Shand J., Bellingham J., Arrese C., Turton M., Peirson S., Foster R.G., Halford S. Isolation and characterization of melanopsin (Opn4) from the Australian marsupial Sminthopsis crassicaudata (fat-tailed dunnart). Proc. Biol. Sci. 2007, 274:2791-2799.
44. 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.
45. 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.
46. Rodriguez A.R., de Sevilla Muller L.P., Brecha N.C. The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina. J.Comp. Neurol. 2014, 522:1411-1443.
47. Schmidt T.M., Alam N.M., Chen S., Kofuji P., Li W., Prusky G.T., Hattar S. Arole for melanopsin in alpha retinal ganglion cells and contrast detection. Neuron 2014, 82:781-788.
48. Schmidt T.M., Kofuji P. Differential cone pathway influence on intrinsically photosensitive retinal ganglion cell subtypes. J.Neurosci. 2010, 30:16262-16271.
49. 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.
50. 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.
51. 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.
52. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J.Anat. 1953, 87:387-406.
53. Sodhi P., Hartwick A.T. Adenosine modulates light responses of rat retinal ganglion cell photoreceptors through cyclic AMP-mediated pathway. J.Physiol. 2014, 592:4201-4220.
54. 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.
55. 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.
56. Thapan K., Arendt J., Skene D.J. An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J.Physiol. 2001, 535:261-267.
57. Tu D.C., Owens L.A., Anderson L., Golczak M., Doyle S.E., McCall M., Menaker M., Palczewski K., Van Gelder R.N. Inner retinal photoreception independent of the visual retinoid cycle. Proc. Natl. Acad. Sci. U S A. 2006, 103:10426-10431.
58. 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.
59. Van Hook M.J., Berson D.M. Hyperpolarization-activated current (I(h)) in ganglion-cell photoreceptors. PLoS One 2010, 5:e15344.
60. Van Hook M.J., Wong K.Y., Berson D.M. Dopaminergic modulation of ganglion-cell photoreceptors in rat. Eur. J. Neurosci. 2012, 35:507-518.
61. 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.
62. Wang F., Zhou J., Lu Y., Chu R. Effects of 530nm green light on refractive status, melatonin, MT1 receptor, and melanopsin in the guinea pig. Curr. Eye Res. 2011, 36:103-111.
63. 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.
64. 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.
65. Weng S., Wong K.Y., Berson D.M. Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J.Biol. Rhythms 2009, 24:391-402.
66. Wong K.Y. Aretinal ganglion cell that can signal irradiance continuously for 10 hours. J.Neurosci. 2012, 32:11478-11485.
67. Wong K.Y., Dunn F.A., Berson D.M. Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 2005, 48:1001-1010.
68. 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.
69. Wong K.Y., Graham D.M., Berson D.M. The retina-attached SCN slice preparation: an invitro mammalian circadian visual system. J.Biol. Rhythms 2007, 22:400-410.
70. Zeitzer J.M., Dijk D.J., Kronauer R., Brown E., Czeisler C. Sensitivity of the human circadian pacemaker to nocturnal light: melatonin phase resetting and suppression. J.Physiol. 2000, 526(Pt 3):695-702.
71. Zhao X., Stafford B.K., Godin A.L., King W.M., Wong K.Y. Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells. J.Physiol. 2014, 592:1619-1636.