Mouse Ganglion-Cell Photoreceptors Are Driven by the Most Sensitive Rod Pathway and by Both Types of Cones

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Weng, Shijun ^a,b   Estevez, Maureen E ^a   Berson, David M ^a  

^a BROWN UNIVERSITY   (United States)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MELANOPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; ELECTRICAL SYNAPSE; GAP JUNCTION; ILLUMINATION; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PATCH CLAMP; PHOTORECEPTOR; PHOTOSENSITIZATION; PHOTOSTIMULATION; PHOTOTRANSDUCTION; RETINA CONE; RETINA GANGLION CELL; RETINA ROD; SPECTROSCOPY; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; VISUAL THRESHOLD;

ANIMALS; CELL SEPARATION; CONNEXINS; GAP JUNCTIONS; LIGHT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL GANGLION CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SENSORY THRESHOLDS; SYNAPSES;

MUS; PRIMATES;

EID: 84878755254     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066480     Document Type: Article

References (85)

1. Lupi D, Oster H, Thompson S, Foster RG (2008) The acute light-induction of sleep is mediated by OPN4-based photoreception. Nat Neurosci.
2. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, et al. (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424: 76-81.
3. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, et al. (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298: 2213-2216.
4. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, et al. (2002) Role of melanopsin in circadian responses to light. Science 298: 2211-2213.
5. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, et al. (2003) Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299: 245-247.
6. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, et al. (2003) Melanopsin is required for non-image-forming photic responses in blind mice. Science 301: 525-527.
7. Semo M, Peirson S, Lupi D, Lucas RJ, Jeffery G, et al. (2003) Melanopsin retinal ganglion cells and the maintenance of circadian and pupillary responses to light in aged rodless/coneless (rd/rd cl) mice. Eur J Neurosci 17: 1793-1801.
8. Zhu Y, Tu DC, Denner D, Shane T, Fitzgerald CM, et al. (2007) Melanopsin-dependent persistence and photopotentiation of murine pupillary light responses. Invest Ophthalmol Vis Sci 48: 1268-1275.
9. Tsai JW, Hannibal J, Hagiwara G, Colas D, Ruppert E, et al. (2009) Melanopsin as a sleep modulator: circadian gating of the direct effects of light on sleep and altered sleep homeostasis in Opn4(-/-) mice. PLoS Biol 7: e1000125.
10. Altimus CM, Guler AD, Villa KL, McNeill DS, Legates TA, et al. (2008) Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc Natl Acad Sci U S A.
11. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, et al. (2005) Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433: 749-754.
12. Wong KY, Dunn FA, Graham DM, Berson DM, (2007) Synaptic influences on rat ganglion-cell photoreceptors. J Physiol 582: 279-296.
13. Perez-Leon JA, Warren EJ, Allen CN, Robinson DW, Lane Brown R, (2006) Synaptic inputs to retinal ganglion cells that set the circadian clock. Eur J Neurosci 24: 1117-1123.
14. Schmidt TM, Taniguchi K, Kofuji P, (2008) Intrinsic and extrinsic light responses in melanopsin-expressing ganglion cells during mouse development. J Neurophysiol 100: 371-384.
15. Belenky MA, Smeraski CA, Provencio I, Sollars PJ, Pickard GE, (2003) Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J Comp Neurol 460: 380-393.
16. Jusuf PR, Lee SCS, Hannibal J, Grunert U, (2007) Characterization and synaptic connectivity of melanopsin-containing ganglion cells in the primate retina. European Journal of Neuroscience 26: 2906-2921.
17. Ostergaard J, Hannibal J, Fahrenkrug J, (2007) Synaptic contact between melanopsin-containing retinal ganglion cells and rod bipolar cells. Invest Ophthalmol Vis Sci 48: 3812-3820.
18. Dumitrescu ON, Pucci FG, Wong KY, Berson DM, (2009) Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: Contacts with dopaminergic amacrine cells and melanopsin ganglion cells. J Comp Neurol 517: 226-244.
19. Hoshi H, Liu WL, Massey SC, Mills SL, (2009) ON inputs to the OFF layer: bipolar cells that break the stratification rules of the retina. J Neurosci 29: 8875-8883.
20. Pickard GE, Baver SB, Ogilvie MD, Sollars PJ, (2009) Light-induced fos expression in intrinsically photosensitive retinal ganglion cells in melanopsin knockout (opn4) mice. PLoS ONE 4: e4984.
21. Lupi D, Sekaran S, Jones SL, Hankins MW, Foster RG, (2006) Light-evoked FOS induction within the suprachiasmatic nuclei (SCN) of melanopsin knockout (Opn4-/-) mice: a developmental study. Chronobiol Int 23: 167-179.
22. Guler AD, Ecker JL, Lall GS, Haq S, Altimus CM, et al. (2008) Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453: 102-105.
23. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N, et al. (2008) Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS ONE 3: e2451.
24. Goz D, Studholme K, Lappi DA, Rollag MD, Provencio I, et al. (2008) Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLoS ONE 3: e3153.
25. Dkhissi-Benyahya O, Gronfier C, De Vanssay W, Flamant F, Cooper HM, (2007) Modeling the role of mid-wavelength cones in circadian responses to light. Neuron 53: 677-687.
26. Altimus CM, Guler AD, Alam NM, Arman AC, Prusky GT, et al. (2010) Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci 13: 1107-1112.
27. Lall GS, Revell VL, Momiji H, Al Enezi J, Altimus CM, et al. (2010) Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 66: 417-428.
28. Aggelopoulos NC, Meissl H, (2000) Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J Physiol 523 Pt 1: 211-222.
29. Drouyer E, Rieux C, Hut RA, Cooper HM, (2007) Responses of suprachiasmatic nucleus neurons to light and dark adaptation: relative contributions of melanopsin and rod-cone inputs. J Neurosci 27: 9623-9631.
30. Baver SB, Pickard GE, Sollars PJ (2008) Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur J Neurosci.
31. Sharpe LT, Stockman A, (1999) Rod pathways: the importance of seeing nothing. Trends Neurosci 22: 497-504.
32. Bloomfield SA, Dacheux RF, (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20: 351-384.
33. Wassle H, (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5: 747-757.
34. Tsukamoto Y, Morigiwa K, Ishii M, Takao M, Iwatsuki K, et al. (2007) A novel connection between rods and ON cone bipolar cells revealed by ectopic metabotropic glutamate receptor 7 (mGluR7) in mGluR6-deficient mouse retinas. J Neurosci 27: 6261-6267.
35. Pang JJ, Gao F, Lem J, Bramblett DE, Paul DL, et al. (2010) Direct rod input to cone BCs and direct cone input to rod BCs challenge the traditional view of mammalian BC circuitry. Proc Natl Acad Sci U S A 107: 395-400.
36. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL, (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31: 477-485.
37. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, et al. (2010) Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67: 49-60.
38. Bassi CJ, Powers MK, (1986) Daily fluctuations in the detectability of dim lights by humans. Physiol Behav 38: 871-877.
39. Bassi CJ, Powers MK, (1987) Circadian rhythm in goldfish visual sensitivity. Invest Ophthalmol Vis Sci 28: 1811-1815.
40. Li L, Dowling JE, (1998) Zebrafish visual sensitivity is regulated by a circadian clock. Vis Neurosci 15: 851-857.
41. Weng S, Wong KY, Berson DM, (2009) Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J Biol Rhythms 24: 391-402.
42. Mangel SC, (2001) Circadian clock regulation of neuronal light responses in the vertebrate retina. Prog Brain Res 131: 505-518.
43. Walker JA, Olton DS, (1979) Circadian rhythm of luminance detectability in the rat. Physiol Behav 23: 17-21.
44. Jeon CJ, Strettoi E, Masland RH, (1998) The major cell populations of the mouse retina. J Neurosci 18: 8936-8946.
45. Penn JS, Williams TP, (1984) A new microspectrophotometric method for measuring absorbance of rat photoreceptors. Vision Res 24: 1673-1676.
46. DeVries SH, Baylor DA, (1995) An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proc Natl Acad Sci U S A 92: 10658-10662.
47. Estevez ME, Fogerson PM, Ilardi MC, Borghuis BG, Chan E, et al. (2012) Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. J Neurosci 32: 13608-13620.
48. Lamb TD, (1995) Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vision Res 35: 3083-3091.
49. Muller LP, Do MT, Yau KW, He S, Baldridge WH, (2010) Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina. J Comp Neurol 518: 4813-4824.
50. Volgyi B, Deans MR, Paul DL, Bloomfield SA, (2004) Convergence and segregation of the multiple rod pathways in mammalian retina. J Neurosci 24: 11182-11192.
51. Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL, (2002) Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36: 703-712.
52. Mills SL, O'Brien JJ, Li W, O'Brien J, Massey SC, (2001) Rod pathways in the mammalian retina use connexin 36. J Comp Neurol 436: 336-350.
53. Lee EJ, Han JW, Kim HJ, Kim IB, Lee MY, et al. (2003) The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur J Neurosci 18: 2925-2934.
54. Dang L, Pulukuri S, Mears AJ, Swaroop A, Reese BE, et al. (2004) Connexin 36 in photoreceptor cells: studies on transgenic rod-less and cone-less mouse retinas. Mol Vis 10: 323-327.
55. Zhang J, Wu SM, (2004) Connexin35/36 gap junction proteins are expressed in photoreceptors of the tiger salamander retina. J Comp Neurol 470: 1-12.
56. Li H, Chuang AZ, O'Brien J, (2009) Photoreceptor coupling is controlled by connexin 35 phosphorylation in zebrafish retina. J Neurosci 29: 15178-15186.
57. Pan F, Mills SL, Massey SC, (2007) Screening of gap junction antagonists on dye coupling in the rabbit retina. Vis Neurosci 24: 609-618.
58. Veruki ML, Hartveit E (2009) Meclofenamic acid blocks electrical synapses of retinal AII amacrine and ON-cone bipolar cells. J Neurophysiol.
59. Abd-El-Barr MM, Pennesi ME, Saszik SM, Barrow AJ, Lem J, et al. (2009) Genetic dissection of rod and cone pathways in the dark-adapted mouse retina. J Neurophysiol 102: 1945-1955.
60. Schmidt TM, Kofuji P, (2010) Differential cone pathway influence on intrinsically photosensitive retinal ganglion cell subtypes. J Neurosci 30: 16262-16271.
61. Haverkamp S, Wassle H, Duebel J, Kuner T, Augustine GJ, et al. (2005) The primordial, blue-cone color system of the mouse retina. J Neurosci 25: 5438-5445.
62. Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB, (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4: 1165.
63. Schmidt TM, Kofuji P, (2009) Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci 29: 476-482.
64. Viney TJ, Balint K, Hillier D, Siegert S, Boldogkoi Z, et al. (2007) Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Curr Biol 17: 981-988.
65. Berson DM, Castrucci AM, Provencio I, (2010) Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol 518: 2405-2422.
66. Brown TM, Allen AE, Wynne J, Paul DL, Piggins HD, et al. (2011) Visual responses in the lateral geniculate evoked by Cx36-independent rod pathways. Vision Res 51: 280-287.
67. Chun MH, Han SH, Chung JW, Wassle H, (1993) Electron microscopic analysis of the rod pathway of the rat retina. J Comp Neurol 332: 421-432.
68. Wassle H, Grunert U, Chun MH, Boycott BB, (1995) The rod pathway of the macaque monkey retina: identification of AII-amacrine cells with antibodies against calretinin. J Comp Neurol 361: 537-551.
69. McGuire BA, Stevens JK, Sterling P, (1984) Microcircuitry of bipolar cells in cat retina. J Neurosci 4: 2920-2938.
70. Kolb H, Famiglietti EV, (1974) Rod and cone pathways in the inner plexiform layer of cat retina. Science 186: 47-49.
71. Nathan J, Reh R, Ankoudinova I, Ankoudinova G, Chang B, et al. (2006) Scotopic and photopic visual thresholds and spatial and temporal discrimination evaluated by behavior of mice in a water maze. Photochem Photobiol 82: 1489-1494.
72. Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicolo M, et al. (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc Natl Acad Sci U S A 97: 13913-13918.
73. Gooley JJ, Rajaratnam SM, Brainard GC, Kronauer RE, Czeisler CA, et al. (2010) Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci Transl Med 2: 31ra33.
74. Hannibal J, Fahrenkrug J, (2004) Target areas innervated by PACAP-immunoreactive retinal ganglion cells. Cell Tissue Res 316: 99-113.
75. Berson DM, Dunn FA, Takao M, (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295: 1070-1073.
76. Wong KY, (2012) A retinal ganglion cell that can signal irradiance continuously for 10 hours. J Neurosci 32: 11478-11485.
77. Tu DC, Zhang D, Demas J, Slutsky EB, Provencio I, et al. (2005) Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48: 987-999.
78. Burkhardt DA, (1994) Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. J Neurosci 14: 1091-1105.
79. Normann RA, Perlman I, (1979) The effects of background illumination on the photoresponses of red and green cones. J Physiol 286: 491-507.
80. Ekesten B, Gouras P, (2005) Cone and rod inputs to murine retinal ganglion cells: evidence of cone opsin specific channels. Vis Neurosci 22: 893-903.
81. Ekesten B, Gouras P, Yamamoto S, (2000) Cone inputs to murine retinal ganglion cells. Vision Res 40: 2573-2577.
82. Yin L, Smith RG, Sterling P, Brainard DH, (2009) Physiology and Morphology of Color-Opponent Ganglion Cells in a Retina Expressing a Dual Gradient of S and M Opsins. J Neurosci 29: 2706-2724.
83. Chang L, Breuninger T, Euler T, (2013) Chromatic Coding from Cone-type Unselective Circuits in the Mouse Retina. Neuron 77: 559-571.
84. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, et al. (2000) The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27: 513-523.
85. Rohlich P, van Veen T, Szel A, (1994) Two different visual pigments in one retinal cone cell. Neuron 13: 1159-1166.