Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins

Journal of Neuroscience

Volumn 29, Issue 9, 2009, Pages 2706-2724

  Yin, Lu ^a   Smith, Robert G ^a   Sterling, Peter ^a   Brainard, David H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELL STRUCTURE; COLOR DISCRIMINATION; COLORIMETRY; CONTROLLED STUDY; DENDRITE; LIGHT; NERVE CELL; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA; RETINA CONE; SYNAPTIC POTENTIAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MEMBRANE; COLOR; COLOR VISION; COLORING AGENTS; CONE OPSINS; ELECTROPHYSIOLOGY; GUINEA PIGS; IMMUNOHISTOCHEMISTRY; MODELS, STATISTICAL; NERVE NET; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL GANGLION CELLS; VISUAL FIELDS;

EID: 63849261211     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5471-08.2009     Document Type: Article

References (78)

1. Ahnelt P, Keri C, Kolb H ( 1990) Identification of pedicles of putative blue-sensitive cones in the human retina. J Comp Neurol 293:39-53.
2. Ahnelt PK, Kolb H (2000) The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res 19:711-777.
3. Arrese CA, Beazley LD, Neumeyer C (2006) Behavioural evidence for marsupial trichromacy. Curr Biol 16:R193-R194.
4. Asher M, de Oliveira ES, Sachser N (2004) Social system and spatial organization of wild guinea pigs (Cavia aperea) in a natural population. J Mammal 85:788-796.
5. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
6. Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20:351-384.
7. Borghuis BG, Ratliff CP, Smith RG, Sterling P, Balasubramanian V (2008) Design of a neuronal array. J Neurosci 28:3178-3189.
8. Caldwell JH, Daw NW (1978) New properties of rabbit retinal ganglion cells. J Physiol 276:257-276.
9. Calkins DJ, Tsukamoto Y, Sterling P (1998) Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. J Neurosci 18:3373-3385.
10. Cassini MH (1991) Foraging under predation risk in the wild guinea pig Cavia aperea. Oikos 62:20-24.
11. Cassini MH, Galante ML (1992) Foraging under predation risk in the wild guinea pig: the effect of vegetation height on habitat utilization. Ann Zool Fenn 29:285-290.
12. Chatterjee S, Callaway EM (2002) S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35:1135-1146.
13. Chichilnisky EJ (2001) A simple white noise analysis of neuronal light responses. Network 12:199-213.
14. Chichilnisky EJ, Kalmar RS (2002) Functional asymmetries in ON and OFF ganglion cells of primate retina. J Neurosci 22:2737-2747.
15. Cleland BG, Levick WR (1974) Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. J Physiol 240:457-492.
16. Cowing JA, Arrese CA, Davies WL, Beazley LD, Hunt DM (2008) Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus). Proc Biol Sci 275:1491-1499.
17. DaceyDM (1993) Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Vis Neurosci 10:1081-1098.
18. Dacey DM (1996) Circuitry for color coding in the primate retina. Proc Natl Acad Sci U S A 93:582-588.
19. Dacey DM (2000) Parallel pathways for spectral coding in primate retina. Annu Rev Neurosci 23:743-775.
20. Dacey DM, Lee BB (1994) The 'blue-on' opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367:731-735.
21. Dacey DM, Packer OS (2003) Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr Opin Neurobiol 13:421-427.
22. Dacey DM, Lee BB, Stafford DK, Pokorny J, Smith VC (1996) Horizontal cells of the primate retina: cone specificity without spectral opponency. Science 271:656-659.
23. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin PD (2005) Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749-754.
24. Davenport CM, Detwiler PB, Dacey DM (2008) Effects of pH buffering on horizontal and ganglion cell light responses in primate retina: evidence for the proton hypothesis of surround formation. J Neurosci 28:456-464.
25. Derrington AM, Lennie P ( 1984) Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol 357:219-240.
26. Do-Nascimento JL, Do-Nascimento RS, Damasceno BA, Silveira LC (1991) The neurons of the retinal ganglion cell layer of the guinea pig: quantitative analysis of their distribution and size. Braz J Med Biol Res 24:199-214.
27. 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.
28. Ekesten B, Gouras P, Yamamoto S (2000) Cone inputs to murine retinal ganglion cells. Vision Res 40:2573-2577.
29. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517-552.
30. Enroth-Cugell C, Robson JG, Schweitzer-Tong DE, Watson AB (1983) Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. J Physiol 341:279-307.
31. Field GD, Sher A, Gauthier JL, Greschner M, Shlens J, Litke AM, Chichilnisky EJ (2007) Spatial properties and functional organization of small bistratified ganglion cells in primate retina. J Neurosci 27:13261-13272.
32. Ghosh KK, Grünert U (1999) Synaptic input to small bistratified (blue-ON) ganglion cells in the retina of a New World monkey, the marmoset Callithrix jacchus. J Comp Neurol 413:417-428.
33. Ghosh KK, Martin PR, Grünert U (1997) Morphological analysis of the blue cone pathway in the retina of a New World monkey, the marmoset Callithrix jacchus. J Comp Neurol 379:211-225.
34. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509-528.
35. Grivich MI, Sher A, Petrusca D, Field GD, Shlens J, Gauthier JL, Chichilnisky EJ, Litke AM (2005) Classification of guinea pig retinal ganglion cells using large-scale multielectrode recordings. Soc Neurosci Abstr 31:246.10.
36. Haverkamp S, Wässle H, Duebel J, Kuner T, Augustine GJ, Feng G, Euler T (2005) The primordial, blue-cone color system of the mouse retina. J Neurosci 25:5438-5445.
37. Hemmi JM, James A, Taylor WR (2002) Color opponent retinal ganglion cells in the tammar wallaby retina. J Vis 2:608-617.
38. Herr S, Klug K, Sterling P, Schein S (2003) Inner S-cone bipolar cells provide all of the central elements for S cones in macaque retina. J Comp Neurol 457:185-201.
39. Hornstein EP, Verweij J, Li PH, Schnapf JL (2005) Gap-junctional coupling and absolute sensitivity of photoreceptors in macaque retina. J Neurosci 25:11201-11209.
40. Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev Camb Philos Soc 68:413-471.
41. Jacobs GH, Deegan JF 2nd (1994) Spectral sensitivity, photopigments, and color vision in the guinea pig (Cavia porcellus). Behav Neurosci 108:993-1004.
42. Jacobs GH, Blakeslee B, Tootell RB (1981) Color-discrimination tests on fibers in ground squirrel optic nerve. J Neurophysiol 45:903-914.
43. Jacobs GH, Williams GA, Cahill H, Nathans J (2007) Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315:1723-1725.
44. Kao YH, Sterling P (2006) Displaced GAD65 amacrine cells of the guinea pig retina are morphologically diverse. Vis Neurosci 23:931-939.
45. Klug K, Herr S, Ngo IT, Sterling P, Schein S (2003) Macaque retina contains an S-cone OFF midget pathway. J Neurosci 23:9881-9887.
46. Kong JH, Fish DR, Rockhill RL, Masland RH (2005) Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 489:293-310.
47. Kouyama N, Marshak DW (1992) Bipolar cells specific for blue cones in the macaque retina. J Neurosci 12:1233-1252.
48. Lee EJ, Han JW, Kim HJ, Kim IB, Lee MY, Oh SJ, Chung JW, Chun MH (2003) The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur J Neurosci 18:2925-2934.
49. Lee PM (1989) Bayesian statistics. London: Oxford UP.
50. Li W, DeVries SH (2006) Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nat Neurosci 9: 669-675.
51. MacNeil MA, Gaul PA (2008) Biocytin wide-field bipolar cells in rabbit retina selectively contact blue cones. J Comp Neurol 506:6-15.
52. Mancuso K, Neitz J, Hauswirth WW, Connor TB, Neitz M (2007) Gene therapy treatment of color blindness in adult primates [Abstract]. J Vis 7:15.
53. Mariani AP (1984) Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature 308:184-186.
54. Martin PR, Szmajda BA, Grunert U (2007) Projection patterns and morphology of koniocellular pathway ganglion cells in marmoset retina. Invest Ophthalmol Vis Sci 48:3177.
55. Michael CR (1966) Receptive fields of opponent color units in the optic nerve of the ground squirrel. Science 152:1095-1097.
56. Müller F, Wässle H, Voigt T (1988) Pharmacological modulation of the rod pathway in the cat retina. J Neurophysiol 59:1657-1672.
57. Nikonov SS, Kholodenko R, Lem J, Pugh EN Jr (2006) Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J Gen Physiol 127:359-374.
58. Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc Biol Sci 272:1745-1752.
59. Packer O, Verweij J, Schnapf JL, Dacey DM (2007) Primate S cones have blue-yellow opponent receptive fields. Invest Ophthalmol Vis Sci 48:2849.
60. Peichl L (2005) Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A Discov Mol Cell Evol Biol 287:1001-1012.
61. Peichl L, Behrmann G, Kröger RH (2001) For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Eur J Neurosci 13:1520-1528.
62. Rockhill RL, Daly FJ, MacNeil MA, Brown SP, Masland RH (2002) The diversity of ganglion cells in a mammalian retina. J Neurosci 22:3831-3843.
63. Röhlich P, van Veen T, Szél A (1994) Two different visual pigments in one retinal cone cell. Neuron 13:1159-1166.
64. Schein S, Sterling P, Ngo IT, Huang TM, Herr S (2004) Evidence that each S cone in macaque fovea drives one narrow-field and several wide-field blue-yellow ganglion cells. J Neurosci 24:8366-8378.
65. Schiviz AN, Ruf T, Kuebber-Heiss A, Schubert C, Ahnelt PK (2008) Retinal cone topography of artiodactyl mammals: influence of body height and habitat. J Comp Neurol 507:1336-1350.
66. Sharpe LT, Stockman A (1999) Rod pathways: the importance of seeing nothing. Trends Neurosci 22:497-504.
67. Silveira LC, Lee BB, Yamada ES, Kremers J, Hunt DM, Martin PR, Gomes FL (1999) Ganglion cells of a short-wavelength-sensitive cone pathway in New World monkeys: morphology and physiology. Vis Neurosci 16:333-343.
68. Solomon SG, Lee BB, White AJ, Rüttiger L, Martin PR (2005) Chromatic organization of ganglion cell receptive fields in the peripheral retina. J Neurosci 25:4527-4539.
69. Sterling P (1983) Microcircuitry of the cat retina. Annu Rev Neurosci 6:149-185.
70. Sterling P (2004) How retinal circuits optimize the transfer of visual information. In: Visual neurosciences (Chalupa LM, Werner JS, eds), pp234-259. Cambridge, MA: MIT.
71. Szél A, Röhlich P, Caffé AR, van Veen T (1996) Distribution of cone photoreceptors in the mammalian retina. Microsc Res Tech 35:445-462.
72. Szél A, Lukáts A, Fekete T, Szepessy Z, Röhlich P (2000) Photoreceptor distribution in the retinas of subprimate mammals. J Opt Soc Am A Opt Image Sci Vis 17:568-579.
73. Verweij J, Li PH, Packer O, Dacey DM, Schnapf JL (2008) Primate blue cones receive rod input. Invest Ophthalmol Vis Sci 49:3250.
74. Wassle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747-757.
75. Wiesel TN, Hubel DH (1966) Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J Neurophysiol 29:1115-1156.
76. Xu Y, Vasudeva V, Vardi N, Sterling P, Freed MA (2008) Different types of ganglion cell share a synaptic pattern. J Comp Neurol 507:1871-1878.
77. Yin L, Smith RG, Sterling P, Brainard DH (2006) Chromatic properties of horizontal and ganglion cell responses follow a dual gradient in cone opsin expression. J Neurosci 26:12351-12361.
78. Zaghloul KA, Boahen K, Demb JB (2003) Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J Neurosci 23: 2645-2654.