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Journal of the Optical Society of America A

Journal of the Optical Society of America A


  • Vol. 17, Iss. 3 — Mar. 1, 2000
  • pp: 568–579

Photoreceptor distribution in the retinas of subprimate mammals

Ágoston Szél, Ákos Lukáts, Tibor Fekete, Zsuzsanna Szepessy, and Pál Röhlich  »View Author Affiliations

JOSA A, Vol. 17, Issue 3, pp. 568-579 (2000)

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Relevant data on the distribution of color cones are summarized, with special emphasis on the marked dorso–ventral asymmetries observed in a number of mammalian species. In addition, an overview is given of studies that demonstrate the coexistence of two visual pigments within the same cone cell. The biological significance of these phenomena is discussed in conjunction with comparative immunocytochemical analyses of subprimate retinas. Based on various cone distribution patterns and temporal and spatial visual pigment coexpression, two models of cone photoreceptor differentiation are suggested.

© 2000 Optical Society of America

OCIS Codes
(180.2520) Microscopy : Fluorescence microscopy
(330.1720) Vision, color, and visual optics : Color vision
(330.5000) Vision, color, and visual optics : Vision - patterns and recognition
(330.5310) Vision, color, and visual optics : Vision - photoreceptors

Original Manuscript: June 4, 1999
Revised Manuscript: September 16, 1999
Manuscript Accepted: September 22, 1999
Published: March 1, 2000

Ágoston Szél, Ákos Lukáts, Tibor Fekete, Zsuzsanna Szepessy, and Pál Röhlich, "Photoreceptor distribution in the retinas of subprimate mammals," J. Opt. Soc. Am. A 17, 568-579 (2000)

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  1. G. A. Osterberg, “Topography of the layer of rods and cones in the human retina,” Acta Ophthalmol. 13, 1–97 (1935).
  2. R. S. Harwerth, H. G. Sperling, “Effects of intense visible radiation on the increment-threshold spectral sensitivity of the rhesus monkey eye,” Vision Res. 15, 1193–1204 (1975). [CrossRef] [PubMed]
  3. P. K. Ahnelt, “Characterization of the color related receptor mosaic in the ground squirrel retina,” Vision Res. 25, 1557–1568 (1985). [CrossRef] [PubMed]
  4. F. M. de Monasterio, S. J. Schein, E. P. McCrane, “Staining of blue-sensitive cones of the macaque retina by a fluorescent dye,” Science 213, 1278–1281 (1981). [CrossRef]
  5. Á. Szél, L. Takács, É. Monostori, T. Diamantstein, I. Vigh-Teichmann, P. Röhlich, “Monoclonal antibody recognizing cone visual pigment,” Exp. Eye Res. 43, 871–883 (1986). [CrossRef]
  6. C. L. Lerea, D. E. Somers, J. B. Hurley, I. B. Klock, A. H. Bunt-Milam, “Identification of specific transducin alfa subunits in retinal rod and cone photoreceptors,” Science 234, 77–80 (1986). [CrossRef] [PubMed]
  7. C. L. Lerea, A. H. Bunt-Milam, J. B. Hurley, “Alfa-transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina,” Neuron 3, 367–376 (1989). [CrossRef] [PubMed]
  8. P. A. Raymond, L. K. Barthel, G. A. Curran, “Developmental patterning of rod and cone photoreceptors in embryonic zebrafish,” J. Comp. Neurol. 359, 537–550 (1995). [CrossRef] [PubMed]
  9. K. Bumsted, C. Jasoni, Á. Szél, A. Hendrickson, “Spatial and temporal expression of cone opsins during monkey retinal development,” J. Comp. Neurol. 378, 117–134 (1997). [CrossRef] [PubMed]
  10. T. S. Vihtelic, C. J. Doro, D. R. Hyde, “Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins,” Visual Neurosci. 16, 571–585 (1999). [CrossRef]
  11. R. E. Marc, H. G. Sperling, “The chromatic organization of the goldfish cone mosaic,” Vision Res. 16, 1211–1224 (1976). [CrossRef] [PubMed]
  12. D. A. Cameron, S. S. Easter, “The cone photoreceptor mosaic of the green sunfish, Lepomis cyanellus,” Visual Neurosci. 10, 375–384 (1993). [CrossRef]
  13. D. L. Stenkamp, O. Hisatomi, L. K. Barthel, F. Tokunaga, P. A. Raymond, “Temporal expression of rod and cone opsins in embryonic goldfish retina predicts the spatial organization of the cone mosaic,” Invest. Ophthalmol. Visual Sci. 37, 363–376 (1996).
  14. L. Beaudet, I. N. Flamarique, C. W. Hawryshyn, “Cone photoreceptor topography in the retina of sexually mature pacific salmonid fishes,” J. Comp. Neurol. 383, 49–59 (1997). [CrossRef] [PubMed]
  15. D. R. Williams, D. I. A. MacLeod, M. M. Hayhoe, “Foveal tritanopia,” Vision Res. 21, 1341–1356 (1981). [CrossRef] [PubMed]
  16. Á. Szél, T. Diamantstein, P. Röhlich, “Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody,” J. Comp. Neurol. 273, 593–602 (1988). [CrossRef] [PubMed]
  17. K. C. Wikler, P. Rakic, “Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates,” J. Neurosci. 10, 3390–3401 (1990). [PubMed]
  18. C. A. Curcio, A. Hendrickson, “Organization and development of the primate photoreceptor mosaic,” Prog. Retinal Res. 10, 89–120 (1991). [CrossRef]
  19. Á. Szél, P. Röhlich, A. R. Caffé, B. Juliusson, G. D. Aguirre, T. van Veen, “Unique topographic separation of two spectral classes of cones in the mouse retina,” J. Comp. Neurol. 325, 327–342 (1992). [CrossRef] [PubMed]
  20. C. L. Cepko, “The patterning and onset of opsin expression in vertebrate retinae,” Curr. Opin. Neurobiol. 6, 542–546 (1996). [CrossRef] [PubMed]
  21. L. Galli-Resta, “Patterning the vertebrate retina: the early appearance of retinal mosaics,” Semin. Cell Biol. 9, 279–284 (1998). [CrossRef]
  22. Á. Szél, P. Röhlich, A. R. Caffé, T. van Veen, “Distribution of cone photoreceptors in the mammalian retina,” Microsc. Res. Tech. 35, 445–462 (1996). [CrossRef] [PubMed]
  23. G. H. Jacobs, J. Neitz, J. F. Deegan, “Retinal receptors in rodents maximally sensitive to ultraviolet light,” Nature 353, 655–656 (1991). [CrossRef] [PubMed]
  24. G. H. Jacobs, “The distribution and nature of colour vision among the mammals,” Biol. Rev. 68, 413–471 (1993). [CrossRef] [PubMed]
  25. G. H. Jacobs, J. F. Deegan, “Sensitivity to ultraviolet light in the gerbil (Meriones unguiculatus): characteristics and mechanisms,” Vision Res. 34, 1433–1441 (1994). [CrossRef] [PubMed]
  26. M. I. Chiu, J. Nathans, “Blue cones and bipolar cells share transcriptional specificity as determined by expression of human blue visual pigment-derived transgenes,” J. Neurosci. 14, 3426–3436 (1994). [PubMed]
  27. J. Nathans, D. Thomas, D. Hogness, “Molecular genetics of human colour vision. The genes encoding blue, green, and red pigments,” Science 232, 193–202 (1986). [CrossRef] [PubMed]
  28. S. Yokoyama, R. Yokoyama, “Molecular evolution of human visual pigment genes,” Mol. Biol. Evol. 6, 186–197 (1989). [PubMed]
  29. M. Neitz, J. Neitz, “Molecular genetics and the biological basis of color vision,” in Color Vision—Perspectives from Different Disciplines, W. Backhaus, G. K. Werner, R. Kliegl, J. K. Werner, eds. (de Gruyter, Berlin, 1998), pp. 101–119.
  30. J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992). [CrossRef] [PubMed]
  31. A. Roorda, D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397, 520–522 (1999). [CrossRef] [PubMed]
  32. M. Von Schantz, Á. Szél, T. van Veen, D. B. Farber, “Expression of soluble phototransduction-associated proteins in ground squirrel retina,” Invest. Ophthalmol. Visual Sci. 35, 3922–3930 (1994).
  33. Y. S. Wang, J. P. Macke, S. L. Merbs, D. J. Zack, B. Klaunberg, J. Bennett, J. Gearhart, J. Nathans, “A locus control region adjacent to the human red and green visual pigment genes,” Neuron 9, 429–440 (1992). [CrossRef] [PubMed]
  34. P. Röhlich, Á. Szél, “Binding sites of photoreceptor-specific antibodies COS-1, OS-2 and AO,” Curr. Eye Res. 12, 935–944 (1993). [CrossRef] [PubMed]
  35. Á. Szél, T. van Veen, P. Röhlich, “Retinal cone differentiation,” Nature 370, 336 (1994). [CrossRef] [PubMed]
  36. K. C. Wikler, D. L. Stull, B. E. Reese, P. T. Johnson, E. Bogenmann, “Localization of protein kinase C to UV-sensitive photoreceptors in the mouse retina,” Visual Neurosci. 15, 87–95 (1998). [CrossRef]
  37. Á. Szél, G. Csorba, A. R. Caffé, G. Szél, P. Röhlich, T. van Veen, “Different patterns of retinal cone topography in two genera of rodents, Mus and Apodemus,” Cell Tissue Res. 276, 143–150 (1994). [CrossRef] [PubMed]
  38. J. B. Calderone, G. H. Jacobs, “Regional variations in the relative sensitivity to UV light in the mouse retina,” Visual Neurosci. 12, 463–468 (1995). [CrossRef]
  39. M. von Schantz, S. M. Argamaso-Herman, Á. Szél, R. G. Foster, “Photopigments and photoentrainment in the Syrian golden hamster,” Brain Res. 770, 131–138 (1997). [CrossRef]
  40. L. Peichl, K. Moutairou, “Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia),” Eur. J. Neurosci. 10, 2586–2594 (1998). [CrossRef] [PubMed]
  41. J. I. Fasick, T. W. Cronin, D. M. Hunt, P. R. Robinson, “The visual pigments of the bottlenose dolphin (Tursiops truncatus),” Visual Neurosci. 15, 643–651 (1998). [CrossRef]
  42. J. B. Calderone, G. H. Jacobs, “Cone receptor variations and their functional consequences in two species of hamster,” Visual Neurosci. 16, 53–63 (1999). [CrossRef]
  43. H. Kolb, “The architecture of functional neural circuits in the vertebrate retina—the proctor lecture,” Invest. Ophthalmol. Visual Sci. 35, 2385–2404 (1994).
  44. F. M. de Monasterio, E. P. McCrane, J. K. Newlander, S. J. Schein, “Density profile of blue-sensitive cones along the horizontal meridian of macaque retina,” Invest. Ophthalmol. Visual Sci. 26, 289–302 (1985).
  45. K. Bumsted, A. Hendrickson, “Distribution and development of short-wavelength cones differ between macaca monkey and human fovea,” J. Comp. Neurol. 403, 502–516 (1999). [CrossRef] [PubMed]
  46. S. N. Archer, J. N. Lythgoe, “The visual pigment basis for cone polymorphism in the guppy, Poecilia reticulata,” Vision Res. 30, 225–233 (1990). [CrossRef] [PubMed]
  47. C. L. Makino, R. L. Dodd, “Multiple visual pigments in a photoreceptor of the salamander retina,” J. Gen. Physiol. 108, 27–34 (1996). [CrossRef] [PubMed]
  48. B. Juliusson, A. Bergström, P. Röhlich, B. Ehinger, T. van Veen, Á. Szél, “Complementary cone fields of the rabbit retina,” Invest. Ophthalmol. Visual Sci. 35, 811–818 (1994).
  49. E. V. Famiglietti, S. J. Sharpe, “Regional topography of rod and immunocytochemically characterized blue and green cone photoreceptors in rabbit retina,” Visual Neurosci. 12, 1151–1175 (1995). [CrossRef]
  50. P. Röhlich, T. van Veen, Á. Szél, “Two different visual pigments in one retinal cone cell,” Neuron 13, 1159–1166 (1994). [CrossRef] [PubMed]
  51. L. Peichl, H. Kunzle, P. Vogel, “Cone photoreceptors in insectivore retinae,” Eur. J. Neurosci. Suppl. 10 (abstr.), 355 (1998).
  52. Á. Szél, P. Röhlich, “Two cone types of the rat retina detected by anti-visual pigment antibodies,” Exp. Eye Res. 55, 47–52 (1992). [CrossRef]
  53. S. Yamamoto, P. Gouras, “Color opponent neurons in mouse retina,” Soc. Neurosci. Symp. 19, 1257 (1993).
  54. A. Reitner, L. T. Sharpe, E. Zrenner, “Is colour vision possible with only rods and blue-sensitive cones?” Nature 352, 798–800 (1991). [CrossRef] [PubMed]
  55. Z. Kryger, L. Galli-Resta, G. H. Jacobs, B. E. Reese, “The topography of rod and cone photoreceptors in the retina of the ground squirrel,” Visual Neurosci. 15, 685–691 (1998). [CrossRef]
  56. M. Glösmann, P. Ahnelt, “Coexpression of M- and S-opsin extends over the entire inferior mouse retina,” Eur. J. Neurosci. Suppl. 10 (abstr.), 357 (1998).
  57. Á. Szél, P. Röhlich, “Four photoreceptor types in the ground squirrel retina as evidenced by immunocytochemistry,” Vision Res. 28, 1297–1302 (1988). [CrossRef] [PubMed]
  58. H. M. Petry, J. T. Erichsen, Á. Szél, “Immunocytochemical identification of photoreceptor populations in the tree shrew retina,” Brain Res. 616, 344–350 (1993). [CrossRef] [PubMed]
  59. A. L. Lyubarsky, B. Falsini, M. E. Pennesi, P. Valentini, E. N. Pugh, “UV- and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments,” J. Neurosci. 19, 442–455 (1999).
  60. G. H. Jacobs, J. C. Fenwick, J. B. Calderone, S. S. Deeb, “Human cone pigment expressed in transgenic mice yields altered vision,” J. Neurosci. 19, 3258–3265 (1999). [PubMed]
  61. Á. Szél, P. Röhlich, K. Mieziewska, G. Aguirre, T. van Veen, “Spatial and temporal differences between the expression of short- and middle-wave sensitive cone pigments in the mouse retina: a developmental study,” J. Comp. Neurol. 331, 564–577 (1993). [CrossRef] [PubMed]
  62. L. D. Carter-Dawson, M. M. LaVail, “Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy,” J. Comp. Neurol. 188, 245–262 (1979). [CrossRef] [PubMed]
  63. S. L. Bruhn, C. L. Cepko, “Development of the pattern of photoreceptors in the chick retina,” J. Neurosci. 16, 1430–1439 (1996). [PubMed]
  64. W. S. Chang, W. A. Harris, “Sequential genesis and determination of cone and rod photoreceptors in Xenopus,” J. Neurobiol. 35, 227–244 (1998). [CrossRef] [PubMed]
  65. J. Robinson, E. A. Schmitt, J. E. Dowling, “Temporal and spatial patterns of opsin gene expression in zebrafish,” Visual Neurosci. 12, 895–906 (1995). [CrossRef]
  66. A. Bergström, B. Ehinger, K. Wilke, C. L. Zucker, A. R. Adolph, Á. Szél, “Development of cell markers in subretinal rabbit retinal transplants,” Exp. Eye Res. 58, 301–313 (1994). [CrossRef] [PubMed]
  67. Á. Szél, B. Juliusson, A. Bergström, K. Wilke, B. Ehinger, T. van Veen, “Reversed ratio of color-specific cones in the rabbit retinal cell transplants,” Dev. Brain Res. 81, 1–9 (1994). [CrossRef]
  68. A. R. Caffé, H. Visser, H. G. Jansen, S. Sanyal, “Histotypic differentiation of neonatal mouse retina in organ culture,” Curr. Eye Res. 8, 1083–1092 (1989). [CrossRef] [PubMed]
  69. A. R. Caffé, A. Söderpalm, T. van Veen, “Photoreceptor-specific protein expression of mouse retina in organ culture and retardation of rd degeneration in vitro by a combination of basic fibroblast and nerve growth factors,” Curr. Eye Res. 12, 719–726 (1993). [CrossRef] [PubMed]
  70. A. Söderpalm, Á. Szél, A. R. Caffé, T. van Veen, “Selective development of one cone photoreceptor type in retinal organ culture,” Invest. Ophthalmol. Visual Sci. 35, 3910–3921 (1994).
  71. K. C. Wikler, Á. Szél, A. L. Jacobsen, “Positional information and opsin identity in retinal cones,” J. Comp. Neurol. 374, 96–107 (1996). [CrossRef] [PubMed]
  72. J. Chen, C. L. Tucker, B. Woodford, Á. Szél, J. Lem, A. Gianella-Borradori, M. I. Simon, E. Bogenmann, “The human blue opsin promoter directs transgene expression in short-wave cones and bipolar cells in the mouse retina,” Proc. Natl. Acad. Sci. USA 91, 2611–2615 (1994). [CrossRef] [PubMed]
  73. Á. Szél, P. Röhlich, T. van Veen, “Short-wave sensitive cones in the rodent retinas,” Exp. Eye Res. 57, 503–505 (1993). [CrossRef] [PubMed]
  74. R. W. Young, “Visual cells and the concept of renewal,” Invest. Ophthalmol. Visual Sci. 15, 700–725 (1976).
  75. D. Bok, “Retinal photoreceptor-pigment epithelium interactions,” Invest. Ophthalmol. Visual Sci. 26, 1659–1694 (1985).
  76. W. A. Harris, S. L. Messersmith, “Two cellular inductions involved in photoreceptor determination in the Xenopus retina,” Neuron 9, 357–372 (1992). [CrossRef] [PubMed]
  77. K. C. Wikler, P. Rakic, N. Bhattacharyya, P. R. MacLeish, “Early emergence of photoreceptor mosaicism in the primate retina revealed by a novel cone-specific monoclonal antibody,” J. Comp. Neurol. 377, 500–508 (1997). [CrossRef] [PubMed]
  78. Á. Szél, Á. Lukáts, T. Fekete, J. Somogyi, H. M. Petry, H. M. Cooper, P. Röhlich, “Visual pigment coexpression in cone cells,” Med. Sci. Mon. 4, 46–56 (1998).
  79. Á. Szél, M. von Schantz, P. Röhlich, D. B. Farber, T. van Veen, “Difference in PNA label intensity between short-wavelength and middle-wavelength sensitive cones in the ground squirrel retina,” Invest. Ophthalmol. Visual Sci. 34, 3641–3645 (1993).
  80. K. C. Wikler, P. Rakic, “Relation of an array of early-differentiating cones to the photoreceptor mosaic in the primate retina,” Nature 351, 397–400 (1991). [CrossRef] [PubMed]
  81. K. C. Wikler, P. Rakic, “An array of early differentiating cones precedes the emergence of the photoreceptor mosaic in the fetal monkey retina,” Proc. Natl. Acad. Sci. USA 91, 6534–6538 (1994). [CrossRef] [PubMed]
  82. M. Constantine-Paton, A. S. Blum, R. Mendez-Otero, C. J. Barnstable, “A cell surface molecule distributed in a dorsoventral gradient in the perinatal rat retina,” Nature 324, 459–462 (1986). [CrossRef] [PubMed]
  83. P. McCaffery, K. C. Posch, J. L. Napoli, L. Gudas, U. C. Dräger, “Changing patterns of the retinoic acid system in the developing retina,” Dev. Biol. 158, 390–399 (1993). [CrossRef]
  84. P. McCaffery, E. Wagner, J. O’Neil, M. Petkovich, U. C. Dräger, “Dorsal and ventral retinal territories defined by retinois acid synthesis, break-down and nuclear receptor expression,” Mech. Dev. 85, 203–214 (1999). [PubMed]
  85. J. Lem, M. L. Applebury, J. D. Falk, J. G. Flannery, M. I. Simon, “Tissue-specific and developmental regulation of rod opsin chimeric genes in transgenic mice,” Neuron 6, 201–210 (1991). [CrossRef] [PubMed]
  86. D. J. Zack, J. Bennett, Y. Wang, C. Davenport, B. Klaunberg, J. Gearhart, J. Nathans, “Unusual topography of bovine rhodopsin promoter-IacZ fusion gene expression in transgenic mouse retinas,” Neuron 6, 187–199 (1991). [CrossRef] [PubMed]

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