Development and morphological organization of photoreceptors
Abstract
A common theme in developmental biology is that orderly structures arise out of initially unorganized assemblages of undifferentiated, proliferating cells, and that cells with specific identities often become organized into highly regular patterns of repeating units. A hallmark of neuronal organization is the partitioning or clustering of neurons into repeating functional modules that are collected into more complex structures. In the vertebrate retina, this type of modular organization is of paramount importance for the proper functioning of the neural circuitry, and regular mosaics are found among all classes of neurons and at all levels (Wässle and Reimann, 1978; Marc, 1986). The general organizational principle of the retina is that major categories of neurons are stratified, like the sheets in a layer cake, and within a given lamina, subtypes of neurons are distributed with a regular spacing, typically abutting but often not overlapping one another, like the tiles on a floor.
Keywords
Visual Pigment Double Cone Retinal Pigment Epithelium Cone Photoreceptor Single ConePreview
Unable to display preview. Download preview PDF.
References
- Adler,R. (1986) Trophic interactions in retinal development and in retinaldegenerations: in vivo and in vitro studies, in The Retina: aModel for Cell Biology Studies (eds R. Adler and D. Farber), AcademicPress, New York, pp.111–50.CrossRefGoogle Scholar
- Ahlbert, I.-B.(1968). The organization of the cone cells in the retinae of four teleosts withdifferent feeding habits (Perca fluviatilis, Lucioperca lucioperca, Acerinacernua, and Coregonus albula). Arkiv for Zoologi, 22, 445–81.Google Scholar
- Ahnelt, P.K.,Kolb, H. and Pflug, R. (1987) Identification of a subtype of conephotoreceptor, likely to be blue sensitive, in the human retina. Journal ofComparative Neurology, 255, 18–34.CrossRefGoogle Scholar
- Altshuler, D.M.,Turner, D.L. and Cepko, C.L. (1991) Specification of cell type in the vertebrateretina, in Development of the Visual System (eds D.M.-K. Lam and C.J.Shatz), MIT Press; Cambridge; Retina Res. Fnd. Symp. Vol. 3, pp.37–58.Google Scholar
- Araki, M.,Watanabe, K. and Yasuda, K. (1984) Immunocytochemical localization ofrhodopsinlike immunoreactivity in the outer segments of the rods and singlecones of chick retina. Cell Structure and Function, 9, 1–12.PubMedCrossRefGoogle Scholar
- Archer, S.N. andLythgoe, J.N. (1990) The visual pigment basis for cone polymorphism in theguppy, Poecilia reticulata. Vision Research, 30, 225–33.PubMedCrossRefGoogle Scholar
- Avery, J.A.,Bowmaker, J.K., Djamgoz, M.B.A. and Downing, J.E.G. (1983) Ultra-violetreceptors in a freshwater fish. Journal of Physiology, 334, 23–4.Google Scholar
- Banerjee, U. andZipursky, S.L. (1990) The role of cell-cell interaction in the development ofthe Drosophila visual system. Neuron, 4, 177–87.PubMedCrossRefGoogle Scholar
- Biffo, S., diCantogno, L.V. and Fasolo, A. (1992) Double labeling with non-isotopic in situhybridization and BrdU immunocytochemistry: calmodulin (CaM) mRNA expression inpost mitotic neurons of the olfactory system. Journal of Histochemistry andCytochemistry, 40, 535–40.CrossRefGoogle Scholar
- Bowmaker, J.K.and Kunz, Y.W. (1987) Ultraviolet receptors, tetrachromatic colour vision andretinal mosaics in the brown trout (Salmo trutta): age-dependentchanges. Vision Research, 27, 2101–8.PubMedCrossRefGoogle Scholar
- Bowmaker, J.K.,Thorpe, A. and Douglas, R.H. (1991) Ultraviolet-sensitive cones in thegoldfish. Vision Research, 31, 349–52.PubMedCrossRefGoogle Scholar
- Braisted, J.E.and Raymond, P. A. (1992) Regeneration of dopaminergic neurons in goldfishretina. Development, 114, 913–19.PubMedGoogle Scholar
- Braisted, J.E.,Essman, T.F. and Raymond, P.A. (1994) Selective regeneration of photoreceptorsin goldfish retina. Development, 120, 2409–19.PubMedGoogle Scholar
- Branchek, T. andBreMiller, R. (1984) The development of photoreceptors in the zebrafish, Brachydaniorerio. I. Structure. Journal of Comparative Neurology, 224, 107–15.PubMedCrossRefGoogle Scholar
- Bumsted, K.,Lerea, C., Szél, A. et al. (1994) Appearance of cone and rod opsins inthe developing primate retina. Investigative Ophthalmology and VisualScience Supplement, 35, 1728.Google Scholar
- Cameron, D.A. andPugh, E.N. (1991) Double cones as a basis for a new type of polarization visionin vertebrates. Nature, 353, 161–4.PubMedCrossRefGoogle Scholar
- Coffman, C.,Harris, W. and Kintner, C. (1990) Xotch, the Xenopus homolog of Drosophila Notch.Science, 249, 1438–41.PubMedCrossRefGoogle Scholar
- Cohen, A.I.(1972) Rods and cones, in Handbook of Sensory Physiology (ed. M.G.F.Fourtes), Springer-Verlag, New York, Vol. VII/2, pp. 63–110.Google Scholar
- Dartnall, H.J.,Bowmaker, J.K. and Mollon, J.D. (1983) Human visual pigments:microspectro-photometric results from the eyes of seven persons. Proceedings of the Royal Society of London SeriesB: Biological Sciences, 220, 115–30.PubMedCrossRefGoogle Scholar
- de Monasterio,F.M., Schein, S.J. and McCrane, E.P. (1981) Staining of blue-sensitive cones ofthe macaque retina by a fluorescent dye. Science, 213, 1278–81.CrossRefGoogle Scholar
- Douglas, R.H.(1986) Photopic spectral sensitivity of a teleost fish, the roach (Rutilusrutilus), with special reference to its ultraviolet sensitivity. Journalof Comparative Physiology A, 159, 415–21.CrossRefGoogle Scholar
- Engström, K.(1960) Cone types and cone arrangement in the retina of some cyprinids. ActaZoologica, 41, 277–95.Google Scholar
- Engström, K.(1963) Cone types and cone arrangements in teleost retinae. Acta Zoologica, 44,179–243.CrossRefGoogle Scholar
- Falk,J.D. and Applebury, M.L. (1987) The molecular genetics of photoreceptor cells. Progressin Retinal Research, 7, 89–112.CrossRefGoogle Scholar
- Goldsmith, T.H.(1990) Optimization, constraint, and history in the evolution of eyes. QuarterlyReview of Biology, 65, 281–322.CrossRefGoogle Scholar
- Hashimoto, Y.,Hárosi, F.I., Ueki, K. and Fukurotani, K. (1988) Ultra-violet-sensitive conesin the color-coding systems of cyprinid retinas. Neuroscience ResearchSupplement, 8, 81–96.Google Scholar
- Hawryshyn, C.W.(1991) Light-adaptation properties of the ultraviolet-sensitive cone mechanismin comparison to the other receptor mechanisms of goldfish. VisualNeuroscience, 6, 293–301.Google Scholar
- Hawryshyn, C.W.and Hárosi, F.I. (1991) Ultraviolet photoreception in carp:microspectrophotometry and behaviorally determined action spectra. VisionResearch, 31, 567–76.CrossRefGoogle Scholar
- Hisatomi, O.,Kayada, S., Aoki, Y. et al. (1994) Phylogenetic relationships amongvertebrate visual pigments. Vision Research 34, 3097–3102.PubMedCrossRefGoogle Scholar
- Hitchcock, P.F.and Raymond, P. A. (1992) Retinal regeneration. Trends in Neuroscience, 15,103–8.CrossRefGoogle Scholar
- Hitchcock, P.F.,and Vanderyt, J.T. (1994) Regeneration of dopamine-cell mosaic in the retina ofthe goldfish. Visual Neuroscience, 11, 209–17.PubMedCrossRefGoogle Scholar
- Hitchcock, P.F.,Lindsey Myhr, K.J., Easter, S.S., et al. (1992) Local regeneration inthe retina of the goldfish. Journal of Neurobiology, 23, 187–203.PubMedCrossRefGoogle Scholar
- Johns, P.A.Raymond (1977) Growth of the adult goldfish eye. III. Source of the new retinalcells. Journal of Comparative Neurology, 176, 343–58.PubMedCrossRefGoogle Scholar
- Johnson, R.L.,Grant, K.B., Zankel, T.C. et al. (1993) Cloning and expression ofgoldfish opsin sequences. Biochemistry, 32, 208–14.PubMedCrossRefGoogle Scholar
- Kljavin, I.J.(1987) Early development of photoreceptors in the ventral retina of thezebrafish embryo. Journal of Comparative Neurology, 260, 461–71.PubMedCrossRefGoogle Scholar
- Knight, J.K. andRaymond, P.A. (1995) Retinal pigmented epithelial (RPE) cells do nottransdifferentiate in adult goldfish. Journal of Neurobiology, in press.Google Scholar
- Kunz, Y.W. (1980)Cone mosaics in a teleost retina: changes during light and dark adaptation. Experientia,36, 1371–4.PubMedCrossRefGoogle Scholar
- Kuwata, O.,Imamoto, Y., Okano, T. et al. (1990) The primary structure of iodopsin,a chicken red-sensitive cone pigment. FEBS Letters, 272, 128– 32.PubMedCrossRefGoogle Scholar
- Larison, K.D. andBreMiller, R. (1990) Early onset of phenotype and cell patterning in theembryonic zebrafish retina. Development, 109, 567–76.PubMedGoogle Scholar
- LaVail, M.M.,Unoki, K., Yasumura, D. et al. (1992) Multiple growth factors,cytokines, and neurotrophins rescue photoreceptors from the damaging effects ofconstant light. Proceedings of the NationalAcademy of Sciences, USA, 89, 11249–53.CrossRefGoogle Scholar
- Lebovitz, R.M.and Ready, D.F. (1986) Ommatidial development in Drosophila eyefragments. Developmental Biology, 117, 663–71.PubMedCrossRefGoogle Scholar
- Levine, J.S. andMacNichol, E.F. (1979) Visual pigments in teleost fishes: effects of habitat,microhabitat, and behavior on visual system evolution. Sensory Proceedings, 3,95–131.Google Scholar
- Lyall, A.H.(1957a) Cone arrangements in teleost retinae.Quarterly Journal of Microscopical Science, 98, 189–201.Google Scholar
- Lyall, A.H.(1957b) The growth of the trout retina. QuarterlyJournal of Microscopical Science, 98,101–10.Google Scholar
- Marc, R.E. (1986)The development of retinal networks, in The Retina: a Model for Cell BiologyStudies (eds R. Adler and D. Farber), Academic Press, New York, pp.17–65.CrossRefGoogle Scholar
- Marc,R.E. and Sperling, H.G. (1976) The chromatic organization of the goldfish conemosaic. Vision Research, 16, 1211–24.PubMedCrossRefGoogle Scholar
- Marc, R.E and,Sperling, H.G. (1977) Chromatic organization of primate cones. Science, 196,454–6.PubMedCrossRefGoogle Scholar
- McConnell, S.K.(1991) The generation of neuronal diversity in the central nervous system. AnnualReview of Neuroscience, 14, 269–300.CrossRefGoogle Scholar
- Mensinger, A.F.and Powers, M.K. (1993) Visual function following surgical removal of retinaltissue. Investigative Ophthalmology and Visual Science Supplement, 34,1176.Google Scholar
- Merbs, S.L. andNathans, J. (1992) Absorption spectra of human cone pigments. Nature, 356,433–5.PubMedCrossRefGoogle Scholar
- Morris,V.B. (1970) Symmetry in a receptor mosaic demonstrated in the chick from thefrequencies, spacing and arrangement of the types of retinal receptor. Journalof Comparative Neurology, 140, 359–98.CrossRefGoogle Scholar
- Müller,H. (1952) Bau und Wachstum der Netzhaut des Guppy (Lebistes reticulatus).Zoologische Jahrbucher Abteilung fürAllegmeine Zoologie und Physiologie der Tiere, 63, 275–324.Google Scholar
- Nathans, J.,Thomas, D. and Hogness, D. (1986) Molecular genetics of human color vision: thegenes encoding blue, green and red pigments. Science, 232, 193–232.PubMedCrossRefGoogle Scholar
- Nawrocki, L.W.(1985) Development of the neural retina in the zebrafish, Brachydanio rerio.PhD Thesis, University of Oregon.Google Scholar
- Nawrocki, L.,BreMiller, R., Streisinger, G. and Kaplan, M. (1985) Larval and adult visualpigments of the zebrafish, Brachydanio rerio. Vision Research, 25,1569–76.PubMedCrossRefGoogle Scholar
- Neumeyer, C.(1992) Tetrachromatic color vision in goldfish: evidence from color mixtureexperiments. Journal of ComparativePhysiology [A], 171, 639–49.Google Scholar
- Okano, T.,Kojima, D., Kukada, Y. et al. (1992) Primary structures of chicken conevisual pigments: vertebrate rhodopsins have evolved out of cone visualpigments. Proceedings of the National Academy of Science, USA, 89,5932–6.CrossRefGoogle Scholar
- Packer, O.,Hendrickson, A.E. and Curcio, C.A. (1990) Developmental redistribution ofphotoreceptors across the Macaca nemestrina (pigtail macaque) retina. Journalof Comparative Neurology, 298, 472–93.CrossRefGoogle Scholar
- Park, CM. andHollenberg, M.J. (1993) Growth factor-induced retinal regeneration in vivo.International Review of Cytology, 146, 49–74.PubMedCrossRefGoogle Scholar
- Powers,D.A. (1989) Fish as model systems. Science, 246, 352–8.PubMedCrossRefGoogle Scholar
- Raymond, P.A.(1985) Cytodifferentiation of photoreceptors in larval goldfish: delayedmaturation of rods. Journal of Comparative Neurology, 236, 90–105.PubMedCrossRefGoogle Scholar
- Raymond, P.A.(1991) Retinal regeneration in teleost fish, in Regeneration of VertebrateSensory Receptor Cells, (ed.) E. Rubel, Ciba Foundation Symposium vol.160, Wiley, Chichester, pp.171–91.Google Scholar
- Raymond,P.A., Reifler, M.J. and Rivlin, P.K. (1988) Regeneration of goldfish retina:rod precursors are a likely source of regenerated cells. Journal ofNeurobiology, 19, 431–63.CrossRefGoogle Scholar
- Raymond, P.A.,Barthel, L.K., Rounsifer, M.E. et al (1993). Expression of rod and conevisual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressedin cones. Neuron, 10, 1161–74.PubMedCrossRefGoogle Scholar
- Raymond,P.A., Barthel, L.K. and Curran, G.A. (1994) Recruitment of photoreceptors inzebra fish embryos. Molecular Biology of the Cell, 4, 374a.Google Scholar
- Ready,D.F., Hanson, T.E. and Benzer, S. (1976) Development of the Drosophila retina,a neurocrystalline lattice. Developmental Biology, 53, 217–40.PubMedCrossRefGoogle Scholar
- Ready, D.F.,Tomlinson, A. and Lebovitz, R.M. (1986) Building an ommatidium: geometry andgenes, in Cell and Developmental Biology of the Eye (eds S.R. Hilfer andJ.B. Sheffield), Springer-Verlag, New York, pp.97–125.Google Scholar
- Reh, T.A. (1991)Determination of cell fate during retinal histogenesis: intrinsic and extrinsicmechanisms, in Development of the Visual System (eds D.M. Lam and C.J.Shatz), MIT Press, Cambridge, Retina Research Foundation Symposium, Vol. 3,pp.79–94.Google Scholar
- Risinger, C. andLarhammar, D.(1993) Multiple loci for synapse protein SNAP-25 in the tetraploid goldfish.Proceedings of the National Academy of Science, USA, 90, 10598–602.CrossRefGoogle Scholar
- Robinson, J.,Schmitt, E.A., Hárosi, F.I. et al. (1993) Zebrafish ultraviolet visualpigment: absorption spectrum, sequence, and localization. Proceedings of theNational Academy of Science, USA, 90, 6009–12.CrossRefGoogle Scholar
- Stell, W.K. andHárosi, F.I. (1975) Cone structure and visual pigment content in the retina ofthe goldfish. Vision Research, 16, 647–57.CrossRefGoogle Scholar
- Sullivan, S.A.,Largent, B.L., Goldman, D.J. and Raymond, P.A. (1992) Isolation of a goldfishhomologue to Drosophila Notch. Investigative Ophthalmology and VisualScience Supplement, 33, 1062.Google Scholar
- Szél, A.,Roehlich, P., Mieziewska, K. et al. (1993) Spatial and temporaldifferences between the expression of short- and middle-wave sensitive conepigments in the mouse retina: a developmental study. Journal of ComparativeNeurology, 331, 564–77.Google Scholar
- Tokunaga, F.,Iwasa, T., Miyagishi, M. and Kayada, S. (1990) Cloning of cDNA and amino acidsequence of one of the chicken cone visual pigments.Biochemical and Biophysical Research Communication, 173,1212–17.CrossRefGoogle Scholar
- Wahl, CM. (1994)Periodic cone cell twists in the walleye, Stizostendion vitreum; a newtype of retinomotor activity, Vision Research, 34, 11–18.PubMedCrossRefGoogle Scholar
- Wald,G., Brown, P.K. and Smith, P.H. (1955) Iodopsin. Journal of GeneralPhysiology, 38, 623–81.Google Scholar
- Walls,G.L. (1967) The Vertebrate Eye and its Adaptive Radiation. Hafner, NewYork, 787pp.Google Scholar
- Wang, S.-Z.,Adler, R. and Nathans, J. (1992) A visual pigment from chicken that resemblesrhodopsin: amino acid sequence, gene structure, and functional expression. Biochemistry,31, 3309–15.PubMedCrossRefGoogle Scholar
- Wassle, H. andReimann, H.J. (1978) The mosaic of nerve cells in the mammalian retina. Proceedingsof the Royal Society of London Series B: Biological Sciences, 200, 441–61.CrossRefGoogle Scholar
- Weinmaster, G.,Roberts, V.J. and Lemke, G. (1991) A homolog of Drosophila Notchexpressed during mammalian development. Development, 113, 199–205.PubMedGoogle Scholar
- Wikler, K.C. andRakic, P. (1990) Distribution of photoreceptor subtypes in the retina ofdiurnal and nocturnal primates. Journal of Neuroscience, 10, 3390–401.PubMedGoogle Scholar
- Wikler, K.C. andRakic, P. (1991) Relation of an array of early-differentiating cones to thephotoreceptor mosaic in the primate retina. Nature, 351, 397–400.PubMedCrossRefGoogle Scholar
- Yokoyama, R. andYokoyama, S. (1990a) Isolation, DNA sequence and evolution of a color visualpigment gene of the blind cave fish Astyanax fasciatus. Vision Research, 6,807–16.CrossRefGoogle Scholar
- Yokoyama, R. andYokoyama, S. (1990b) Convergent evolution of the red- and green-like visualpigment genes in fish, Astyanax fasciatus, and human. Proceedings ofthe National Academy of Sciences USA, 87, 9315–18.CrossRefGoogle Scholar