Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-27T22:45:26.180Z Has data issue: false hasContentIssue false
  • English
  • Français

Asymmetric retinal growth: Evidence for regulation by a retinotopic mechanism

Published online by Cambridge University Press:  02 June 2009

David A. Cameron
David A. Cameron
Affiliation:
Department of Biomedical Engineering, Boston University, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

Adult teleost retinas grow throughout life, in part by the addition of cells from an encircling, proliferative neuroepithelium. In some species, this proliferative growth is asymmetric around the retina. The present study evaluated two hypotheses regarding asymmetric proliferative growth in adult green sunfish retina: (1) the generation of rod photoreceptors in central retina from proliferative rod precursor cells is also asymmetric; and (2) asymmetric proliferative growth patterns are regulated by mechanisms that are organized retinotopically and are independent of body-axis coordinates. In all retinas examined, rod precursor distribution and rod production were asymmetric, and both were in coarse spatial register with the asymmetric pattern of cellular addition at the retinal margin. In adult eyes that were surgically rotated, the asymmetric patterns of proliferative growth were present and appropriate for the retina's prerotation orientation. The results suggest that proliferative growth at both marginal and central adult sunfish retina is asymmetric, and that these asymmetric growth patterns are regulated by a retinotopic mechanism that is independent of body-axis coordinates.

Keywords

RetinaDevelopmentProliferationEye rotationFishRods
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 3 , May 1996 , pp. 493 - 500
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ali, M.A. (1965). Retinal structure in the arctic char (Salvelinus alpinus L.). Journal of the Fisheries Research Board of Canada 22, 221–222.CrossRefGoogle Scholar
Anchan, R.M., Reh, T.A., Angello, J., Balliet, A. & Walker, M. (1991). EGF and TGF-α stimulate retinal neuroepithelial cell proliferation in vitro. Neuron 6, 923–936.CrossRefGoogle ScholarPubMed
Ashkenazi, A., Ramachandran, J. & Capon, D.J. (1989). Acetylcholine analogue stimulates DNA synthesis in brain-derived cells via specific muscarinic subtypes. Nature 340, 146–150.CrossRefGoogle Scholar
Barbera, A.J., Marchase, R.B. & Roth, S. (1973). Adhesive recognition and retinotectal specificity. Proceedings of the National Academy of Sciences of the U.S.A. 70, 2482–2486.CrossRefGoogle ScholarPubMed
Boucher, S.E.M. & Hitchcock, P.P. (1994). lnsulin-likegrowthfactor-1 (IGF-1) stimulates proliferation of neuronal progenitors in the adult goldfish retina in vitro. Society for Neuroscience Abstracts 20, 544.5.Google Scholar
Braisted, J.E. & Raymond, P.A. (1993). Continued search for the cellular signals that regulate regeneration of dopaminergic neurons in goldfish retina. Developmental Brain Research 76, 221–232.CrossRefGoogle ScholarPubMed
Braisted, J.E., Essman, T.F. & Raymond, P.A. (1994). Selective regeneration of photoreceptors in goldfish retina. Development 120, 2409–2419.CrossRefGoogle ScholarPubMed
Brockes, J.P. (1984). Mitogenic growth factors and nerve dependence of limb regeneration. Science 225, 1280–1286.CrossRefGoogle Scholar
Brockes, J.P., Lemke, G.E. & Balzar, D.R. (1980). Purification and preliminary characterization of a glial growth factor from the bovine pituitary. Journal of Biological Chemistry 255, 8374–8377.CrossRefGoogle ScholarPubMed
Burgess, W.H. & Maciag, T. (1989). The heparin-binding (fibroblast) growth factor family of proteins. Annual Review of Biochemistry 58, 575–606.CrossRefGoogle ScholarPubMed
Burrill, J.D. & Easter, S.S. Jr. (1995). The first retinal axons and their microenvironment in zebrafish: Cryptic pioneers and the pre-tract. Journal of Neuroscience 15, 2935–2947.CrossRefGoogle Scholar
Cameron, D.A. (1995). Asymmetric retinal growth in the adult teleost green sunfish (Lepomis cyanellus). Visual Neuroscience 12, 95–102.CrossRefGoogle ScholarPubMed
Cameron, D.A. & Easter, S.S. Jr. (1993). The cone photoreceptor mosaic of the green sunfish, Lepomis cyaneltus. Visual Neuroscience 10, 375–384.CrossRefGoogle Scholar
Cameron, D.A. & Easter, S.S. Jr. (1995). Cone photoreceptor regeneration in adult fish retina: Phenotypic determination and mosaic pattern formation. Journal of Neuroscience 15, 2255–2271.CrossRefGoogle ScholarPubMed
Chiu, J.F., Mack, A.F. & Fernald, R.D. (1995). Daily rhythm of cell proliferation in the teleost retina. Brain Research 673, 119–125.CrossRefGoogle ScholarPubMed
Collin, S.P. & Pettiorew, J.D. (1989). Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain, Behavior, and Evolution 34, 184–192.Google Scholar
Constantine-Paton, M., Blum, A.S., Mendez-Otero, R. & Barnstable, C.J. (1986). A cell surface molecule distributed in a dorsoventral gradient in the perinatal rat retina. Nature 324, 459–462.CrossRefGoogle Scholar
Davies, A.M. (1994). The role of neurotrophins in the developing nervous system. Journal of Neurobiotogy 25, 1334–1348.CrossRefGoogle ScholarPubMed
Deitcher, D.L., Fekete, D.M. & Cepko, C.L. (1994). Asymmetric expression of a novel homeobox gene in vertebrate sensory organs. Journal of Neuroscience 14, 486–498.CrossRefGoogle ScholarPubMed
Easter, S.S. Jr. (1992). Retinal growth in foveated teleosts: Nasotem-poral asymmetry keeps the fovea in temporal retina. Journal of Neuroscience 12, 2381–2392.CrossRefGoogle Scholar
Easter, S.S. Jr. & Schmidt, J.T. (1977). Reversed visuomotor behavior mediated by induced ipsilateral retinal projections in goldfish. Journal of Neurophysiology 40, 1245–1254.CrossRefGoogle ScholarPubMed
Einat, M., Resnitzky, D. & Kimsky, A. (1985). Close link between reduction of c-myc expression by interferon and G0/G1 arrest. Nature 313, 597–600.CrossRefGoogle ScholarPubMed
Evans, B.I. & Fernald, R.D. (1993). Retinal transformation at metamorphosis in the winter flounder (Pseudopleuronectes americanus). Visual Neuroscience 10, 1055–1064.CrossRefGoogle ScholarPubMed
Gong, Q. & Shipley, M.T. (1995). Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb. Neuron 14, 91–101.CrossRefGoogle ScholarPubMed
Gottlieb, D.I., Rock, K. & Glaser, L. (1976). A gradient of adhesive specificity in developing avian retina. Proceedings of the National Academy of Sciences of the U.S.A. 73, 410–414.CrossRefGoogle Scholar
Henken, D.B. & Yoon, M.G. (1989). Optic nerve crush modulates proliferation of rod precursor cells in the goldfish retina. Brain Research 501, 247–259.CrossRefGoogle ScholarPubMed
Hitchcock, P.F., Lindsey, Lindsey K.J., Easter, S.S. Jr., Mangione-Smith, R. & Dwyer, J.D. (1992). Local regeneration in the retina of the goldfish. Journal of Neurobiology 23, 187–203.CrossRefGoogle Scholar
Johns, P.R. & Fernald, R.D. (1981). Genesis of rods in teleost fish retina. Nature 293, 141–142.CrossRefGoogle ScholarPubMed
Kimmel, C.B., Warga, R.M. & Kane, D.A. (1994). Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 120, 265–276.CrossRefGoogle Scholar
Kuavin, I.J. (1987). Early development of photoreceptors in the ventral retina of the zebrafish embryo. Journal of Comparative Neurology 260, 461–471.Google Scholar
Larison, K.D. & BreMiller, R. (1990). Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development 109, 567–576.CrossRefGoogle ScholarPubMed
Lillien, L. & Cepko, C. (1992). Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF-α. Development 115, 253–266.CrossRefGoogle ScholarPubMed
Mack, A.F. & Fernald, R.D. (1993). Regulation of cell division and rod differentiation in the teleost retina. Developmental Brain Research 16, 183–187.CrossRefGoogle Scholar
McCaffery, P., Lee, M.-O., Wagner, M.A., Sladek, N.E. & Dräger, U.C. (1992). Asymmetric retinoic acid synthesis in the dorsoven-tral axis of the retina. Development 115, 371–382.CrossRefGoogle ScholarPubMed
McLoon, S.C. (1991). A monoclonal antibody that distinguishes between temporal and nasal retinal axons. Journal of Neuroscience 11, 1470–1477.CrossRefGoogle ScholarPubMed
Müller, H. (1952). Bau und Wachtstum der Netzhaut des Guppy (Lebistes reticulatus). Zoologische Jahrbuecher (Zoologie und Physiologie) 63, 275–324.Google Scholar
Murphey, R.K. (1985). Competition and chemoaffinity in insect sensory systems. Trends in Neurosciences 8, 120–125.CrossRefGoogle Scholar
Nawrocki, L., BreMiller, R., Streisinger, G. & Kaplan, M. (1985). Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Research 25, 1569–1576.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T., Kato, S. & Nakamura, Y. (1988). Immunohistochemical and autoradiographic studies on retinal regeneration in teleost fish. Neuroscience Research (Suppl.) 8, S43–S57.Google ScholarPubMed
Nornes, H.O., Dressler, G.R., Knapik, E.W., Deutsch, U. & Gruss, P. (1990). Spatially and temporally restricted expression of Pax2 during murine neurogenesis. Development 109, 797–809.CrossRefGoogle ScholarPubMed
Owusu-Yaw, V., Kyle, A.L. & Stell, W.K. (1992). Effects of lesions of the optic nerve, optic tectum and nervus terminalis on rod precursor proliferation in the goldfish retina. Brain Research 576, 220–230.CrossRefGoogle Scholar
Page, L.M. & Burr, B.M. (1991). A Field Guide to Freshwater Fishes. Boston, Massachusetts: Houghton Mifflin Company.Google Scholar
Powers, M.K. & Raymond, P.A. (1990). Development of the visual system. In The Visual System of Fish, ed. Douglas, R.H. & Djamgoz, M.B.A., pp. 419–442. London: Chapman & Hall.CrossRefGoogle Scholar
Ratner, N., Hong, D., Lieberman, M.A., Bunge, R.B. & Glaser, L. (1988). The neuronal cell-surface molecule mitogenic for Schwann cells is a heparin-binding proteoglycan. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6992–6996.CrossRefGoogle Scholar
Raymond, P.A. (1985). The unique origin of rod photoreceptors in the teleost retina. Trends in Neurosciences 8, 12–17.CrossRefGoogle Scholar
Raymond, P.A. & Rivlin, P.K. (1987). Germinal cells in the goldfish retina that produce rod photoreceptors. Developmental Biology 122, 120–138.CrossRefGoogle ScholarPubMed
Raymond, P.A., Easter, S.S. Jr., Burnham, J.A. & Powers, M.K. (1983). Postembryonic growth of the optic tectum in goldfish. II. Modulation of cell proliferation by retinal fiber input. Journal of Neuroscience 3, 1092–1099.CrossRefGoogle ScholarPubMed
Richman, D.P., Steward, R.M., Hutchinson, H.W. & Caviness, V.S. (1975). Mechanical model of brain convolution development. Science 189, 18–21.CrossRefGoogle ScholarPubMed
Savitt, M., Trisler, D. & Hill, D.C. (1995). Molecular cloning of TOPAP: A topographically graded protein in the developing chick visual system. Neuron 14, 253–261.CrossRefGoogle ScholarPubMed
Schlessinger, R. & Ullrich, A. (1992). Growth factor signalling by receptor tyrosine kinases. Neuron 9, 383–391.CrossRefGoogle ScholarPubMed
Scott, W.B. & Grossman, E.J. (1973). Freshwater Fishes of Canada, Bulletin 184. Ottawa: Fisheries Research Board of Canada.Google Scholar
Sperry, R.W. (1943). Effect of 180 degree rotation of the retinal field on visuomotor coordination. Journal of Experimental Zoology 92, 263–279.CrossRefGoogle Scholar
Sperry, R.W. (1948). Patterning of central synapses in regeneration of the optic nerve in teleosts. Physiological Zoology 28, 351–361.CrossRefGoogle Scholar
Sperry, R.W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proceedings of the National Academy of Sciences of the U.S.A. 50, 703–710.CrossRefGoogle ScholarPubMed
Stone, L.S. (1944). Functional polarization in retinal development and its reestablishment in regenerating retinae of rotated grafted eyes. Proceedings of the Society for Experimental Biology and Medicine 57, 13–14.CrossRefGoogle Scholar
Thompson, P., Desbordes, J.M., Giraud, J., Pouliquen, Y., Barritault, D. & Courtois, Y. (1982). The effect of an eye derived growth factor (EDGF) on corneal epithelial regeneration. Experimental Eye Research 34, 191–199.CrossRefGoogle ScholarPubMed
Trisler, D. (1990). Cell recognition and pattern formation in the developing nervous system. Journal of Experimental Biology 153, 11–27.CrossRefGoogle ScholarPubMed
Trisler, D. & Collins, F. (1987). Corresponding spatial gradients of TOP molecules in the developing retina and optic tectum. Science 237, 1208–1209.CrossRefGoogle Scholar
Trisler, G.D., Schneider, M.D. & Nirenberg, M. (1981). A topographic gradient of molecules in retina can be used to identify neuron position. Proceedings of the National A cademy of Sciences of the U.S.A. 78, 2145–2149.CrossRefGoogle ScholarPubMed