Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T08:21:50.541Z Has data issue: false hasContentIssue false
  • English
  • Français

Visual function in regenerating teleost retina following surgical lesioning

Published online by Cambridge University Press:  29 May 2007

ALLEN F. MENSINGER  and
MAUREEN K. POWERS
ALLEN F. MENSINGER
Affiliation:
Vision Research Center and Department of Psychology, Vanderbilt University, Nashville, Tennessee Department of Biology, University of Minnesota, Duluth, Minnesota
MAUREEN K. POWERS
Affiliation:
Vision Research Center and Department of Psychology, Vanderbilt University, Nashville, Tennessee Gemstone Vision Research Institute, Rodeo, California
Get access Rights & Permissions [Opens in a new window]

Abstract

Regeneration of the teleost retina following surgical extirpation of 25% to 100% of the neural retina was investigated in goldfish (Carrasius auratus) and sunfish (Lepomis cyanellus). The retina will regenerate following removal of up to 95% of the neural retina, however complete extirpation prevented regeneration. Visual sensitivity was assessed by examining components of the electroretinogram (ERG) and the dorsal light reflex (DLR) during regeneration. B-wave amplitudes in the experimental eyes increased throughout the study and central connections were reestablished as indicated by the progressive improvement in the dorsal light reflex. The recovery of visual function was closely correlated with retinal regeneration. Visual recovery progressed more slowly than following complete cytotoxic destruction of the mature retina (Mensinger & Powers, 1999) because the surgery removed a large number of the pluripotent cell population and restricted the number and distribution of regenerating foci.

Keywords

RegenerationRetinaVisionElectroretinogramPhotoreceptors
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 299 - 307
Copyright
© 2007 Cambridge University Press

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

REFERENCES

Callahan, M.P. & Mensinger, A.F. (2007). Restoration of Visual Function Following Optic Nerve Regeneration in Bluegill (Lepomis Macrochirus) X Pumpkinseed (Lepomis Gibbosus) Hybrid Sunfish. Visual Neuroscience 24, 309–317.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.Google Scholar
Cameron, D.A. & Carney, L.H. (2004). Cellular patterns in the inner retina of adult zebrafish: Quantitative analyses and a computational model of their formation. Journal of Comparative Neurology 471, 11–25.CrossRefGoogle Scholar
Cameron, D.A., Cornwall, M.C. & MacNichol, E.F., Jr. (1997). Visual pigment assignments in regenerated retina. Journal of Neuroscience 17, 917–923.Google Scholar
Del Cerro, M., Notter, M.F., Seigel, G., Lazar, E., Chader, G. & del Cerro, C. (1992). Intraretinal xenografts of differentiated human retinoblastoma cells integrate with the host retina. Journal of Neuroscience 15, 2255–2271.Google Scholar
Fischer, A.J. & Reh, T.A. (2001). Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nature Neuroscience 4, 247–252.CrossRefGoogle Scholar
Hitchcock, P., Ochocinska, M., Sieh, A. & Otteson, D. (2004). Persistent and injury-induced neurogenesis in the vertebrate retina. Progress in Retinal and Eye Research 23, 183–194.CrossRefGoogle Scholar
Hitchcock, P.F. & Cirenza, P. (1994). Synaptic organization of regenerated retina in the goldfish. Journal of Comparative Neurology 343, 609–616.CrossRefGoogle Scholar
Hitchcock, P.F. & Raymond, P.A. (1992). Retinal regeneration. Trends in Neuroscience 15, 103–108.CrossRefGoogle Scholar
Hitchcock, P.F. & Raymond, P.A. (2004). The teleost retina as a model for development and regeneration biology. Zebrafish 1, 257–271.CrossRefGoogle Scholar
Hitchcock, P.F., Lindsey Myhr, K.J., Easter, S.S., Mangione-Smith, R. & Dwyer Jones, D. (1992). Local regeneration in the retina of the goldfish. Journal of Neurobiology 23, 187–203.CrossRefGoogle Scholar
Johns, P.R. & Easter, S.S., Jr. (1977). Growth of the adult goldfish eye. II Increase in retinal cell number. Journal of Comparative Neurology 176, 331–342.Google Scholar
Johns, P.R. (1982). The formation of photoreceptors in the growing retinas of larval and adult goldfish. Journal of Neuroscience 2, 179–198.Google Scholar
Johns, P.R. & Fernald, R.D. (1981). Genesis of rods in teleost fish retina. Nature 293, 141–142.CrossRefGoogle Scholar
Julian, D., Ennis, K. & Korenbrot, J.I. (1998). Birth and fate of proliferative cells in the inner nuclear layer of the mature fish retina. Journal of Comparative Neurology 394, 271–282.3.0.CO;2-Z>CrossRefGoogle Scholar
Knight, J.K. & Raymond, P.A. (1994). Retinal pigmented epithelium does not transdifferentiate in adult goldfish. Journal of Neurobiology 27, 447–456.Google Scholar
Kurz-Isler, G. & Wolburg, H. (1982). Morphological study on the regeneration of the retina in the rainbow trout after ouabain damage: Evidence of dedifferentiation of photoreceptors. Cell Tissue Research 225, 165–178.CrossRefGoogle Scholar
Lin, Z-S. & Yazulla, S. (1994). Depletion of retinal dopamine increases brightness perception in goldfish. Visual Neuroscience 1, 683–693.CrossRefGoogle Scholar
Maier, W. & Wolburg, H. (1978). Regeneration of the goldfish retina after exposure to different doses of ouabain. Cell Tissue Research 202, 99–118.Google Scholar
Mensinger, A.F. & Powers, M.K. (1999). Visual function in regenerating teleost retina following cytotoxic lesioning. Visual Neuroscience 16, 241–251.Google Scholar
Meyer, R.L. (1977). Eye-in-water electrophysiology mapping of goldfish with and without tectal lesions. Experimental Neurology 56, 23–41.CrossRefGoogle Scholar
Meyer, R.L. (1980). Mapping the normal and regenerating retinotectal projection of goldfish with autoradiographic methods. Journal of Comparative Neurology 189, 273–289.CrossRefGoogle Scholar
Meyer, R.L., Sakurai, K. & Schauwecker, E. (1985). Topography of regenerating optic nerve fibers in goldfish traced with local wheat germ injections into retina: Evidence for discontinuous microtopography in the retinotectal projection. Journal of Comparative Neurology 239, 27–43.CrossRefGoogle Scholar
Mitsuda, S., Yoshii, C., Ikegami, Y. & Araki, M. (2005). Tissue interaction between the retinal pigment epithelium and the choroid triggers retinal regeneration of the newt Cynops pyrrhogaster. Developmental Biology 280, 122–132.CrossRefGoogle Scholar
Northmore, D.P.M. & Masino, T. (1984). Recovery of vision in fish after optic nerve crush: A behavioral and electrophysiological study. Experimental Neurology 84, 109–125.CrossRefGoogle Scholar
Otteson, D.C., D'Costa, A.R. & Hitchcock, P.F. (2001). Putative stem cells and the lineage of rod photoreceptors in the mature retina of the goldfish. Developmental Biology 232, 62–76.CrossRefGoogle Scholar
Powers, M.K. (1978). Light-adapted spectral sensitivity of the goldfish: A reflex measure. Vision Research 18, 1131–1136.CrossRefGoogle Scholar
Raymond, P.A, Barthel, L.K., Bernardos, R.L. & Perkowski, J.J. (2006). Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Developmental Biology 6, 36.CrossRefGoogle Scholar
Raymond, P.A. & Hitchcock, P.F. (1997). Retinal regeneration: Common principles but a diversity of mechanisms. Advances in Neurology 72, 171–184.Google Scholar
Raymond, P.A. & Hitchcock, P.F. (2000). How the neural retina regenerates. In Vertebrate Eye Development. Volume 31, ed. Fini, M.E., pp. 197–218. Berlin, Germany: Springer Verlag.CrossRef
Raymond, P.A., Reifler, M.J. & Rivlin, P.K. (1988). Regeneration of goldfish retina: Rod precursors are a likely source of regenerating cells. Journal of Neurobiology 19, 431–463.CrossRefGoogle Scholar
Schmidt, J.S., Cicerone, C.M. & Easter, S.S. (1978). Expansion of half retinal projection to tectum in goldfish-electrophysiological and anatomical study. Journal of Comparative Neurology 177, 257–277.CrossRefGoogle Scholar
Schmidt, J.T. & Edwards, D.L. (1983). Activity sharpens the map during regeneration of the retinotectal projection in goldfish. Brain Research 269, 29–39.CrossRefGoogle Scholar
Silver, P.H. (1974). Photopic spectral sensitivity of the neon tetra (Paracheirodon innesi (Myers)) found by the use of a dorsal light reaction. Vision Research 14, 329–334.CrossRefGoogle Scholar
Sperry, R.W. (1949). Reimplantation of eyes in fishes (Bathygobius soporator) with recovery of vision. Society of Experimental Biology Medical Proceedings 71, 80–81.CrossRefGoogle Scholar
Stenkamp, D.L. & Cameron, D.A. (2002). Cellular pattern formation in the retina: Retinal regeneration as a model system. Molecular Vision 8, 280–293.Google Scholar
Stenkamp, D.L., Powers, M.K., Carney, L.H. & Cameron, D.A. (2001). Evidence for two distinct mechanisms of neurogenesis and cellular pattern formation in regenerated goldfish retinas. Journal of Comparative Neurology 431, 363–381.3.0.CO;2-7>CrossRefGoogle Scholar
Stuermer, C.A.O., Niepenberg, A. & Wolburg, H. (1985). Aberrant axonal paths in regenerated goldfish retina and tectum following intraocular injection of ouabain. Neuroscience Letters 58, 333–338.CrossRefGoogle Scholar
Vihtelic, T.S. & Hyde, D.R. (2000). Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. Journal of Neurobiology 44, 289–307.3.0.CO;2-H>CrossRefGoogle Scholar
Walls, G.L. (1967). The Vertebrate Eye and its Adaptive Radiation. New York: Hafner.
Wu, D.M., Schneiderman, T., Burgett, J., Gokhale, P., Barthel, L. & Raymond, P.A. (2001). Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Investigative Ophthalmology and Visual Science 42, 2115–2124.Google Scholar
Yoshii, C., Ueda, Y., Okamoto, M. & Araki, M. (2007). Neural retinal regeneration in the anuran amphibian Xenopus laevis post-metamorphosis: Transdifferentiation of retinal pigmented epithelium regenerates the neural retina. Developmental Biology 303, 45–56.CrossRefGoogle Scholar
Yurco, P. & Cameron, D.A. (2005). Responses of Muller glia to retinal injury in adult zebrafish. Vision Research 45, 991–1002.CrossRefGoogle Scholar