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Visual behavior of adult goldfish with regenerating retina

Published online by Cambridge University Press:  26 June 2007

AMY E. LINDSEY
Affiliation:
Department of Psychology and Vanderbilt Vision Research Center, Vanderbilt University, Nashville, Tennessee
MAUREEN K. POWERS
Affiliation:
Department of Psychology and Vanderbilt Vision Research Center, Vanderbilt University, Nashville, Tennessee

Abstract

To determine whether regenerating neural pathways can support visual behavior, adult goldfish (Carassius auratus) were injected intraocularly with ouabain and tested for the presence of reflexive visual behaviors (dorsal light reflex and optokinetic nystagmus) and the ability to respond to visual stimuli in a classical conditioning paradigm. All visual behaviors were absent or greatly diminished until 8 to 10 weeks, when retinal layering had returned. At 10 weeks post-ouabain, reflexive behaviors to supra-threshold stimuli were near normal; however the ability to detect supra-threshold stimuli in the conditioning paradigm did not recover until 13 weeks. Absolute dark-adapted threshold and light-adapted spectral sensitivity measured at 13 to 17 weeks were abnormal: Dark-adapted threshold was elevated by 1.5 log units and light-adapted spectral sensitivity was markedly narrower than normal. No responses to 50% contrast sinusoidal gratings could be obtained through ouabain-treated eyes using the classical conditioning technique, even though responses through the untreated eye remained. Results demonstrate that: (a) visually mediated behaviors return in goldfish with ouabain-treated retinas; (b) the time course of recovery of reflexive responses in luminance and spatial domains parallels return of ERG function and of tectal activity; and (c) visual function that is mediated by regenerating retina appears not to be as sensitive as vision via normally developed retinal pathways.

Type
Research Article
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Bassi, C.J. & Powers, M.K. (1987). Circadian rhythm in goldfish visual sensitivity. Investigative Ophthalmology and Visual Science 28, 18111815.Google Scholar
Bassi, C.J., Williams, R.C., Jr. & Powers, M.K. (1984). Light transmittance by goldfish eyes of different sizes. Vision Research 24, 14151419.Google Scholar
Bilotta, J., Lynd, F.M. & Powers, M.K. (1998). Effects of mean luminance on goldfish temporal contrast sensitivity. Vision Research 38, 5559.Google Scholar
Bilotta, J. & Powers, M.K. (1991). Spatial contrast sensitivity of goldfish: Mean luminance, temporal frequency, and a new psychophysical technique. Vision Research 31, 577588.Google Scholar
Bilotta, J. & Powers, M.K. (1992). Weak stimulus generalization using sinusoidal gratings: A cautionary note in animal psychophysics. Behavioral Research Methods 24, 507510.Google Scholar
Braisted, J.E., Essman, T.F. & Raymond, P.A. (1994). Selective regeneration of photoreceptors in goldfish retina. Development 120, 24092419.Google Scholar
Braisted, J.E. & Raymond, P.A. (1992). Regeneration of dopminergic neurons in goldfish retina. Development 114, 913919.Google Scholar
Cameron, D.A. & Powers, M.K. (2000). Morphology and visual pigment content of photoreceptors from native and injured goldfish retina. Visual Neuroscience 17, 623630.Google Scholar
DeMarco, P.J., Jr., Nussdorf, J.D., Brockman, D.A. & Powers, M.K. (1989). APB activity reduces visual responses in goldfish to high spatiotemporal frequencies. Visual Neuroscience 2, 1518.Google Scholar
Hitchcock, P.F., Ochocinska, M., Sieh, A. & Otteson, D. (2004). Persistent and injury-induced neurogenesis in the vertebrate retina. Progress in Retinal and Eye Research 23, 183.Google Scholar
Hitchcock, P.F., Lindsey Myhr, K.J., Easter, S.S., Jr., Mangione-Smith, R. & Dwyer Jones, D. (1992). Local regeneration in the retina of the goldfish. Journal of Neurobiology 23, 187203.Google Scholar
Johns, P.R. (1982). Formation of photoreceptors in larval and adult goldfish. Journal of Neuroscience 2, 178198.Google Scholar
Johns, P.R. & Fernald, R.D. (1981). Genesis of rods in teleost fish retina. Nature 293, 141142.Google 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, 271282.Google Scholar
Kastner, R. & Wolburg, H. (1982). Functional regeneration of the visual system in teleosts. Comparative investigation after optic nerve crush and damage to the retina. Zeitschrift fur Naturforschung 37, 12741280.Google Scholar
Knowles, A. & Dartnall, H.J.A. (1977). The characterization of visual pigments by absorption spectroscopy. In The Eye, ed. Davson, H. pp. 53101. New York: Academic Press.
Kurz-Isler, G. & Wolburg, H. (1982). Morphological study on regeneration of the retina in the rainbow trout after ouabain-induced damage: Evidence for differentiation of photoreceptors. Cell Tissue Research 225, 165178.Google Scholar
Mader, M.M. & Cameron, D.A. (2004). Photoreceptor differentiation during retinal development, growth, and regeneration in a metamorphic vertebrate. Journal of Neuroscience 24, 1146311472.Google Scholar
Maier, W. & Wolburg, H. (1979). Regeneration of the goldfish retina after exposure to different doses of ouabain. Cell Tissue Research 202, 99118.Google Scholar
Melzer, P. & Powers, M.K. (2001). Metabolic activity in optic tectum during regeneration of retina in adult goldfish. Visual Neuroscience 18, 599604.Google Scholar
Mensinger, A.F. & Powers, M.K. (1999). Visual function in regenerating teleost retina following cytotoxic lesioning. Visual Neuroscience 16, 241251.Google Scholar
Otteson, D.C., D'Costa, D.R. & Hitchcock, P.F. (2001). Putative stem cells and the linage of rod photoreceptors in the mature retina of the goldfish. Developmental Biology 232, 6276.Google Scholar
Otteson, D.C. & Hitchcock, P.F. (2003). Stem cells in the teleost retina: Persistent neurogenesis and injury-induced regeneration. Vision Research 43, 927936.Google Scholar
Powers, M.K. (1978). Light-adapted spectral sensitivity of the goldfish: A reflex measure. Vision Research 18, 11311136.Google Scholar
Powers, M.K., Bassi, C.J. & Raymond, P.A. (1988). Lighting conditions and retinal development in goldfish: Absolute visual sensitivity. Investigative Ophthalmology and Visual Science 29, 3743.Google Scholar
Powers, M.K. & Easter, S.S., Jr. (1978). Absolute visual threshold of the goldfish. Vision Research 18, 11371147.Google Scholar
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 122, 10921099.Google Scholar
Raymond, P.A. & Hitchcock, P.F. (2000). How the retina regenerates. Results and Problems in Cell Differentiation 31, 197218.Google Scholar
Raymond, P.A., Reifler, M.J. & Rivlin, P.K. (1988). Regeneration of goldfish retina: Rod precursors are a likely source of regenerated cells. Journal of Neurobiology 19, 431463.Google Scholar
Raymond, P.A. & Rivlin, P.K. (1987). Germinal cells in the goldfish retina that produce rod photoreceptors. Developmental Biology 122, 120138.Google Scholar
Sharma, R.M. & Ungar, F. (1980). Histogenesis of the goldfish retina. Journal of Comparative Neurology 191, 373382.Google Scholar
Springer, A.D., Easter, S.D., Jr. & Agranoff, B.W. (1977). The role of optic tectum in various visually mediated behaviors of goldfish. Brain Research 128, 393404.Google Scholar
Stenkamp, D.L., Cameron, D.S., 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. The Journal of Comparative Neurology 431, 363381.Google Scholar
Stuermer, C.A., Niepenberg, A. & Wolburg, H. (1985). Aberrant axonal paths in regenerated goldfish retina and tectum opticum following intraocular injection of ouabain. Neuroscience Letters 58, 333338.CrossRefGoogle Scholar
von Holst, E. (1935). Ueber den Lichtrückenreflex bei Fischen. Pubblicazioni Della Stazione Zoologica di Napoli 15, 143158.Google Scholar
Wu, D.M., Schneiderman, T., Burgett, L., Gokehale, 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, 21152124.Google Scholar
Yurco, P. & Cameron, D.A. (2005). Responses to Müller glia to retinal injury in adult zebrafish. Vision Research 45, 9511002.Google Scholar