Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-19T15:37:34.920Z Has data issue: false hasContentIssue false

Visual processing of the zebrafish optic tectum before and after optic nerve damage

Published online by Cambridge University Press:  23 June 2004

ANGELA L. McDOWELL
Affiliation:
Department of Psychology and Biotechnology Center, Western Kentucky University, Bowling Green Department of Psychology, Indiana University, Bloomington
LEE J. DIXON
Affiliation:
Department of Psychology and Biotechnology Center, Western Kentucky University, Bowling Green Department of Psychology, University of Tennessee, Knoxville
JENNIFER D. HOUCHINS
Affiliation:
Department of Psychology and Biotechnology Center, Western Kentucky University, Bowling Green
JOSEPH BILOTTA
Affiliation:
Department of Psychology and Biotechnology Center, Western Kentucky University, Bowling Green

Abstract

Although the zebrafish has become an important model in visual neuroscience, little has been done to examine the processing of its higher visual centers. The purpose of this work was twofold. The first purpose was to examine the physiology of the zebrafish retinotectal system and its relationship to retinal physiology. Spectral sensitivity functions were derived from visually evoked tectal responses and these functions were compared to the functions of electroretinogram (ERG) responses obtained using the same stimulus conditions. The second purpose was to examine the recovery of visual functioning of the tectum following optic nerve damage. The optic nerves of adult zebrafish were damaged (crushed), and tectal visual processing was assessed following damage. The results showed that the spectral sensitivity functions based on the On-responses of the tectum and ERG were qualitatively similar. The functions based on each response type received similar cone contributions including both nonopponent and opponent contributions. However, the spectral sensitivity functions based on the Off-responses of the tectum and ERG differed. The results also showed that the zebrafish visual system is capable of neural regeneration. By 90 days following an optic nerve crush, the spectral sensitivity function based on the tectal On-response was similar to functions obtained from normal zebrafish. Although the tectal Off-response did recover, the spectral sensitivity based on the Off-response was not the same as the function of normal zebrafish. These results support the notion that different levels of the visual system process information differently and that the zebrafish visual system, like those of other lower vertebrates, is capable of functional regeneration.

Type
Research Article
Copyright
2004 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

Baier, H., Klostermann, S., Trowe, T., Karlstrom, R.O., & Nusslein-Volhard, C. (1996). Genetic dissection of the retinotectal projection. Development 123, 415425.Google Scholar
Beaudet, L., Browman, H.I., & Hawryshyn, C.W. (1993). Optic nerve response and retinal structure in rainbow trout of different sizes. Vision Research 33, 17391746.CrossRefGoogle Scholar
Bilotta, J. & Saszik, S. (2001). The zebrafish as a model visual system. International Journal of Developmental Neuroscience 19, 621629.CrossRefGoogle Scholar
Cameron, D.A. (2002). Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Visual Neuroscience 19, 365372.CrossRefGoogle Scholar
Cassidy, J. & Bilotta, J. (2000). Spectral sensitivity of the goldfish ERG and optic tectum. Investigative Ophthalmology and Visual Science (Suppl.) 41, S498.Google Scholar
DeMarco, P.J., Jr. & Powers, M.K. (1991). Spectral sensitivity of ON and OFF responses from the optic nerve of goldfish. Visual Neuroscience 6, 207217.CrossRefGoogle Scholar
Gallagher, S.P. & Northmore, D.P.M. (1997). The effect of cobalt blockade on stimulus-evoked activity in the goldfish optic tectum. Investigative Ophthalmology and Visual Science (Suppl.) 38, S361.Google Scholar
Hays, W.L. (1994). Statistics. Fort Worth, Texas: Holt, Rinehart and Winston, Inc.
Hughes, A., Saszik, S., Bilotta, J., DeMarco, P.J., Jr., & Patterson, W.F., II. (1998). Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience 15, 10291037.CrossRefGoogle Scholar
Jacobson, M. & Gaze, R.M. (1965). Selection of appropriate tectal connections by regenerating optic nerve fibers in adult goldfish. Experimental Neurology 13, 418430.CrossRefGoogle Scholar
Marcus, R.C., Delaney, C.L., & Easter, S.S., Jr. (1999). Neurogenesis in the visual system of embryonic and adult zebrafish (Danio rerio). Visual Neuroscience 16, 417424.CrossRefGoogle Scholar
McDonald, C.G. (2001). Electrophysiological and neuroethological investigations of the teleostean optic tectum. Unpublished doctoral dissertation. Victoria, British Columbia, Canada: University of Victoria.
Meyer, R.L. (1980). Mapping the normal and regenerating retinotectal projection of goldfish with audoradiographic methods. Journal of Comparative Neurology 189, 273289.CrossRefGoogle Scholar
Mills, S.L. & Sperling, H.G. (1990). Red/green opponency in the rhesus macaque ERG spectral sensitivity is reduced by bicuculline. Visual Neuroscience 5, 217221.CrossRefGoogle Scholar
Northmore, D.P.M. (1987). Neural activity in the regenerating optic nerve of the goldfish. Journal of Physiology 391, 299312.CrossRefGoogle Scholar
Northmore, D.P.M. (1989a). Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish—I. Early recovery of dimming sensitivity in tectum and torus longitudinalis. Neuroscience 32, 739747.Google Scholar
Northmore, D.P.M. (1989b). Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish—II. Delayed recovery of sensitivity to small light flashes. Neuroscience 32, 749757.Google Scholar
Northmore, D.P.M. & Oh, D.J. (2001). Sequential recovery of sensitivity to negative and positive contrasts during optic nerve regeneration in goldfish. Visual Neuroscience 18, 197201.CrossRefGoogle Scholar
Northmore, D.P.M. & Gallagher, S.P. (2003). Functional relationship between nucleus isthmi and tectum in teleosts: Synchrony but no topography. Visual Neuroscience 20, 335348.CrossRefGoogle Scholar
Oh, D.J. & Northmore, D.P.M. (1998). Functional properties of retinal ganglion cells during optic nerve regeneration in the goldfish. Visual Neuroscience 15, 11451155.CrossRefGoogle Scholar
Palacios, A.G., Goldsmith, T.H., & Bernard, G.D. (1996). Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light. Visual Neuroscience 13, 411421.CrossRefGoogle Scholar
Press, W.H., Teukolsky, S.A., Vetterling, W.T., & Flannery, B.P. (1992). Numerical Recipes in C: The Art of Scientific Computing. New York: Cambridge University Press.
Robinson, J., Schmitt, E.A., Harosi, F.I., Reece, R.J., & Dowling, J.E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the U.S.A. 90, 60096012.CrossRefGoogle Scholar
Saszik, S. & Bilotta, J. (1999). The effects of temperature on the dark-adapted spectral sensitivity function of the adult zebrafish. Vision Research 39, 10511058.CrossRefGoogle Scholar
Saszik, S., Bilotta, J., & Givin, C.M. (1999). ERG assessment of zebrafish retinal development. Visual Neuroscience 16, 881888.CrossRefGoogle Scholar
Saszik, S., Alexander, A.L., Lawrence, T., & Bilotta, J. (2002). APB differentially affects on the cone contributions to the zebrafish ERG. Visual Neuroscience 19, 521529.CrossRefGoogle Scholar
Sperling, H.G. & Harwerth, R.S. (1971). Red–green cone interactions in the increment-threshold spectral sensitivity of primates. Science 172, 180184.CrossRefGoogle Scholar
Sperry, R.W. (1972). The eye and the brain. In Perception: Mechanisms and Models, ed. Held, R. & Richards, W., pp. 362366. San Francisco, California: W. H. Freeman and Company.
Stirling, R.V., Bartlett, C.A., Dunlop, S.A., & Beazley, L.D. (2001). Light evoked responses recorded from the optic tectum are postsynaptic. International Union of Physiological Sciences Abstract 34, 1260.Google Scholar
Wheeler, T.G. (1979). Retinal ON and OFF responses convey different chromatic information to the CNS. Brain Research 160, 145149.CrossRefGoogle Scholar