Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T06:27:07.102Z Has data issue: false hasContentIssue false
  • English
  • Français

Restoration of visual function following optic nerve regeneration in bluegill (Lepomis macrochirus) × pumpkinseed (Lepomis gibbosus) hybrid sunfish

Published online by Cambridge University Press:  29 May 2007

MICHAEL P. CALLAHAN  and
ALLEN F. MENSINGER
MICHAEL P. CALLAHAN
Affiliation:
Department of Biology, University of Minnesota, Duluth, Duluth, Minnesota Biology Department, University of Southern Maine, Portland, Maine
ALLEN F. MENSINGER
Affiliation:
Department of Biology, University of Minnesota, Duluth, Duluth, Minnesota
Get access Rights & Permissions [Opens in a new window]

Abstract

Simple (dorsal light reflex) and complex (predator-prey interactions) visually mediated behaviors were used concurrently with morphological examination to assess restoration of visual function following optic nerve crush in bluegill (Lepomis macrochirus) × pumpkinseed (Lepomis gibbosus) hybrid sunfish. Regenerating optic nerve axons projected into the stratum opticum-stratum fibrosum et griseum superficiale by week 2, the stratum griseum centrale by week 4, and stratum album centrale by week 6. Initial projections into the laminae were diffuse and less stratified compared to controls. By week 12, the projection pattern of regenerating nerve fibers closely resembled the innervation of normal tecta. Visual improvements were correlated with increasing projections into the tectum. The dorsal light reflex improved from a 45° vertical deviation following nerve crush to 4.5° by week 16. Initial predator-prey interactions were exclusively mediated by the control eye. As regeneration progressed, there was a gradual expansion of the visual field. The reaction distance and attack angles within the visual field of the experimental eye were initially less than controls, however, these differences disappeared by week 10. Improvements in visual function were closely correlated with an increase of regenerating ganglion cell axons into the optic tectum indicating sufficient synaptogenesis to mediate both simple and complex visual behavior.

Keywords

Optic nerve regenerationDorsal light reflexPredator-prey interactionsFish visionVisually mediated behavior
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 309 - 317
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

Batty, R.S., Blaxter, J.H.S. & Richard, J.M. (1990). Light intensity and feeding behaviour of herring, Clupea harengus. Marine Biology 107, 383–388.CrossRefGoogle Scholar
Bisazza, A., Lippolis, G. & Vallortigara, G. (2001). Lateralization of ventral fins use during object exploration in the blue gourami (Trichogaster trichopterus). Physiology & Behavior 72, 575–578.CrossRefGoogle Scholar
Cook, J.E. (1979). Interactions between optic fibers controlling the locations of their terminals in the goldfish optic tectum. Journal of Embryology and Experimental Morphology 52, 89–103.Google Scholar
Dadda, M. & Bisazza, A. (2006). Lateralized female topminnows can forage and attend to a harassing male simultaneously. Behavioral Ecology 17, 358–363.CrossRefGoogle Scholar
De Santi, A., Bisazza, A. & Vallortigara, G. (2002). Complementary left and right eye use during predator inspection and shoal-mate scrutiny in minnows. Journal of fish Biology 60, 116–1125.Google Scholar
Fine, M.L., McElroy, D., Rafi, J., King, C.B., Loesser, K.E. & Newton, S. (1996). Lateralization of pectoral stridulation sound production in the channel catfish. Physiology & Behavior 60, 753–757.CrossRefGoogle Scholar
Gibbs, M.A. & Northmore, D.P.M. (1996). The role of torus longitudinalis in equilibrium orientation measure with the dorsal light reflex. Brain, Behavior and Evolution 48, 115–120.CrossRefGoogle Scholar
Hayes, W.P. & Meyer, R.L. (1988). Normal and regenerating optic fibers in goldfish tectum: HRP-EM evidence for rapid synaptogenesis and optic fiber-fiber affinity. Journal of Comparative Neurology 274, 516–538.CrossRefGoogle Scholar
Hayes, W.P. & Meyer, R.L. (1989). Normal numbers of retinotectal synapses during the activity-sensitive period of optic regeneration in goldfish: HRP-EM evidence implicating synapse rearrangement and collateral elimination during map refinement. Journal of Neuroscience 9, 1400–1413.Google Scholar
Hori, M. (1993). Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260, 216–219.CrossRefGoogle Scholar
Howick, G.L. & O'Brien, W.J. (1983). Piscivorous feeding behavior of largemouth bass: An experimental analysis. Transactions of the American Fisheries Society 112, 508–516.2.0.CO;2>CrossRefGoogle Scholar
Janssen, J. & Corcoran, J. (1993). Lateral line stimuli can override vision to determine sunfish strike trajectory. Journal of Experimental Biology 176, 299–305.Google Scholar
Jolly, D.W., Mawdesley-Thomas, L.E. & Bucke, D. (1972). Anesthsia of Fish. Veterinary Record 91, 424–426.CrossRefGoogle Scholar
McMahon, T.E. & Holanov, S.H. (1995). Foraging success of largemouth bass at different light intensities: Implications for time and depth of feeding. Journal of Fish Biology 46, 759–767.CrossRefGoogle 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. (1980). Mapping the normal and regenerating retinotectal projection of goldfish with autoradiographic methods. Journal of Comparative Neurology 189, 175–190.Google Scholar
Meyer, R.L., Sakurai, K. & Schauwecker, E. (1985). Topography of regenerating optic fibers in goldfish traced with local wheat germ injections into retina: Evidence for discontinuous microtopography in retinotectal projection. Journal of Comparative Neurology 239, 27–43.CrossRefGoogle Scholar
Meyer, R.L. & Kageyama, G.H. (1999). Large-scale synaptic errors during map formation by regenerating optic axons in the goldfish. Journal of Comparative Neurology 409, 299–312.3.0.CO;2-C>CrossRefGoogle Scholar
Mittelbach, G.G. (1984). Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65, 499–513.CrossRefGoogle Scholar
Nakae, M. & Sasaki, K. (2002). A scale-eating triacanthodid, Macrorhamphosodes uradoi: Prey fishes and mouth “handedness” (Tetraodontiformes, Triacanthoidei). Ichthyological Research 49, 7–14.CrossRefGoogle Scholar
Northcutt, R.G. & Butler, A.B. (1991). Retinofugal and retinopetal projections in the green sunfish, Lepomis cyanellus. Brain, Behavior and Evolution 37, 333–354.CrossRefGoogle Scholar
Northmore, D.P.M. (1981). Visual localization after rearrangement of retinotectal maps in fish. Nature 293, 142–144.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
Northmore, D.P.M. (1989). Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish I. Early recovery of dimming sensitivity in tectum and torus longitudinalis. Neuroscience 32, 739–747.Google Scholar
Northmore, D.P.M. (1991). Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Research 31, 525–535.CrossRefGoogle Scholar
Northmore, D.P.M. & Celenza, M.A. (1992). Recovery of contrast sensitivity during optic nerve regeneration in fish. Experimental Neurology 115, 69–72.CrossRefGoogle Scholar
Nyberg, D.W. (1971). Prey capture in the largemouth bass. American Midland Naturalist 86, 128–144.CrossRefGoogle Scholar
Rankin, E.C.C. & Cook, J.E. (1986). Topographic refinement of regenerating retinotectal projection of the goldfish in standard laboratory conditions: A quantitative WGA-HRP study. Experimental Brain Research 63, 409–420.Google Scholar
Richmond, H.E., Hrabik, T.R. & Mensinger, A.F. (2004). Light intensity, prey detection and foraging mechanisms of age-0 year yellow perch (Perca flavescens). Journal of Fish Biology 65, 195–205.CrossRefGoogle Scholar
Schmidt, J.T. & Edwards, D.L. (1983). Activity sharpens the map during the regeneration of the retinotectal projection in goldfish. Brain Research 269, 29–39.CrossRefGoogle Scholar
Schmidt, J.T., Turcotte, J.C., Buzzard, M. & Tieman, D.G. (1988). Staining of regenerated optic arbors in goldfish tectum: Progressive changes in immature arbors and a comparison of mature regenerated arbors with normal arbors. Journal of Comparative Neurology 269, 565–591.CrossRefGoogle Scholar
Schwassmann, H.O. & Kruger, L. (1965). Organization of the visual projection upon the optic tectum of some freshwater fish. Journal of Comparative Neurology 124, 113–126.CrossRefGoogle Scholar
Schwassmann, H.O. & Krag, M.H. (1970). The relation of visual field defects to retinotectal topography in teleost fish. Vision Research 10, 29–42.CrossRefGoogle Scholar
Sovrano, V.A., Rainoldi, C., Bisazza, A. & Vallortigara, G. (1999). Roots of brain specializations: Preferential left-eye use during mirror-image inspection in six species of teleost fish. Behavioural Brain Research 106, 175–180.CrossRefGoogle Scholar
Sovrano, V.A., Bisazza, A. & Vallortigara, G. (2001). Lateralization of response to social stimuli in fishes: A comparison between different methods and species. Physiology & Behavior 74, 237–244.CrossRefGoogle Scholar
Sovrano, V.A. (2004). Visual lateralization in response to familiar and unfamiliar stimuli in fish. Behavioural Brain Research 152, 385–391.CrossRefGoogle Scholar
Sperry, R.W. (1948). Patterning of central synapses in regeneration of the optic nerve in teleosts. Physiological Zoology 21, 351–361.Google Scholar
Springer, A.D., Easter, S.E. & Agranoff, B.W. (1977). The role of the optic tectum in various visually mediated behaviors of goldfish. Brain Research 128, 393–404.CrossRefGoogle Scholar
Springer, A.D. & Agranoff, B.W. (1977). Effect of temperature on rate of goldfish optic nerve regeneration: A radioautographic and behavioral study. Brain Research 128, 405–415.CrossRefGoogle Scholar
Striedter, G.F. & Northcutt, R.G. (1989). Two distinct visual pathways through the superficial pretectum in a percomorph teleost. Journal of Comparative Neurology 283, 342–354.CrossRefGoogle Scholar
Stuermer, C.A.O. & Easter, S.S., Jr. (1984). A comparison of the normal and regenerated retinotectal pathways of goldfish. Journal of Comparative Neurology 223, 57–76.CrossRefGoogle Scholar
Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. Michigan: Cranbrook Institute of Science.CrossRef
Walton, W.E., Hairston, N.G., Jr. & Wetterer, J.K. (1992). Growth-related constraints on diet selection by sunfish. Ecology 73, 429–437.CrossRefGoogle Scholar
Werner, E.E. & Hall, D.J. (1974). Optimal foraging and the size selection of prey by the bluegill sunfish (Lepomis macrochirus). Ecology 55, 1042–1052.CrossRefGoogle Scholar
Yanagihara, D., Watanabe, S. & Mitarai, G. (1993). Neuroanatomical substrate for the dorsal light response I. Differential afferent connections of the lateral lobe of the valvula cerebelli in goldfish (Carassius auratus). Neuroscience Research 16, 25–32.Google Scholar