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Differential intertectal delay between Rana pipiens and Xenopus laevis: Implications for species-specific visual plasticity

Published online by Cambridge University Press:  02 June 2009

Warren J. Scherer
Affiliation:
W.K. Kellogg Eye Center, University of Michigan, Ann Arbor
Susan B. Udin
Affiliation:
Department of Physiology, State University of New York at Buffalo, Buffalo

Abstract

In the frog Xenopus laevis, the isthmotectal projection, which relays input from the ipsilateral eye, exhibits anatomical reorganization following surgical eye rotation performed during tadpole stages while the isthmotectal projection in the frog Rana pipiens fails to show reorganization. This plasticity has been shown to be dependent upon activation of the N-methyl-D-aspartate (NMDA) receptor located on tectal cell dendrites. The reorganization process in Xenopus is hypothesized to employ a Hebbian mechanism requiring correlated firing of ipsilateral and contralateral inputs to a given tectal cell; when an ipsilateral axon synapses onto a tectal cell that receives input from a contralateral axon with a matching receptive-field location, the correlation in activity triggers stabilization of the ipsilateral synapse. However, in neither Xenopus nor Rana do ipsilateral and contralateral inputs begin to fire simultaneously in response to a given visual stimulus; the ipsilateral input is delayed because it reaches the tectum indirectly, through a polysynaptic relay via the opposite tectum and nucleus isthmi. The objective of this experiment was to test whether there is a significant difference in this intertectal delay between Xenopus laevis and Rana pipiens in order to determine whether intertectal delay could be a contributing factor in this species-specific ability to exhibit visual plasticity. We have found that intertectal delay is 26.16 ms longer in Rana pipiens (36.53 ms) than in Xenopus laevis (10.37 ms).

Type
Short Communications
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Debski, E.A. & Constantine-Paton, M. (1990). Evoked pre- and post-synaptic activity in the optic tectum of the cannulated tadpole. Journal of Comparative Physiology A 167, 377390.CrossRefGoogle ScholarPubMed
Dowben, R.M. & Rose, J.E. (1953). A metal-filled microelectrode. Science 118, 2224.CrossRefGoogle ScholarPubMed
Feldman, J.D., Gaze, R.M. & Keating, M.J. (1971). The effect on intertectal neuronal connections of rearing Xenopus in total darkness. Journal of Physiology (London) 212, 4445P.Google ScholarPubMed
Fite, K.V. (1969). Single-unit analysis of binocular neurons in the frog optic tectum. Experimental Neurology 24, 475486.CrossRefGoogle ScholarPubMed
Gaze, R.M. & Jacobson, M. (1962). The projection of the binocular visual field on the optic tecta of the frog. Quarterly Journal of Experimental Physiology 47, 273280.CrossRefGoogle Scholar
Gaze, R.M. & Jacobson, M. (1963). The path from the retina to the ipsilateral optic tectum of the frog. Journal of Physiology (London) 165, 7374P.Google Scholar
Grant, S., Brickley, S.G. & Keating, M.J. (1993). Plasticity of binocular visual connections in the frog: From R.M. Gaze to NMDA. In Formation and Regeneration of Nerve Connections, ed. Sharma, S.C. & Fawcett, J.W., pp. 6071. Boston, Massachusetts: Birkhaüser.CrossRefGoogle Scholar
Gruberg, E.R., Hughes, T.E. & Karten, H.J. (1994). Synaptic inter-relationships between the optic tectum and the ipsilateral nucleus isthmi in Rana pipiens. Journal of Comparative Neurology 339, 353364.CrossRefGoogle Scholar
Gustafsson, B. & Wigström, H. (1986). Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents. Journal of Neuroscience 6, 15751582.CrossRefGoogle ScholarPubMed
Hickmott, P.W. & Constantine-Paton, M. (1993). The contributions of NMDA, non-NMDA, and GABA receptors to postsynaptic responses in neurons of the optic tectum. Journal of Neuroscience 13, 43394353.CrossRefGoogle ScholarPubMed
Jacobson, M. & Hirsch, H.V.B. (1973). Development and maintenance of connectivity in the visual system of the frog. I. The effects of eye rotation and visual deprivation. Brain Research 49, 4765.CrossRefGoogle ScholarPubMed
Jahr, C.E. & Lester, R.A.J. (1992). Synaptic excitation mediated by glutamate-gated ion channels. Current Opinion in Neurobiology 2, 270274.CrossRefGoogle ScholarPubMed
Keating, M.J. (1974). The role of visual function in the patterning of binocular visual connexions. British Medical Bulletin 30, 145151.CrossRefGoogle ScholarPubMed
Keating, M.J., Beazley, L., Feldman, J.D. & Gaze, R.M. (1975). Binocular interaction and intertectal neuronal connexions: Dependence upon developmental stage. Proceedings of the Royal Society B (London) 191, 445466.Google ScholarPubMed
Keating, M.J. & Grant, S. (1992). The critical period for experience-dependent plasticity in a system of binocular visual connections in Xenopus laevis: Its temporal profile and relation to normal developmental requirements. European Journal of Neuroscience 4, 2736.CrossRefGoogle Scholar
Kennard, C. & Keating, M.J. (1985). A species difference between Rana and Xenopus in the occurrence of intertectal neuronal plasticity. Neuroscience Letters 58, 365370.CrossRefGoogle ScholarPubMed
Lettvin, J.Y., Maturana, H.R., McCulloch, W.S. & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of the Institute of Radio Engineers of New York 47, 19401951.Google Scholar
Levy, W.B. & Steward, O. (1983). Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8, 791797.CrossRefGoogle ScholarPubMed
McCart, R. & Straznicky, C. (1988). The ultrastructural organization of the isthmic nucleus in Xenopus. Anatomy and Embryology 177, 325330.CrossRefGoogle ScholarPubMed
Raybourn, M.S. (1975). Spatial and temporal organization of the binocular input to frog optic tectum. Brain, Behavior and Evolution 11, 161178.CrossRefGoogle ScholarPubMed
Scherer, W.J. & Udin, S.B. (1989). N-methyl-D-aspartate antagonists prevent interaction of binocular maps in Xenopus tectum. Journal of Neuroscience 9, 38373843.CrossRefGoogle ScholarPubMed
Scherer, W.J. & Udin, S.B. (1991). Latency and temporal overlap of visually-elicited contralateral and ipsilateral firing in Xenopus tectum during and after the critical period. Developmental Brain Research 58, 129132.CrossRefGoogle ScholarPubMed
Scherer, W.J. & Udin, S.B. (1992). Xenopus exhibits seasonal variation in retinotectal latency but not tecto-isthmo-tectal latency. Journal of Comparative Physiology A 171, 207212.CrossRefGoogle Scholar
Udin, S.B. (1987). A projection from the mesencephalic tegmentum to the nucleus isthmi in the frogs Rana pipiens and Acris crepitans. Neuroscience 21, 631637.CrossRefGoogle Scholar
Udin, S.B. (1993). NMDA Receptors and Intertectal Plasticity in Xenopus. Formation and Regeneration of Nerve Connections. Boston, Massachusetts: Birkhaüser.Google Scholar
Udin, S.B., Fisher, M.D. & Norden, J.J. (1990). Ultrastructure of the crossed isthmotectal projection in Xenopus frogs. Journal of Comparative Neurology 292, 246254.CrossRefGoogle ScholarPubMed