Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T12:06:42.244Z Has data issue: false hasContentIssue false

Chronic effects of NMDA and APV on tectal output in Xenopus laevis

Published online by Cambridge University Press:  02 June 2009

Warren J. Scherer
Affiliation:
Department of Physiology, State University of New York, Buffalo
Susan B. Udin
Affiliation:
Department of Physiology, State University of New York, Buffalo

Abstract

In the South African clawed-toed frog Xenopus laevis, visual experience plays a crucial role in the formation of matching binocular maps in the tectum. The ipsilateral eye's projection, relayed through the crossed isthmotectal projection, displays marked plasticity in response to altered visual input during a critical period of development. This plasticity and the events responsible for the end of the critical period are mediated by N-methyl-D-aspartate (NMDA) receptor function. We have previously reported that chronic blockade of tectal NMDA receptors with the NMDA antagonist 5-amino-phosphonovaleric acid (APV) prevents plasticity of the crossed isthmotectal projection during the critical period, while chronic treatment with NMDA restores this plasticity after the end of the critical period. These results raise the question of whether the effects on plasticity are due to changes in electrical responsiveness of the treated tissue. In this study, we have quantitatively assessed the actions of APV and NMDA on certain aspects of tectal cell activity in Xenopus during and after the critical period by recording the output of the nucleus isthmi cells that are activated by the tectum after three weeks of treatment. We have found that chronic APV treatment does not alter tectal output, as indicated by the firing of isthmotectal axons, during the critical period and that chronic NMDA treatment increases tectal output in postcritical period Xenopus. Tectal output does not differ between normal Xenopus during and after the end of the critical period.

These results indicate that the effect of APV on blocking isthmotectal plasticity is not due to a nonspecific inhibition of the segment of the retinotectal relay that activates the nucleus isthmi. The enhancement of tectal output in postcritical period Xenopus by chronic NMDA treatment may promote the effectiveness of NMDA in restoring isthmotectal plasticity after the end of the critical period, but the finding that tectal activity does not differ between normal Xenopus during and after the critical period implies that a reduction in tectal activity in not the cause of the loss of plasticity at the end of the critical period.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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

Bear, M.F., Cooper, L.N. & Ebner, F.F. (1987). A physiological basis for a theory of synapse modification. Science 237, 4248.Google Scholar
Bear, M.F., Kleinschmidt, A., Gu, Q. & Singer, W. (1990). Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. Journal of Neuroscience 10, 909925.Google Scholar
Cline, H.T. & Constantine-Paton, M. (1989). NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3, 413426.Google Scholar
Cline, H.T., Debski, E.A. & Constantine-Paton, M. (1987). N-methyl-D-aspartate receptor antagonist desegregates eye-specific stripes. Proceedings of the National Academy of Sciences of the U.S.A. 84, 43424345.Google Scholar
Collingridge, G.L., Kehl, S.J. & McLennan, H. (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. Journal of Physiology (London) 334, 3346.Google Scholar
Debski, E.A., Cline, H.T. & Constantine-Paton, M. (1989). Chronic application of NMDA or APV affects the NMDA sensitivity of the evoked tectal response in Rana pipiens, Society for Neuroscience Abstracts 15, 495.Google Scholar
Dowben, R.M. & Rose, J.E. (1953). A metal-filled microelectrode. Science 118, 2224.CrossRefGoogle ScholarPubMed
Fox, K., Sato, H. & Daw, N. (1989). The location and function of NMDA receptors in cat and kitten visual cortex. Journal of Neuroscience 9, 24432454.Google Scholar
Gaze, R.M., Keating, M.J., Székely, G. & Beazley, L. (1970). Binocular interaction in the formation of specific intertectal neuronal connexions. Proceedings of the Royal Society B (London) 175, 107147.Google ScholarPubMed
Glasser, S. & Ingle, D. (1978). The nucleus isthmus as a relay station in the ipsilateral visual projection to the frog's optic tectum. Brain Research 159, 214218.Google Scholar
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. & Gaze, R.M. (1970). The ipsilateral retinotectal pathway in the frog. Quarterly Journal of Experimental Physiology 55,284292.Google Scholar
Kleinschmidt, A., Bear, M.F. & Singer, W. (1987). Blockage of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355358.Google Scholar
Levine, R.L. (1980). An autoradiographic study of the retinal projection in Xenopus laevis with comparisons to Rana. Journal of Comparative Neurology 189, 129.Google Scholar
Lynch, M.A., Elements, M.P., Voss, K.L., & Bliss, T.V.P. (1989). Increased postsynaptic release and presynaptic actions of arachidonic acid suggest a retrograde messenger role in long-term potentiation. Society for Neuroscience Abstracts 15, 86.Google Scholar
MacDermott, A.B., Mayer, M.L., Westbrook, G.L., Smith, S.J. & Barker, J.L. (1986). NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519522.CrossRefGoogle ScholarPubMed
McDonald, J.W., Cline, H.T., Constantine-Paton, M., Maragos, W.F., Johnston, M.V. & Young, A.B. (1989). Quantitative autoradiographic localization of NMDA, quisqualate, and PCP receptors in the frog tectum. Brain Research 482, 155158.Google Scholar
Miller, K.D., Chapman, B. & Stryker, M.P. (1989). Responses of cells in cat visual cortex depend on NMDA receptors. Proceedings of the National Academy of Sciences of the U.S.A. 86, 51835187.CrossRefGoogle Scholar
Nowak, L., Bregestovski, P., Ascher, A.H.P. & Prochiantz, A. (1984). Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307, 462465.Google Scholar
Scherer, W.J. & Udin, S.B. (1989 a). 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. (1989 b). NMDA restores plasticity of binocular tectal maps in postcritical period Xenopus. Society for Neuroscience Abstracts 15, 1212.Google Scholar
Schmidt, J.T. (1990). Long-term potentiation and activity-dependent retinotopic sharpening in the regenerating retinotectal projection of goldfish: Common sensitive period and sensitivity to NMDA blockers. Journal of Neuroscience 10, 233246.Google Scholar
Silberstein, G.B. & Daniel, C.W. (1982). Elvax 40P implants: sustained, local release of bioactive molecules influencing mammary ductal development. Developmental Biology 93, 272278.Google Scholar
Tremblay, E., Roisin, M.P., Represa, A., Charriaut-Marlangue, C. & Ben-Ari, Y. (1988). Transient increased density of NMDA binding sites in the developing rat hippocampus. Brain Research 461, 393396.Google Scholar
Tsumoto, T., Hagihara, K., Sato, H. & Hata, Y. (1987). NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats. Nature 327, 513514.Google Scholar
Udin, S.B. & Keating, M.J. (1981). Plasticity in a central nervous pathway in Xenopus: Anatomical changes in the isthmotectal projection after larval eye rotation. Journal of Comparative Neurology 203, 575594.Google Scholar
Udin, S.B. & Scherer, W.J. (1990). Restoration of the plasticity of binocular maps by NMDA after the critical period in Xenopus. Science 249, 669672.CrossRefGoogle ScholarPubMed
Williams, J.H., Errington, M.L., Lynch, M.A. & Bliss, T.V.P. (1989). Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341, 739742.CrossRefGoogle ScholarPubMed