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Development of the nucleus isthmi in Xenopus, II: Branching patterns of contralaterally projecting isthmotectal axons during maturation of binocular maps

Published online by Cambridge University Press:  02 June 2009

Susan B. Udin
Susan B. Udin
Affiliation:
Department of Physiology, State University of New York, Buffalo
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Abstract

The tectum of Xenopus frogs receives input from both eyes. The contralateral eye's projection reaches the tectum directly, via the optic nerve, and the ipsilateral eye's projection reaches the tectum indirectly, via the nucleus isthmi. Under normal conditions, the topography of the ipsilateral map relayed from the nucleus isthmi is in register with the topography of the retinotectal map from the contralateral eye. During development, the process of aligning the two maps is complicated by the dramatic changes in binocular overlap of the two eyes' visual fields which take place during late tadpole and juvenile stages. The goal of this study is to determine the branching patterns of contralaterally projecting isthmotectal axons before, during, and after the period of rapid eye migration.

Isthmotectal axons were filled by anterograde transport of horseradish peroxidase (HRP) from the nucleus isthmi. The results show that crossed isthmotectal axons enter the entire extent of the tectum before binocular overlap begins to increase. Therefore, binocular overlap is not necessary for the initial isthmotectal projection to span the tectum. The density of isthmotectal branches rises dramatically at the same time that the eyes begin to shift. During the period when eye migration is most rapid, many isthmotectal axons form arbors which resemble adult arbors but which extend over greater proportions of the tectal surface.

The axons appear to be directed toward appropriate mediolateral positions as they enter the tectum. Their trajectories are roughly rostocaudal, with relatively little change along the mediolateral dimension. These data, when combined with available physiological data, suggest that mediolateral order is initially established by vision-independent mechanisms but can be altered by vision-dependent mechanisms. Rostrocaudal order becomes discernable only at the time when binocular visual cues become available and appears to be established primarily on the basis of the activity of the retinotectal and isthmotectal axons.

Keywords

FrogNucleus isthmiDevelopmentArborizationBinocular vision
Type
Research Articles
Information
Visual Neuroscience , Volume 2 , Issue 2 , February 1989 , pp. 153 - 163
Copyright
Copyright © Cambridge University Press 1989

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References

Adams, J.C. (1981). Heavy-metal intensification of DAB-based HRP reaction product. Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Pettigrew, J.D. (1971). Lack of specificity of neurones in the visual cortex of young kittens. Journal of Physiology 218, 98–100.Google Scholar
Beazley, L.D. (1975). Development of intertectal neuronal connections in Xenopus: the effects of contralateral transposition of the eye and of eye removal. Experimental Brain Research 23, 505–518.Google Scholar
Beazley, L., Keating, J.M. & Gaze, R.M. (1972). The appearance, during development, of responses in the optic tectum following visual stimulation of the ipsilateral eye in Xenopus laevis. Vision Research 12, 407–410.Google Scholar
Berman, N. & Payne, B.R. (1983). Alterations in connections of the corpus callosum following convergent and divergent strabismus. Brain Research 274, 201–212.Google Scholar
Chung, S.H., Bliss, T.V.P. & Keating, M.J. (1974). The synaptic organization of optic afferents in the amphibian tectum. Proceedings of Royal Society B (London) 187, 421–447.Google Scholar
Dowben, R.M. & Rose, J.E. (1953). A metal-filled microelectrode. Science 118, 22–24.Google Scholar
Dunlop, S.A. & Beazley, L.D. (1984). A morphometric study of the retinal ganglion cell layer and optic nerve from metamorphosis in Xenopus laevis. Vision Research 24, 417–427.Google Scholar
Easter, S.S. & Stuermer, C.A.O. (1984). An evaluation of the hypothesis of shifting terminals in goldfish optic tectum. Journal of Neuroscience 4, 1052–1063.CrossRefGoogle ScholarPubMed
Elberger, A.J., Smith, E.L. & White, J.M. (1983). Spatial dissociation of visual inputs alters the origin of the corpus callosum. Neuroscience Letters 35, 19–24.Google Scholar
Frank, E., Harris, W.A. & Kennedy, B.M. (1980). Lysophosphatidyl choline facilitates labeling of CNS projections with horseradish peroxidase. Journal of Neuroscience Methods 2, 183–189.Google Scholar
Fraser, S.E. (1983). Fiber optic mapping of the Xenopus visual system: shift in the retinotectal projection during development. Developmental Biology 95, 505–511.Google Scholar
Freeman, J.A. (1977). Possible regulatory function of acetylcholine. Nature 269, 218–222.CrossRefGoogle ScholarPubMed
Gaze, R.M., Chung, S.-H. & Keating, M.J. (1972). Development of the retinotectal projection in Xenopus. Nature (New Biology) 236, 133–135.Google Scholar
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, 273–280.Google Scholar
Gaze, R.M., Keating, M.J., Sźekely, G., & Beazley, L. (1970). Binocular interaction in the formation of specific intertectal neuronal connexions. Proceedings of Royal Society B (London) 175, 107–147.Google ScholarPubMed
George, S.A. & Marks, W.B. (1974). Optic nerve terminal arborizations in the frog: shape and orientation inferred from electrophysiological measurements. Experimental Neurology 42, 467–482.Google Scholar
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, 214–218.CrossRefGoogle Scholar
Grant, S. (1982). The development and modification of binocular neuronal connections in Xenopus laevis. Ph.D. Thesis, University of London, 405 pp.Google Scholar
Grant, S. & Keating, M.J. (1986). Normal maturation involves systematic changes in binocular visual connections in Xenopus laevis. Nature 322, 258–261.Google Scholar
Graybiel, A.M. & Devor, M. (1974). A microelectrophoretic delivery technique for use with horseradish peroxidase. Brain Research 68, 167–173.Google Scholar
Grobstein, P. & Comer, C. (1977). Post-metamorphic eye migration in Rana and Xenopus. Nature 269, 54–56.Google Scholar
Grobstein, P. & Comer, C. (1983). The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frog. Rana pipiens. Journal of Comparative Neurology 217, 54–74.Google Scholar
Grobstein, P., Comer, C., Hollyday, M. & Archer, S.M. (1978). A crossed isthomtectal projection in Rana pipiens and its involvement in the ipsilateral visuo-tectal projection. Brain Research 156, 117–123.CrossRefGoogle Scholar
Gruberg, E.R. & Lettvin, J.Y. (1980). Anatomy and physiology of a binocular system in the frog, Rana pipiens. Brain Research 192, 313–325.Google Scholar
Gruberg, E.R. & Udin, S.B. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog, Rana pipiens. Journal of Comparative Neurology 179, 487–500.Google Scholar
Holt, C.E. & Harris, W.A. (1983). Order in the initial retinotectal map in Xenopus: a new technique for labeling growing nerve fibres. Nature 301, 150–152.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Innocenti, G.M. & Frost, D.O. (1979). Effects of visual experience on the maturation of the efferent system to the corpus callosum. Nature 280, 231–233.Google Scholar
Keating, M.J. (1974). The role of visual function in the patterning of binocular visual connections. British Medical Bulletin 30, 145–151.CrossRefGoogle 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, 445–466.Google ScholarPubMed
Keating, M.J. & Feldman, J. (1975). Visual deprivation and intertectal neuronal connections in Xenopus laevis. Proceedings of the Royal Society B (London) 191, 467–474.Google ScholarPubMed
Keating, M.J. & Gaze, R.M. (1970). The depth distribution of visual units in the contralateral optic tectum following regeneration of the optic nerve in the frog. Brain Research 21, 197–206.Google Scholar
Keating, M.J. & Kennard, C. (1978). The effect of visual deprivation on the maturation of neuronal connections in the visual system of Xenopus. Neuroscience Letters (Suppl.) 1, 392.Google Scholar
Koenig, E., Kinsman, S., Repasky, E. & Sultz, L. (1985). Rapid mobility of motile varicosities and inclusions containing spectrin, actin, and calmodulin in regenerating axons in vitro. Journal of Neuroscience 5, 715–729.Google Scholar
Lázár, G.y. (1973). The development of the optic tectum in Xenopus laevis: a Golgi study. Journal of Anatomy 116, 347–355.Google Scholar
Lund, R.D., Mitchell, D.E. & Henry, G.H. (1978). Squint-induced modification of callosal connections in cats. Brain Research 144, 169–172.Google Scholar
Meyer, R.L. (1983). Tetrodotoxin inhibits the formation of refined retinotopography in goldfish. Developmental Brain Research 6, 293–298.Google Scholar
Murray, M. (1976). Regeneration of retinal axons into goldfish optic tectum. Journal of Comparative Neurology 168, 175–196.CrossRefGoogle ScholarPubMed
Nieuwkoop, P.D. & Faber, J. (1967). Normal Table of Xenopus laevis (Daudin), 2nd Edition. Amsterdam: North Holland.Google Scholar
Niu, M.C. & Twitty, V. (1953). The differentiation of gastrula ectoderm in medium conditioned by axial mesoderm. Proceedings of the National Academy of Sciences, USA 39, 985–989.Google Scholar
Potter, H.D. (1969). Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana). Journal of Comparative Neurology 136, 203–232.Google Scholar
Reh, T.A. & Constantine-Paton, M. (1983). Qualitative and quantitative measures of plasticity during the normal development of the Rana pipiens retinotectal projection. Developmental Brain Research 10, 187–200.Google Scholar
Sachs, G.M., Jacobson, M. & Caviness, V.S. (1986). Postnatal changes in arborization patterns of murine retinocollicular axons. Journal of Comparative Neurology 246, 395–408.CrossRefGoogle ScholarPubMed
Sakaguchi, D.S. & Murphey, R.K. (1985). Map formation in the developing Xenopus retinotectal system: an examination of ganglion cell arborizations. Journal of Neuroscience 5, 3228–3245.Google Scholar
Schmidt, J.T. (1979). The laminar organization of optic nerve fibres in the tectum of goldfish. Proceedings of the Royal Society B (London) 205, 287–306.Google Scholar
Schmidt, J.T. & Edwards, D.L. (1983). Activity sharpens the map during the regeneration of the retinotectal projection in goldfish. Brain Research 209, 29–39.Google Scholar
Schneider, G.E. & Jhaveri, S. (1984). Rapid postnatal establishment of topography in the hamster retinotectal projection. Society for Neuroscience Abstracts 10, 467.Google Scholar
Shlaer, R. (1971). Shift in binocular disparity causes compensatory change in the cortical structure of kittens. Science 173, 638–641.Google Scholar
Sperry, R.W. (1944). Optic nerve regeneration with return of vision in anurans. Journal of Neurophysiology 7, 57–69.CrossRefGoogle Scholar
Sretavan, D. & Shatz, C.J. (1984). Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 306, 845–848.CrossRefGoogle Scholar
Sretavan, D. & Shatz, C.J. (1987). Axon trajectories and pattern of terminal arborization during the prenatal development of the cat's retinogeniculate pathway. Journal of Comparative Neurology 255, 386–400.CrossRefGoogle ScholarPubMed
Straznicky, C. & Hiscock, J. (1984). Post-metamorphic retinal growth in Xenopus. Anatomy and Embryology 169, 103–109.CrossRefGoogle ScholarPubMed
Udin, S. (1975). Regeneration and plasticity in the visual system of Rana pipiens. Ph.D. Thesis, Massachusetts Institute of Technology, 214 pp.Google Scholar
Udin, S. (1983). Abnormal visual input leads to development of abnormal axon trajectories in frogs. Nature 301, 336–338.Google Scholar
Udin, S.B. (1984). The morphology of isthmotectal axon arbors in developing Xenopus frogs. Society for Neuroscience Abstracts 10, 1033.Google Scholar
Udin, S.B. (1985). The role of visual experience in the formation of binocular projections in frogs. Cellular and Molecular Neurobiology 5, 85–102.Google Scholar
Udin, S.B. (1986 a). The development of the map from the nucleus isthmi—the influence of visual experience on the formation of orderly connections in the visual system. In Cell and Developmental Biology of the Eye, Vol. 5: Development of Order in the Visual System, ed. Hilfer, S.R. & Sheffield, J.B., pp. 15–34. New York: Springer-Verlag.Google Scholar
Udin, S.B. (1986 b). Electron microscopy of crossed isthmotectal axons in Xenopus. Society for Neuroscience Abstracts 12, 1028.Google Scholar
Udin, S. & Fisher, M.D. (1983). Visualization of HRP-filled axons in unsectioned, flattened optic tecta of frogs. Journal of Neuroscience Methods 9, 283–285.Google Scholar
Udin, S.B. & fisher, M.D. (1985). The development of the nucleus isthmi in Xenopus laevis, I: Cell genesis and the formation of connections with the tectum. Journal of Comparative Neurology 232, 25–35.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, 575–594.Google Scholar