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The optic tract in embryonic hamsters: Fasciculation, defasciculation, and other rearrangements of retinal axons

Published online by Cambridge University Press:  02 June 2009

Sonal Jhaveri ,
Reha S. Erzurumlu  and
Gerald E. Schneider
Sonal Jhaveri
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
Reha S. Erzurumlu
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
Gerald E. Schneider
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
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Abstract

The early development of the optic tract in hamsters was studied by labeling retinal axons with Dil applied to the eye, and then examining the labeled axons in flatmount preparations of the rostral brain stem. This technique permits a panoramic view of the entire retinal projection, from the chiasm to the caudal end of the superior colliculus. In the Ell embryo, retinal axons have reached the chiasm. They defasciculate as they emerge from the nerve, prior to reaching the ventral midline of the diencephalon, then converge again as they pass over to the opposite side. At the midline, many axonal trajectories crisscross, implying some shuffling of relative positions. Retinal axons are tightly bundled within the optic tract. Upon reaching the ventral border of the lateral geniculate body (LGB), they splay out over the nucleus, revealing a wavefront of pioneer axons individually distributed across the rostro-caudal extent of the LGB. Later-emerging retinal axons course over the surface of the thalamus in waves; subsequent waves of axons interdigitate between the lead fibers without fasciculating along them. Past the LGB, the axons undergo a second change in relative positions as the ribbon of fibers swerves caudally, prior to entering the superior colliculus. Retinal axons are tipped with growth cones of varying morphologies. No strong correlation is evident between the Structural complexity of the growth cone and its position within the tract. In the majority of cases, ipsilaterally and contralaterally directed axons follow a similar developmental course along the optic tract, without any indication of a temporal lag in the ipsilateral projection as claimed in earlier reports. Understanding the changes in spatial distribution of embryonic retinal axons as they navigate along the optic tract provides a further step towards elucidating how point-to-point projections form in developing sensory systems.

Keywords

ChiasmGrowth conesPioneer axonsLateral geniculate bodySuperior colliculusDil
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 359 - 374
Copyright
Copyright © Cambridge University Press 1996

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References

Baker, G.E. (1990). Prechiasmatic reordering of fibre diameter classes in the retinofugal pathway of ferrets. European Journal of Neuroscience 2, 24–33.CrossRefGoogle ScholarPubMed
Bhide, P.G. & Frost, D.O. (1991). Stages of growth of hamster retinofugal axons: Implications for developing axonal pathways with multiple targets. Journal of Neuroscience 11, 485–504.CrossRefGoogle ScholarPubMed
Bovolenta, P. & Mason, C. (1987). Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. Journal of Neuroscience 7, 1447–1460.CrossRefGoogle ScholarPubMed
Bunt, S.M. & Horder, T.J. (1983). Evidence for an orderly arrangement of optic axons within the optic nerves of the major nonmammalian vertebrate classes. Journal of Comparative Neurology 213, 94–114.CrossRefGoogle ScholarPubMed
Bunt, S.M., Lund, R.D. & Land, P.W. (1983). Prenatal development of the optic projection in albino and hooded rats. Developmental Brain Research 6, 149–168.CrossRefGoogle Scholar
Cavalcante, L.A. & Rocha-Miranda, C.E. (1978). Postnatal development of retinogeniculate, retinopretectal and retinotectal projections in the opossum. Brain Research 146, 231–248.CrossRefGoogle ScholarPubMed
Cohen, J., Burne, J.F., McKinlay, C. & Winter, J. (1987). The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons. Experimental Biology 122, 407–418.Google ScholarPubMed
Colello, R.J. & Guillery, R.W. (1990). The early development of retinal ganglion cells with uncrossed axons in the mouse: Retinal position and axonal course. Development 108, 515–523.CrossRefGoogle ScholarPubMed
Crossland, W.J. & Uchwat, C.J. (1982). Neurogenesis in the central visual pathways of the golden hamster. Developmental Brain Research 5, 99–103CrossRefGoogle Scholar
Cucchiaro, J. & Guillery, R.W. (1984). The development of the retinogeniculate pathways in normal and albino ferrets. Proceedings of the Royal Society B (London) 223, 141–164.Google ScholarPubMed
Drager, U.C. (1985). Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proceedings of the Royal Society B (London) 224, 57–77.Google Scholar
Edwards, M.A., Caviness, V.S. Jr. & Schneider, G.E. (1986 a). Development of cell and fiber lamination of the mouse superior colliculus. Journal of Comparative Neurology 248, 395–409.CrossRefGoogle ScholarPubMed
Edwards, M.A., Schneider, G.E. & Caviness, V.S. Jr. (1986 b). Development of the crossed retinocollicular projection in the mouse. Journal of Comparative Neurology 248, 410–421CrossRefGoogle ScholarPubMed
Erzurumlu, R.S., Jhaveri, S. & Schneider, G.E. (1990). The use of brainstem flat-mounts for visualizing Dil filled axons in the developing rodent visual system. Journal of Neuroscience Methods 33, 81–89.CrossRefGoogle Scholar
Frost, D.O., So, K.-F. & Schneider, G.E. (1979). Postnatal development of retinal projections in Syrian hamsters: A study using auto-radiographic and anterograde degeneration techniques. Neuroscience 4, 1649–1677.CrossRefGoogle Scholar
Fujisawa, H. (1987). Axonal growth in developing and regenerating amphibian retinotectal projection. Progress in Brain Research 71, 75–88.CrossRefGoogle ScholarPubMed
Godement, P., Salaun, J. & Imbert, M. (1984). Prenatal and post-natal development of retinogeniculate and retinocollicular projections in the mouse. Journal of Comparative Neurology 230, 552–575.CrossRefGoogle Scholar
Godement, P., Vanselow, J., Thanos, S. & Bonhoeffer, F. (1987). A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101, 697–713.CrossRefGoogle ScholarPubMed
Godement, P., Salaun, J. & Mason, C.A. (1990). Retinal axon path-finding in the optic chiasm: Divergence of crossed and uncrossed fibers. Neuron 5, 173–186.CrossRefGoogle Scholar
Hall, D.E., Neugebauer, K.M. & Reichardt, L.F. (1987). Embryonic neural retinal cell response to extracellular matrix proteins: Developmental changes and effects of the cell substratum attachment antibody (CSAT). Journal of Cell Biology 104, 623–634.CrossRefGoogle ScholarPubMed
Hammarback, J.A., McCarthy, J.B., Palm, S.L., Furcht, L.T. & Letourneau, P.C. (1988). Growth cone guidance by substrate-bound laminin pathways is correlated with neuron-to-pathway adhesivity. Developmental Biology 126, 29–221.CrossRefGoogle ScholarPubMed
Hankin, M.H. & Lund, R.D. (1990). Induction of target-directed optic axon outgrowth: Effect of retinae transplanted to anophthalmic mice. Developmental Biology 138, 136–146.CrossRefGoogle ScholarPubMed
Harris, W.A. (1986). Homing behaviour of axons in the embryonic vertebrate brain. Nature 320, 266–269.CrossRefGoogle ScholarPubMed
Harris, W.A. (1989). Local positional cues in the neuroepithelium guide retinal axons in embryonic Xenopus brain. Nature 339, 218–221.CrossRefGoogle ScholarPubMed
Hayhow, W.R., Webb, C. & Jervine, A. (1960). The accessory optic fibers in the rat. Journal of Comparative Neurology 115, 187–215.CrossRefGoogle ScholarPubMed
Holt, C. (1991). Pathfinding and specificity in the early Xenopus retinofugal projection. In Development of the Visual System, Proceedings of the Retina Research Foundation Symposia, Vol. 3, ed. Lam, D. & Shatz, C.J., pp. 109–122. Cambridge, Massachusetts: MIT Press.Google Scholar
Honig, M. & Hume, R. (1986). Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. Journal of Cell Biology 103, 171–187.CrossRefGoogle ScholarPubMed
Horton, J.C., Greenwood, M.M. & Hubel, D.H. (1979). Non-retinolopic arrangement of fibers in cat optic nerve. Nature 282, 720–722.CrossRefGoogle ScholarPubMed
Jhaveri, S. (1973). Altered retinal connections following partial tectum lesions in neonate hamsters. M.S. Thesis, Massachusetts Institute of Technology, Cambridge, Massachusetts.Google Scholar
Jhaveri, S., Edwards, M.A. & Schneider, G.E. (1983). Relationship of lateral geniculate neuron migration to stages of optic tract growth in the hamster. Society for Neuroscience Abstracts 9, 702.Google Scholar
Jhaveri, S., Schneider, G.E. & Erzurumlu, R.S. (1991 a). Axonal plasticity in the context of development. In Vision and Visual Dysfunction: Vol.II, Development and Plasticity of the Visual System, ed. Cronly-Dillon, J.R., pp. 232–256. London: Macmillan Press.Google Scholar
Jhaveri, S., Edwards, M.A. & Schneider, G.E. (1991 b). Initial stages of retinofugal axon development in the hamster: Evidence for two distinct modes of growth. Experimental Brain Research 87, 371–382.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1988). Development of retino-geniculate axon arbors in a primate. Visual Neuroscience 1, 103–123.CrossRefGoogle Scholar
Landmesser, L., Dahm, L., Schultz, K. & Rutishauser, U. (1988). Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Developmental Biology 130, 645–670.CrossRefGoogle ScholarPubMed
Landmesser, L., Dahm, L., Tang, J. & Rutishauser, U. (1990). Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 4, 655–667.CrossRefGoogle ScholarPubMed
Langdon, R.B. & Frost, D.O. (1991). Transient retinal axon collaterals to visual and somatosensory thalamus in neonatal hamsters. Journal of Comparative Neurology 310, 200–214.CrossRefGoogle ScholarPubMed
Lemmon, V. & McLoon, S.C. (1986). The appearance of an Ll-like molecule in the chick primary visual pathway. Journal of Neuroscience 6, 2987–2994.CrossRefGoogle Scholar
Lund, R.D. & Bunt, A.H. (1976). Prenatal development of the central optic pathways in the albino rats. Journal of Comparative Neurology 165, 247–274.CrossRefGoogle ScholarPubMed
McLoon, S.C., McLoon, L.K., Palm, S.L. & Furcht, L.T. (1986). Transient expression of laminin in the optic nerve of the developing rat. Journal of Neuroscience 8, 1981–1990.CrossRefGoogle Scholar
Norris, C.R. & Kalil, K (1990). Morphology and cellular interactions of growth cones in the developing corpus callosum. Journal of Comparative Neurology 293, 268–281.CrossRefGoogle ScholarPubMed
O'leary, D.D.M. & Terashima, T. (1988). Cortical axons branch to multiple subcortical targets by interstitial axon budding: Implications for target recognition and “waiting periods”. Journal of Neuroscience 1, 901–910.Google ScholarPubMed
Rakic, P. (1977). Prenatal development of the visual system in rhesus monkey. Philosophical Transactions of the Royal Society B (London) 278, 245–260.Google ScholarPubMed
Reese, B.E. & Baker, G.E. (1990). The course of fibre diameter classes through the chiasmatic region in the ferret. European Journal of Neuroscience 2, 34–49.CrossRefGoogle ScholarPubMed
Reese, B.E. & Cowey, A. (1990). Fibre organization of the monkey's optic tract: I. Segregation of functionally distinct optic axons. Journal of Comparative Neurology 295, 385–400.CrossRefGoogle ScholarPubMed
Rutishauser, U. (1985). Influences of the neural cell adhesion molecule on axon growth and guidance. Journal of Neuroscience Research 13, 123–131.CrossRefGoogle ScholarPubMed
Rutishauser, U. & Jessell, T.M. (1988). Cell adhesion molecules in vertebrate neural development. Physiological Reviews 68, 819–857.CrossRefGoogle ScholarPubMed
Sachs, G.M., Jacobson, M. & Caviness, V.S. Jr. (1986). Postnatal changes in the pattern of arborization of murine retinocollicular axons. Journal of Comparative Neurology 246, 395–408.CrossRefGoogle ScholarPubMed
Scalia, F. & Fite, K. (1974). A retinotopic analysis of the central connections of the optic nerve in the frog. Journal of Comparative Neurology 158, 455–478.CrossRefGoogle ScholarPubMed
Schneider, G.E. & Jhaveri, S.R. (1974). Neuroanatomical correlates of spared or altered function after brain lesions in the newborn hamster. In Plasticity and Recovery of Function in the Central Nervous System, ed. Stein, D.G., Rosen, J.J. & Butters, N., pp. 65–109. New York, Academic Press.Google Scholar
Schneider, G.E. & Jhaveri, S. (1983). Projections of the internal optic tract: Retinal projections which survive superficial thalamic lesions in hamsters. Society for Neuroscience Abstracts 9, 809.Google Scholar
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Silver, J. & Robb, R.M. (1979). Studies on the development of the eye cup and optic nerve in normal mice and in mutants with congenital optic nerve aplasia. Developmental Biology 68, 175–190.CrossRefGoogle ScholarPubMed
Silver, J. & Rutishauser, U. (1984). Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithelial endfeet. Developmental Biology 106, 485–499.CrossRefGoogle ScholarPubMed
Silver, J. & Sapiro, J. (1981). Axonal guidance during development of the optic nerve: The role of pigmented epithelium and other extrinsic factors. Journal of Comparative Neurology 202, 521–538.CrossRefGoogle ScholarPubMed
Silver, J. & Sidman, R.L. (1980). A mechanism for the guidance and topographic patterning of retinal ganglion cell axons. Journal of Comparative Neurology 189, 101–111.CrossRefGoogle ScholarPubMed
Simon, D.K. & O'Leary, D.D.M. (1990). Limited topographic specificity in the targeting and branching of mammalian retinal axons. Developmental Biology 137, 125–134.CrossRefGoogle ScholarPubMed
Simon, D.K. & O'Leary, D.D.M. (1992). Influence of position along the medial-lateral axis of the superior colliculus on the topographic targeting and survival of retinal axons. Developmental Brain Research 69, 167–172.CrossRefGoogle ScholarPubMed
Singer, M., Nordlander, R.H. & Egar, M. (1979). Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt. The Blueprint hypothesis of neuronal pathway patterning. Journal of Comparative Neurology 185, 1–22.CrossRefGoogle ScholarPubMed
So, K.-F., Schneider, G.E. & Frost, D.O. (1978). Postnatal development of retinal projections to the lateral geniculate body in Syrian hamsters. Brain Research 142, 342–352.CrossRefGoogle Scholar
So, K.-F., Woo, H.H. & Jen, L.S. (1984). The normal and abnormal postnatal development of retinogeniculate projections in golden hamsters: An anterograde horseradish peroxidase tracing study. Developmental Brain Research 12, 191–205.CrossRefGoogle Scholar
Sretavan, D.W. (1990). Specific routing of retinal ganglion cell axons at the mammalian optic chiasm during embryonic development. Journal of Neuroscience 10, 1995–2005.CrossRefGoogle ScholarPubMed
Sretavan, D.W. & Shatz, C.J. (1986). Prenatal development of retinal ganglion cell axons: Segregation into eye-specific layers within the cat's lateral geniculate nucleus. Journal of Neuroscience 6, 234–251.CrossRefGoogle ScholarPubMed
Taylor, J.S.H. (1990). The directed growth of retinal axons towards surgically transposed tecta in Xenopus—An examination of homing behaviour by retinal ganglion cell axons. Development 108, 147–158.CrossRefGoogle ScholarPubMed
Terubayashi, H. & Fujisawa, H. (1984). The accessory optic system of rodents: A wholemount HRP study. Journal of Comparative Neurology 227, 285–295.CrossRefGoogle ScholarPubMed
Torrealba, F., Guillery, R.W., Eysel, U., Polley, E.H. & Mason, C.A. (1982). Studies of retinal representations within the cat's optic tract. Journal of Comparative Neurology 211, 377–396.CrossRefGoogle ScholarPubMed
Tosney, K.W. & Landmesser, L.T. (1985). Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. Journal of Neuroscience 5, 2345–2358.CrossRefGoogle ScholarPubMed
Walsh, C. (1986). Age-related fiber order in the ferret's optic nerve and optic chiasm. Journal of Neuroscience 6, 1635–1642.CrossRefGoogle ScholarPubMed
Walsh, C. & Guillery, R.W. (1985). Age-related fiber order in the optic tract of the ferret. Journal of Neuroscience 5, 3061–3069.CrossRefGoogle ScholarPubMed
Williams, R.W. & Chalupa, L.M. (1982). Prenatal development of retinocollicular projections in the cat: An anterograde tracer transport study. Journal of Neuroscience 3, 133–144.CrossRefGoogle Scholar
Williams, R.W. & Rakic, P. (1985). Dispersion of growing axons within the optic nerve of the embryonic monkey. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3906–3910.CrossRefGoogle ScholarPubMed
Wu, D.Y., Jhaveri, S. & Schneider, G.E. (1989). Recrossing of retinal axons after early tectal lesions in hamsters occurs only where vimentin- and GFAP-positive midline cells are damaged. Society for Neuroscience Abstracts 15, 873.Google Scholar
Wu, D.Y., Schneider, G.E. & Jhaveri, S. (1990). Retinotectal axons cross to the wrong side following disruption of tectal midline cells in the hamster. Society for Neuroscience Abstracts 16, 336.Google Scholar
Wu, D.-Y., Silver, J., Schneider, G.E. & Jhaveri, S. (1991). The barrier function of tectal midline glial cells and its association with proteoglycan distribution. Society for Neuroscience Abstracts 17, 740.Google Scholar