Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T12:32:35.411Z Has data issue: false hasContentIssue false
  • English
  • Français

The re-establishment of the representation of the dorso-ventral retinal axis in the chiasmatic region of the ferret

Published online by Cambridge University Press:  02 June 2009

Benjamin E. Reese  and
Gary E. Baker
Benjamin E. Reese
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara
Gary E. Baker
Affiliation:
W.M. Keck Center for Integrative Neuroscience and Department of Physiology, University of California at San Francisco
Get access Rights & Permissions [Opens in a new window]

Abstract

This study has examined the representation of the dorso-ventral retinal axis in the optic nerve and tract of the ferret, as well as the associated fiber transformations which take place within the chiasmatic region. In one series of experiments, dorsal or ventral retinal lesions were made to induce fiber degeneration along the pathway, from which semi-thin sections were then stained for degenerating myelin. In a second series, implants of the carbocyanine dye, Dil, were made into the caudo-medial or rostro-lateral optic tract in order to label retrogradely the axons as they course through the chiasmatic region. Additional observations were made from the optic pathways of ferrets that had been similarly lesioned or implanted, but employing either a reduced-silver technique to reveal the degenerating axons or horseradish peroxidase as the retrograde label.

The axons arising from the dorsal and ventral retina course in the dorsal and ventral parts of the optic nerve posterior to the eye, but as they continue along the nerve they disperse producing a highly impoverished retinotopy in the prechiasmatic portion of the nerve. As they course through the chiasmatic region, however, they become segregated again: dorsal fibers cross the midline relatively caudally while ventral fibers cross further rostrally, although there is overlap between them. Nearer the threshold of the optic tract, the fibers from dorsal and ventral retina undergo a further and more striking segregation, placing the dorsal fibers caudo-medially and the ventral fibers rostro-laterally within the tract. This re-emergence of retinotopic order implicates a fiber-substrate interaction as being responsible for the axonal reordering, and suggests that fiber pre-ordering in the tract contributes to the formation of the orderly projection of the dorso-ventral retinal axis upon central visual targets.

Keywords

Optic nerveOptic chiasmOptic tractRetinal ganglion cellFiber orderRetinotopy
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 5 , September 1993 , pp. 957 - 968
Copyright
Copyright © Cambridge University Press 1993

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

Aebersold, H., Creutzfeldt, O.D., Kuhnt, U. & Sanides, D. (1981). Representation of the visual field in the optic tract and optic chiasma of the cat. Experimental Brain Research 42, 127–145.Google Scholar
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
Baker, G.E. & Jeffery, G. (1989). Distribution of uncrossed axons along the course of the optic nerve and chiasm of rodents. Journal of Comparative Neurology 289, 455–461.Google Scholar
Baker, G.E. & Reese, B.E. (1993). Using confocal laser scanning microscopy to investigate the organization and development of neuronal projections labelled with Dil. In Methods in Cell Biology: Cell Biological Applications of Confocal Microscopy, ed. Matsumoto, B., Orlando, Florida: Academic Press (in press).Google Scholar
Bonhoeffer, F. & Huf, J. (1985). Position-dependent properties of retinal axons and their growth cones. Nature 315, 409–411.Google Scholar
Bunt, S.M. (1982). Retinotopic and temporal organization of the optic nerve and tracts in the adult goldfish. Journal of Comparative Neurology 206, 209–226.CrossRefGoogle ScholarPubMed
Constantine-Paton, M., Blum, A.S., Mendez-Otero, R. & Barn-Stable, C.J. (1986). A cell surface molecule distributed in a dorso-ventral gradient in the perinatal rat retina. Nature 324, 459–462.CrossRefGoogle Scholar
Eysel, U.T. & Wolfhard, U. (1983). Morphological fine tuning of ret-inotopy within the cat lateral geniculate nucleus. Neuroscience Letters 39, 15–20.Google Scholar
Fink, R.P. & Heimer, L. (1967). Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Research 4, 369–374.CrossRefGoogle ScholarPubMed
Fitzgibbon, T. & Burke, W. (1989). Representation of the temporal raphe within the optic tract of the cat. Visual Neuroscience 2, 255–267.Google Scholar
Guillery, R.W., Polley, E.H. & Torrealba, F. (1982). The arrangement of axons according to fiber diameter in the optic tract of the cat. Journal of Neuroscience 2, 714–721.Google Scholar
Hanker, J.S., Yates, P.E., Metz, C.B. & Rustioni, A.J. (1977). A new, specific, and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochemistry Journal 9, 789–792.Google Scholar
Hollander, H. & Vaaland, J.L. (1968). A reliable staining method for semi-thin sections in experimental neuroanatomy. Brain Research 10, 120–126.Google Scholar
Horton, J.C., Greenwood, M.M. & Hubel, D.H. (1979). Nonretinotopic arrangement of fibres in cat optic nerve. Nature 282, 720–722.Google Scholar
Hoyt, W.F. & Luis, O. (1962). Visual fiber anatomy in the infrageniculate pathway of the primate: Uncrossed and crossed retinal quadrant fiber projections studied with Nauta silver stain. Archives of Ophthalmology 68, 94–106.CrossRefGoogle Scholar
Hoyt, W.F. & Luis, O. (1963). The primate chiasm. Archives of Ophthalmology 69, 69–85.CrossRefGoogle Scholar
Maggs, A. & Scholes, J. (1986). Glial domains and nerve fiber patterns in the fish retinotectal pathway. Journal of Neuroscience 6, 424–438.CrossRefGoogle ScholarPubMed
Marotte, L.R. & Mark, R.F. (1988). Retinal projections to the superior colliculus and dorsal lateral geniculate nucleus in the tammar wallaby (Macropus eugenii): II. Topography after rotation of an eye prior to retinal innervation of the brain. Journal of Comparative Neurology 271, 274–292.Google Scholar
Naito, J. (1986). Course of retinogeniculate projection fibers in the cat optic nerve. Journal of Comparative Neurology 251, 376–387.CrossRefGoogle ScholarPubMed
Natto, J. (1989). Retinogeniculate projection fibers in the monkey optic nerve: A demonstration of the fiber pathways by retrograde axonal transport of WGA-HRP. Journal of Comparative Neurology 284, 174–186.Google Scholar
O'Leary, D.D.M., Fawcett, J.W. & Cowan, W.M. (1986). Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. Journal of Neuroscience 6, 3692–3705.Google Scholar
Rabacchi, S.A., Neve, R.L. & Dräger, U.C. (1990). A positional marker for the dorsal embryonic retina is homologous to the high-affinity laminin receptor. Development 109, 521–531.CrossRefGoogle Scholar
Racer, U., Rager, G. & Kabiersch, A. (1988). Transformations of the retinal topography along the visual pathway of the chicken. Anatomy and Embryology 179, 135–148.Google Scholar
Reese, B.E. (1986). The topography of expanded uncrossed retinal projections following neonatal enucleation of one eye: Differing effects in dorsal lateral geniculate nucleus and superior colliculus. Journal of Comparative Neurology 250, 8–32.Google Scholar
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.Google Scholar
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.Google Scholar
Reese, B.E. & Guillery, R.W. (1987). Distribution of axons according to diameter in the monkey's optic tract. Journal of Comparative Neurology 260, 453–460.Google Scholar
Reese, B.E., Guillery, R.W., Marzi, C.A. & Tassinari, G. (1991). Position of axons in the cat's optic tract in relation to their retinal origin and chiasmatic pathway. Journal of Comparative Neurology 306, 539–553.Google Scholar
Rusoff, A.C. & Easter, S.S. (1980). Order in the optic nerve of goldfish. Science 208, 311–312.Google Scholar
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of Histochemistry and Cytochemistry 36, 555–559.Google Scholar
Scholes, J.H. (1979). Nerve fibre topography in the retinal projection to the tectum. Nature 278, 620–624.Google Scholar
Simon, D.K. & O'Leary, D.D.M. (1991). Relationship of retinotopic ordering of axons in the optic pathway to the formation of visual maps in central targets. Journal of Comparative Neurology 307, 393–404.Google Scholar
Simon, D.K. & O'Leary, D.D.M. (1992 a). Development of topographic order in the mammalian retinocollicular projection. Journal of Neuroscience 12, 1212–1232.Google Scholar
Simon, D.K. & O'Leary, D.M. (1992 b). Responses of retinal axons in vivo and in vitro to position-encoding molecules in the embryonic superior colliculus. Neuron 9, 977–989.Google Scholar
Simon, D.K. & O'Leary, D.M. (1992 c). 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.Google Scholar
Springer, A.D. & Mednick, A.S. (1986). Simple and complex retinal ganglion cell axonal rearrangements at the optic chiasm. Journal of Comparative Neurology 247, 233–245.CrossRefGoogle ScholarPubMed
Stahl, B., Muller, B., Von Boxberg, Y., Cox, E.C. & Bonhoeffer, F. (1990). Biochemical characterization of a putative axonal guidance molecule of the chick visual system. Neuron 5, 735–743.Google Scholar
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
Trisler, D. & Collins, F. (1987). Corresponding spatial gradients of TOP molecules in the developing retina and optic tectum. Science 237, 1208–1209.Google Scholar
Voigt, T., Naito, J. & Wässle, H. (1983). Retinotopic scatter of optic tract fibres in the cat. Experimental Brain Research 52, 25–33.CrossRefGoogle ScholarPubMed
Walter, J., Kern-Veits, B., Huf, J., Stolze, B. & Bonhoeffer, F. (1987 a). Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101, 685–696.Google Scholar
Walter, J., Henke-Fahle, S. & Bonhoeffer, F. (1987 b). Avoidance of posterior tectal membranes by temporal retinal axons. Development 101, 909–913.CrossRefGoogle ScholarPubMed
Williams, R.W., Borodkin, M. & Rakic, P. (1991). Growth cone distribution patterns in the optic nerve of fetal monkeys: Implications for mechanisms of axon guidance. Journal of Comparative Neurology 11, 1081–1094.Google 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.Google Scholar
Zahs, K.R. & Stryker, M.P. (1985). The projection of the visual field onto the lateral geniculate nucleus of the ferret. Journal of Comparative Neurology 241, 210–224.Google Scholar