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Organization of retinal ganglion cell axons in the optic fiber layer and nerve of fetal ferrets

Published online by Cambridge University Press:  02 June 2009

T. Fitzgibbon  and
B. E. Reese
T. Fitzgibbon
Affiliation:
Department of Clinical Ophthalmology, University of Sydney, NSW, Australia
B. E. Reese
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara
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Abstract

Previous authors have hypothesized that retinotopic projections may be influenced by ‘preordering’ of the axons as they grow towards their targets. In some nonmammalian species, axons are reorganized at or near the optic nerve head to establish a retinotopic order. Data are ambiguous concerning the retinotopy of the mammalian retinal nerve fiber layer and whether fibers become reorganized at the optic nerve head. We have examined this question in fetal and newborn ferrets (Mustela putorius furo) by comparing the arrangement of axons in the retinal nerve fiber layer with that in the optic nerve. Dil or DiA crystals were implanted into fixed tissue in the innermost layers of the retinal periphery, or at a location midway between the periphery and the optic nerve head. Fluorescence labelling was examined in 100–200 μm Vibratome sections, or the eyecup and nerve were photooxidized and 1–2 μm longitudinal or transverse sections were examined. Regardless of fetal age, eccentricity or quadrant of the implant site, a segregation of labelled peripheral axons from unlabelled central ones was not detected within the nerve fiber layer. Axons coursed into the nerve head along the margin of their retinal quadrant of origin, often entering the optic nerve as a radial wedge, thus preserving a rough map of retinal circumference. However, peripheral axons were in no way restricted to the peripheral (nor central) portions of the nerve head or nerve, indicating that the optic axons do not establish a map of retinal eccentricity. Our results demonstrate that (1) the nerve fiber layer is retinotopic only with respect to circumferential position and (2) optic axons are not actively reorganized to establish a retinotopic ordering at the nerve head. The present results suggest that any degree of order present within the optic nerve is a passive consequence of combining the fascicles of the retinal nerve fiber layer; optic axons are not instructed to establish, nor constrained to maintain, a retinotopic order within the optic nerve.

Keywords

RetinotopyChronotopyOptic nerve headOptic chiasm
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 847 - 861
Copyright
Copyright © Cambridge University Press 1996

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References

Allodi, S., Cavalcante, L.A., Hokoc, J.N. & Bernardes, R.F. (1992). Genesis of neurons of the retinal ganglion cell layer in the opossum. Anatomy and Embryology 185, 489–499.CrossRefGoogle ScholarPubMed
Baier, H. & Bonhoeffer, F. (1992). Axon guidance by gradients of a target-derived component. Science 255, 472–475.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.CrossRefGoogle ScholarPubMed
Baker, G.E. & Reese, B.E. (1993 a). Chiasmatic course of temporal retinal axons in the developing ferret. Journal of Comparative Neurology 330, 95–104.CrossRefGoogle ScholarPubMed
Baker, G.E. & Reese, B.E. (1993 b). Using confocal laser scanning microscopy to investigate the organization and development of neu-ronal projections labeled with Dil. In Methods in Cell Biology: Cell Biological Applications of Confocal Microscopy, Vol. 38, ed. Matsumoto, B., pp. 325–344. Orlando, Florida: Academic Press, Inc.CrossRefGoogle Scholar
Bodick, N. & Levinthal, C. (1980). Growing optic nerve fibres follow neighbors during embryogenesis. Proceedings of the National Academy of Sciences of the U.S.A. 77, 4374–4378CrossRefGoogle ScholarPubMed
Brittis, P., Canning, D. & Silver, J. (1992). Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 225, 733–736.CrossRefGoogle Scholar
Brouwer, B. & Zeeman, W.P.C. (1926). The projection of the retina in the primary optic neuron in monkeys. Brain 49, 1–35.CrossRefGoogle Scholar
Bunt, S.M. & Horder, T.J. (1983). Evidence for an orderly arrangement of optic axons within the optic nerves of the major nonmam-malian vertebrate classes. Journal of Comparative Neurology 213, 94–114.CrossRefGoogle ScholarPubMed
Chan, S.O. & Guillery, R.W. (1994). Changes in fibre order in the optic nerve and tract of rat embryos. Journal of Comparative Neurology 344, 20–32.CrossRefGoogle 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
Colello, R.J. & Guillery, R.W. (1992). Observations on the early development of the optic nerve and tract of the mouse. Journal of Comparative Neurology 317, 357–378.CrossRefGoogle ScholarPubMed
Constantine-Paton, M., Cline, H.T. & Debski, E. (1990). Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Review of Neuroscience 13, 129–154.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B. (1991). Early development of the retinal line of decussation in normal and albino ferrets. Journal of Comparative Neurology 312, 193–206.CrossRefGoogle ScholarPubMed
Dräger, U. (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
Easter, S.S., Johns, P.R. & Baumann, L.R. (1977). Growth of the adult goldfish eye. I. Optics. Vision Research 17, 469–477.CrossRefGoogle ScholarPubMed
Easter, S.S., Bratton, B. & Scherer, S.S. (1984). Growth-related order in the retinal fibre layer in goldfish. Journal of Neuroscience 4, 2173–2190.CrossRefGoogle ScholarPubMed
Fawcett, J.W. (1981). How axons grow down the Xenopus optic nerve. Journal of Embryology and Experimental Morphology 65, 219–233.Google ScholarPubMed
FitzGibbon, T. & Burke, W. (1989). Representation of the temporal raphe within the optic tract of the cat. Visual Neuroscience 2, 255–267.CrossRefGoogle ScholarPubMed
FitzGibbon, T. & Reese, B.E. (1992). Position of growth cones within the retinal nerve fibre layer of fetal ferrets. Journal of Comparative Neurology 323, 153–166.CrossRefGoogle ScholarPubMed
Galli, L., Rao, K. & Lund, R.D. (1989). Transplanted rat retinae do not project in a topographic fashion on the host tectum. Experimental Brain Research 74, 427–430.CrossRefGoogle ScholarPubMed
Godement, P., Salaun, J. & Mason, C.A. (1990). Retinal axon path-finding in the optic chiasma: Divergence of crossed and uncrossed fibres. Neuron 5, 173–186.CrossRefGoogle Scholar
Goldberg, S. & Coulombre, A.J. (1972). Topographical development of the ganglion cell fibre layer in the chick retina. A wholemount study. Journal of Comparative Neurology 146, 507–518.CrossRefGoogle Scholar
Guillery, R.W. (1982). The optic chiasm of the vertebrate brain. Contributions to Sensory Physiology 7, 39–73.CrossRefGoogle Scholar
Guillery, R.W. & Walsh, C. (1987). Changing glial organization relates to changing fibre order in the developing optic nerve of ferrets. Journal of Comparative Neurology 265, 203–217.CrossRefGoogle ScholarPubMed
Henderson, Z., Finlay, B.L. & Wikler, K.C. (1988). Development of ganglion cell topography in ferret retina. Journal of Neuroscience 8, 1194–1205.CrossRefGoogle ScholarPubMed
Horder, T.J. & Martin, K.A.C. (1978). Morphogenetics as an alternative to chemospecificity in the formation of nerve connections. In Cell-Cell Recognition, Vol. 32, ed. Curtis, A.S.G., Society for Experimental Biology Symposium, pp. 275–358. Cambridge: Cambridge University Press.Google Scholar
Horton, J.C., Greenwood, M.M. & Hubel, D.H. (1979). Nonretinotopic arrangement of fibres in cat optic nerve. Nature 282, 720–722.CrossRefGoogle ScholarPubMed
Hoyt, W.F. & Luis, O. (1962). Visual fibre anatomy in the infrageniculate pathway of the primate: Uncrossed and crossed retinal quadrant fibre 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
Johns, P.R. (1977). Growth of the adult goldfish eye. III. Source of the new retinal cells. Journal of Comparative Neurology 176, 343–358.CrossRefGoogle ScholarPubMed
Krayanek, S. & Goldberg, S. (1981). Orientated extracellular channels and axonal guidance in the embryonic chick retina. Developmental Biology 84, 41–50.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.CrossRefGoogle Scholar
Meyer, R.L. (1978). Evidence from thymidine labeling for continued growth of retina and tectum in juvenile goldfish. Experimental Neurology 59, 99–111.CrossRefGoogle ScholarPubMed
Minckler, D.S. (1980). The organization of nerve fibre bundles in the primate optic nerve head. Archives of Ophthalmology 98, 1630–1636.CrossRefGoogle ScholarPubMed
Naito, J. (1986). Course of retinogeniculate projection fibres in the cat optic nerve. Journal of Comparative Neurology 251, 376–387.CrossRefGoogle ScholarPubMed
Naito, J. (1989). Retinogeniculate projection fibres in the monkey optic nerve: A demonstration of the fibre pathways by retrograde axonal transport of WGA-HRP. Journal of Comparative Neurology 284, 174–186.CrossRefGoogle ScholarPubMed
Naito, J. (1994). Retinogeniculate projection fibres in the monkey optic chiasm: A demonstration of the fibre arrangement by means of wheat germ agglutinin conjugated to horseradish peroxidase. Journal of Comparative Neurology 346, 559–571.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1982). Growth zone of the juvenile goldfish retina revealed by fluorescent flat mounts. Journal of Neuroscience Research 7, 321–330.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1983 a). Nerve fibre layer of the macaque retina: Retino-topic organization. Investigative Ophthalmology and Visual Science 24, 85–98.Google Scholar
Ogden, T.E. (1983 b). Nerve fibre layer of the owl monkey retina: Ret-inotopic organization. Investigative Ophthalmology and Visual Science 24, 265–269.Google ScholarPubMed
Ogden, T.E. (1984). Nerve fibre layer of the primate retina: Morpho-metric organization. Investigative Ophthalmology and Visual Science 25, 19–29.Google Scholar
Polyak, S. (1957). The Vertebrate Visual System. Chicago, Illinois: Chicago University Press.Google Scholar
Quigley, H.A. & Addicks, E.A. (1982). Quantitative studies of retinal nerve fibre layer defects. Archives of Ophthalmology 100, 807–814.CrossRefGoogle Scholar
Radius, R.L. & Anderson, D.R. (1979). The course of axons through the retina and optic nerve head. Archives of Ophthalmology 97, 1154–1158.CrossRefGoogle ScholarPubMed
Racer, G. (1983). Structural analysis of fibre organization during development. Progress in Brain Research 58, 313–319.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.CrossRefGoogle ScholarPubMed
Reese, B.E. & Colello, R.J. (1992). Neurogenesis in the retinal ganglion cell layer of the rat. Neuroscience 46, 419–429.CrossRefGoogle ScholarPubMed
Reese, B.E. & Baker, G.E. (1993). The re-establishment of the representation of the dorso-ventral retinal axis in the chiasmatic region of the ferret. Visual Neuroscience 10, 957–968.CrossRefGoogle ScholarPubMed
Reese, B.E., Thompson, W.F. & Peduzzi, J.D. (1994 a). Birthdates of neurons in the retinal ganglion cell layer of the ferret. Journal of Comparative Neurology 341, 464–475.CrossRefGoogle ScholarPubMed
Reese, B.E., Maynard, T.M. & Hocking, D.R. (1994 b). Glial domains and axonal reordering in the chiasmatic region of the developing ferret. Journal of Comparative Neurology 349, 303–324.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of His-tochemistry and Cytochemistry 36, 555–559.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Tieman, S.B. (1989). Activity, growth cones and the selectivity of visual connections. Comments in Developmental Biology 1, 11–28.Google Scholar
Sengelaub, D.R., Dolan, R.P. & Finlay, B.L. (1986). Cell generation, death, and retinal growth in the development of the hamster retinal ganglion cell layer. Journal of Comparative Neurology 246, 527–543.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Simon, D.K. & O'Leary, D.M. (1992). Responses of retinal axons in vivo and in vitro to position-encoding molecules in the embryonic superior colliculus. Neuron 9, 977–989.CrossRefGoogle ScholarPubMed
Springer, A.D. & Mednick, A.S. (1986). Retinotopic and chronotopic organization of goldfish retinal ganglion cell axons throughout the optic nerve. Journal of Comparative Neurology 247, 221–232.CrossRefGoogle ScholarPubMed
Sretavan, D.W. (1990). Specific routing of retinal ganglion cell axons at the mammalian optic chiasm during embryonic development. Journal of Neuroscience 10, 1995–2007.CrossRefGoogle ScholarPubMed
Steineke, T.C. & Kirby, M.A. (1993). Early axon outgrowth of retinal ganglion cells in the fetal rhesus macaque. Developmental Brain Research 74, 151–162.CrossRefGoogle ScholarPubMed
Straznicky, K. & Gaze, R.M. (1971). The growth of the retina in Xenopus laevis: An autoradiographic study. Journal of Embryology and Experimental Morphology 26, 67–79.Google ScholarPubMed
Taylor, J.S.H. (1987). Fibre organization and reorganization in the retinotectal projection of Xenopus. Development 99, 393–410.CrossRefGoogle ScholarPubMed
Taylor, S.F. & FitzGibbon, T. (1994). Are the human retinal fibre layer and optic nerve retinotopically ordered? Proceedings of the Australian Neuroscience Society 5, 212.Google Scholar
Thanos, S., Bonhoeffer, F. & Rutishauser, U. (1984). Fiber-fibre interaction and tectal clues influence the development of the chicken retinotectal projection. Proceedings of the National Academy of Sciences of the U.S.A. 81, 1906–1910.CrossRefGoogle Scholar
Thompson, I.D. & Morgan, J.E. (1993). The development of retinal ganglion cell decussation patterns in postnatal pigmented and albino ferrets. European Journal of Neuroscience 5, 341–356.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
Vrabec, F. (1966). The temporal raphe of the human retina. American Journal of Ophthalmology 62, 926–938.CrossRefGoogle ScholarPubMed
Walsh, C., Polley, E.H., Hickey, T.L. & Guillery, R.W. (1983). Generation of cat retinal ganglion cells in relation to central pathways. Nature 302, 611–614.CrossRefGoogle ScholarPubMed
Walsh, C. & Guillery, R.W. (1985). Age-related fibre order in the optic tract of the ferret. Journal of Neuroscience 5, 3061–3069.CrossRefGoogle ScholarPubMed
Walsh, C. & Polley, E.H. (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741–750.CrossRefGoogle ScholarPubMed
Wikler, K.C., Perez, G. & Finlay, B.L. (1989). Duration of retinogenesis: Its relationship to retinal organization in two cricetine rodents. Journal of Comparative Neurology 285, 157–176.CrossRefGoogle ScholarPubMed
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
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 ScholarPubMed
Wolff, E. & Penmann, G.G. (1950). The position occupied by the peripheral retinal fibres in the nerve-fibre layer and at the nerve head. Transactions of the Ophthalmological Society of the United Kingdom, LXX, 35, 35.Google Scholar
Yamadori, T. (1981). An experimental anatomical study on the topographic termination of the optic nerve fibres in the rat. Journal für Hirnforschung 22, 313–326.Google Scholar