Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T11:10:25.142Z Has data issue: false hasContentIssue false

The human fetal retinal nerve fiber layer and optic nerve head: A DiI and DiA tracing study

Published online by Cambridge University Press:  02 June 2009

T. Fitzgibbon
Affiliation:
Department of Clinical Ophthalmology, University of Sydney, NSW 2006, Australia

Abstract

The organization of the primate nerve fiber layer and optic nerve head with respect to the positioning of central and peripheral axons remains controversial. Data were obtained from 32 human fetal retinae aged between 15 and 21 weeks of gestation. Crystals of the carbocyanine dyes, DiI or DiA, and fluorescence microscopy were used to identify axonal populations from peripheral retinal ganglion cells. Peripheral ganglion cell axons were scattered throughout the vitreal-scleral depth of the nerve fiber layer. Such a scattered distribution was maintained as the fibers passed through the optic nerve head and along the optic nerve. There was a rough topographic representation within the optic nerve head according to retinal quadrant such that both peripheral and central fibers were mixed within a wedge extending from the periphery to the center of the nerve. There was no indication that the fibers were reorganized in any way as they passed through the optic disc and into the nerve. The present results suggest that any degree of order present within the fiber layer and optic nerve is not an active process but a passive consequence of combining the fascicles of the retinal nerve fiber layer. Optic axons are not instructed to establish a retinotopic order and the effect of guidance cues in reordering fibers, particularly evident prechiasmatically and postchiasmatically, does not appear to be present within the nerve fiber layer or optic nerve head in humans.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

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

REFERENCES

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, 43744378.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, 14471460.CrossRefGoogle ScholarPubMed
Brittis, P.A., Canning, D.R. & Silver, J. (1992). Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 255, 733736.CrossRefGoogle ScholarPubMed
Brouwer, B. & Zeeman, W.P.C. (1926). The projection of the retina in the primary optic neuron in monkeys. Brain 49, 135.CrossRefGoogle Scholar
Bunt, S.M. (1982). Retinotopic and temporal organization of the optic nerve and tracts in the adult goldfish. Journal of Comparative Neurology 206, 209226.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, 94114.CrossRefGoogle ScholarPubMed
Chan, H. & Guillery, R.W. (1994). Changes in fibre order in the optic nerve and tract of rat embryos. Journal of Comparative Neurology 344, 2032.CrossRefGoogle ScholarPubMed
Chelvanayagam, D.K. & Beazley, L.D. (1994). Optic axons are ordered from early development in the visual pathway of the quokka setonix brachyurus. Proceedings of the Australian Neuroscience Society 5, 121.Google Scholar
Cook, J.E. (1982). Errant optic axons in the normal goldfish retina reach retinotopic sites. Brain Research 250, 154158.CrossRefGoogle ScholarPubMed
Cook, J.E. & Horder, T.J. (1977). The multiple factors determining retinotopic order in the growth of optic fibers into the optic tectum. Philosophical Transactions of the Royal Society B (London) 278, 261276.Google ScholarPubMed
Diaz-Araya, C.M., Provis, J.M. & Penfold, P.L. (1995). Ontogeny and cellular expression of MHC and leucocyte antigens in human retina. Glia 15, 458470.CrossRefGoogle ScholarPubMed
Duke-Elder, S.S. & Cook, L. (1963). System of Ophthalmology. Vol. III Part I. Embryology. London: Henry Kimton.Google Scholar
Easter, S.S., Bratton, B. & Scherer, S.S. (1984). Growth-related order in the retinal fibre layer in goldfish. Journal of Neuroscience 4, 21732190.CrossRefGoogle ScholarPubMed
Easter, S.S., Rusoff, A.C. & Kish, K.E. (1981). The growth and organization of the optic nerve and tract in juvenile and adult goldfish. Journal of Neuroscience 1, 793811.CrossRefGoogle ScholarPubMed
Fawcett, J.W. (1981). How axons grow down the Xenopus optic nerve. Journal of Embryology and Experimental Morphology 65, 219233.Google ScholarPubMed
Fitzgibbon, T. & Burke, W. (1989). Representation of the temporal raphe within the optic tract of the cat. Visual Neuroscience 2, 255267.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, 153166.CrossRefGoogle ScholarPubMed
Fitzgibbon, T. & Reese, B.E. (1996). Organization of retinal ganglion cell axons in the optic fiber layer and nerve of fetal ferrets. Visual Neuroscience 13, 847862.CrossRefGoogle ScholarPubMed
Fitzgibbon, T., Funke, K. & Eysel, U.T. (1991). Anatomical correlations between soma size, axon diameter and intraretinal length for the alpha ganglion cells of the cat retina. Visual Neuroscience 6, 159174.CrossRefGoogle ScholarPubMed
Godement, P., Salaün, J. & Mason, C.A. (1990). Retinal axon pathfinding in the optic chiasm: Divergence of crossed and uncrossed fibres. Neuron 5, 173186.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, 507518.CrossRefGoogle Scholar
Guillery, R.W., Mason, C.A. & Taylor, J.S.H. (1995). Developmental determinants at the mammalian optic chiasm. Journal of Neuroscience 15, 47274737.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Walsh, C. (1987). Changing glial organization relates to changing fiber order in the developing optic nerve of ferrets. Journal of Comparative Neurology 265, 203217.CrossRefGoogle ScholarPubMed
Harris, W.A. & Holt, C.E. (1990). Early events in the embryogenesis of the vertebrate visual system: Cellular determination and pathfinding. Annual Review of Neuroscience 13, 155169.CrossRefGoogle ScholarPubMed
Herrick, C.J. (1942). Optic and postoptic systems in the brain of Amblystoma tigrinum. Journal of Comparative Neurology 77, 191353.CrossRefGoogle Scholar
Honig, M.G. & Hume, R.I. (1989). Dil and DiO: Versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends in Neurosciences 12, 333341.CrossRefGoogle ScholarPubMed
Horder, T.J. & Martin, K.A.C. (1978). Morphogenetics as an alternative to chemospecificity in the formation of nerve connections. Society Experimental Biology Symposium 32, 275358.Google ScholarPubMed
Horsburgh, G.M. & Sefton, A.J. (1986). The early development of the optic nerve and chiasm in embryonic rat. Journal of Comparative Neurology 243, 547560.CrossRefGoogle ScholarPubMed
Horton, J.C., Greenwood, M.M. & Hubel, D.H. (1979). Non-retinotopic arrangement of fibres in cat optic nerve. Nature 282, 720722.CrossRefGoogle ScholarPubMed
Hoyt, W.F. & Luis, O. (1962). Visual fiber anatomy in the infrageniculate pathway of the primate. Archives of Ophthalmology 68, 124136.CrossRefGoogle ScholarPubMed
Kirby, M.A. & Steineke, T.C. (1992). Morphogenesis of retinal ganglion cells during formation of the fovea in the rhesus macaque. Visual Neuroscience 9, 603616.CrossRefGoogle ScholarPubMed
Krayanek, S. & Goldberg, S. (1981). Orientated extracellular channels and axonal guidance in the embryonic chick retina. Developmental Biology 84, 4150.CrossRefGoogle ScholarPubMed
Lavail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86114.CrossRefGoogle Scholar
Maggs, A. & Scholes, J. (1986). Glial domains and nerve fibre patterns in the fish retinotectal pathway. Journal of Neuroscience 6, 424438.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 eugnii): II. Topography after rotation of an eye prior to retinal innervation of the brain. Journal of Comparative Neurology 271, 274292.CrossRefGoogle Scholar
Meissirel, C. & Chalupa, L.M. (1994). Organization of pioneer retinal axons within the optic tract of the rhesus monkey. Proceedings of the National Academy of Sciences of the U.S.A. 91, 39063910.CrossRefGoogle ScholarPubMed
Minckler, D.S. (1980). The organization of nerve fibre bundles in the primate optic nerve head. Archives of Ophthalmology 98, 16301636.CrossRefGoogle ScholarPubMed
Murakami, D., Sesma, M.A. & Rowe, M.H. (1982). Characteristics of nasal and temporal retina in Siamese and normally pigmented cats: Ganglion cell composition, axon trajectory and laterality of projection. Brain, Behavior, and Evolution 21, 67113.CrossRefGoogle ScholarPubMed
Naito, J. (1986). Course of retinogeniculate projection fibers in the cat optic nerve. Journal of Comparative Neurology 251, 376387.CrossRefGoogle ScholarPubMed
Naito, 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, 174186.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1974). The nerve-fiber layer of the primate retina: An autoradiographic study. Investigative Ophthalmology and Visual Science 13, 95100.Google ScholarPubMed
Ogden, T.E. (1983 a). Nerve fibre layer of the macaque retina: Retinotopic organization. Investigative Ophthalmology and Visual Science 24, 8598.Google ScholarPubMed
Ogden, T.E. (1983 b). Nerve fiber layer of the owl monkey retina: Retinotopic organization. Investigative Ophthalmology and Visual Science 24, 265269.Google ScholarPubMed
Ogden, T.E. (1984). Nerve fiber layer of the primate retina: Morphometric organization. Investigative Ophthalmology and Visual Science 25, 1929.Google Scholar
Polyak, S. (1957). The Vertebrate Visual System. Chicago, Illinois: University of Chicago Press.Google Scholar
Provis, J.M. (1987). Patterns of cell death in the ganglion cell layer of the human fetal retina. Journal of Comparative Neurology 259, 237246.CrossRefGoogle ScholarPubMed
Provis, J.M. & Penfold, P.L. (1988). Cell death and the elimination of retinal axons during development. Progress in Neurobiology 31, 331347.CrossRefGoogle ScholarPubMed
Provis, J.M., Van Driel, D., Billson, F.A. & Russell, P. (1985 a). Development of the human retina: Patterns of cell distribution and redis-tribution in the ganglion cell layer. Journal of Comparative Neurology 233, 429451.CrossRefGoogle ScholarPubMed
Provis, J.M., Van Driel, D., Billson, F.A. & Russell, P. (1985 b). Human fetal optic nerve: Overproduction and elimination of retinal axons during development. Journal of Comparative Neurology 238, 92100.CrossRefGoogle ScholarPubMed
Quigley, H.A. & Addicks, E.A. (1982). Quantitative studies of retinal nerve fiber layer defects. Archives of Ophthalmology 100, 807814.CrossRefGoogle ScholarPubMed
Radius, R.L. & Anderson, D.R. (1979). The course of axons through the retina and optic nerve head. Archives of Ophthalmology 97, 11541158.CrossRefGoogle ScholarPubMed
Rager, G. (1983). Structural analysis of fiber organization during development. Progress in Brain Research 58, 313319.CrossRefGoogle ScholarPubMed
Rakic, P. & Riley, K. (1983). Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science 219, 14411444.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, 957968.CrossRefGoogle ScholarPubMed
Reese, B.E., Maynard, T.M. & Hocking, D.R. (1994 a). Glial domains and axonal reordering in the chiasmatic region of the developing ferret. Journal of Comparative Neurology 349, 303324.CrossRefGoogle ScholarPubMed
Reese, B.E., Thompson, W.F. & Peduzzi, J.D. (1994 b). Birthdates of neurons in the retinal ganglion cell layer of the ferret. Journal of Comparative Neurology 341, 464475.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of Histochemistry and Cytochemistry 36, 555559.CrossRefGoogle ScholarPubMed
Silveira, L.C.L. & Perry, V.H. (1990). A neurofibrillar staining method for retina and skin: A simple modification for improved staining and reliability. Journal of Neuroscience Methods 33, 1121.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, 101111.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, 393404.CrossRefGoogle Scholar
Spira, A.W. & Hollenberg, M.J. (1973). Human retinal development: Ultrastructure of the inner retinal layers. Developmental Biology 31, 121.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, 151162.CrossRefGoogle ScholarPubMed
Stirling, R.V. & Dunlop, S.A. (1995). The dance of the growth cones—where to next. Trends in Neurosciences 18, 111115.CrossRefGoogle ScholarPubMed
Taylor, J.S.H. (1987). Fibre organization and reorganization in the retinotectal projection of Xenopus. Development 99, 393410.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-fiber 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, 19061910.CrossRefGoogle Scholar
Udin, S.B. & Fawcett, J.W. (1988). Formation of topographic maps. Annual Review of Neuroscience 11, 289327.CrossRefGoogle ScholarPubMed
Vrabec, F. (1966). The temporal raphe of the human retina. American Journal of Ophthalmology 62, 926938.CrossRefGoogle ScholarPubMed
Walsh, C. & Polley, E.H. (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741750.CrossRefGoogle ScholarPubMed
Williams, R.W., Bastiani, M.J., Lia, B. & Chalupa, L.M. (1986). Growth cones, dying axons, and developmental fluctuations in the fiber population of the cat's optic nerve. Journal of Comparative Neurology 246, 3269.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 Neuroscience 11, 10811094.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, 39063910.CrossRefGoogle ScholarPubMed
Wolff, E. & Penmann, G.G. (1951). The position occupied by the peripheral retinal fibres in the nerve-fibre layer and at the nerve head. Acta XVI Concillium Ophthalmologicum (1950), 625635.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, 313326.Google Scholar