Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T08:38:10.918Z Has data issue: false hasContentIssue false
  • English
  • Français

Changes in fiber organization within the chiasmatic region of mammals

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

Abstract

Introduction

Classical views of the optic chiasm maintain four propositions about the retinofugal pathways: (1) each optic nerve contains a retinotopic representation of its respective retinal surface; (2) this retinotopic map in the nerve is the basis for the subsequent segregation of the decussating from the non-decussating fibers; (3) this retinotopy in the nerve is also the basis for the presence of retinotopy found within the half-retinal maps in the optic tracts; and (4) the half-retinal maps from each optic nerve are brought together within the chiasm to yield a unified, binocularly congruent, map in the optic tract (Brodal, 1969; DukeElder, 1961; Polyak, 1957; Wolff, 1940). The appeal of this classical view is in its simplicity, based on the assumption that the retinofugal pathway should replicate the sensory surface along its course. We now know that each of these four propositions is incorrect, and that the error is not one simply of degree or extent (Guillery, 1982, 1991). Rather, the above description of the visual pathway is fundamentally flawed because it has failed to take into account the constraints under which the pathway develops. We shall first consider the evidence for rejecting the classical view, from recent studies on the organization of the retinofugal pathway in adult animals and on the development of that organization. We shall then describe three transformations in the fiber order which all occur in the chiasmatic region, two of which were only recently recognized, and for which we must account.

Observations from adult organization

The difference in the fiber order in the optic nerve and tract

Keywords

Retinal ganglion cellOptic nerveOptic tractDecussation patternRetinoptic mapChronotopic order
Type
Review
Information
Visual Neuroscience , Volume 9 , Issue 6 , December 1992 , pp. 527 - 533
Copyright
Copyright © Cambridge University Press 1992

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

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
Allodi, S., Reese, B.E. & Cavalcante, L.A. (1990). Observations on the arrangement of axons according to diameter in the optic tract of the opossum Didelphis marsupialis. Brazilian Journal of Medicine and Biological Research 23, 539–542.Google ScholarPubMed
Baier, H. & Bonhoeffer, F. (1992). Axon guidance by gradients of a target-derived component. Science 255, 472–475.CrossRefGoogle ScholarPubMed
Baker, G.E. (1990). Prechiasmatic reordering of fibre diameter classes in the retinofugal pathway of ferrets. European Journal of Neuromscience 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.CrossRefGoogle ScholarPubMed
Baker, G.E. & Stryker, M.P. (1990). Retinofugal fibres change conduction velocity and diameter between the optic nerve and tract in ferrets. Nature 344, 342–345.CrossRefGoogle ScholarPubMed
Bastmeyer, M., Schlosshauer, B. & Stuermer, C.A.O. (1990). The spatiotemporal distribution of N-CAM in the retinotectal pathway of adult goldfish detected by the monoclonal antibody D3. Development 108, 299–311.CrossRefGoogle ScholarPubMed
Bishop, G.H. & Clare, M.H. (1955). Organization and distribution of fibers in the optic tract of the cat. Journal of Comparative Neurology 103, 269–304.CrossRefGoogle ScholarPubMed
Bishop, G.H., Clare, M.H. & Landau, W.M. (1969). Further analysis of fiber groups in the optic tract of the cat. Experimental Neurology 24, 386–399.CrossRefGoogle ScholarPubMed
Bonhoeffer, F. & Huf, J. (1982). In vitro experiments on axon guidance demonstrating an anterior-posterior gradient on the tectum. European Molecular Biology Organization Journal 1, 427–431.CrossRefGoogle ScholarPubMed
Bonhoeffer, F. & Huf, J. (1985). Position-dependent properties of retinal axons and their growth cones. Nature 315, 409–411.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 204, 397–419.CrossRefGoogle Scholar
Brodal, A. (1969). Neurological Anatomy in Relation to Clinical Medicine. Oxford: Oxford University Press.Google Scholar
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
Chan, S.-O. & Guillery, R.W. (1990). Fiber arrangements in the optic stalk of normal and albino rats. Society for Neuroscience Abstracts 16, 336.Google Scholar
Chang, H.T. (1952). Fiber groups in primary optic pathway of cat. Research Publications of the Association for Research in Nervous and Mental Disorders 30, 224–231.Google Scholar
Chang, H.T. & Cheng, T.H. (1961). An analysis of fiber constitution of optic tract of cat. Scientia Sinica 10, 538–556.Google Scholar
Cohen, J., Burne, J.R., McKinlay, C. & Winter, J. (1987). The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons. Developmental Biology 122, 407–418.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., Blum, A.S., Mendez-Otero, R. & Barnstable, C.J. (1986). A cell surface molecule distributed in a dorsoventral gradient in the perinatal rat retina. Nature 324, 459–462.CrossRefGoogle Scholar
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
Drazba, J. & Lemmon, V. (1990). The role of cell adhesion molecules in neurite outgrowth on Müller cells. Developmental Biology 138, 82–93.CrossRefGoogle ScholarPubMed
Duke-Elder, S. (1961). System of Ophthalmology. London: Henry Klimpton.Google Scholar
Fitzgibbon, T. & Reese, B.E.Position of growth cones within the retinal nerve fibre layer of fetal ferrets. Journal of Comparative Neurology (in press).Google Scholar
Fukuda, Y. & Stone, J. (1974). Retinal distribution and central projections of Y-, X-, and W-cells of the cat's retina. Journal ofNeurophysiology 37, 749–772.CrossRefGoogle Scholar
Godement, P. & Bonhoeffer, F. (1989). Cross-species recognition of tectal cues by retinal fibers in vitro. Development 106, 313–320.CrossRefGoogle ScholarPubMed
Godement, P. & Mason, C.A. (1990). Behavior of live retinal axon growth cones in the optic chiasm. Society for Neuroscience Abstracts 16, 1125.Google Scholar
Godement, P., Salaun, J. & Mason, C.A. (1990). Retinal axon pathfinding in the optic chiasma: Divergence of crossed and uncrossed fibers. Neuron 5, 173–186.CrossRefGoogle ScholarPubMed
Guillaume, P., Wang, L.-C., Mason, C.A. & Godement, P. (1991). Retinal axon-optic chiasm cellular interactions in vitro. Society for Neuroscience Abstracts 17, 40.Google Scholar
Guillery, R.W. (1982). The optic chiasm of the vertebrate brain. Contributions to Sensory Physiology 7, 39–73.CrossRefGoogle Scholar
Guillery, R.W. (1991) Rules that govern the development of the pathways: From the eye to the optic tract in mammals. In Development of the Visual System, ed. LAM, D.M.-K. & Shatz, C.J., pp. 153–171. Cambridge, Massachusetts: MIT Press.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.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, 203–217.CrossRefGoogle ScholarPubMed
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 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
Lmsi, P. & Silver, J. (1988). Is astrocyte laminin involved in axon guidance in the mammalian CNS? Developmental Biology 130, 774–785.Google Scholar
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
Mason, C.A., Blazeski, R., Dodd, J. & Godement, P. (1991). The midline of the mouse optic chiasm: Cellular composition and antigen expression during retinal axon growth. Society for Neuroscience Abstracts 17, 39.Google Scholar
Mason, C.A., Misson, J.P., Blazeski, R. & Godement, P. (1990). Retinal axon navigation in the mouse optic chiasm: Midline cues and cell-cell relations. Society for Neuroscience Abstracts 16, 1125.Google Scholar
McKanna, J.A. (1991). Axon guidance at the developing rat optic chiasm: p35 annexin appears in a glial raphe prior to arrival of pioneer fibers. Association for Research in Vision and Ophthalmology Abstracts 32, 925.Google Scholar
Naito, J. (1986). Course of retinogeniculate projection fibers in the cat optic nerve. Journal of Comparative Neurology 251, 376–387.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, 174–186.CrossRefGoogle ScholarPubMed
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.CrossRefGoogle Scholar
Polyak, S. (1957). The Vertebrate Visual System. Chicago, Illinois: Chicago University Press.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
Reese, B.E. (1987). The distribution of axons according to diameter in the optic nerve and optic tract of the rat. Neuroscience 22, 1015–1024.CrossRefGoogle 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., Baker, G.E., Tassinari, G. & Marzi, C.A. (1991a). Fiber re-organization in the mammalian optic chiasm: De novo establishment of the dorso-ventral retinal axis. Society for Neuroscience Abstracts 16, 1132.Google Scholar
Reese, B.E., Baker, G.E., Thompson, W.F. & Peduzzi, J.D. (1992a). Genesis of retinal ganglion cells and the chiasmatic course of their axons in the ferret. Society for Neuroscience Abstracts 18, (in press).Google Scholar
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., Colello, R.J. & Thompson, W. (1992b). Cell survival in the uncrossed projection of the mammalian retina is independent of birthdate. European Journal of Neuroscience 4, 177–182.CrossRefGoogle ScholarPubMed
Reese, B.E. & Cowey, A. (1990a). Fibre organization of the monkey's optic tract: 1. Segregation of functionally distinct optic axons. Journal of Comparative Neurology 295, 385–400.CrossRefGoogle Scholar
Reese, B.E. & Cowey, A. (1990b). Fibre organization of the monkey's optic tract: II. Noncongruent representation of the two half-retinae. Journal of Comparative Neurology 295, 401–412.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Reese, B.E., Guillery, R.W., Marzi, C.A. & Tassinari, G. (1991b). 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.CrossRefGoogle ScholarPubMed
Reese, B.E., Mallarino, C. & Burkhalter, R. (1992c). Determinants of decussation patterns in carnivores: Selective cell death in the temporal retina or selective axonal guidance in the chiasm? Investigative Ophthalmology and Visual Science (Suppl.) 33, 1213.Google Scholar
Sakaguchi, D.S., Moeller, J.F., Coffman, C.R., Gallenson, N. & Harris, W.A. (1989). Growth cone interactions with a glial cell line from embryonic Xenopus retina. Developmental Biology 134, 158–174.CrossRefGoogle ScholarPubMed
Silver, J. (1984). Studies on the factors that govern directionality of axonal growth in the embryonic optic nerve and at the chiasm of mice. Journal of Comparative Neurology 223, 238–251.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. (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
Sretavan, D.W. (1990a). Specific routing of retinal ganglion cell axons at the mammalian optic chiasm during embryonic development. Journal of Neuroscience 10, 1995–2007.CrossRefGoogle ScholarPubMed
Sretavan, D.W. (1990b). Axon navigation at the mammalian optic chiasm: Direct observation using fluorescent time-lapse video microscopy. Society for Neuroscience Abstracts 16, 1126.Google Scholar
Stone, J. & Fukuda, Y. (1974). The naso-temporal division of the cat's retina re-examined in terms of X-, Y-, and W-cells. Journal of Comparative Neurology 155, 722–747.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.CrossRefGoogle ScholarPubMed
Vielmetter, J. & Stuermer, C.A.O. (1989). Goldfish retinal axons respond to position-specific properties of tectal cell membranes in vitro. Neuron 2, 1331–1339.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
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
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
Walter, J., Henke-Fahle, S. & Bonhoeffer, F. (1987b). Avoidance of posterior tectal membranes by temporal retinal axons. Development 101, 909–913.CrossRefGoogle ScholarPubMed
Walter, J., Kern-Veits, B., Huf, J., Stolze, B. & Bonhoeffer, F. (1987a). Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101, 685–696.CrossRefGoogle ScholarPubMed
Wikler, K.C., Raabe, J.I. & Finlay, B.L. (1985). Temporal Retina Is Preferentially Represented In The Early Retinotectal Projection In The Hamster. Developmental Brain Research, 21, 152–155.CrossRefGoogle Scholar
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, 32–69.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
Williams, R.W. & Chalupa, L.M. (1983). An analysis of axon caliber within the optic nerve of the cat: Evidence of size groupings and regional organization. Journal of Neuroscience 3, 1554–1564.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
Wolff, E. (1940). The Anatomy of the Eye and Orbit. London: Lewis and Co.Google Scholar