Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T00:33:52.911Z Has data issue: false hasContentIssue false
  • English
  • Français

Topographic organization of the retinocollicular projection in the neonatal rat

Published online by Cambridge University Press:  02 June 2009

J. Peter ,
A. Yhip  and
Michael A. Kirby
J. Peter
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda
A. Yhip
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda
Michael A. Kirby
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda
Get access Rights & Permissions [Opens in a new window]

Abstract

The topographic order of the retinocollicular projection in the rat was examined from birth until maturity. Small, localized deposits of rhodamine-filled latex microspheres were placed into the superior colliculus at different locations. To minimize labeling fibers of passage deposit sites were typically, although not exclusively, placed into the caudal-lateral pole of the colliculus. Examination of the area and density of labeled cells in the retinae of these animals led to the following conclusions: (1) At each age examined, the location of the majority of labeled cells was observed to be in appropriate topographic register with the deposit site in the superior colliculus. (2) Confirming the work of previous investigators, errors in topographic projection were observed. These were present in both the contralateral and ipsilateral retinae and decreased with increasing postnatal age. The mature pattern was present by P10. (3) Quantitatively, the number of retinal ganglion cells terminating nontopographically within the colliculus constituted a relatively minor proportion of the total number of labeled cells in both retinae. It is concluded that the majority of the retinal ganglion cells make topographically appropriate terminations within the superior colliculus during development.

Keywords

DevelopmentRetinocollicularTopographyRetinaRat
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 4 , April 1990 , pp. 313 - 329
Copyright
Copyright © Cambridge University Press 1990

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

Albers, F.J., Meek, J. & Nieuwenhuys, R. (1988). Morphometric parameters of the superior colliculus of albino and pogmented rats. Journal of Comparative Neurology 274, 357–370.CrossRefGoogle ScholarPubMed
Baisinger, J., Lund, R.D. & Miller, B. (1977). Aberrant retinothalamic projections resulting from unilateral tectal lesions made in fetal and neonatal rats. Experimental Neurology 54, 369–382.CrossRefGoogle ScholarPubMed
Bennett, M.R. (1983). Development of neuromuscular synapses. Physiology Reviews 63, 915–1048.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
Campbell, G. &Frost, D.O. (1987). Target-controlled differentiation of axon terminals and synaptic organization. Proceedings of the National Academy of Science of the U.S.A. 84, 6929–6933.CrossRefGoogle ScholarPubMed
Campbell, G., So, K.-F. & Lieberman, A.R. (1984). Normal postnatal development of retinogeniculate axons and terminals and identification of inappropriately located transient synapses: electron-microscope studies of HRP-labeled retinal axons in the hamster. Neuroscience 13, 743–759.CrossRefGoogle Scholar
Card-Linden, D., Guillery, R.W. & Cucchiaro, J. (1981). The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. Journal of Comparative Neurology 203, 189–211.CrossRefGoogle Scholar
Cavalcante, L.A. & Rocha-Miranda, C.E. (1978). PLostnatal development of retinogeniculate, retinopretectal, and retinotectal projections in the opossum. Brain Research 146, 231–248.CrossRefGoogle ScholarPubMed
Chalupa, L.M. (1984). Visual physiology of the mammalian superior colliculus. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 775–818. New York: Plenum Press.CrossRefGoogle Scholar
Cooper, A.M. & Cowey, A. (1987). A neonatal crossed aberrant, exuberant projection to the inferior colliculus, visualized in whole-brain preparations of the pigmented rat. Society for Neuroscience Abstracts 13, 1690.Google Scholar
Cowey, A. & Perry, H. (1979). The projection of the temporal retina in rats: studies by retrograde transport of horseradish peroxidase. Experimental Brain Research 35, 457–464.CrossRefGoogle Scholar
Crespo, D., O'Leary, D.D.M. & Cowan, M. (1985). Changes in the number of optic nerve fibers during late prenatal and postnatal development in the albino rat. Developmental Brain Research 19, 129–134.CrossRefGoogle Scholar
Cusick, C.G. & Kaas, J.H. (1982). Retinal projections in adult and newborn grey squirrels. Developmental Brain Research 4, 275–284.CrossRefGoogle Scholar
Drager, U.C. & Hubel, D.H. (1975). Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. Journal of Neurophysiology 38, 690–713.CrossRefGoogle ScholarPubMed
Dreher, B., Potts, R.A. & Bennett, M.R. (1983). Evidence that the early postnatal reduction in the number of rat retinal ganglion cells is due to a wave of ganglion cell death. Neuroscience Letters 36, 255–260.CrossRefGoogle ScholarPubMed
Dreher, B., Sefton, A.J., Ni, S.K.Y. & Nisbett, G. (1985). The morphology, number, distribution, and central projections of class I retinal ganglion cells in albino and hooded rats. Brain, Behavior, and Evolution 26, 10–48.Google Scholar
Finlay, B.L., Berg, A.T. & Sengelaub, D.R. (1982). Cell death in the mammalian visual system during normal development, II: Superior colliculus. Journal of Comparative Neurology 204, 318–324.CrossRefGoogle ScholarPubMed
Finlay, B.L., Wilson, K.G. & Schneider, G.E. (1979). Anomalous ipsilateral retinotectal projections in Syrian hamsters with early lesions: topography and functional capacity. Journal of Comparative Neurology 183, 721–740.CrossRefGoogle ScholarPubMed
Forrester, J. & Peters, A. (1967). Nerve fibres in optic nerve of rat. Nature 241, 245–247.CrossRefGoogle Scholar
Frost, D.O., So, K.F. & Schneider, G.E. (1979). Postnatal development of retinal projections in Syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. Neuroscience 4, 1649–1677.CrossRefGoogle ScholarPubMed
Frost, D.O. & Schneider, G.E. (1979). Plasticity of retinofugal projections after partial lesions of the retina in newborn Syrian hamsters. Journal of Comparative Neurology 185, 517–567.CrossRefGoogle ScholarPubMed
Fukuda, Y., Sugimoto, T. & Shirokawa, T. (1982). Strain differences in quantitative analysis of the rat optic nerve. Experimental Neurology 75, 525–532.CrossRefGoogle ScholarPubMed
Godement, P., Saillour, P. & Imbert, M. (1980). The ipsilateral optic pathway to the dorsal lateral geniculate nucleus and superior colliculus in mice with the prenatal or postnatal loss of one eye. Journal of Comparative Neurology 190, 611–626.CrossRefGoogle ScholarPubMed
Godement, P., Salaun, J. & Imbert, M. (1984). Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. Journal of Comparative Neurology 230, 552–575.CrossRefGoogle ScholarPubMed
Gunderson, H.J.G. (1977). Notes on the estimation of the numerical density of arbitary profiles: the edge effect. Journal of Microscopy 111, 219–223.CrossRefGoogle Scholar
Hayhow, W.R., Sefton, A. & Webb, C. (1962). Primary optic centers of the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers. Journal of Comparative Neurology 112, 295–307.CrossRefGoogle Scholar
Hofbauer, A. & Drager, U.C. (1985). Depth segregation of retinal ganglion cells projecting to mouse superior colliculus. Journal of Comparative Neurology 234, 465–474.CrossRefGoogle 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, 547–560.CrossRefGoogle ScholarPubMed
Hughes, A. (1977). The pigmented-rat optic nerve: fibre count and fibre diameter spectrum. Journal of Comparative Neurology 176, 263–268.CrossRefGoogle ScholarPubMed
Insausti, R., Blakemore, C. & Cowan, W.M. (1984). Ganglion cell death during development of ipsilateral retino-collicular projection in golden hamster. Nature 308, 362–365.CrossRefGoogle ScholarPubMed
Itaya, S.K. & Van, Hoesen G.W. (1982). Retinal innervation of the inferior colliculus in rat and monkey. Brain Research 233, 45–52.CrossRefGoogle Scholar
Jeffery, G. (1984). Retinal ganglion cell death and terminal-field retraction in the developing rodent visual system. Developmental Brain Research 13, 81–96.CrossRefGoogle Scholar
Jeffery, G. (1985). Retinotopic order appears before ocular segregation in developing pathways. Nature 313, 575–576.CrossRefGoogle Scholar
Jeffery, G. & Perry, H. (1982). Evidence for ganglion cell death during development of the ipsilateral retinal projection in the rat. Developmental Brain Research 2, 176–180.CrossRefGoogle Scholar
Kaas, J.H., Harting, J.K. & Guillery, R.W. (1974). Representation of the complete retina in the contralateral superior colliculus of some mammals. Brain Research 65, 343–346.CrossRefGoogle ScholarPubMed
Kato, T. (1983). Transient retinal fibers to the inferior colliculus in the newborn albino rat. Neuroscience Letters 37, 7–9.CrossRefGoogle Scholar
Katz, L.C., Burkhalter, A. & Dreyer, W.D. (1984). Fluorescent latex microspheres as a retrograde neuronal marker for in vivo studies of visual cortex. Nature 310, 498–500.CrossRefGoogle ScholarPubMed
Kruger, L. (1970). The topography of the visual projection to the mesencephalon: a comparative survey. Brain, Behavior, and Evolution 3, 169–177.Google Scholar
Laemle, L.K. & Labriola, A.R. (1982). Retinocollicular projections in the neonatal rat: an anatomical basis for plasticity. Developmental Brain Research 3, 317–322.CrossRefGoogle Scholar
Lam, K., Sefton, A.J. & Bennett, M.R. (1982). Loss of axons from the optic nerve of the rat during early postnatal development. Developmental Brain Research 3, 487–491.CrossRefGoogle Scholar
Land, P.W. & Lund, R.D. (1979). Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science 205, 698–700.CrossRefGoogle ScholarPubMed
Lashley, K.S. (1934). The projection of the retina upon the primary optic centers of the rat. Journal of Comparative Neurology 34, 341–373.CrossRefGoogle Scholar
Lia, B., Williams, R.W. & Chalupa, L.M. (1986). Does axonal branching contribute to the overproduction of optic nerve fibers during early development of the cat's visual system? Developmental Brain Research 25, 296–301.CrossRefGoogle Scholar
Linden, R. & Perry, V.H. (1983). Massive retinotectal projection in rats. Brain Research 272, 145–149.CrossRefGoogle ScholarPubMed
Lund, R.D. (1965). Uncrossed visual pathways of hooded and albino rats. Science 149, 1506–1507.CrossRefGoogle ScholarPubMed
Lund, R.D. & Bunt, A.H. (1976). Prenatal development of the central optic pathways in albino rats. Journal of Comparative Neurology 165, 247–274.CrossRefGoogle ScholarPubMed
Lund, R.D., Cunningham, T.J. & Lund, J.S. (1973). Modified optic projections afZter unilateral eye removal in young rats. Brain, Behavior, and Evolution 8, 51–72.Google ScholarPubMed
Martin, P.R., Sefton, A.J. & Dreher, B. (1983). The retinal location and fate of ganglion cells which project to the ipsilateral superior colliculus in neonatal albino and hooded rats. Neuroscience Letters 41, 219–226.CrossRefGoogle Scholar
McLoon, S.C. (1985). Evidence for shifting connections during development of the chick retinotectal projection. Journal of Neuroscience 5, 2570–2580.CrossRefGoogle ScholarPubMed
Morest, K.D. (1970). The pattern of neurogenesis in the retina of the rat. Zeitschrift für Anatomie und Entiwicklungsgeschichte (Berlin) 131, 45–67.CrossRefGoogle ScholarPubMed
Naegele, J.R., Jhaveri, S. & Schneider, G.E. (1988). Sharpening of topographical projections and maturation of geniculocortical axon arbors in the hamster. Journal of Comparative Neurology 277, 593–607.CrossRefGoogle ScholarPubMed
O'Leary, D.D.M., Fawcett, J.W. & Cowan, W.M. (1986). Topographical targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. Journal of Neuroscience 6, 3692–3705.CrossRefGoogle ScholarPubMed
Ostrach, L.H., Kirby, M.A. & Chalupa, L.M. (1986). Topographic organizalion of retinocollicular projections in the fetal cat. Society for Neuroscience Abstracts 12, 119.Google Scholar
Perry, V.H. & Cowey, A. (1979 a). The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats. Experimental Brain Research 35, 85–95.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1979 b). Changes in the retinofugal pathways following cortical and tectal lesions in neonatal and adult rats. Experiniental Brain Research 35, 97–108.Google ScholarPubMed
Perry, V.H. & Cowey, A. (1982). A sensitive period for ganglion cell degeneration and the formation of aberrant retinofugal connections following tectal lesions in rats. Neuroscience 7, 583–594.CrossRefGoogle ScholarPubMed
Perry, V.H., Henderson, Z. & Linden, R. (1983). Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. Journal of Comparative Neurology 219, 356–368.CrossRefGoogle ScholarPubMed
Potts, R.A., Dreher, B. & Bennett, M.R. (1982). The loss of ganglion cells in the developing retina of the rat. Brain Research 3, 481–486.CrossRefGoogle Scholar
Purves, D. & Lichtman, J.W. (1985). Principles of Neural Development. Sunderland: Sinauer Press.Google Scholar
Rakic, P. (1977). Prenatal development of the visual system in rhesus monkey. Philosophical Transactions of the Royal Society (London) 278, 245–260.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Reese, B.E. & Cowey, A. (1986). Large retinal ganglion cells in the rat: their distribution and laterality of projection. Experimental Brain Research 61, 375–385.CrossRefGoogle ScholarPubMed
Reese, B.E. & Cowey, A. (1987). The crossed projection from the temporal retina to the dorsal lateral geniculate nucleus in the rat. Neuroscience 20, 951–959.CrossRefGoogle Scholar
Robinson, S.R., Horsburgh, G.M., Dreher, B. & McCall, M.J. (1987). Changes in the number of retinal ganglion cells and optic nerve axons in the developing albino rabbit. Developmental Brain Research 35, 161–174.CrossRefGoogle Scholar
Sachs, G.M., Jacobson, M. & Caviness, V.S. Jr., (1986). Postnatal changes in arborization patterns of murine retinocollicular axons. Journal of Comparsative Neurology 246, 395–408.CrossRefGoogle ScholarPubMed
Sanderson, K.J., Haight, J.R. & Pettigrew, J.D. (1984). The dorsal lateral geniculate nucleus of macropodial marsupials: cytoarchitecture and retinal projections. Journal of Comparative Neurology 224, 85–106.CrossRefGoogle ScholarPubMed
Schneider, G.E. & Jhaveri, S. (1984). Rapid postnatal establishment of topography in the hamster retinotectal projections. Society for Neuroscience Abstracts 10, 467.Google Scholar
Schneider, G.E., Jhaveri, S. & Davis, W.F. (1987). On the development of neuronal arbors. In Developmental Neurobiology of Mammals, ed. Chagas, C. & Linden, R., pp. 31–64. Civitate Viticana: Pontificia Academia Scientiarum.Google Scholar
Schneider, G.E., Jhaveri, S., Edwards, M.A. & So, K.-F. (1985). Regeneration, re-routing, and redistribution of axons after early lesions: changes with age and functional impact. In Recent Achievements in Restorative Neurology, I: Upper Motor Neuron Functions and Dysfunctions, ed. Eccles, J. & Dimitrijevic, M., pp. 291–310. Basel: Karger.Google Scholar
Schneider, G.E., Rava, L., Sachs, G.M. & Jhaveri, S. (1981). Widespread branching of retinofugal axons: transient in normal development and anomalous in adults with neonatal lesions. Society for Neuroscience Abstracts 7, 732.Google Scholar
Sefton, A.J. & Lam, K. (1984). Quantitative and morphological studies on the developing optic nerve of the albino rat. Experimental Brain Research 57, 107–117.CrossRefGoogle Scholar
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Siminoff, R., Schwassmann, H.O. & Kruger, L. (1966). An electrophysiological study of the visual projection to the superior colliculus of the rat. Journal of Comparative Neurology 127, 435–444.CrossRefGoogle Scholar
Simon, D.K. & O'Leary, D.D.M. (1989). Limited topographic specificity in the targeting of mammalian retinal axons. Society for Neuroscience Abstracts 15, 495.Google Scholar
Sretavan, D. & Shatz, C.J. (1984). Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 308, 845–848.CrossRefGoogle ScholarPubMed
Sretavan, D. & Shatz, C.J. (1986). Prenatal development of retinal ganglion cell axons: segregation into eye-specific geniculate layers from the intermixed state. Journal of Neuroscience 6, 234–251.CrossRefGoogle Scholar
Sretavan, D.W. & Shatz, C.J. (1987). Axon trajectories and pattern of terminal arborization during the prenatal development of the cat's retinogemculate pathway. Journal of Comparative Neurology 255, 386–400.CrossRefGoogle ScholarPubMed
Sretavan, D.W., Shatz, C.J. & Stryker, M.P. (1988). Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336, 468–471.CrossRefGoogle ScholarPubMed
Stone, J. (1981). The Wholemount Handbook: A Guide to the Preparation and Analysis of Retinal Wholemounts. Sidney: Maitland Publishers.Google Scholar
Stuermer, C.A.O. (1988). Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. Journal of Neuroscience 8, 4513–4530.CrossRefGoogle ScholarPubMed
Thanos, S. & Bonhoeffer, F. (1987). Axonal arborization in the developing chick retinotectal system. Journal of Comparative Neurology 261, 155–164.CrossRefGoogle ScholarPubMed
Treff, W.M., Meyer-Koning, E. & Schlote, W. (1972). Morphometnc analysis of a fibre system in the central nervous system. Journal of Microscopy 95, 337–343.CrossRefGoogle ScholarPubMed
Williams, R.W. & Chalupa, L.M. (1982). Prenatal development of retinocollicular projection in the cat: an autoradiographic tracer transport study. Journal of Neuroscience 2, 604–622.CrossRefGoogle Scholar