Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T23:15:03.620Z Has data issue: false hasContentIssue false
  • English
  • Français

Synchronous neurite branchings in single goldfish retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

A. T. Ishida  and
M.- H. Cheng
A. T. Ishida
Affiliation:
Department of Animal Physiology, University of California, Davis
M.- H. Cheng
Affiliation:
Department of Animal Physiology, University of California, Davis
Get access Rights & Permissions [Opens in a new window]

Abstract

We have examined the time course of branch formation in neurites of retinal ganglion cells isolated from adult goldfish (Carassius auratus). These neurites elongate at approximately 13 μm/h, and usually branch by bifurcation of growth cones at their tips. The times elapsed between branchings in different neurites of single cells can be described by a Poisson distribution with a mean interval of approximately 2 h. As predicted by this distribution, a relatively large number of branchings occur simultaneously in different neurites of individual cells. Simultaneous branchings of neurites elongating at a common rate generate branch points that lay equidistant from their soma. Since similar branching patterns can be seen in dendrites of retinal ganglion and amacrine cells in situ, these results are consistent with the possibility that dendrites of individual neurons branch synchronously and grow at common rates during development.

Keywords

Retinal ganglion cellsBranching patternsNeuritesDendritic development
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 5 , May 1991 , pp. 537 - 549
Copyright
Copyright © Cambridge University Press 1991

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

Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397–419.CrossRefGoogle ScholarPubMed
Bray, D. (1970). Surface movements during the growth of single cx- planted neurons. Proceedings of the National Academy of Sciences of the U.S.A. 65, 905–910.CrossRefGoogle Scholar
Bray, D. (1973). Branching patterns of individual sympathetic neurons in culture. Journal of Cell Biology 56, 702–712.CrossRefGoogle ScholarPubMed
Brown, J.E. (1965). Dendritic fields of retinal ganglion cells of the rat. Journal of Neurophysiology 28, 1091–1110.CrossRefGoogle ScholarPubMed
Cáceres, A., Banker, G.A. & Binder, L. (1986). Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. Journal of Neuroscience 6, 714–722.CrossRefGoogle ScholarPubMed
Cajal, S.R. Y(1972). The Structure of the Retina. Translated by Thorpe, S.A. & Glickstein, M., pp. 3–132. Springfield: C.C. Thomas.Google Scholar
Dann, J.F., Buhl, E.H. & Peichl, L. (1987). Dendritic maturation in cat retinal ganglion cells: a Lucifer yellow study. Neuroscience Letters 80, 21–26.CrossRefGoogle ScholarPubMed
Dann, J.F., Buhl, E.H. & Peichl, L. (1988). Postnatal dendritic maturation of alpha and beta ganglion cells in cat retina. Journal of Neuroscience 8, 1485–1499.CrossRefGoogle ScholarPubMed
Dotti, C.G., Sullivan, C.A. & Banker, G.A. (1988). Establishment of polarity by hippocampal neurons in culture. Journal of Neuroscience 8, 1454–1468.CrossRefGoogle ScholarPubMed
Eyzel, U.T., Peichl, L. & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: quantitative characteristics and the sensitive period. Journal of Comparative Neurology 242, 134–145.CrossRefGoogle Scholar
Fukuda, Y., Morigiwa, K. & Tauchi, M. (1988). Morphology of alpha ganglion cells in the albino rat retina. Biomedical Research (Suppl.) 9, 139–142.Google Scholar
Goslon, K., Schreyer, D.J., Skene, J.H.P. & Banker, G. (1988). Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature 336, 672–674.CrossRefGoogle Scholar
Grafstein, B. (1986). The retina as a regenerating organ. In The Retina: A Model for Cell Biology Studies, Pt. II, ed. Adler, R. & Farber, D., pp. 275–335. New York: Academic Press.CrossRefGoogle Scholar
Hall, G.F. & Cohen, M.J. (1988). Dendritic amputation redistributes sprouting evoked by axotomy in lamprey central neurons. Journal of Neuroscience 8, 3598–3606.CrossRefGoogle ScholarPubMed
Harris, W.A., Holt, C.E. & Bonhoeffer, F. (1987). Retinal axons with and without their somata, growing to and arborizing in the tecturn of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development 101, 123–133.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. (1987). Constant dendritic coverage by ganglion cells with growth of the goldfish's retina. Vision Research 27, 17–22.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. & Easter, S.S. (1986). Retinal ganglion cells in goldfish: a qualitative classification into four morphological types, and a quantitative study of the development of one of them. Journal of Neuroscience 6, 1037–1050.CrossRefGoogle Scholar
Ishida, A.T. & Cheng, M.-H. (1991). Cold inhibits neurite outgrowth from single retinal ganglion cells isolated from adult goldfish. Experimental Eye Research 52, 175–191.CrossRefGoogle ScholarPubMed
Ishida, A.T. & Cheng, M.-H. (1991). Dendrites of single retinal ganglion and arnacrine cells may branch synchronously during development. Investigative Ophthalmology and Visual Science 32, 94.Google Scholar
Ishida, A.T., Cheng, M.-H. & Bindokas, V.P. (1990). A dihydropyridine-sensitive calcium conductance in regenerating retinal ganglion cells. Investigative Ophthalmology and Visual Science 31, 390.Google Scholar
Ishida, A.T. & Cohen, B.N. (1988). GABA-activated whole-cell cur-Temporal patterns in neurite branchings rents in isolated retinal ganglion cells. Journal of Neurophysiology 60, 381–396.CrossRefGoogle Scholar
Kirby, M.A. & Chalupa, L.M. (1986). Retinal crowding alters the morphology of alpha ganglion cells. Journal of Comparative Neurology 251, 532–541.CrossRefGoogle ScholarPubMed
Kock, J.-H. (1982). Dendritic tree structure and dendritic hypertrophy during growth of the crucian carp eye. Journal of Comparative Neurology 209, 275–286.CrossRefGoogle ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells, and ganglion cells of the cat retina: a Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
Kolb, H., Perlman, I. & Normann, R.A. (1988). Neural organization of the retina of the turtle (Mauremys caspica): A light-microscope and Golgi study. Visual Neuroscience 1, 47–72.CrossRefGoogle ScholarPubMed
Kosik, K.S. & Finch, E.A. (1987). MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. Journal of Neuroscience 7, 3142–3153.CrossRefGoogle ScholarPubMed
Landreth, G.E. & Agranoff, B.W. (1976). Explant culture of adult goldfish retina: effect of prior optic nerve crush. Brain Research 118, 299–303.CrossRefGoogle ScholarPubMed
Lipton, S.A., Frosch, M.P., Phillips, M.D., Tauck, D.L. & Aizenman, E. (1988). Nicotinic antagonists enhance process outgrowth by rat retinal ganglion cells in culture. Science 239, 1293–1296.CrossRefGoogle ScholarPubMed
Martin, A.R. (1965). Quantal nature of synaptic transmission. Physiological Reviews 46, 51–66.CrossRefGoogle Scholar
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 382–402.CrossRefGoogle ScholarPubMed
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1984). Nonuniform postnatal growth of the cat retina. Journal of Comparative Neurology 228, 598–608.CrossRefGoogle ScholarPubMed
Montague, P.R. & Friedlander, M.J. (1989). Expression of an intrinsic growth strategy by mammalian retinal neurons. Proceedings of NationalAcademy of Sciences of the U.S.A. 86, 7223–7227.CrossRefGoogle ScholarPubMed
Morest, D.K. (1970). The pattern of neurogenesis in the retina of the rat. Zeitschrift für Anatomie und Entwicklungsgeschichte 131, 45–67.CrossRefGoogle ScholarPubMed
Murakami, M. & Shimoda, Y. (1977). Identification of amacrine and ganglion cells in the carp retina. Journal of Physiology 264, 801–818.CrossRefGoogle ScholarPubMed
Murray, M. & Grafstein, B. (1969). Changes in the morphology and amino-acid incorporation of regenerating goldfish optic neurons. Experimental Neurology 23, 544–560.CrossRefGoogle ScholarPubMed
Nishimura, Y., Inoue, Y. & Shimat, K. (1979). Morphological development of retinal ganglion cells in the chick embryo. Experimental Neurology 64, 44–60.CrossRefGoogle ScholarPubMed
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.CrossRefGoogle ScholarPubMed
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1987). Transient morpho logical features of identified ganglion cells in living fetal and neonatal retina. Science 237, 522–525.CrossRefGoogle Scholar
Sakaguchi, D.S., Murphey, R.K., Hunt, R.K. & Tompkins, R. (1984). The development of retinal ganglion cells in a tetraploid strain of Xenopus laevis: a morphological study utilizing intracellular dye injection. Journal of Comparative Neurology 224, 231–251.CrossRefGoogle Scholar
Shatz, C.J. & Sretavan, D.W. (1986). Interactions between retinal ganglion cells during the development of the mammalian visual system. Annual Reviews of Neuroscience 9, 171–207.CrossRefGoogle ScholarPubMed
Shiosaka, S., Kiyama, H. & Tohyama, M. (1984). A simple method for the separation of retinal sublayers from the entire retina with special reference to application for cell culture. Journal of Neuroscience Methods 10, 229–235.CrossRefGoogle ScholarPubMed
Stell, W.K. & Witkovsky, P. (1973). Retinal structure in the smooth dogfish (Mustelus canis): general description and light microscopy of giant ganglion cells. Journal of Comparative Neurology 148, 1–32.CrossRefGoogle ScholarPubMed
Tauchi, M. & Masland, R.H. (184). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google Scholar
Thanos, S. (1988). Alterations in the morphology of ganglion cell dendrites in the adult rat retina after optic nerve transection and grafting of peripheral nerve segments. Cell and Tissue Research 254, 599–609.CrossRefGoogle ScholarPubMed
Truman, J.W. & Reiss, S.E. (1976). Dendritic reorganization of an identified motoneuron during metamorphosis of the tobacco horn- worm moth. Science 192, 477–479.CrossRefGoogle Scholar
Vaney, D.I. (1986). Morphological identification of serotoninaccumulating neurons in the living retina. Science 233, 444–445.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L. & Boycott, B.B. (1988). Neurofibrillar long- range amacrine cells in mammalian retinae. Proceedings of the Royal Society B (London) 235, 203–219.Google ScholarPubMed
Wagner, H.-J. & Wagner, E. (1988). Amacrine cells in the retina of a teleost fish, the roach (Rutilus rutilus): a Golgi study on differentiation and layering. Philosophical Transactions of the Royal Society (London) 321, 263–324.Google Scholar
Wakshull, E., Johnson, M.I. & Burton, H. (1979). Postnatal rat sympathetic neurons in culture, I: A comparison with embryonic neurons. Journal of Neurophysiology 42, 1410–1425.CrossRefGoogle Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1981). Dendritic territories of cat retinal ganglion cells. Nature 292, 344–345.CrossRefGoogle ScholarPubMed
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google ScholarPubMed
Yawo, H. (1987). Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy. Journal of Neuroscience 7, 3703–3711.CrossRefGoogle ScholarPubMed