Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-30T20:37:07.291Z Has data issue: false hasContentIssue false
  • English
  • Français

Dendritic competition in the developing retina: Ganglion cell density gradients and laterally displaced dendrites

Published online by Cambridge University Press:  02 June 2009

Rafael Linden
Rafael Linden
Affiliation:
Instituto de Biofisica da UFRJ, Rio de Janeiro, Brazil
Get access Rights & Permissions [Opens in a new window]

Abstract

Dendrites of retinal ganglion cells (RGCs) tend to be distributed preferentially toward areas of reduced RGC density. This, however, does not occur in the retina of normal pigmented rats, in which it has been suggested that the centro-peripheral gradient of RGC density is too shallow to provide directional guidance to growing dendrites. In this study, laterally displaced dendrites of RGCs retrogradely labeled with horseradish peroxidase were related to cell density gradients induced experimentally in the rat retina. Neonatal unilateral lesions of the optic tract produced retrograde degeneration of contralaterally projecting RGCs, but spared ipsilaterally projecting neurons in the same retina. These lesions created an anomalous temporal to nasal gradient of cell density across the decussation line, opposite to the nasal to temporal gradient found along the same axis in either normal rats or rats that had the contralateral eye removed at birth. RGCs in rats that received optic tract lesions had their dendrites displaced laterally toward the depleted nasal retina, while in either normal or enucleated rats there was no naso-temporal asymmetry. The lateral displacement affected both primary dendrites and higher-order branches. However, the gradient of cell density after optic tract lesions was less steep than the gradient in either normal or enucleated rats. To test for the presence of steeper gradients at early stages of development, RGC density gradients were also examined at postnatal day 5 (P5). In normal rats, the RGCs were homogeneously distributed throughout the retina, while rats given optic tract lesions at birth already showed a temporo-nasal density gradient at P5. Still, this anomalous gradient was less steep than that found in normal adults. It is concluded that the time course, rather than the steepness of the RGC density gradient, is the major determinant of the lateral displacement of dendritic arbors with respect to the soma in developing RGCs. The data are consistent with the idea that the overall shape of dendritic arbors depends in part on dendritic competition during retinal development.

Keywords

RetinaDevelopmentDendritesCell deathCompetition
Type
Research Article
Information
Visual Neuroscience , Volume 10 , Issue 2 , March 1993 , pp. 313 - 324
Copyright
Copyright © Cambridge University Press 1993

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

Beazley, I.D., Perry, V.H., Baker, B. & Darby, J.E. (1987). An investigation into the role of ganglion cells in the regulation of division and death of other retinal cells. Developmental Brain Research 33, 169–184CrossRefGoogle Scholar
Cowey, A. & Perry, V.H. (1979). The projection of the temporal retina in rats, studied by retrograde transport of horseradish peroxidase. Experimental Brain Research 35, 457–464CrossRefGoogle ScholarPubMed
Eysel, U.T., Peichl, L. & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134–145CrossRefGoogle ScholarPubMed
Fukuda, Y. (1977). A three-group classification of rat retinal ganglion cells: Histological and physiological studies. Brain Research 119, 327–344CrossRefGoogle ScholarPubMed
Guhlery, R.W. (1988). Competition in the development of visual pathways. In The Making of the Nervous System, ed. Parnavelas, J.G., Stern, C.D. & Stirling, R.V., pp. 356–380. Oxford: Oxford University Press.Google Scholar
Hanker, J.S., Yates, P.E., Metz, C.B. & Rustioni, A. (1977). A new, specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochemical Journal 9, 789–792CrossRefGoogle ScholarPubMed
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organization. In Handbook of Sensory Physiology, Vol. VII/5. The Visual System in Evolution. A: Vertebrates, ed. Crescitelli, F., pp. 613–756. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Hughes, A. (1979). A schematic eye for the rat. Vision Research 19, 569–588CrossRefGoogle ScholarPubMed
Kirby, M.A. & Steineke, T.C. (1991). Evidence for the radial migration of retinal ganglion cells (RGCs) during formation of the foveal depression in the primate. Abstracts of the III IBRO World Congress of Neuroscience, Montreal, Canada, p. 315.Google Scholar
Kriegstein, A.R. & Dichter, M.A. (1983). Morphological classification of rat cortical neurons in cell culture. Journal of Neuroscience 3, 1634–1647CrossRefGoogle ScholarPubMed
Lau, K.C., So, K.F., Tay, D. & Jen, L.S. (1991). Elimination of transient dendritic spines in ipsilaterally projecting retinal ganglion cells in rats with unilateral thalamectomy. Neuroscience Letters 121, 255–258CrossRefGoogle Scholar
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. Journal of Comparative Neurology 237, 216–226CrossRefGoogle ScholarPubMed
Leventhal, A.G. & Schall, J.D. (1983). Structural basis for orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465–475CrossRefGoogle ScholarPubMed
Leventhal, A.G., Schall, J.D. & Ault, S.J. (1988). Extrinsic determinants of retinal ganglion cell structure in the cat. Journal of Neuroscience 8, 2028–2038CrossRefGoogle ScholarPubMed
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology (London) 329, 243–261CrossRefGoogle ScholarPubMed
Levinthal, F., Macagno, E. & Levinthal, C. (1975). Anatomy and development of identified cells in isogenic organisms. Cold SpringHarbor Symposia of Quantitative Biology 40, 321–333CrossRefGoogle Scholar
Lia, B., Williams, R.W. & Chalupa, L.M. (1987). Formation of retinal ganglion cell topography during prenatal development. Science 236, 848–851CrossRefGoogle ScholarPubMed
Linden, R. (1992). Dendritic competition: A principle of retinal development. In The Visual System from Genesis to Maturity, ed. Lent, R., pp. 86–103. Boston, Massachusetts: Birkhauser.CrossRefGoogle Scholar
Linden, R., Cavalcante, L.A. & Barradas, P.C. (1986). Mononu-Clear phagocytes in the retina of developing rats. Histochemistry 85, 335–340CrossRefGoogle Scholar
Linden, R. & Esbérard, C.E.L. (1987). Displaced amacrine cells in the ganglion cell layer of the hamster retina. Vision Research 27, 1071–1076CrossRefGoogle ScholarPubMed
Linden, R. & Perry, V.H. (1982). Ganglion cell death within the developing retina: A regulatory role for retinal dendrites? Neuroscience 7, 2813–2827CrossRefGoogle ScholarPubMed
Linden, R. & Serfaty, C.A. (1985). Evidence for differential effects of terminal and dendritic competition upon developmental neuronal death in the retina. Neuroscience 15, 853–868CrossRefGoogle ScholarPubMed
Maffei, L. & Perry, V.H. (1988). The axon initial segment as a possible determinant of retinal ganglion cell dendritic geometry. Developmental Brain Research 41, 185–194CrossRefGoogle Scholar
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 382–402CrossRefGoogle ScholarPubMed
McCall, M.J., Robinson, S.R. & Dreher, B. (1987). Differential retinal growth appears to be the primary factor producing the ganglion cell density gradient in the rat. Neuroscience Letters 79, 78–84CrossRefGoogle ScholarPubMed
Montague, P.R. & Friedlander, M.J. (1989). Expression of an intrinsic growth strategy by mammalian retinal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 86, 7223–7227CrossRefGoogle ScholarPubMed
Nakatani, M. & Linden, R. (1991). Axon orientation and axo-den-dritic polarity of retinal ganglion cells during postnatal development in the rat. Brazilian Journal of Medical and Biological Research 24, 937–941Google ScholarPubMed
Peichl, L. & Wässle, H. (1983). The structural correlate of the receptive field centre of alpha ganglion cells in the cat retina. Journal of Physiology (London) 341, 309–324CrossRefGoogle ScholarPubMed
Perry, V.H. (1979). The ganglion cell layer of the rat retina: A Golgi study. Proceedings of the Royal Society B (London) 204, 363–375Google ScholarPubMed
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944CrossRefGoogle 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, 583–594CrossRefGoogle 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, 356–368CrossRefGoogle ScholarPubMed
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685CrossRefGoogle ScholarPubMed
Perry, V.H. & Maffei, L. (1988). Dendritic competition: Competition for what? Developmental Brain Research 41, 195–200CrossRefGoogle Scholar
Perry, V.H. & Walker, M. (1980). Morphology of cells in the ganglion cell layer during development of the rat retina. Proceedings of the Royal Society B (London) 208, 433–445Google ScholarPubMed
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1988). Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. Journal of Neuroscience 8, 4239–4261CrossRefGoogle ScholarPubMed
Rapaport, D.H. & Stone, J. (1984). The area centralis of the retina in the cat and other mammals: Focal point for function and development of the visual system. Neuroscience 11, 289–300CrossRefGoogle Scholar
Rowe, M.H. & Dreher, B. (1982). Functional morphology of beta cells in the area centra/is of the cat’s retina: A model for the evolution of central retinal specializations. Brain, Behavior, and Evolution 21, 1–23CrossRefGoogle Scholar
Schall, J.D. & Leventhal, A.G. (1987). Relationships between ganglion cell dendritic structure and retinal topography in the cat. Journal of Comparative Neurology 257, 149–159CrossRefGoogle ScholarPubMed
Schall, J.D., Perry, V.H. & Leventhal, A.G. (1987). Ganglion cell dendritic structure and retinal topography in the rat. Journal of Comparative Neurology 257, 160–165CrossRefGoogle ScholarPubMed
Serfaty, C.A., Reese, B.E. & Linden, R. (1990). Cell death and interocular interactions among retinofugal axons: Lack of binocularly matched specificity. Developmental Brain Research 56, 198–204CrossRefGoogle ScholarPubMed
Tiao, Y.-C. & Blakemore, C. (1976). Regional specialization in the golden hamster retina. Journal of Comparative Neurology 168, 439–456Google 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, 32–69CrossRefGoogle ScholarPubMed