Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-05-17T03:06:58.766Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of dendritic trees of rabbit retinal alpha ganglion cells: Relation to differential retinal growth

Published online by Cambridge University Press:  02 June 2009

C. Deich ,
B. Seifert ,
L. Peichl  and
A. Reichenbach
C. Deich
Affiliation:
Carl-Ludwig-Institut für Physiologie, Universität Leipzig, Leipzig, Germany
B. Seifert
Affiliation:
Carl-Ludwig-Institut für Physiologie, Universität Leipzig, Leipzig, Germany
L. Peichl
Affiliation:
Max-Planck-Institut für Hirnforschung, Abteilung für Neuroanatomie, Frankfurt/Main, Germany
A. Reichenbach
Affiliation:
Carl-Ludwig-Institut für Physiologie, Universität Leipzig, Leipzig, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

To provide a quantitative description of the postnatal development of dendritic trees in alpha ganglion cells of the rabbit retina, these cells were stained either by intracellular injection of Lucifer yellow or by application of the lipophilic dye Oil. This was done at three developmental stages: postnatal day (P) 8/9, P 16/17, and in adults. For different retinal locations we quantified the alpha cell dendritic field area, the number of dendritic branch points, and the average dendritic length between branch points. According to the alpha cell location, the data were collected in three groups representing the retinal center, midperiphery, and far periphery, respectively. The data were then correlated with the postnatal retinal expansion which is known to differ among the above topographic regions of the retinae (Reichenbach et al., 1993). Our results show that the growth of alpha ganglion cell dendrites is not proportional to, but significantly exceeds, that of the local retinal tissue. Between P 8/9 and adulthood, the area of central alpha cells increases almost six-fold from 26,000 to 144,000 μm2 (retinal expansion: 2.2-fold), and that of peripheral cells more than 15-fold from 35,000 to 556,000 μm2 (retinal expansion: four-fold). During this period, the coverage factor of alpha cell dendritic fields increases about three-fold, and reaches adult levels of about 3 (retinal center) and 2.2 (periphery), respectively. The number of dendritic branch points remains nearly constant, and the distance between them increases by a factor close to the square root of the factor by which the dendritic field area grows. Thus, it appears that, from the second postnatal week on, dendritic trees of rabbit alpha ganglion cells increase by intense “interstitial growth,” rather than by outgrowth of (new) dendritic branches. This growth pattern is different from that of some other rabbit retinal ganglion cell types, and of alpha ganglion cells of the cat retina, whose dendritic trees expand at a rate equal to or less than that of the surrounding retinal tissue. The consequences for synaptic contacts with bipolar and amacrine cells are discussed; they suggest a high degree of synaptic plasticity during normal postnatal retinal growth.

Keywords

Retinal growthAlpha ganglion cellsMorphometryGrowth mechanicsRabbit retina
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 979 - 988
Copyright
Copyright © Cambridge University Press 1994

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

Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1983). Quantitative morphology of rabbit retinal ganglion cells. Proceedings of the Royal Society B (London) 217, 341–355.Google ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.CrossRefGoogle ScholarPubMed
Ault, S.J. & Leventhal, A.G. (1994). Postnatal development of different classes of cat retinal ganglion cells. Journal of Comparative Neurology 339, 106–116.CrossRefGoogle ScholarPubMed
Bowe-Anders, C., Miller, R.F. & Dacheux, R.F. (1975). Developmental characteristics of receptive field organization in the isolated retina eye-cup of the rabbit. Brain Research 87, 61–65.Google Scholar
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
Coulombre, A.J. (1956). The role of intraocular pressure in the development of the chick eye. Journal of Experimental Zoology 133, 211–223.CrossRefGoogle 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.Google Scholar
Famiglietti, E.V. (1987). Morphological classification of ganglion cells in rabbit retina. Society for Neuroscience Abstracts 13, 380.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.Google Scholar
Godement, P., Vanselow, J., Thanos, S. & Bonhoeffer, F. (1987). A study of developing visual systems with a new method for staining neurones and their processes in fixed tissue. Development 101, 697–713.Google Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–442.Google Scholar
Honig, M.G. & Hume, R.I. (1986). Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. Journal of Cell Biology 103, 171–187.Google Scholar
Kelling, S.T., Sengelaub, D.R., Wikler, K.C. & Finlay, B.L. (1989). Differential elasticity of the immature retina: A contribution to the development of the area centralis? Visual Neuroscience 2, 117–120.CrossRefGoogle Scholar
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Ault, S.J., Vitek, D.J. & Shou, T. (1989). Extrinsic determinants of retinal ganglion cell development in primates. Journal of Comparative Neurology 286, 170–189.Google Scholar
Leventhal, A.G. & Schall, J.D. (1989). Extrinsic determinants of retinal ganglion cell development in cats and monkeys. In Development of the Vertebrate Retina, ed. Finlay, B.L. & Sengelaub, D.R., pp. 173–195. New York & London: Plenum Press.Google Scholar
Leventhal, A.G., Schall, J.D. & Ault, S.J. (1988). Extrinsic determinants of retinal ganglion cell structure in the cat. Journal of Neuroscience 8, 2028–2038.CrossRefGoogle ScholarPubMed
Masland, R.H. (1977). Maturation of function in the developing rabbit retina. Journal of Comparative Neurology 175, 275–286.CrossRefGoogle ScholarPubMed
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 382–402.Google Scholar
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1984). Non-uniform postnatal growth of the cat retina. Journal of Comparative Neurology 228, 598–608.Google Scholar
McArdle, C.B., Dowling, J.E. & Masland, R.H. (1977). Development of outer segments and synapses in the rabbit retina. Journal of Comparative Neurology 175, 253–278.Google Scholar
Mitrofanis, J., Robinson, S.R. & Ashwell, K. (1992). Development of catecholaminergic, indoleamine-accumulating and NADPH-diaphorase amacrine cells in rabbit retinae. Journal of Comparative Neurology 319, 560–585.Google Scholar
Nelson, R., Kolb, H., Robinson, M.M. & Mariani, A.P. (1981). Neural circuitry of the cat retina: Cone pathways to ganglion cells. Vision Research 21, 1527–1536.CrossRefGoogle ScholarPubMed
Peichl, L. (1991). Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells. Visual Neuroscience 7, 155–169.CrossRefGoogle ScholarPubMed
Peichl, L., Buhl, E.H. & Boycott, B.B. (1987 a). Alpha ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 25–41.CrossRefGoogle ScholarPubMed
Peichl, L., Ott, H. & Boycott, B.B. (1987 b). Alpha ganglion cells in mammalian retinae. Proceedings of the Royal Society B (London) 231, 169–197.Google Scholar
Perry, V.H. & Maffel, L. (1988). Dendritic competition: competition for what? Developmental Brain Research 41, 195–208.Google Scholar
Provis, J.M. (1981). Rabbit retinal ganglion cell morphology. Proceedings Australian Physiological and Pharmacological Society 12, 162 P.Google Scholar
Pu, M. & Amthor, F.R. (1990). Dendritic morphologies of retinal ganglion cells projecting to the lateral geniculate nucleus in the rabbit. Journal of Comparative Neurology 302, 675–693.Google Scholar
Ramoa, A.S. & Yamasaki, Y.N. (1992). Mechanisms of dendritic tree development in mammalian retinal ganglion cells. In The Visual System from Genesis to Maturity, ed. Lent, R., pp. 71–85. New York: Birkhauser.Google Scholar
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1988). Dendritic growth and remodelling of cat retinal ganglion cells during fetal and postnatal development. Journal of Neuroscience 8, 4239–4261.Google Scholar
Reh, T.A., Tetzlaff, W., Ertlmaier, A. & Zwiers, H. (1993). Developmental study of the expression of B50/GAP-43 in rat retina. Journal of Neurobiology 24, 949–958.Google Scholar
Reichenbach, A., Schnitzer, J., Friedrich, A., Ziegert, W., Brückner, G. & Schober, W. (1991 a). Development of the rabbit retina. I. Size of eye and retina, and postnatal cell proliferation. Anatomy and Embryology 183, 287–297.Google Scholar
Reichenbach, A., Schnitzer, J., Friedrich, A., Knothe, A.-K. & Henke, A. (1991 b). Development of the rabbit retina. II. Müller cells. Journal of Comparative Neurology 311, 33–44.CrossRefGoogle ScholarPubMed
Reichenbach, A., Eberhardt, W., Scheibe, R., Deich, C., Seifert, B., Reichelt, W., Dähnert, K. & Rödenbeck, M. (1991 c). Development of the rabbit retina. IV. Tissue tensility and elasticity in dependence on topographic specializations. Experimental Eye Research 53, 241–251.CrossRefGoogle ScholarPubMed
Reichenbach, A., Schnitzer, J., Reichelt, E., Osborne, N.N., Fritzsche, B., Puls, A., Richter, U., Friedrich, A., Knothe, A.-K., Schober, W. & Timmermann, U. (1993). Development of the rabbit retina, III: Differential retinal growth, and density of projection neurons and interneurons. Visual Neuroscience 10, 479–498.Google Scholar
Robinson, S.R. (1991). Development of the mammalian retina. In Neuroanatomy of the Visual Pathways and their Development, ed. Dreher, B. & Robinson, S.R., pp. 69–128. (Vol. 3 of Cronly-Drlon, J.R. (series ed.): Vision and Visual Dysfunction). England: Macmillan.Google Scholar
Robinson, S.R., Dreher, B. & McCall, M.J. (1989). Nonuniform retinal expansion during the formation of the rabbit's visual streak: Implications for the ontogeny of mammalian retinal topography. Visual Neuroscience 2, 201–219.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurones in the rabbit retina. Journal of Neuroscience 6, 3331–3347.Google Scholar
Scheibe, R., Schnitzer, J., Rührenbeck, J., Wohlrab, F. & Reichen-Bach, A. (1994). Development of A-type (axonless) horizontal cells in the rabbit retina. Journal of Comparative Neurology (submitted).Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurones in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google ScholarPubMed
Wässle, H. (1988). Dendritic maturation of retinal ganglion cells. Trends in Neurosciences 11, 87–89.Google Scholar
Watanabe, M., Fukuda, Y., Hsiao, C.-F. & Ito, H. (1985). Electron microscopic analysis of amacrine and bipolar cell inputs on Y-, X-and W-cells in the cat retina. Brain Research 358, 229–240.CrossRefGoogle Scholar
Wong, R.O.L. (1990). Differential growth and remodelling of ganglion cell dendrites in the postnatal rabbit retina. Journal of Comparative Neurology 294, 109–132.Google Scholar
Wong, R.O.L. & Collin, S.P. (1989). Dendritic maturation of displaced putative cholinergic amacrine cells in the rabbit retina. Journal of Comparative Neurology 287, 164–178.Google Scholar