Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-25T14:23:43.569Z Has data issue: false hasContentIssue false

The morphological characterization and distribution of displaced ganglion cells in the anuran retina

Published online by Cambridge University Press:  02 June 2009

Pál Tóth
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia, Bedford Park, Australia
Charles Straznicky
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia, Bedford Park, Australia

Abstract

The number, dendritic morphology, and retinal distribution of displaced ganglion cells were studied in two anuran species, Xenopus laevis and Bufo marinus. Horseradish peroxidase or cobaltic lysine complex was applied to the cut end of the optic nerve, and the size, shape, and retinal position of retrogradely filled ganglion cells displaced into the inner nuclear layer were determined in retinal wholemount and sectioned material. Approximately 1% of ganglion cells in Xenopus and 0.1% in Bufo were found to be displaced. In both species, many of the previously described orthotopic ganglion cell types (Straznicky & Straznicky, 1988; Straznicky et al., 1990) were present among displaced ganglion cells. In Xenopus more displaced ganglion cells were found in the retinal periphery than in the retinal center, and they formed 3 or 4 distinct bands around the optic nerve head. In Bufo the incidence of displaced ganglion cells was higher along the visual streak than in the dorsal and ventral peripheral retina. These results indicate that the distribution of displaced ganglion cells approximates the retinal distribution of orthotopic ganglion cells. One of the likely mechanisms to account for this developmental paradox may be that the formation of the inner plexiform layer, adjacent to the ciliary margin, acts as a mechanical barrier by preventing the entry of some of the late developing ganglion cells into the ganglion cell layer.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1989

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

Adams, J.C. (1981). Heavy-metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Beach, D.H & Jacobson, M. (1979). Patters of cell proliferation in the retina of the clawed frog during development. Journal of Comparative Neurology 183, 603614.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transations of Royal Society B (London) 225, 109184.Google Scholar
Buhl, E.H. & Dann, J.F. (1988). Morphological diversity of displaced retinal ganglion cells in the rat: a Lucifer yellow study. Journal of Comparative Neurology 269, 210218.CrossRefGoogle Scholar
Bunt, A.H. & Minckler, D.S. (1977). Displaced ganlion cells in the retian of the monkey. Investigative Opthalmology 16, 9598.Google Scholar
Bunt, A.H., Lund, R.D. & Lund, J.S. (1974). Retrograde axonal transport of horseradish peroxidase by ganglion cells of albino rat retina. Brain Research 73, 215228.CrossRefGoogle ScholarPubMed
Coleman, L-A., Dunlop, S.A. & Beazley, L.D. (1984). Patterns of cell division during visual streak formation in the frog Limnodynastes dorsalis. Journal of Embryology and Experimental Morphology 83, 119135.Google ScholarPubMed
Coleman, L-A., Harman, A.M. & Beazley, L.D. (1987). Dispalced ganglion cells in the wallaby Setonix brachyurus. Vision Research 27, 12691277.CrossRefGoogle Scholar
Crandall, J.E., Heaton, M.B. & Bronwell, W.E. (1977). Tectal projection of displaced ganglion cells in avian retina. Investigative Ophthalmology 16, 774776.Google ScholarPubMed
Dräger, U.C. & Olsen, J.F. (1980). Origins of crossed and uncrossed retinal projection in pigmented and albino mice. Journal of Comparative Neurology 191, 383412.CrossRefGoogle ScholarPubMed
Dreher, B., Sefton, A.J., Νi, S.Y.K. & Nisbett, G. (1985). The morphology, number, distribution, and central projection of class I retinal ganglion cells in albino and hooded rats. Brain, Behavior, and Evolution, 26, 1048.CrossRefGoogle Scholar
Dunlop, S.A. & Beazley, L.D. (1981). Changing retinal ganglion cell distribution in the frog (Limnodynastes dorsalis). Journal of Comparative Neurology 202, 221236.CrossRefGoogle Scholar
Dunlop, S.A. & Beazley, L.D. (1984). A morphometric study of the retinal ganglion cell layer and optic nerve from metamorphosis in Xenopus laevis. Vision Research 24, 417427.CrossRefGoogle ScholarPubMed
Dunlop, S.A., Humphrey, M.F. & Beazley, L.D. (1989). Displaced retinal ganglion cells in the frog (Hyla moorei). Neuroscience Letters (Suppl.) 34, S78.Google Scholar
Fite, K.V., Brecha, N., Karten, H.J. & Hunt, S.P. (1981). Displaced ganglion cells and the accessory optic system of pigeon. Journal of Comparative Neurology 195, 279288.CrossRefGoogle ScholarPubMed
Frank, B.D.. & Hollyfield, J.G. (1987 a). Retinal ganglion cell morphology in the frog (Rana pipiens). Journal of Comparative Neurology 266, 421434.Google ScholarPubMed
Frank, B.D. & Hollyfield, J.G. (1987 b). Retina of the tadpole and frog: delayed dendritic development in a subpopulation of ganglion cells coincident with metamorphosis. Journal of Comparative Neurology 266, 435444.CrossRefGoogle Scholar
Gallyas, F. (1979). Light insensitive physical developers. Stain Technology 54, 173176.CrossRefGoogle ScholarPubMed
Görcs, T., Antal, M., Oláh, E. & Székely, G. (1979). An improved cobalt-labeling technique with complex compounds. Acta Biologica Hungarica 30, 7986.Google ScholarPubMed
Grant, P., Rubin, E., & Cima, P. (1980). Ontogeny of the retina and optic nerve in Xenopus laevis, I: Stages in the early development of the retina. Journal of Comparative Neurology 189, 593613.CrossRefGoogle ScholarPubMed
Halász, P. & Martin, P.. (1984). A microcomputer-based system for semiautomatic analysis of histochemical sections. Royal Microscopic Society Proceedings 19, 312p.Google Scholar
Hiscock, J. & Straznicky, C. (1989). Development of amacrine cells with neuropeptide Y- or substance P-like immunoreactivity in Xenopus laevis. Neuroscience Letters (Suppl.) 34, S145.Google Scholar
Hollyfleld, J.G. (1968). Differential addition of cells to the retina in Rana pipiens tadpoles. Developmental Biology 18, 163179.CrossRefGoogle Scholar
Hughes, A. (1975). A quantitative analysis of the cat retinal ganglion cell topography. Journal of Comparative Neurology 163, 107128.CrossRefGoogle ScholarPubMed
Jenkins, S. & Straznicky, C. (1986). Naturally occurring and induced ganglion cell death: a retinal wholemount autoradiographic study in Xenopus. Anatomy and Embryology 174, 5966.CrossRefGoogle ScholarPubMed
Karten, H.J., Fite, K.V. &. Brecha, N. (1977). Specific projection of displaced ganglion cells upon the accessory optic system in the pigeon. Proceedings of the National Academy of Sciences of the U.S.A. 74, 17531756.CrossRefGoogle ScholarPubMed
Kock, J-H., Mecke, E., Orlov, O.Y., Reuter, T. & Vaisanen, R.A. (1989). Ganglion cells in the frog retina: discriminant analysis of histological classes. Vision Research 29, 118.CrossRefGoogle ScholarPubMed
Linden, R. (1987). Displaced ganglion cells in the retina of the rat. Journal of Comparative Neurology 258, 138143.CrossRefGoogle ScholarPubMed
Maslim, J.M., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of the retinal ganglion cells. Journal of Comparative Neurology 254, 382402.CrossRefGoogle ScholarPubMed
Montgomery, N., Fite, K.V. & Bengston, L. (1981). The accessory optic system of Rana pipiens: neuroanatomical considerations and intrinsic organization. Journal of Comparative Neurology 203, 595612.CrossRefGoogle Scholar
Nguyen, V-S. & Straznicky, C. (1989). The development and the topographic organization of the retinal ganglion layer in Bufo marinus. Experimental Brain Research 75, 345353.CrossRefGoogle ScholarPubMed
Nieuwkoop, P.D. & Faber, J. (1956). Normal Tale of Xenopus laevis. Amsterdam: North Holland Publishing Company.Google Scholar
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931944.CrossRefGoogle ScholarPubMed
Stirling, V.R. & Merrill, E.G. (1987). Functional morphology of forgretinal ganglion cells and their central projections: the dimming detectors. Journal of Comparative Neurology 258, 477495.CrossRefGoogle ScholarPubMed
Straznicky, K. & Gaze, R.M. (1971). The growth of the retina in Xenopus laevis: an autoraadiographic study. Journal of Embryology and Experimental Morphology 26, 6779.Google ScholarPubMed
Straznicky, C. & Hiscock, J. (1984). Postmetamorphic retinal growth in Xenopus. Anatomy and Embryology 169, 103109.CrossRefGoogle ScholarPubMed
Straznicky, C. & Straznicky, I.T. (1988). Morphological classification of retinal ganglion cells in adult Xenopus laevis. Anatomy and Embryology 178, 143153.CrossRefGoogle ScholarPubMed
Straznicky, C., Tóth, P. & Nguyen, V-S. (1989). Morphological classification and retinal distribution of large ganglion cells in the retina of Bufo marinus. Experimental Brain Research 77 (in press).Google Scholar
Tay, D., Hiscock, J. & Straznicky, C. (1982). Temporo-nasal asymmetry in the accretion of retinal ganglion cells in late larval and post- metamorphic Xenopus. Anatomy and Embryology 164, 87115.CrossRefGoogle Scholar
Tóth, P. & Straznicky, C. (1989 a). Dendritic morphology of identified retinal ganglion cells in Xenopus laevis: a comparison between the results of horseradish peroxidase and cobaltic-lysine retrograde labeling. Archive Histology and Cytology 52, 8793.CrossRefGoogle Scholar
Tóth, P. & Straznicky, C. (1989 b). Biplexiform ganglion cells in the retina of Xenopus laevis. Brain Research 497, (in press).Google Scholar
Zhu, B-S., Hiscock, J. & Straznicky, C. (1990). The development of the inner nuclear layer of the anuran retina: a morphometric analysis. Anatomy and Embryology (in press).CrossRefGoogle Scholar