Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-07-01T09:38:25.542Z Has data issue: false hasContentIssue false
  • English
  • Français

Large retinal ganglion cells in the pipid frog Xenopus laevis form independent, regular mosaics resembling those of teleost fishes

Published online by Cambridge University Press:  02 June 2009

K. M. Shamim ,
P. Tóth  and
J. E. Cook
K. M. Shamim
Affiliation:
Department of Anatomy, Institute of Postgraduate Medicine and Research, Dhaka, Bangladesh
P. Tóth
Affiliation:
Department of Anatomy, University Medical School, Szigeti út 12, Pécs H-7643, Hungary
J. E. Cook
Affiliation:
Department of Anatomy and Developmental Biology, University College London, Gower Street, London WCIE 6BT, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Population-based studies of retinal neurons have helped to reveal their natural types in mammals and teleost fishes. In this, the first such study in a frog, labeled ganglion cells of the mesobatrachian Xenopus laevis were examined in flatmounts. Cells with large somata and thick dendrites could be divided into three mosaic-forming types, each with its own characteristic stratification pattern. These are named αa, αab, and αc, following a scheme recently used for teleosts. Cells of the αa mosaic (~0.4% of all ganglion cells) had very large somata and trees, arborizing diffusely within sublamina a (the most sclerad). Their distal dendrites were sparsely branched but achieved consistent coverage by intersecting those of their neighbors. Displaced and orthotopic cells belonged to the same mosaic, as did cells with symmetric and asymmetric trees. Cells of the αab mosaic (~1.2%) had large somata, somewhat smaller trees that appeared bistratified at low magnification, and dendrites that branched extensively. Their distal dendrites arborized throughout sublamina b and the vitread part of a, tessellating with their neighbors. All were orthotopic; most were symmetric. Cells of the αc mosaic (~0.5%) had large somata and very large, sparse, flat, overlapping trees, predominantly in sublamina c. All were orthotopic; some were asymmetric. Nearest-neighbor analyses and spatial correlograms confirmed that each mosaic was regular and independent, and that spacings were reduced in juvenile frogs. Densities, proportions, sizes, and mosaic statistics are tabulated for all three types, which are compared with types defined previously by size and symmetry in Xenopus and potentially homologous mosaic-forming types in teleosts. Our results reveal strong organizational similarities between the large ganglion cells of teleosts and frogs. They also demonstrate the value of introducing mosaic analysis at an early stage to help identify characters that are useful markers for natural types and that distinguish between within-type and between-type variation in neuronal populations.

Keywords

Dendritic treeTessellationClassificationNatural typeHomology
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 811 - 826
Copyright
Copyright © Cambridge University Press 1997

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. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience) 2, 141–145.CrossRefGoogle ScholarPubMed
Chung, S.H., Stirling, R.V. & Gaze, R.M. (1975). The structural and functional development of the retina in larval Xenopus. Journal of Embryology and Experimental Morphology 33, 915–940.Google ScholarPubMed
Cook, J.E. (1987). A sharp retinal image increases the topographic precision of the goldfish retinotectal projection during optic nerve regeneration in stroboscopic light. Experimental Brain Research 68, 319–328.CrossRefGoogle ScholarPubMed
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 15–30.CrossRefGoogle ScholarPubMed
Cook, J.E. & Becker, D.L. (1991). Regular mosaics of large displaced and non-displaced ganglion cells in the retina of a cichlid fish. Journal of Comparative Neurology 306, 668–684.CrossRefGoogle ScholarPubMed
Cook, J.E., Becker, D.L. & Kapila, R. (1992). Independent mosaics of large inner- and outer-stratified ganglion cells in the goldfish retina. Journal of Comparative Neurology 318, 355–366.CrossRefGoogle ScholarPubMed
Cook, J.E., Kondrashev, S.L. & Podugolnikova, T.A. (1996). Biplexiform ganglion cells, characterized by dendrites in both outer and inner plexiform layers, are regular, mosaic-forming elements of teleost fish retinae. Visual Neuroscience 13, 517–528.CrossRefGoogle ScholarPubMed
Cook, J.E. & Sharma, S.C. (1995). Large retinal ganglion cells in the channel catfish (Ictalurus punctatus): Three types with distinct dendritic stratification patterns form similar but independent mosaics. Journal of Comparative Neurology 362, 331–349.CrossRefGoogle ScholarPubMed
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, 417–427.CrossRefGoogle ScholarPubMed
Dunn-Meynell, A.A. & Sharma, S.C. (1986). The visual system of the channel catfish (Ictalurus punctatus). I. Retinal ganglion cell morphology. Journal of Comparative Neurology 247, 32–55.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Light insensitive physical developers. Slain Technology 54, 173–176.Google ScholarPubMed
Görcs, T, Antal, M., Oláh, É. & Székely, G. (1979). An improved cobalt labeling technique with complex compounds. Acta Biologica Academiae Scientiarum Hungaricae 30, 78–86.Google ScholarPubMed
Graydon, M.L. & Giorgi, P.P. (1984). Topography of the retinal ganglion cell layer of Xenopus. Journal of Anatomy 139, 145–157.Google ScholarPubMed
Hoskins, S.G. & Grobstein, P. (1985). Development of the ipsilateral retinothalamic projection in the frog Xenopus laevis. I. Retinal distribution of ipsilaterally projecting cells in normal and experimentally manipulated frogs. Journal of Neuroscience 5, 911–919.CrossRefGoogle ScholarPubMed
Krauth, J. (1983). The interpretation of significance tests for independent and dependent samples. Journal of Neuroscience Methods 9, 269–281.CrossRefGoogle ScholarPubMed
Lázár, G., Tóth, P., Csank, G. & Kicliter, E. (1983). Morphology and location of tectal projection neurons in frogs: A study with HRP and cobalt-filling. Journal of Comparative Neurology 215, 108–120.CrossRefGoogle ScholarPubMed
Levick, W.R. & Thibos, L.N. (1983). Receptive fields of cat ganglion cells: Classification and construction. Progress in Retinal Research 2, 267–319.CrossRefGoogle Scholar
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
Podugolnikova, T.A. (1985). Morphology of bipolar cells and their participation in spatial organization of the inner plexiform layer of jack mackerel retina. Vision Research 25, 1843–1851.CrossRefGoogle ScholarPubMed
Ramóny Cajal, S. (1892). La rétine des vertébrés. La Cellule 9, 121–255. English translation (1972). The Structure of the Retina, ed. Thorpe S.A. & Glickstein M., pp. 1–196. Springfield, Illinois: Thomas.Google Scholar
Rodieck, R.W. (1991). The density recovery profile: A method for the analysis of points in the plane applicable to retinal studies. Visual Neuroscience 6, 95–111.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior, and Evolution 23, 121–164.CrossRefGoogle ScholarPubMed
Rowe, M.H. & Stone, J. (1980). The interpretation of variation in the classification of nerve cells. Brain, Behavior, and Evolution 17, 123–151.CrossRefGoogle ScholarPubMed
Sakaguchi, D.S., Murphey, R.K., Hunt, R.K. & Tomkins, 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
Shu, S., Ju, G. & Fan, L. (1988). The glucose oxidase–DAB–nickel method in peroxidase histochemistry of the nervous system. Neuroscience Letters 85, 169–171.CrossRefGoogle ScholarPubMed
Straznicky, C. & Straznicky, I.T. (1988). Morphological classification of retinal ganglion cells in adult Xenopus laevis. Anatomy and Embryology 178, 143–153.CrossRefGoogle ScholarPubMed
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 labelling. Archives of Histology and Cytology 52, 87–93.CrossRefGoogle ScholarPubMed
Tóth, P. & Straznicky, C. (1989 b). Biplexiform ganglion cells in the retina of Xenopus laevis. Brain Research 499, 378–382.CrossRefGoogle ScholarPubMed
Tóth, P. & Straznicky, C. (1989 c). The morphological characterization and distribution of displaced ganglion cells in the anuran retina. Visual Neuroscience 3, 551–561.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1994 a). Patterns of neuronal coupling in the retina. Progress in Retinal and Eye Research 13, 301–355.CrossRefGoogle Scholar
Vaney, D.I. (1994 b). Territorial organization of direction–selective ganglion cells in rabbit retina. Journal of Neuroscience 14, 6301–6316.CrossRefGoogle ScholarPubMed
Van Haesendonck, E. & Missotten, L. (1979). Synaptic contacts of the horizontal cells in the retina of the marine teleost, Callionymus lyra L. Journal of Comparative Neurology 184, 167–192.CrossRefGoogle ScholarPubMed
Vrabec, F. (1966). A new finding in the retina of a marine teleost, Callionymus lyra L. Folia Morphologica 14, 143–147.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.CrossRefGoogle ScholarPubMed
Wäussle, 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 Scholar
Zug, G.R. (1993). Herpetology: An Introductory Biology of Amphibians and Reptiles. San Diego, California: Academic Press.Google Scholar