Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-04T21:15:54.801Z Has data issue: false hasContentIssue false

Large retinal ganglion cells that form independent, regular mosaics in the ranid frogs Rana esculenta and Rana pipiens

Published online by Cambridge University Press:  02 June 2009

K. M. Shamim
Affiliation:
Department of Anatomy and Developmental Biology, University College London, Gower Street, London WC1E 6BT, U.K. Department of Anatomy, Institute of Postgraduate Medicine and Research, Dhaka, Bangladesh
F. Scalia
Affiliation:
Department of Anatomy and Cell Biology, State University of New York Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn
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 WC1E 6BT, U.K.

Abstract

Population-based studies of ganglion cells in retinal flatmounts have helped to reveal some of their natural types in mammals, teleost fish and, recently, the aquatic mesobatrachian frog Xenopus laevis. Here, ganglion cells of the semiterrestrial neobatrachian frogs Rana esculenta and Rana pipiens have been studied similarly. Ganglion cells with large somata and thick dendrites could again be divided into three mosaic-forming types with distinctive stratification patterns. Cell dimensions correlated inversely with density, being smallest in the visual streak. Cells of the αa mosaic (<0.2% of all ganglion cells) had the largest somata at each location (often displaced) and their trees were confined to one shallow plane within sublamina a of the inner plexiform layer. In regions of high regularity, many trees were symmetric. Elsewhere, asymmetric, irregular trees predominated and their dendrites, although sparsely branched, achieved consistent coverage by intersecting in complex ways. Cells of the αab mosaic were more numerous (≈0.7%) and had large somata, smaller (but still large) trees, and dendrites that branched extensively in two separate shallow planes in sublaminae a and b. The subtrees did not always match in symmetry, and each subtree tessellated independently with its neighbors. Cells of the αc mosaic (≈0.1%) had large, orthotopic somata and large, sparse trees (often asymmetric and irregular) close to the ganglion cell layer. Nearest-neighbor analyses and spatial correlograms confirmed that each mosaic was regular and independent. Densities, proportions, sizes, and mosaic statistics are tabulated for all three types, which are compared with types defined by size and symmetry in R. pipiens, by discriminant analysis in R. temporaria, by physiological response in both, and by mosaic analysis in Xenopus and several teleosts. The variable stratification of these otherwise similar types across species is consistent with other evidence that stratification may be determined, in part, by functional interactions.

Type
Research Articles
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, 141145.CrossRefGoogle ScholarPubMed
Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Bodnarenko, S.R. & Chalupa, L.M. (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364, 144146.CrossRefGoogle Scholar
Bodnarenko, S.R., Jeyarasasingam, G. & Chalupa, L.M. (1995). Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. Journal of Neuroscience 15, 70377045.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397419.CrossRefGoogle ScholarPubMed
Carras, P.L., Coleman, P.A. & Miller, R.F. (1992). Site of action potential initiation in amphibian retinal ganglion cells. Journal of Neurophysiology 67, 292304.CrossRefGoogle ScholarPubMed
Constantine-Paton, M. (1990). NMDA receptor as a mediator of activity-dependent synaptogenesis in the developing brain. Cold Spring Harbor Symposia on Quantitative Biology 55, 431443.CrossRefGoogle ScholarPubMed
Cook, J.E. (1982). Errant optic axons in the normal goldfish retina reach retinotopic tectal sites. Brain Research 250, 154158.CrossRefGoogle 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, 319328.CrossRefGoogle ScholarPubMed
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 1530.CrossRefGoogle ScholarPubMed
Cook, J.E. & Becker, D.L. (1990). Spontaneous activity as a determinant of axonal connections: Darkness and light are equally effective for activity-dependent refinement of the regenerating retinotectal projection in goldfish. European Journal of Neuroscience 2, 162169.CrossRefGoogle Scholar
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, 668684.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, 355366.CrossRefGoogle ScholarPubMed
Cook, J.E. & Noden, A.J. (1997). Somatic and dendritic mosaics formed by large ganglion cells in the retina of the common house gecko (Hemidactylus frenatus). Brain, Behavior, and Evolution (in press).Google Scholar
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, 331349.CrossRefGoogle ScholarPubMed
Cook, J.E., Kondrashev, S.L. & Podugolnikova, T.A. (1996). Biplex-iform ganglion cells, characterized by dendrites in both outer and inner plexiform layers, are regular, mosaic-forming elements of teleost fish retinae. Visual Neuroscience 13, 517528.CrossRefGoogle ScholarPubMed
Cook, J.E., Podugolnikova, T.A. & Kondrashev, S.L. (1997). Species-dependent variation in dendritic stratification in apparently homologous neuronal mosaics: Large retinal ganglion cells in two neoteleost fishes of the order Perciformes. (Submitted).Google Scholar
Diamond, J.S. & Copenhagen, D.R. (1993). The contribution of NMDA and non-NMDA receptors to the light-evoked input-output characteristics of retinal ganglion cells. Neuron 11, 725738.CrossRefGoogle Scholar
Duellman, W.E. & Truer, L. (1986). Biology of Amphibians. New York: McGraw-Hill.Google Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle ScholarPubMed
Frank, B.D. & Hollyfield, J.G. (1987). Retinal ganglion cell morphology in the frog, Rana pipiens. Journal of Comparative Neurology 266, 413434.CrossRefGoogle ScholarPubMed
Görcs, T., Antal, M., Oláh, É. & Székely, G. (1979). An improved cobalt labeling technique with complex compounds. Acta Biologica Academiae Scientiarum Hungaricae 30, 7886.Google ScholarPubMed
Hitchcock, P.F. (1987). Constant dendritic coverage by ganglion cells with growth of the goldfish's retina. Vision Research 27, 1722.CrossRefGoogle ScholarPubMed
Kalinina, A.V. (1976). Quantity and topography of frog's retinal ganglion cells. Vision Research 16, 929934.CrossRefGoogle ScholarPubMed
Katz, L.C. & Constantine-Paton, M. (1988). Relationships between segregated afferents and postsynaptic neurons in the optic tectum of three-eyed frogs. Journal of Neuroscience 8, 31603180.CrossRefGoogle ScholarPubMed
Kirby, M.A. & Steineke, T.C. (1991). Early dendritic outgrowth of primate retinal ganglion cells. Visual Neuroscience 7, 513530.CrossRefGoogle ScholarPubMed
Kock, J.-H. & Reuter, T. (1978). Retinal ganglion cells in the crucian carp (Carassius carassius). II. Overlap, shape and tangential orientation of dendritic trees. Journal of Comparative Neurology 179, 549568.CrossRefGoogle ScholarPubMed
Kock, J., Mecke, E., Orlov, O.Y., Reuter, T., Väisänen, R.A. & Wallgren, J.E. (1989). Ganglion cells in the frog retina: Discriminant analysis of histological classes. Vision Research 29, 118.CrossRefGoogle ScholarPubMed
Kossel, A., Löwel, S. & Bolz, J. (1995). Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. Journal of Neuroscience 15, 39133926.CrossRefGoogle ScholarPubMed
Lettvin, J.Y., Maturana, H.R., McCulloch, W.S. & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of the Institute of Radio Engineers 47, 19401951.Google Scholar
Levick, W.R. & Thibos, L.N. (1983). Receptive fields of cat ganglion cells: Classification and construction. Progress in Retinal Research 2, 267319.CrossRefGoogle Scholar
Marshak, D., Ariel, M. & Brown, E. (1988). Distribution of synaptic inputs onto goldfish retinal ganglion cell dendrites. Experimental Eye Research 46, 965978.CrossRefGoogle ScholarPubMed
Maslim, J. & Stone, J. (1988). Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Developmental Brain Research 44, 8793.CrossRefGoogle ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399425.CrossRefGoogle Scholar
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S. & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog ( Rana pipiens). Journal of General Physiology 43, 129175.CrossRefGoogle Scholar
Maximov, V.V., Orlov, O.Y. & Reuter, T. (1985). Chromatic properties of the retinal afferents in the thalamus and tectum of the frog (Rana temporaria). Vision Research 25, 10371049.CrossRefGoogle ScholarPubMed
Muntz, W.R.A. (1962). Microelectrode recordings from the diencephalon of the frog ( Rana pipiens) and a blue-sensitive system. Journal of Neurophysiology 25, 699711.CrossRefGoogle Scholar
Nikrui, N. (1969). Fibre sizes and frequencies in the optic nerve of Rana esculenta. Zeitschrift für mikroskopisch-anatomische Forschung 80, 450456.Google ScholarPubMed
Peichl, L. (1991). Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells. Visual Neuroscience 7, 155169.CrossRefGoogle ScholarPubMed
Podugolnikova, T.A., Orlov, O.Y. & Reuter, T. (1991). Morphology of frog retina ganglion cells projecting to the basal optic nucleus. Sensory Systems (English translation of Sensornye Sistemy in Russian). 5, 2132.Google Scholar
Ramón y Cajal, S. (1892). La rétine des vertébrés. La Cellule 9, 121255. English translation (1972). The Structure of the Retina, ed. Thorpe S.A. & Glickstein M., 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, 95111.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and transspecies comparisons. Brain, Behavior, and Evolution 23, 121164.CrossRefGoogle ScholarPubMed
Rowe, M.H. & Stone, J. (1980). The interpretation of variation in the classification of nerve cells. Brain, Behavior, and Evolution 17, 123151.CrossRefGoogle ScholarPubMed
Scalia, F., Arango, V. & Singman, E.L. (1985). Loss and displacement of ganglion cells after optic nerve regeneration in adult Rana pipiens. Brain Research 344, 267280.CrossRefGoogle ScholarPubMed
Shamim, K.M., Tóth, P. & Cook, J.E. (1997). Large retinal ganglion cells in the pipid frog Xenopus laevis form independent, regular mosaics resembling those of teleost fish. Visual Neuroscience 14, 811826.CrossRefGoogle Scholar
Sperry, R.W. (1944). Optic nerve regeneration with return of vision in Anurans. Journal of Neurophysiology 7, 5769.CrossRefGoogle Scholar
Stelzner, D.J. & Strauss, J.A. (1986). A quantitative analysis of frog nerve regeneration: Is retrograde ganglion cell death or collateral axonal loss related to selective reinnervation? Journal of Comparative Neurology 245, 83106.CrossRefGoogle ScholarPubMed
Stirling, R.V. & Merrill, E.G. (1987). Functional morphology of frog retinal ganglion cells and their central projections: The dimming detectors. Journal of Comparative Neurology 258, 477495.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
Tóth, P. & Straznicky, C. (1989). 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, 8793.CrossRefGoogle ScholarPubMed
Wässle, H., Peichl, L. & Boycott, B.B. (1981). Morphology and topography of on- and off-alpha cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157175.Google Scholar
Wong, R.O.L., Herrmann, K. & Shatz, C.J. (1991). Remodeling of retinal ganglion cell dendrites in the absence of action potential activity. Journal of Neurobiology 22, 685697.CrossRefGoogle ScholarPubMed