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Biplexiform ganglion cells, characterized by dendrites in both outer and inner plexiform layers, are regular, mosaic-forming elements of teleost fish retinae

Published online by Cambridge University Press:  02 June 2009

J. E. Cook
Affiliation:
Department of Anatomy and Developmental Biology, University College London, Cower Street, London WCIE 6BT, United Kingdom
S. L. Kondrashev
Affiliation:
lnstitute of Marine Biology, Russian Academy of Sciences (Far East Branch), Vladivostok-41 690041, Russia
T. A. Podugolnikova
Affiliation:
Institute for Problems of Information Transmission, Russian Academy of Sciences, Ermolovoy ul. 19, Moscow 101447, Russia

Abstract

Biplexiform ganglion cells were labelled by retrograde transport of HRP in five species of marine fish from the neoteleost acanthopterygian orders Perciformes and Scorpaeniformes. Their forms and spatial distributions were studied in retinal flatmounts and thick sections. Biplexiform ganglion cells possessed sparsely branched, often varicose, dendrites that ramified through the inner nuclear layer (INL) to reach the outer plexiform layer (OPL), as well as conventional arborizations in the most sclerad part of the inner plexiform layer (IPL). Their somata were of above-average size and were displaced into the vitread border of the INL. Mean soma areas ranged from 99 ± 6 μm2 in Bathymaster derjugini (Perciformes) to 241 ± 12 μm2 in Hexagrammos stelleri (Scorpaeniformes), but were similar in each species to those of the outer-stratified alpha-like ganglion cells, whose dendritic trees occupied the same IPL sublamina. In the best-labelled specimens, biplexiform cells formed clear mosaics with spacings and degrees of regularity much like those of other large ganglion cells, but spatially independent of them. Biplexiform mosaics were plotted in three species, and analyzed by nearest-neighbor distance and spatial correlogram methods. The exclusion radius, an estimate of minimum mosaic spacing, ranged from 113 urn in Hexagrammos stelleri, through 150 μm in Ernogrammus hexagraminus (Perciformes), to 240 μm in Myoxocephalus stelleri (Scorpaeniformes). A spatial cross-correlogram analysis of the distributions of biplexiform and outer-stratified alpha-like cells in Hexagrammos demonstrated the spatial independence of their mosaics. Similar cells were previously observed not only in the freshwater cichlid Oreochromis spilurus (Perciformes) but also in the goldfish Carassius auratiis (Cypriniformes) which, being an ostariophysan teleost, is only distantly related. Thus, biplexiform ganglion cells may be regular elements of all teleost fish retinae. Their functional role remains unknown.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Arkin, M.S. & Miller, R.F. (1988). Mudpuppy retinal ganglion cell morphology revealed by an HRP impregnation technique which provides Golgi-like staining. Journal of Comparative Neurology 270, 185208.CrossRefGoogle ScholarPubMed
Baldridge, W.H. & Ball, A.K. (1993). A new type of interplexiform cell in the goldfish retina is PNMT-immunoreactive. NeuroReport 4, 10151018.CrossRefGoogle ScholarPubMed
Collin, S.P. & Northcutt, R.G. (1993). The visual system of the Florida garfish, Lepisosteus platyrhincus(Ginglymodi). III. Retinal ganglion cells. Brain, Behavior, and Evolution 42, 295320.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, 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. (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. & 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
Dowling, J.E. & Ehinger, B. (1975). Synaptic organization of the amine-containing interplexiform cells of the goldfish and Cebus monkey retinas. Science 188, 270273.CrossRefGoogle ScholarPubMed
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
Hitchcock, P.F. & Easter, S.S. Jr. (1986). Retinal ganglion cells in goldfish: A qualitative classification into four morphological types, and a quantitative study of the development of one of them. Journal of Neuroscience 6, 10371050.CrossRefGoogle Scholar
Kauoniatis, M. & Marc, R.E. (1990). Interplexiform cells of the goldfish retina. Journal of Comparative Neurology 297, 340358.CrossRefGoogle Scholar
Marc, R.E. & Lam, D.M.K. (1981). Glycinergic pathways in the goldfish retina. Journal of Neurosdence 1, 152165.Google ScholarPubMed
Marc, R.E. & Liu, W.-L.S. (1984). Horizontal cell synapses onto glycine-accumulating interplexiform cells. Nature 312, 266269.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1982). Biplexiform cells: Ganglion cells of the primate retina that contact photoreceptors. Science 216, 11341136.CrossRefGoogle ScholarPubMed
Masland, R.H., Rizzo, J.F. & Sandell, J.H. (1993). Developmental variation in the structure of the retina. Journal of Neurosdence 13, 51945202.Google ScholarPubMed
Prada, C., Medina, J.I., López, R., Génis-Gélvez, J.M. & Prada, F.A. (1992). Development of retinal displaced ganglion cells in the chick: Neurogenesis and morphogenesis. Journal of Neuroscience 12, 37813788.CrossRefGoogle ScholarPubMed
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 16791688.CrossRefGoogle 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
Sakai, H.M. & Naka, K.-I. (1988). Dissection of the neuron network in the catfish inner retina. 11. Interactions between ganglion cells. Journal of Neurophysiology 60, 15681583.CrossRefGoogle Scholar
Sakai, H.M., Naka, K.-l. & Dowling, J.E. (1986). Ganglion cell den-drites are presynaptic in catfish retina. Nature 319, 495497.CrossRefGoogle ScholarPubMed
Stone, J.S., Holländer, H. & Dreher, Z. (1991). “Sunbursts” in the inner plexiform layer: A spectacular feature of Miiller cells in the retina of the cat. Journal of Comparative Neurology 303, 400411.CrossRefGoogle Scholar
Straznicky, C. & Gábriel, R. (1995). Synapses of biplexiform ganglion cells in the outer plexiform layer of the retina in Xenopus laevis. Journal of Brain Research 36, 135141.Google ScholarPubMed
Tóth, P. & Straznicky, C. (1989). Biplexiform ganglion cells in the retina of Xenopus laevis. Brain Research 499, 378382.CrossRefGoogle ScholarPubMed
Van Haesendonck, E., Marc, R.E. & Missotten, L. (1993). New aspects of dopaminergic interplexiform cell organization in the goldfish retina. Journal of Comparative Neurology 333, 503518.CrossRefGoogle ScholarPubMed
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Dearry, A. (1991). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247292.CrossRefGoogle Scholar
Yazulla, S. & Studholme, K.M. (1991). Glycinergic interplexiform cells make synaptic contact with amacrine cell bodies in goldfish retina. Journal of Comparative Neurology 310, 110.CrossRefGoogle ScholarPubMed
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopaminergic interplexiform cells in the goldfish retina. Visual Neuroscience 1, 1329.CrossRefGoogle ScholarPubMed
Zrenner, E., Nelson, R. & Mariani, A. (1983). Intraceltular recordings from a biplexiform ganglion cell in macaque retina, stained with horseradish peroxidase. Brain Research 262, 181185.CrossRefGoogle ScholarPubMed
Zucker, C.L. & Dowling, J.E. (1987). Centrifugal fibres synapse on dopaminergic interplexiform cells in the teleost retina. Nature 330, 166168.CrossRefGoogle ScholarPubMed