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The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina

Published online by Cambridge University Press:  02 June 2009

Péter Buzás ,
Sára Jeges  and
Robert Gábriel
Péter Buzás
Affiliation:
Department of Zoology, Janus Pannonius University, Pécs, Ifjúsá;g útja 6. H-7624 Hungary
Sára Jeges
Affiliation:
Central Research Laboratory, University Medical School, Pécs, Szigeti út 12. H-7624 Hungary
Robert Gábriel
Affiliation:
Department of Zoology, Janus Pannonius University, Pécs, Ifjúsá;g útja 6. H-7624 Hungary
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Abstract

The main route of information flow through the vertebrate retina is from the photoreceptors towards the ganglion cells whose axons form the optic nerve. Bipolar cells of the frog have been so far reported to contact mostly amacrine cells and the majority of input to ganglion cells comes from the amacrines. In this study, ganglion cells of frogs from two species (Bufo marinus, Xenopus laevis) were filled retrogradely with horseradish peroxidase. After visualization of the tracer, light-microscopic cross sections showed massive labeling of the somata in the ganglion cell layer as well as their dendrites in the inner plexiform layer. In cross sections, bipolar output and ganglion cell input synapses were counted in the electron microscope. Each synapse was assigned to one of the five equal sublayers (SLs) of the inner plexiform layer. In both species, bipolar cells were most often seen to form their characteristic synaptic dyads with two amacrine cells. In some cases, however, the dyads were directed to one amacrine and one ganglion cell dendrite. This type of synapse was unevenly distributed within the inner plexiform layer with the highest occurrence in SL2 both in Bufo and Xenopus. In addition, SL4 contained also a high number of this type of synapse in Xenopus. In both species, we found no or few bipolar to ganglion cell synapses in the marginal sublayers (SLs 1 and 5). In Xenopus, 22% of the bipolar cell output synapses went onto ganglion cells, whereas in Bufo this was only 10%. We conclude that direct bipolar to ganglion cell information transfer exists also in frogs although its occurrence is not as obvious and regular as in mammals. The characteristic distribution of these synapses, however, suggests that specific type of the bipolar and ganglion cells participate in this process. These contacts may play a role in the formation of simple ganglion cell receptive fields.

Keywords

Bufo marinusXenopus laevisSynaptologyBipolar cellsGanglion cellsAmacrine cellsRetrograde labeling
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 1099 - 1107
Copyright
Copyright © Cambridge University Press 1996

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References

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141–145.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1991). Morphological classification of bipolar cells of the primate retina. European Journal of Neuroscience 3, 1069–1088.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1972). The retina of batrachians (frog). In The Structure of the Retina, ed. Thorpe, S.A. & Glickstein, M., pp. 39–59. Springfield: Charles C. Thomas.Google Scholar
Chng, S.K. & Straznicky, C. (1992). The generation and changing retinal distribution of displaced amacrine cells in Bufo marinus from metamorphosis to adult. Anatomy and Embryology 186, 175–181.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1968). Synaptic organization of the frog retina: An electron microscopic analysis comparing retinas of frogs and primates. Proceedings of the Royal Society B (London) 170, 205–228.Google ScholarPubMed
Dowling, J.E. (1987). The Retina. An Approachable Part of the Brain. Cambridge, London: The Belknap Press of Harvard University Press.Google Scholar
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479–506.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
Frederick, J.M., Rayborn, M.E. & Hollyfield, J.G. (1989). Serotoninergic neurons in the retina of Xenopus laevis; Selective staining, identification, development, and content. Journal of Comparative Neurology 281, 516–531.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Gábriel, R., Zhu, B. & Straznicky, C. (1992). Synaptic contacts of lyrosine hydroxylase-immunoreactive elements in the inner plexiform layer of the retina of Bufo marinus. Cell and Tissue Research 267, 525–534.CrossRefGoogle Scholar
Gábriel, R. & Straznicky, C. (1993). Quantitative analysis of GABA-immunoreactive synapses in the inner plexiform layer of the Bufo marinus retina: Identification of direct output to ganglion cells and contacts with dopaminergic amacrine cells. Journal of Neurocytology 22, 26–38.CrossRefGoogle ScholarPubMed
Gábriel, R., Zhu, B.S. & Straznicky, C. (1993). Synaptic contacts of serotonin-like immunoreactive and 5, 7-dihydroxytryptamine-accumulating neurons in the anuran retina. Neuroscience 54, 1103–1114.CrossRefGoogle ScholarPubMed
Gábriel, R. & Wilhelm, M. (1994). Quantitative synaptology of the inner plexiform layer of the retina of Bufo marinus. European Journal of Morphology 32, 19–33.Google ScholarPubMed
Goldman, K.A. & Fisher, S.K. (1978). Synaptic organization of the inner plexiform layer of the retina of Xenopus laevis. Proceedings of the Royal Society B (London) 201, 57–72.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
Grüsser, O.J. & Grüsser-Cornehls, U. (1976). Neurophysiology of the anuran visual system. In Frog Neurobiology, ed. Llinas, R. & Precht, W., pp. 297–385. Berlin: Springer.CrossRefGoogle Scholar
Guiloff, G.D., Jones, J. & Kolb, H. (1988). Organization of the inner plexiform layer of the turtle retina: An electron miscroscopic study. Journal of Comparative Neurology 272, 280–292.CrossRefGoogle Scholar
Hiscock, J. & Straznicky, C. (1989 a). Morphological characterization of substance P-like immunoreactive amacrine cells in the anuran retina. Vision Research 29, 293–301.CrossRefGoogle ScholarPubMed
Hiscock, J. & Straznicky, C. (1989 b). Neuropeptide Y-like immunoreactive amacrine cells in the retina of Bufo marinus. Brain Research 494, 55–64.CrossRefGoogle ScholarPubMed
Kleinschmidt, J. & Yazulla, S. (1984). Uptake of 3H-glycine in the outer plexiform layer of the retina of the toad, Bufo marinus. Journal of Comparative Neurology 230, 352–360.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
Kolb, H. (1982). The morphology of the bipolar cells, amacrine cells and ganglion cells in the retina of the turtle Pseudemys scripta elegans. Philosophical Transactions of the Royal Society B (London) 298, 355–393.Google ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. Journal of Neuroscience 4, 2920–2938.CrossRefGoogle ScholarPubMed
Nguyen, V.S. & Straznicky, C. (1989). The development and the topographic organization of the retinal ganglion cell layer in Bufo marinus. Experimental Brain Research 75, 345–353.CrossRefGoogle ScholarPubMed
Raviola, G. & Raviola, E. (1967). Light and electron microscopic observations on the inner plexiform layer of the rabbit retina. American Journal of Anatomy 120, 403–426.CrossRefGoogle ScholarPubMed
Rayborn, M.E., Sarthy, P.V., Lam, D.M.K. & Hollyfield, J.G. (1981). The emergence, localization and maturation of neurotransmitter systems during the development of the retina in Xenopus laevis. H. Glycine. Journal of Comparative Neurology 195, 585–593.CrossRefGoogle Scholar
Schütte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of the clawed frog Xenopus laevis. Journal of Neurocytology 19, 504–518.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.CrossRefGoogle Scholar
Smiley, J.F. & Yazulla, S. (1990). Glycinergic contacts in the outer plexiform layer of the Xenopus laevis retina characterized by antibodies to glycine, GABA and glycine receptors. Journal of Comparative Neurology 299, 375–388.CrossRefGoogle ScholarPubMed
Stone, S. & Schütte, M. (1991). Physiological and morphological properties of off- and on-center bipolar cells in the Xenopus retina: Effects of glycine and GABA. Visual Neuroscience 7, 363–376.CrossRefGoogle ScholarPubMed
Straznicky, C. (1993). Development of the anuran retina: Past and present. In Formation and Regeneration of Nerve Connections, ed. Fawcett, J.W. & Sharma, S.C., pp. 162–184. Boston, Massachusetts: Birkhauser.CrossRefGoogle Scholar
Straznicky, C. & Gábriel, R. (1991). NADPH-diaphorase positive neurons in the retina of Bufo marinus: Selective staining of bipolar and amacrine cells. Archives of Histology and Cytology 54, 213–220.CrossRefGoogle ScholarPubMed
Straznicky, C. & Straznicky, l.T. (1988). Morphological classification of retinal ganglion cells in adult Xenopus laevis. Anatomy and Embryology 178, 143–153.CrossRefGoogle ScholarPubMed
Straznicky, C., Tóth, P. & Nguyen, V.S. (1990). Morphological classification and retinal distribution of large ganglion cells in the retina of Bufo marinus. Experimental Brain Research 79, 345–356.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, 87–93.CrossRefGoogle ScholarPubMed
Wássle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.CrossRefGoogle ScholarPubMed
Watt, C.B. & Wilson, E.A. (1990). Synaptic organization of serotoninlike immunoreactive amacrine cells in the larval tiger salamander retina. Neuroscience 35, 715–723.CrossRefGoogle ScholarPubMed
Witkovsky, P. (1992). Functional anatomy of the retina. In Douane's Foundation of Clinical Ophthalmology, ed. Tasman, W. & Jaeger, E.A., pp. 1–29. Philadelphia, Pennsylvania: J.B. Lippincott Co.Google Scholar
Witkovsky, P., Zhang, J. & Blam, O. (1994). Dopaminergic neurons in the retina of Xenopus laevis: Amacrine vs. interplexiform subtypes and relation to bipolar cells. Cell and Tissue Research 278, 45–56.Google ScholarPubMed
Zhang, Y.D. & Straznicky, C. (1991). The morphology and distribution of photoreceptors in the retina of Bufo marinus. Anatomy and Embryology 183, 97–104.CrossRefGoogle ScholarPubMed
Zhu, B.S., Gábriel, R. & Straznicky, C. (1992). Serotonin synthesis and accumulation by neurons of the anuran retina. Visual Neuroscience 9, 377–388.CrossRefGoogle ScholarPubMed
Zhu, B.S., Hiscock, J. & Straznicky, C. (1990). The changing distribution of neurons in the inner nuclear layer from metamorphosis to adult: A morphometric analysis of the anuran retina. Anatomy and Embryology 181, 585–594.CrossRefGoogle ScholarPubMed
Zhu, B.S. & Straznicky, C. (1990 a). Dendritic morphology and retinal distribution of tyrosine hydroxylase-like immunoreactive amacrine cells in Bufo marinus. Anatomy and Embryology 181, 365–371.CrossRefGoogle ScholarPubMed
Zhu, B.S. & Straznicky, C. (1990 b). Morphology and distribution of serotonin-like immunoreactive amacrine cells in the retina of Bufo marinus. Visual Neuroscience 5, 371–378.CrossRefGoogle ScholarPubMed
Zhu, B.S., Straznicky, C. & Gibbins, I. (1995). Synaptic circuitry of serotonin-synthesizing and serotonin-accumulating amacrine cells in the retina of the cane toad, Bufo marinus. Visual Neuroscience 12, 11–19.CrossRefGoogle ScholarPubMed