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The rod bipolar cell of the mammalian retina

Published online by Cambridge University Press:  02 June 2009

Heinz Wässle ,
Masayuki Yamashita ,
Ursula Greferath ,
Ulrike Grünert  and
Frank Müller
Heinz Wässle
Affiliation:
Max-Planck Institut für Hirnforschung, Deutschordenstrasse 46, Frankfurt 71, Germany
Masayuki Yamashita
Affiliation:
Max-Planck Institut für Hirnforschung, Deutschordenstrasse 46, Frankfurt 71, Germany
Ursula Greferath
Affiliation:
Max-Planck Institut für Hirnforschung, Deutschordenstrasse 46, Frankfurt 71, Germany
Ulrike Grünert
Affiliation:
Max-Planck Institut für Hirnforschung, Deutschordenstrasse 46, Frankfurt 71, Germany
Frank Müller
Affiliation:
Max-Planck Institut für Hirnforschung, Deutschordenstrasse 46, Frankfurt 71, Germany
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Abstract

Three approaches to study the function of mammalian rod bipolar cells are described. Extracellular recordings from the intact cat eye under light- and dark-adapted conditions showed that in dark-adapted retina all light responses can be blocked by 2-amino-4-phosphonobutyrate (APB). Immunocytochemical staining with an antibody against protein kinase C (PKC) labeled rod bipolar cells in all mammalian retinae tested. When rat retinae were dissociated, PKC immunoreactivity was also found in isolated bipolar cells and could be used for their identification as rod bipolars. Patch-clamp recordings were performed from such dissociated rod bipolar cells and their responses to APB were measured. APB closed a nonselective cation channel in the cell membrane. The actions of GABA and glycine were also tested and both opened chloride channels in dissociated rod bipolar cells. These results suggest that rod bipolar cells are depolarized by a light stimulus and that GABA as well as glycine modulate their light responses.

Keywords

Rod bipolar cells2-amino-4-phosphonobutyrate (APB)patch-clamp recordingsprotein kinase C immunocytochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 1-2 , August 1991 , pp. 99 - 112
Copyright
Copyright © Cambridge University Press 1991

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References

Arkin, M.S. & Miller, R.F. (1987). Subtle actions of 2-amino-phosphonobutyrate (APB) on the OFF-pathway in the mudpuppy retina. Brain Research 426, 142–148.CrossRefGoogle ScholarPubMed
Attwell, D., Mobbs, P., Tessier, Lavigne M. & Wilson, M. (1987). Neurotransmitter induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. Journal of Physiology (London) 387, 125–161.Google Scholar
Barnard, E.A., Darlison, M.G. & Seeburg, P. (1987). Molecular biology of the GABAA receptor: the receptor/channel superfamily. Trends in Neurosciences 10, 502–509.CrossRefGoogle Scholar
Bloomfield, S.A. & Dowling, J.E. (1985). Roles of aspartate and glutamate in synaptic transmission in rabbit retina. 1. Outer plexiform layer. Journal of Neurophysiology 53, 699–713.CrossRefGoogle Scholar
Boycott, B.B. & Kolb, H. (1973). The connections between bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 91–114.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1893). La rétine des vertébrés. La Cellule 9, 119–255.Google Scholar
Chase, L. & Dowling, J.E. (1990). A comparison of rod and cone pathways in the primate retina. Investigative Ophthalmology and Visual Science 31, 4 (ARVO Abstract, 1017).Google Scholar
Chun, M.H. & Wässle, H. (1989). GABA-like immunoreactivity in the cat retina: electron microscopy. Journal of Comparative Neurology 279, 55–67.CrossRefGoogle ScholarPubMed
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogeneous excitatory amino acids from turtle photoreceptors. Nature (London) 341, 536–539.Google Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Daw, N.W., Jensen, R.W. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neurosciences 13, 110–115.CrossRefGoogle ScholarPubMed
Ehinger, B. (1988). Glutamate as a retinal neurotransmitter. In Neurobiology of the Inner Retina, NATO ASI Series, Vol. H31, ed. Weiler, R. & Osborne, N.N., pp. 1–14. Berlin, Heidelberg: Springer Verlag.Google Scholar
Enroth-Cugell, C. & Harding, T.H. (1980). Summation of rod signals within the receptive field centre of cat retinal ganglion cells. Journal of Physiology (London) 298, 253–260.Google Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Freed, M.A., Smith, R.A. & Sterling, P. (1987). Rod bipolar array in the cat retina: pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.CrossRefGoogle ScholarPubMed
Gouras, P. & Evers, H.U. (1985). The neurocircuitry of primate retina. In Neurocircuitry of the Retina: A Cajal memorial, ed. Gallego, A. & Gouras, P., pp. 233–244. New York, Amsterdam, Oxford: Elsevier.Google Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Grünert, U. & Martin, P.R. (1990). Rod bipolar cells in the macaque monkey retina: light and electron microscopy. Investigative Ophthalmology and Visual Science 31, 4 (ARVO Abstract, 2634).Google Scholar
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: a light and electron microscopic study. Journal of Comparative Neurology 297, 509–524.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archives 391, 85–100.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988). Localization of glycine-containing neurons in the Macaca monkey retina. Journal of Comparative Neurology 273, 473–487.CrossRefGoogle ScholarPubMed
Horn, R. & Marty, A. (1988). Muscarinic activation of ionic currents measured by a new whole-cell recording method. Journal of General Physiology 92, 145–159.CrossRefGoogle ScholarPubMed
Huba, R. & Hofmann, H.D. (1988). Tetanus toxin binding to isolated and cultured rat retinal glial cells. Glia 1, 156–164.CrossRefGoogle ScholarPubMed
Hughes, E.G., Grünert, U. & Karten, H.J. (1991). GABAA receptors in the retina of the cat: an immunohistochemical study of wholemounts, sections, and dissociated cells. Visual Neuroscience (in press).CrossRefGoogle Scholar
Kaneko, A., Pinto, L.H. & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology (London) 410, 613–629.Google Scholar
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Schiller, P.H. (1984). The contribution of ON-bipolar cells to the electroretinogram of rabbits and monkeys: a study using 2-aminophosphonobutyrate (APB). Vision Research 24, 1841–1846.CrossRefGoogle Scholar
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. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Kurachi, Y., Asano, Y., Takikawa, R. & Sugimoto, T. (1989). Cardiac Ca2+ current does not run down and is very sensitive to isoprenaline in the nystatin-method of whole cell recording. Naunyn-Schmiedeberg's Archives of Pharmacology 340, 219–222.CrossRefGoogle Scholar
Lasater, E.M., Dowling, J.E. & Ripps, H. (1984). Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. Journal of Neuroscience 4, 1966–1975.CrossRefGoogle ScholarPubMed
Levine, M.W. & Shefner, J.M. (1977). Variability in ganglion cell firing patterns: implications for separate on and off processes. Vision Research 17, 765–776.CrossRefGoogle ScholarPubMed
Marc, R.E., Massey, S.C., Kalloniatis, M. & Basinger, S.F. (1989). Immunocytochemical evidence that the fast neurotransmitter of rods, cones, bipolar and ganglion cells is glutamic acid. Investigative Ophthalmology and Visual Science 30, 3(ARVO Abstract, 320).Google Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N.N. & Chader, J., Oxford: Pergamon Press.Google Scholar
Massey, S.C., Redburn, D.A. & Crawford, M.L.J. (1983). The effects of 2-amino-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Research 23, 1607–1613.CrossRefGoogle Scholar
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcuitry of bipolar cells in cat retina. Journal of Neuroscience 4, 2920–2938.CrossRefGoogle ScholarPubMed
Miller, R.F. & Dowling, J.E. (1970). Intracellular responses of the Müller (glial) cells of the mudpuppy retina: their relation to the bwave of the electroretinogram. Journal of Neurophysiology 33, 323–341.CrossRefGoogle Scholar
Müller, B. & Peichl, L. (1989). Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology 282, 581–594.CrossRefGoogle ScholarPubMed
Müller, B. & Peichl, L. (1991). Rod bipolar cells in the cone-dominated retina of the tree shrew (Tupaia belangeri). Visual Neuroscience (in press).CrossRefGoogle Scholar
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1990). Time-dependent reduction of glutamate current in retinal bipolar cells. Neuroscience Letters 108, 279–283.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 108, 279–283.Google Scholar
Nelson, R. (1977). Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109–134.CrossRefGoogle ScholarPubMed
Nelson, R. (1982). All Amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1985). A17: a broad field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.CrossRefGoogle ScholarPubMed
Newman, E.A. (1988). Electrophysiology of retinal glial cells. In Progress in Retinal Research, Vol. 8, ed. Osborne, N.N. & Chader, G., pp. 153–171. Oxford: Pergamon Press.Google Scholar
Onoda, N. (1988). A monoclonal antibody specific for a subpopulation of retinal bipolar cells in vertebrates. Neuroscience Research 8, 113–125.Google ScholarPubMed
Onoda, N. & Fujita, S.C. (1987). A monoclonal antibody specific for a subpopulation of retinal bipolar cells in the frog and other vertebrates. Brain Research 416, 359–363.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of [3H]-glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogeneous glycine in cat retina: an immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: a light- and electron-microscopic study. Visual Neuroscience 2, 425–435.CrossRefGoogle ScholarPubMed
Raviola, E. & Dacheux, R.F. (1987). Excitatory dyad synapse in rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 7324–7328.CrossRefGoogle ScholarPubMed
Saito, T. (1987). Physiological and morphological differences between ON-and OFF-center bipolar cells in the vertebrate retina. Vision Research 27, 135–142.CrossRefGoogle ScholarPubMed
Shiells, R.A., Falk, S. & Naghshineh, S. (1981). Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature (London) 294, 592–594.Google Scholar
Slaughter, M.M. & Miller, R.F. (1985). Characterization of an extended glutamate receptor of the ON-bipolar neuron in the vertebrate retina. Journal of Neuroscience 5, 224–233.CrossRefGoogle ScholarPubMed
Smith, R.G., Free, M. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: functional architecture of the rod–cone network. Journal of Neuroscience 6, 3505–3517.CrossRefGoogle ScholarPubMed
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1986). Microcircuitry and functional architecture of the cat retina. Trends in Neurosciences 9, 186–192.CrossRefGoogle Scholar
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the ON-beta ganglion cell. Journal of Neuroscience 8, 623–642.CrossRefGoogle Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B-wave of the electroretinogram: a reflection of ON-bipolar cell activity. Journal of General Physiology 93, 101–122.CrossRefGoogle ScholarPubMed
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.CrossRefGoogle ScholarPubMed
Suzuki, S., Tachibana, M. & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology (London) 421, 645–662.Google Scholar
Szél, A. & Röhlich, P. (1990). Two immunologically different cone types in the rat retina. Investigative Ophthalmology and Visual Science, 31, 4 (ARVO Abstract 188).Google Scholar
Tachibana, M. & Kaneko, A. (1984). γ-Aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types. Proceedings of the National Academy of Sciences of the U.S.A. 81, 7961–7964.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1987). γ-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proceedings of the National Academy of Sciences of the U.S.A. 84, 3501–3505.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N.N. & Chader, G., pp. 49–100. Oxford: Pergamon Press.Google Scholar
Veruki, M.L., Lee, M.B., Cheun, J.E. & Yeh, M.H. (1990). GABA-and glycine-mediated membrane currents in rod bipolar and ganglion cells of the rat retina. Investigative Ophthalmology and Visual Science 31, 4 (ARVO Abstract 1030).Google Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of All amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle ScholarPubMed
Wässle, H., Schaefer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. Journal of Neuroscience 6, 594–604.CrossRefGoogle ScholarPubMed
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: light microscopy. Journal of Comparative Neurology 279, 43–54.CrossRefGoogle ScholarPubMed
Wood, J.G., Hart, C.E., Mazzei, G.J., Girard, P.R. & Kuo, J.F. (1988). Distribution of protein kinase C immunoreactivity in rat retina. Histochemistry Journal (London) 20, 63–68.Google Scholar
Yamashita, M. & Wässle, H. (1991). Responses to the glutamate agonist 2-amino-4-phosphonobutyric acid (APB) of rod bipolar cells isolated from the rat retina. Journal of Neuroscience (in press).CrossRefGoogle Scholar
Yeh, H.H., Lee, M.B. & Cheun, J.E. (1990). Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Visual Neuroscience 4, 349–357.CrossRefGoogle ScholarPubMed