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Co-stratification of GABAA receptors with the directionally selective circuitry of the rat retina

Published online by Cambridge University Press:  02 June 2009

J.H. Brandstätter ,
U. Greferath ,
T. Euler  and
H. Wässle
J.H. Brandstätter
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstr. 46, D-60528 Frankfurt, Germany
U. Greferath
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstr. 46, D-60528 Frankfurt, Germany
T. Euler
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstr. 46, D-60528 Frankfurt, Germany
H. Wässle
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstr. 46, D-60528 Frankfurt, Germany
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Abstract

Direction-selective (DS) ganglion cells of the mammalian retina have their dendrites in the inner plexiform layer (IPL) confined to two narrow strata. The same strata are also occupied by the dendrites of cholinergic amacrine cells which are probably presynaptic to the DS ganglion cells. GABA is known to play a crucial role in creating DS responses. We examined the types of GABAA receptors expressed by the cholinergic amacrine cells and also those expressed by their presynaptic and postsynaptic neurons, by applying immunocytochemical markers to vertical sections of rat retinas. Double-labelling experiments with antibodies against choline acetyltransferase (ChAT) and specific antibodies against different GABAA receptor subunits were performed. Cholinergic amacrine cells seem to express an unusual combination of GABAA receptor subunits consisting of α2-, β1-, β2/3-, γ2-, and δ-subunits. Bipolar cells, which could provide synaptic input to the DS circuitry, were stained with antibodies against the glutamate transporter GLT-1. The axon terminals of these bipolar cells are narrowly stratified in close proximity to the dendritic plexus of displaced cholinergic amacrine cells. The retinal distribution of synaptoporin, a synaptic vesicle associated protein, was studied. Strong reduction of immunolabelling was observed in the two cholinergic strata. The anatomical findings are discussed in the context of models of the DS circuitry of the mammalian retina.

Keywords

GABAA receptor subunitsCholinergic amacrine cellsExpression of glutamate transporter GLT-1Localization of synaptoporinMolecular basis of directional selectivity
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 2 , March 1995 , pp. 345 - 358
Copyright
Copyright © Cambridge University Press 1995

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References

Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1991). Nonlinearity of the inhibition underlying retinal directional selectivity. Visual Neuroscience 6, 197–206.CrossRefGoogle ScholarPubMed
Amthor, F.R. & Grzywacz, N.M. (1993). Inhibition in ON-OFF directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 2174–2187.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 a). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology (London) 324, 135–160.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–185.CrossRefGoogle ScholarPubMed
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. Journal of Physiology (London) 173, 377–407.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in the rabbit's retina. Journal of Physiology (London) 178, 477–504.CrossRefGoogle ScholarPubMed
Baughman, R.W. & Bader, C.R. (1977). Biochemical characterization and cellular localization of the cholinergic system in the chicken retina. Brain Research 138, 469–485.CrossRefGoogle ScholarPubMed
Benke, D., Cicin-Sain, A., Mertens, S. & Möhler, H. (1991). Immunochemical identification of the α1- and α 3-subunit of the GABAA-receptor in the rat brain. Journal of Receptor Research 11, 407–424.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of N europhysiology 68, 711–725.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 1–13.CrossRefGoogle Scholar
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmittergated currents of All-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.CrossRefGoogle Scholar
Borg-Graham, L.J. & Grzywacz, N. (1992). A model of the direction selectivity circuit in retina: Transformations by neurons singly and in concert. In Single Neuron Computation Neural Nets: Foundations to Applications, ed. McKenna, T., pp. 347–375. New York: Academic Press.CrossRefGoogle Scholar
Borst, A. & Egelhaaf, M. (1989). Principles of visual motion detection. Trends in Neuroscience 12, 297–306.CrossRefGoogle ScholarPubMed
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Research 401, 385–391.CrossRefGoogle ScholarPubMed
Brandstätter, J.H., Löhrke, S., Bommert, K. & Wässle, H. (1993). Differential distribution of two synaptic vesicle proteins, synapto-porin and synaptophysin, in the mammalian retina. In Gene-Brain-Behavior, ed. Elsner, N. & Heisenberg, M., p. 413. Stuttgart: Germany: Georg Thieme Verlag.Google Scholar
Brandstätter, J.H., Hartveit, E., Sassoè-Pognetto, M. & Wässle, H. (1994). Expression of NMDA and high-affinity kainate receptor subunit mRNAs in the adult rat retina. European Journal of Neuroscience 6, 1100–1112.CrossRefGoogle ScholarPubMed
Brecha, N.C. (1983). Retinal neurotransmitters: Histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Brecha, N.C. (1992). Expression of GABAA receptors in the vertebrate retina. Progress in Brain Research 90, 3–28.CrossRefGoogle ScholarPubMed
Brecha, N.C., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decar-boxylase and γ-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.CrossRefGoogle Scholar
Buhl, E.H. & Dann, J.F. (1988). Morphological diversity of displaced retinal ganglion cells in the rat: A Lucifer Yellow study. Journal of Comparative Neurology 269, 210–218.CrossRefGoogle Scholar
Conley, M., Fitzpatrick, D. & Lachica, E.A. (1986). Laminar asymmetry in the distribution of choline acetyltransferase immunoreac-tive neurons in the retina of the tree shrew (Tupaia belangen). Brain Research 399, 332–338.CrossRefGoogle Scholar
Danbolt, N.C., Pines, G. & Kanner, B.I. (1990). Purification and reconstitution of the sodium-and potassium-coupled glutamate transport glycoprotein from rat brain. Biochemistry 29, 6734–6740.CrossRefGoogle ScholarPubMed
Danbolt, N.C., Storm-Mathisen, J. & Kanner, B.I. (1992). An [Na+ + K+] coupled L-glutamate transporter purified from rat brain is located in glial cell processes. Neuroscience 51, 295–310.CrossRefGoogle ScholarPubMed
Dann, J.F. & Buhl, E.H. (1987). Retinal ganglion cells projecting to the accessory optic system in the rat. Journal of Comparative Neurology 262, 141–158.CrossRefGoogle Scholar
Eckenstein, F. & Thoenen, H. (1982). Production of specific antisera and monoclonal antibodies to choline acetyltransferase: Characterization and use for identification of cholinergic neurons. EMBO Journal (Oxford) 1, 363–368.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.Google Scholar
Famiglietti, E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. Journal of Comparative Neurology 309, 40–70.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992 a). New metrics for analysis of dendritic branching patterns demonstrating similarities and differences in ON and ON-OFF directionally selective retinal ganglion cells. Journal of Comparative Neurology 324, 295–321.CrossRefGoogle Scholar
Famiglietti, E.V. (1992 b). Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. Journal of Comparative Neurology 324, 322–335.Google Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.Google Scholar
Freed, M.A. (1992). GABAergic circuits in the mammalian retina. Progress in Brain Research 90, 107–131.Google Scholar
Friedmann, D.L. & Redburn, D.A. (1990). Evidence for functionally distinct subclasses of γ-aminobutyric acid receptors in rabbit retina. Journal of Neurochemislry 55, 1189–1199.Google Scholar
Fritschy, J.-M., Benke, D., Mertens, S., Oertel, W.H., Bachi, T. & Möhler, H. (1992). Five subtypes of type A γ-aminobutyric acid receptors identified in neurons by double and triple immunofluo-rescence staining with subunit-specific antibodies. Proceedings of the National Academy of Sciences of the U.S.A. 89, 6726–6730.CrossRefGoogle Scholar
Gao, B., Fritschy, J.-M., Benke, D. & Möhler, H. (1993). Neuron specific expression of GABAA-receptor subtypes: Differential association of the α1- and α3-subunits with serotonergic and GABAergic neurons. Neuroscience 54, 881–892.CrossRefGoogle 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
Greferath, U., Müller, F., Wässle, H., Shtvers, B. & Seeburg, P. (1993 a). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.CrossRefGoogle ScholarPubMed
Greferath, U., Grünert, U., Möhler, H. & Wässle, H. (1993 b). Cholinergic amacrine cells of the rat retina express the δ-subunit of the GABAA receptor. Neuroscience Letters 163, 71–73.Google Scholar
Greferath, U., Grünert, U., Fritschy, J.-M., Stephenson, A., Möhler, H. & Wässle, H. (1995). GABAA receptor subunits have differential distributions in the rat retina: In situ hybridization and immunohistochemistry. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
Grünert, U. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. Journal of Comparative Neurology 335, 523–537.CrossRefGoogle ScholarPubMed
Grzywacz, N.M. & Koch, C. (1987). Functional properties of models for direction selectivity in the retina. Synapse 1, 417–434.Google Scholar
Hamassaki-Britto, D.E., Hermans-Boromeyer, I., Heinemann, S. & Hughes, T.E. (1993). Expression of glutamate receptor genes in the mammalian retina: The localization of G1uR1 through G1uR7 mRNAs. Journal of Neuroscience 13, 1888–1898.CrossRefGoogle Scholar
Hughes, T.E., Hermans-Borgmeyer, I. & Heinemann, S. (1992). Differential expression of glutamate receptor genes (GluR1−5) in the rat retina. Visual Neuroscience 8, 49–55.Google Scholar
Ishida, A.T. (1992). The physiology of GABAA receptors in retinal neurons. Progress in Brain Research 90, 29–45.Google Scholar
Jensen, R.J. (1994). Extracellular recordings from displaced starburst amacrine cells in normal, unlesioned rabbit retinas. Investigative Ophthalmology and Visual Science (Abstract) 35, 3725.Google Scholar
Kittila, C.A., Linn, D.M. & Massey, S.C. (1994). Effect of APB on ON-OFF directionally selective ganglion cells in rabbit. Investigative Ophthalmology and Visual Science (Abstract) 35, 3723.Google Scholar
Knaus, P., Marquèze-Pouey, B., Scherer, H. & Betz, H. (1990). Synaptoporin, a novel putative channel protein of synaptic vesicles. Neuron 5, 453–462.Google Scholar
Kosaka, T., Tauchi, M. & Dahl, J.L. (1988). Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Experimental Brain Research 70, 605–617.Google Scholar
Laurie, D., Seeburg, P. H. & Wisden, W. (1992). The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. Journal of Neuroscience 12, 1063–1076.Google Scholar
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina. Journal of Physiology (London) 188, 285–307.CrossRefGoogle Scholar
Levick, W.R., Oyster, C.W. & Takahashi, E.S. (1969). Rabbit lateral geniculate nucleus: A sharpener of directional information. Science 165, 712–714.CrossRefGoogle ScholarPubMed
Macdonald, L.L. & Olsen, R.W. (1994). GABAA receptor channels. Annual Review of Neuroscience 17, 569–602.CrossRefGoogle ScholarPubMed
Mandell, J.W., Townes-Anderson, E., Czernik, A.J., Cameron, R., Greencard, P. & De Camilli, P. (1990). Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5, 19–33.Google Scholar
Mandell, J.W., Czernik, A.J., De Camilli, P., Greencard, P. & Townes-Anderson, E. (1992). Differential expression of synapsis I and II among rat retinal synapses. Journal of Neuroscience 12, 1736–1749.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269–280.Google Scholar
Marksitzer, R., Benke, D., Fritschy, J.-M., Trzeciak, A., Bann-Warth, W. & Möhler, H. (1993). GABAA receptors: Drug binding profile and distribution of receptors containing the α2-subunit in situ. Journal of Receptive Research 13, 467–477.Google Scholar
Masland, R.H. & Ames, A. III, (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.Google Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159–178.Google Scholar
Masland, R.H., Cassidy, C. & O'Malley, D.M. (1989). The release of acetylcholine and GABA by neurons of the rabbit retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 15–26. Berlin, Germany: Springer Verlag.Google Scholar
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.Google Scholar
Müller, F., Greferath, U., Wässle, H., Wisden, W. & Seeburg, P. (1992). Glutamate receptor expression in the rat retina. Neuroscience Letters 138, 179–182.CrossRefGoogle ScholarPubMed
Nirenberg, S.A., Wu, E., Soucy, E. & Meister, M. (1994). Direction-selective ganglion cells in the mouse retina. Investigative Ophthalmology and Visual Science (Abstract) 35, 3724.Google Scholar
O'Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and γ-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 86, 3414–3418.Google Scholar
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. Journal of Physiology (London) 199, 613–635.CrossRefGoogle ScholarPubMed
Oyster, C.W., Simpson, J.I., Takahashi, E.S. & Soodak, R.E. (1980). Retinal ganglion cells projecting to the rabbit accessory optic system. Journal of Comparative Neurology 190, 49–61.CrossRefGoogle Scholar
Oyster, C.W., Amthor, F.R. & Takahashi, E.S. (1993). Dendritic architecture of ON-OFF direction-selective ganglion cells in the rabbit retina. Vision Research 33, 579–608.Google Scholar
Pourcho, R.G. & Osman, K. (1986). Cytochemical identification of cholinergic amacrine cells in cat retina. Journal of Comparative Neurology 247, 497–504.CrossRefGoogle ScholarPubMed
Rauen, T. & Kanner, B.I. (1994). Localization of the glutamate transporter GLT-1 in rat and macaque monkey retinae. Neuroscience Letters 169, 137–140.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1989). Starburst amacrine cells of the primate retina. Journal of Comparative Neurology 285, 18–37.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque, and baboon retinas. Journal of Comparative Neurology 321, 46–64.Google Scholar
Sassoè-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the al subunit of the glycine receptor. Journal of Neuroscience 14, 5131–5146.CrossRefGoogle Scholar
Sassoè-Pognetto, M., Kirsch, J., Grünert, U., Greferath, U., Fritschy, J.-M., Möhler, H., Betz, H. & Wässle, H. (1995). Colocalization of gephyrin and GABAA-receptor subunits in thè rat retina. Journal of Comparative Neurology (in press).Google Scholar
Saxena, N.C. & Macdonald, R.L. (1993). Electrophysiological characterization of recombinant GABAA receptors containing delta sub-unit in mouse L929 cells. Society for Neuroscience Abstracts 19, 852.Google Scholar
Schmidt, M., Wässle, H. & Humphrey, M.F. (1985). Number and distribution of putative cholinergic neurons in the cat retina. Neuroscience Letters 59, 235–240.CrossRefGoogle ScholarPubMed
Seeburg, P.H., Wisden, W., Verdoorn, T.A., Pritchett, D.B., Werner, P., Herb, A., Lüddens, H., Sprengel, R. & Sakmann, B. (1990). The GABAA receptor family: Molecular and functional diversity. Cold Spring Harbor Symposia on Quantitative Biology 55, 29–40.CrossRefGoogle ScholarPubMed
Shivers, B.D., Killisch, I., Sprengel, R., Sontheimer, H., Köhler, M., Schofield, P.R. & Seeburg, P.H. (1989). Two novel GABAA receptor subunits exist in distinct neuronal subpopulations. Neuron 3, 327–337.Google Scholar
Simpson, J.I. (1984). The accessory optic system. In Annual Review of Neuroscience, Vol. 7, ed. Cowan, W.M., pp. 13–41, Palo Alto, California: Annual Reviews.Google Scholar
Stone, C. & Pinto, L.H. (1992). Receptive-field organization of retinal ganglion cells in the spastic mutant mouse. Journal of Physiology (London) 456, 125–142.CrossRefGoogle ScholarPubMed
Südhof, T.C. & Jahn, R. (1991). Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6, 665–677.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google Scholar
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501–508.Google ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Resarch 9, 49–100.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L. & Boycott, B.B. (1981 a). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373–391.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L., Wässle, H. & Illing, R.-B. (1981 b). Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Research 212, 447–453.CrossRefGoogle Scholar
Vaney, D.I., Collin, S.P. & Young, H.M. (1989). Dendritic relationships between cholinergic amacrine cells and direction-selective ganglion cells. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 157–168. Berlin, Germany: Springer Verlag.CrossRefGoogle Scholar
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.CrossRefGoogle ScholarPubMed
Wisden, W., Laurie, D., Monyer, H. & Seeburg, P.H. (1992). The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. Journal of Neuroscience 12, 1040–1062.CrossRefGoogle Scholar
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204–205.CrossRefGoogle ScholarPubMed
Zarbin, M.A., Wamsley, J.K., Palacios, J.M. & Kuhar, M.J. (1986). Autoradiographic localization of high affinity GABA, benzodiazepine, dopaminergic, adrenergic and muscarinic cholinergic receptors in the rat, monkey, and human retina. Brain Research 374, 75–92.Google Scholar