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Glycine receptors in the rod pathway of the macaque monkey retina

Published online by Cambridge University Press:  02 June 2009

Ulrike Grünert
Affiliation:
Max-Planck-lnstitut für Hirnforschung, Deutschordenstr. 46, D-60528 Frankfurt am Main, Germany Department of Physiology F 13, University of Sydney, NSW 2006, Australia
Heinz Wässle
Affiliation:
Max-Planck-lnstitut für Hirnforschung, Deutschordenstr. 46, D-60528 Frankfurt am Main, Germany

Abstract

The distribution of glycinergic synapses in macaque monkey retina was investigated. The monoclonal antibody (mAb2b) against the αl subunit of the glycine receptor produced a punctate immunoreactivity that was localized to synapses. In central retina about 70% of the αl subunit-containing synapses were located in strata 1 and 2 of the inner plexiform layer, about 30% were located in strata 3 and 4, and immunoreactivity was absent in stratum 5. Electron microscopy showed that the majority of the synapses in strata 1 and 2 were on cone bipolar axons. The presynaptic profile always belonged to an amacrine cell. Presynaptic and postsynaptic profiles were further characterized using double-label immunofluorescence with cell-type specific antibodies against calcium-binding proteins. An antiserum against calretinin was used to label A<doubt/>II amacrine cells and an antiserum against recoverin was used to label flat midget bipolar cells. In the outer part of the IPL, 75% of the αl-immunoreactive puncta were colocalized with calretinin-immunoreactive An processes and 61% of the αl-immunoreactive puncta were colocalized with recoverin-positive midget bipolar axons. These results suggest that the αl subunit of the glycine receptor is present at the chemical synapse made by A<doubt/>II amacrine cells with flat midget bipolar cells, thus providing a pathway for rod signals to reach midget ganglion cells.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Bolz, J., Twer, P., Voigt, T. & Wässle, H. (1985). Action and localization of glycine and taurine in the cat retina. Journal of Physiology 362, 395413.CrossRefGoogle ScholarPubMed
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of A<doubt/>II-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 28742888.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109176.Google Scholar
Boycott, B.B. & Wässle, H. (1991). Morphological classification of bipolar cells of the primate retina. European Journal of Neuroscience 3, 10691088.CrossRefGoogle ScholarPubMed
Chen, B., Goebel, D.J. & Pourcho, R. (1994). Calretinin immuno-reactivity and transmitter specificity of neurons in the cat retina. ARVO Abstracts. Investigative Ophthalmology and Visual Science 35, 1582.Google Scholar
Chun, M.-H., Han, S.-H., Chung, J.-W. & Wässle, H. (1993). Electron microscopic analysis of the rod pathway of the rat retina. Journal of Comparative Neurology 332, 421432.CrossRefGoogle ScholarPubMed
Cohen, E.D., Zhou, Z.J. & Fain, G.L. (1994). Ligand-gated currents of alpha and beta ganglion cells in the cat retinal slice. Journal of Neurophysiology 72, 12601269.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, gluta-mate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287302.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331345.CrossRefGoogle ScholarPubMed
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Gluta-mate, GABA, and glycine in the human retina: An immunocyto-chemical investigation. Journal of Comparative Neurology 311, 483494.CrossRefGoogle Scholar
Daw, N.W., Jensen, R.J. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neurosciences 13, 110115.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society B (London) 166, 80111.Google ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293300.CrossRefGoogle Scholar
Greferath, U., Brandstätter, J.H., Wässle, H., Kirsch, J., Kuhse, J. & Grünert, U. (1994). Differential expression of glycine receptor subunits in the retina of the rat: A study using immunohisto-chemistry and in situ hybridization. Visual Neuroscience 11, 721729.CrossRefGoogle Scholar
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 27422758.CrossRefGoogle ScholarPubMed
Grunert, U., Martin, P.R. & Wassle, H. (1994). Immunocytochem-ical analysis of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 348, 607627.CrossRefGoogle Scholar
Grünert, U. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. Journal of Comparative Neurology 335, 523537.CrossRefGoogle ScholarPubMed
Harlow, E. & Lane, D. (1988). Antibodies. A Laboratory Manual. Michigan: Cold Spring Harbor Laboratory.Google Scholar
Heizmann, C.W., Röhrenbeck, J. & Kamphuis, W. (1989). Paralbumin, molecular and functional aspects. In Calcium Binding Proteins in Normal and Transformed Cells, ed. Pochet, R., Lawson, D.E.M. & Heizmann, C.W., pp. 5766. New York: Plenum Publishing Corporation.Google Scholar
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, 473487.CrossRefGoogle ScholarPubMed
Hsu, S.-M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577580.CrossRefGoogle ScholarPubMed
Karschin, A., & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of the rat retina. Journal of Neurophysiology 63, 860876.CrossRefGoogle ScholarPubMed
Kirsch, J. & Betz, H. (1993). Widespread expression of gephyrin, a putative glycine receptor-tubulin linker protein, in rat brain. Brain Research 621, 301310.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295329.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 4749.CrossRefGoogle ScholarPubMed
Koontz, M.A., Hendrickson, L.E., Brace, S.T. & Hendrickson, A.E. (1993). Immunocytochemical localization of CABA and glycine in amacrine and displaced amacrine cells of macaque monkeyretina. Vision Research 33, 26172628.CrossRefGoogle Scholar
Lambrecht, H.-G. & Koch, K.-W. (1991). A 26–kd calcium-binding protein from bovine rod outer segments as modulator of photoreceptor guanylate cyclase. EMBO Journal 10, 793798.CrossRefGoogle Scholar
Lambrecht, H.-G. & Koch, K.-W. (1992). Recoverin, a novel calcium-binding protein from vertebrate photoreceptors. Biochimica et Biophysica Acta 1160, 6366.CrossRefGoogle ScholarPubMed
Marc, R.E. & Liu, W.-L.S. (1985). (3H) Glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241260.CrossRefGoogle ScholarPubMed
Marlani, A.P. (1990). Amacrine cells of the rhesus monkey retina. Journal of Comparative Neurology 301, 382400.CrossRefGoogle Scholar
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreac-tivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269287.CrossRefGoogle ScholarPubMed
Milam, A.H., Dacey, D.M. & Dizhoor, A.M. (1993). Recoverin immu-noreactivity in mammalian cone bipolar cells. Visual Neuroscience 10, 112.CrossRefGoogle Scholar
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 16571672.CrossRefGoogle ScholarPubMed
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 116.CrossRefGoogle ScholarPubMed
Pinol, M.R., Kägi, U., Heizmann, C.W., Vogel, B., Séquier, J.-M., Haas, W. & Hunziker, W. (1990). Poly- and monoclonal antibodies against recombinant rat brain calbindin D-28K were produced to map its selective distribution in the central nervous system. Journal of Neurochemistry 54, 18271833.CrossRefGoogle ScholarPubMed
Pinto, L.H., Grünert, U., Studholme, K., Yazulla, S., Kirsch, J. & Becker, C.-M. (1994). Glycine receptors in the retinas of normal and spastic mutant mice. Investigative Ophthalmology and Visual Science 35, 36333639.Google ScholarPubMed
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.Google Scholar
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, 473480.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). A combined Golgi and autoradiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 11781188.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1991). Glycine receptor immu-noreactivity is localized at amacrine synapses in cat retina. Visual Neuroscience 7, 611618.CrossRefGoogle Scholar
Rogers, J.H. (1987). Calretinin: A gene for a novel calcium-binding protein expressed principally in neurons. Journal of Cell Biology 105, 13431353.CrossRefGoogle ScholarPubMed
Rogers, J.H. (1989). Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31, 697709.CrossRefGoogle ScholarPubMed
Röhrenbeck, J., Wässle, H. & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium-binding proteins. European Journal of Neuroscience 1, 407420.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Jacobowitz, D.M. (1992). The distribution of calretinin-like immunoreactivity and correlation with mRNA expres-sion in the retina. ARVO Abstracts. Investigative Ophthalmology and Visual Science 33, 1032.Google Scholar
Sassoè-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glyciner-gic synapses in the rod pathway of the rat retina: Cone bipolar cells express the αl subunit of the glycine receptor. Journal of Neuro-science 14, 51315146.Google Scholar
Schröder, S., Hoch, W., Becker, C.-M., Grenningloh, G. & BETZ, H. (1991). Mapping of antigenic epitopes on the αl subunit of the inhibitory glycine receptor. Biochemistry 30, 4247.CrossRefGoogle Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149185.CrossRefGoogle ScholarPubMed
Stichel, C.C., Kägi, U. & Heizmann, C.W. (1986). Parvalbumin in cat brain: Isolation, characterization and localization. Journal of Neurochemistry 47, 4653.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, 449466.CrossRefGoogle ScholarPubMed
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (An) in the rabbit retina. Journal of Comparative Neurology 325, 152168.CrossRefGoogle Scholar
Suzuki, S., Tachibana, M. & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology 421, 645662.CrossRefGoogle ScholarPubMed
Tauck, D.L., Frosch, M.P. & Lipton, S.A. (1988). Characterization of GABA- and glycine-induced currents of solitary rodent retinal ganglion cells in culture. Neuroscience 27, 193203.CrossRefGoogle ScholarPubMed
Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99112.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U. & Röhrenbeck, J. (1993). Immunocyto-chemical staining of Aii amacrine cells in the rat retina with antibodies against parvalbumin. Journal of Comparative Neurology 332, 407420.CrossRefGoogle Scholar
Wässle, H., Grünert, U., Martin, P.R. & Boycott, B.B. (1994). Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Research 34, 561579.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Chun, M.-H. & Boycott, B. B. (1995). The rod pathway of the macaque monkey retina: Identification of Aii-amacrine cells with antibodies against calretinin. Journal of Comparative Neurology (in press).CrossRefGoogle ScholarPubMed
Zhou, Z.J., Marshak, D.W. & Fain, G.L. (1994). Amino acid receptors of midget and parasol cells in primate retina. Proceedings of the National Academy of Sciences of the U.S.A. 91, 49074911.CrossRefGoogle ScholarPubMed