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Ionotropic glutamate receptors of amacrine cells of the mouse retina

Published online by Cambridge University Press:  09 March 2006

OLIVIA N. DUMITRESCU ,
DARIO A. PROTTI ,
SRIPARNA MAJUMDAR ,
HANNS ULRICH ZEILHOFER  and
HEINZ WÄSSLE
OLIVIA N. DUMITRESCU
Affiliation:
Department of Neuroanatomy, Max-Planck-Institute for Brain Research, Frankfurt/Main, Germany
DARIO A. PROTTI
Affiliation:
Department of Physiology, University of Sydney, Sydney, Australia
SRIPARNA MAJUMDAR
Affiliation:
Department of Neuroanatomy, Max-Planck-Institute for Brain Research, Frankfurt/Main, Germany
HANNS ULRICH ZEILHOFER
Affiliation:
Department of Experimental and Clinical Pharmacology and Toxicology, University of Erlangen, Erlangen, Germany
HEINZ WÄSSLE
Affiliation:
Department of Neuroanatomy, Max-Planck-Institute for Brain Research, Frankfurt/Main, Germany
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Abstract

The mammalian retina contains approximately 30 different morphological types of amacrine cells, receiving glutamatergic input from bipolar cells. In this study, we combined electrophysiological and pharmacological techniques in order to study the glutamate receptors expressed by different types of amacrine cells. Whole-cell currents were recorded from amacrine cells in vertical slices of the mouse retina. During the recordings the cells were filled with Lucifer Yellow/Neurobiotin allowing classification as wide-field or narrow-field amacrine cells. Amacrine cell recordings were also carried out in a transgenic mouse line whose glycinergic amacrine cells express enhanced green fluorescent protein (EGFP). Agonist-induced currents were elicited by exogenous application of NMDA, AMPA, and kainate (KA) while holding cells at −75 mV. Using a variety of specific agonists and antagonists (NBQX, AP5, cyclothiazide, GYKI 52466, GYKI 53655, SYM 2081) responses mediated by AMPA, KA, and NMDA receptors could be dissected. All cells (n = 300) showed prominent responses to non-NMDA agonists. Some cells expressed AMPA receptors exclusively and some cells expressed KA receptors exclusively. In the majority of cells both receptor types could be identified. NMDA receptors were observed in about 75% of the wide-field amacrine cells and in less than half of the narrow-field amacrine cells. Our results confirm that different amacrine cell types express distinct sets of ionotropic glutamate receptors, which may be critical in conferring their unique temporal responses to this diverse neuronal class.

Keywords

Mouse retinaAmacrine cellsIonotropic glutamate receptors
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 1 , January 2006 , pp. 79 - 90
Copyright
2006 Cambridge University Press

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References

REFERENCES

Barry, P.H. (1994). JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. Journal of Neuroscience Methods 51, 107–116.Google Scholar
Bertolino, M., Baraldi, M., Paenti, C., Braghiroli, D., diBella, M., Vicini, S., & Costa, E. (1993). Modulation of AMPA/kainate receptors by analogoues of diazoxide and cyclothiazide in thin slices of rat hippocampus. Receptors and Channels 1, 267–278.Google Scholar
Bleakman, D., Ballyk, B.A., Schöpp, D.D., Palmer, A.J., Bath, C.P., Sharpe, E.F., Woolley, M.L., Bufton, H.R., Kamboj, R.K., Tarnawa, I., & Lodge, D. (1996). Activity of 2,3-benzodiazepines at native rat and recombinant human glutamate receptors in vitro: Stereospecificity and selectivity profiles. Neuropharmacology 35, 1689–1702.Google Scholar
Boos, R., Schneider, H., & Wässle, H. (1993). Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.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.Google Scholar
Brandstätter, J.J., Koulen, P., & Wässle, H. (1997). Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. Journal of Neuroscience 17, 9298–9307.Google Scholar
Brandstätter, J.H., Koulen, P., & Wässle, H. (1998). Diversity of glutamate receptors in the mammalian retina. Vision Research 38, 1385–1397.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 246, 435–458.Google Scholar
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.Google Scholar
Dingledine, R., Borges, K., Bowie, D., & Traynelis, S.F. (1999). The glutamate receptor ion channels. Pharmacological Reviews 51, 7–61.Google Scholar
Dixon, D.B. & Copenhagen, D.R. (1992). Two types of glutamate receptors differential excite amacrine cells in the tiger salamander retina. Journal of Physiology 449, 589–606.Google Scholar
Donevan, S.D. & Rogawski, M.A. (1993). GYKI 52466, a 2,3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses. Neuron 10, 51–59.Google Scholar
Donevan, S.D., Beg, A., Gunther, J.M., & Twyman, R.E. (1998). The methylglutamate, SYM 2081, is a potent and highly selective agonist at kainate receptors. The Journal of Pharmacology and Experimental Therapeutics 285, 539–545.Google Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society B (London) 166, 80–111.Google Scholar
Firth, S.I., Li, W., Massey, S.C., & Marshak, D.W. (2003). AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina. Journal of Comparative Neurology 466, 80–90.Google Scholar
Fletcher, E.L., Hack, I., Brandstätter, J.H., & Wässle, H. (2000). Synaptic localization of NMDA receptor subunits in the rat retina. Journal of Comparative Neurology 420, 98–112.Google Scholar
Ghosh, K.K., Haverkamp, S., & Wässle, H. (2001). Glutamate receptors in the rod pathway of the mammalian retina. Journal of Neuroscience 21, 8636–8647.Google Scholar
Grünert, U., Haverkamp, S., Fletcher, E., & Wässle, H. (2002). Synaptic distribution of ionotropic glutamate receptors in the inner plexiform layer of the primate retina. Journal of Comparative Neurology 447, 138–151.Google Scholar
Grünert, U., Lin, B., & Martin, P.R. (2003). Glutamate receptors at bipolar synapses in the inner plexiform layer of primate retina: Light microscopic analysis. Journal of Comparative Neurology 466, 136–147.Google Scholar
Gu, Z.-Q., Hesson, D.P., Pelletier, J.C., & Maccecchini, M.-L. (1995). Synthesis, resolution, and biological evaluation of the four stereoisomers of 4-methylglutamic acid: Selective probes of kainate receptors. Journal of Medicinal Chemistry 38, 2518–2520.Google Scholar
Habermann, C.J., Wässle, H., & Protti, D.A. (2001). AII amacrine cells show a distinct distribution of voltage-dependent calcium channels and ionotropic glutamate receptors. Investigative Ophthalmology and Visual Science 42, E-Abstract 3622.Google Scholar
Hack, I., Frech, M., Dick, O., Peichl, L., & Brandstätter, J.H. (2001). Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. European Journal of Neuroscience 13, 15–24.Google Scholar
Hartveit, E. & Veruki, M.L. (1997). AII amacrine cells express functional NMDA receptors. NeuroReport 8, 1219–1223.Google Scholar
Hartveit, E., Brandstätter, J.H., Sassoè-Pognetto, M., Laurie, D.J., Seeburg, P.H., & Wässle, H. (1994). Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. Journal of Comparative Neurology 348, 570–582.Google Scholar
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. Journal of Comparative Neurology 424, 1–23.Google Scholar
Haverkamp, S., Müller, U., Zeilhofer, H.U., Harvey, R.J., & Wässle, H. (2004). Diversity of glycine receptors in the mouse retina: Localization of the α2 subunit. Journal of Comparative Neurology 477, 399–411.Google Scholar
Hollmann, M. & Heinemann, S. (1994). Clones glutamate receptors. Annual Review of Neuroscience 17, 31–108.Google 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
Kalloniatis, M., Sun, D., Foster, L., Haverkamp, S., & Wässle, H. (2004). Localization of NMDA receptor subunits and mapping NMDA drive within the mammalian retina. Visual Neuroscience 21, 587–597.Google Scholar
Kew, J.N.C. & Kemp, J.A. (2005). Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology 179, 4–29.Google Scholar
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 47–49.Google Scholar
Lee, E.J., Kim, H.J., Lim, E.J., Kim, I.B., Kang, W.S., Oh, S.J., Rickman, D.W., Chung, J.W., & Chun, M.H. (2004). AII amacrine cells in the mammalian retina show disabled-1 immunoreactivity. Journal of Comparative Neurology 470, 372–381.Google Scholar
Li, W., Trexler, E.B., & Massey, S.C. (2002). Glutamate receptors at rod bipolar ribbon synapses in the rabbit retina. Journal of Comparative Neurology 448, 230–248.Google Scholar
Linn, D.M. & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by NMDA receptors. Journal of Neuroscience 11, 123–133.Google Scholar
Linn, D.M., Blazynski, C., Redburn, D.A., & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by kainate receptors. Journal of Neuroscience 11, 111–122.Google Scholar
Lodge, D., Jones, M.G., & Palmer, A.J. (1991). Excitatory amino acids: New tools for old stories or pharmacological subtypes of glutamate receptors: Electrophysiological studies. Canadian Journal of Physiology and Pharmacology 69, 1123–1128.Google Scholar
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971–982.Google Scholar
Maguire, G. (1999). Rapid desensitization converts prolonged glutamate release into a transient EPSC at ribbon synapses between retinal bipolar and amacrine cells. European Journal of Neuroscience 11, 353–362.Google Scholar
Marc, R.E. (1999a). Mapping glutamatergic drive in the vertebrate retina with a channel-permeant organic cation. Journal of Comparative Neurology 407, 47–64.Google Scholar
Marc, R.E. (1999b). Kainate activation of horizontal, bipolar, amacrine, and ganglion cells in the rabbit retina. Journal of Comparative Neurology 407, 65–76.Google Scholar
Masland, R.H. (2001). The fundamental plan of the retina. Nature Neuroscience 4, 877–886.Google Scholar
Massey, S.C. & Miller, R.F. (1988). Glutamate receptors of ganglion cells in the rabbit retina: Evidence for glutamate as a bipolar cell transmitter. Journal of Physiology 405, 635–655.Google Scholar
Menger, N. & Wässle, H. (2000). Morphological and physiological properties of the A17 amacrine cells of the rat retina. Visual Neuroscience 17, 769–780.Google Scholar
Menger, N., Pow, D.V., & Wässle, H. (1998). Glycinergic amacrine cells of the rat retina. Journal of Comparative Neurology 401, 34–46.Google Scholar
Mørkve, S.H., Veruki, M.L., & Hartveit, E. (2002). Functional characteristics of non-NMDA-type ionotropic glutamate receptor channels in AII amacrine cells in rat retina. Journal of Physiology 542, 147–165.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.Google Scholar
O'Brien, B.J., Annies, M., & Wässle, H. (2002). Ionotropic glutamate receptors of amacrine and ganglion cells in mouse retina. Investigative Ophthalmology and Visual Science 43, E-Abstract 4768.Google Scholar
Ozawa, S., Kamiya, H., Tsuzuki, K. (1998). Glutamate receptors in the mammalian central nervous system. Progress in Neurobiology 54, 581–618.Google Scholar
Palmer, A.J. & Lodge, D. (1993). Cyclothiazide reverses AMPA receptor antagonism of the 2,3-benzodiazepine, GYKI 53655. European Journal of Pharmacology 244, 193–194.Google Scholar
Peng, Y.-W., Blackstone, C.D., Huganir, R.L., & Yau, K.-W. (1995). Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66, 483–497.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, 473–480.Google Scholar
Qin, P. & Pourcho, G. (1996). Distribution of AMPA-selective glutamate receptor subunits in cat retina. Brain Research 710, 303–307.Google Scholar
Qin, P. & Pourcho, G. (1999a). Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 16, 169–177.Google Scholar
Qin, P. & Pourcho, G. (1999b). AMPA-selective glutamate receptor subunits GluR2 and GluR4 in the cat retina: An immunocytochemical study. Visual Neuroscience 16, 1105–1114.Google Scholar
Qin, P. & Pourcho, G. (2001). Immunocytochemical localization of kainate-selective glutamate receptor subunits GluR5, GluR6, and GluR7 in the cat retina. Brain Research 890, 211–221.Google Scholar
Sheardown, M.J., Nielsen, E.O., Hansen, A.J., Jacobsen, P., & Honore, T. (1990). 2,3-dihydroxy-6-nitro-7-sulfamoyl-benzo(F)quinoxaline: A neuroprotectant for cerebral ischemia. Science 247, 571–574.Google Scholar
Shen, Y., Zhou, Y., & Yang, X.-L. (1999). Characterization of AMPA receptors on isolated amacrine-like cells in carp retina. European Journal of Neuroscience 11, 4233–4240.Google Scholar
Shen, W., Finnegan, S.G., & Slaughter, M.M. (2004). Glutamate receptor subtypes in human retinal horizontal cells. Visual Neuroscience 21, 89–95.Google Scholar
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. Journal of Neuroscience 23, 10923–10933.Google Scholar
Slaughter, M.M. & Miller, R.F. (1983). The role of excitatory amino acid transmitters in the mudpuppy retina: An analysis with kainic acid and N-methyl aspartate. Journal of Neuroscience 3, 1701–1711.Google Scholar
Thoreson, W.B. & Witkovsky, P. (1999). Glutamate receptors and circuits in the vertebrate retina. Progress in Retinal and Eye Research 18, 765–810.Google Scholar
Tran, M.N., Higgs, M.H., & Lukasiewicz, P.D. (1999). AMPA receptor kinetics limit retinal amacrine cell excitatory synaptic responses. Visual Neuroscience 16, 835–842.Google Scholar
Trexler, E.B., Li, W., & Massey, S.C. (2003). Expression of NMDA-sensitive glutamate receptors on AII amacrine cells. Investigative Ophthalmology and Visual Science 44, E-Abstract 2070.Google Scholar
Vaney, D.I. (1991). The mosaic of amacrine cells in mammalian retina. Progress in Retinal Research 9, 49–100.Google Scholar
Veruki, M.L., Mørkve, S.H., & Hartveit, E. (2003). Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. Journal of Physiology 549, 759–774.Google Scholar
Vigh, J. & Witkovsky, P. (2004). Neurotransmitter actions on transient amacrine and ganglion cells of the turtle retina. Visual Neuroscience 21, 1–11.Google Scholar
Vyklicky, L.Jr., Patneau, D.K., & Mayer, M.L. (1991). Modulation of excitatory synaptic transmission by drugs that reduce desensitization at AMPA/kainate receptors. Neuron 7, 971–984.Google Scholar
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews Neuroscience 5, 747–757.Google Scholar
Wilding, T.J. & Huettner, J.E. (1995). Differential antagonism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-preferring and kainate-preferring receptors by 2,3-benzodiazepines. Molecular Pharmacology 47, 582–587.Google Scholar
Zafra, F., Aragon, C., Olivares, L., Danbolt, N.C., Giménez, C., & Storm-Mathisen, J. (1995). Glycine transporters are differentially expressed among CNS cells. Journal of Neuroscience 15, 3952–3969.Google Scholar
Zeilhofer, H.U., Studler, B., Arabadzisz, D., Schweizer, C., Ahmadi, S., Layh, B., Bösl, M.R., & Fritschy, J.-M. (2005). Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. Journal of Comparative Neurology 482, 123–141.Google Scholar
Zhang, C., Hamassaki-Britto, D.E., Britto, L.R.G., & Duvoisin, R.M. (1996). Expression of glutamate receptor subunit genes during development of the muse retina. NeuroReport 8, 335–340.Google Scholar
Zhou, Z.J. & Fain, G.L. (1995). Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices. Journal of Neuroscience 15, 5334–5345.Google Scholar
Zhou, L.-M., Gu, Z.-Q., Costa, A.M., Yamada, K.A., Mansson, P.E., Giordano, T., Skolnick, P., & Jones, K.A. (1997). (2S,4R)-4-Methylglutamic acid (SYM 2081): A selective, high-affinity ligand for kainate receptors. Journal of Pharmacology and Experimental Therapeutics 280, 422–427.Google Scholar
Zhou, C. & Dacheux, R.F. (2004). AII amacrine cells in the rabbit retina possess AMPA-, NMDA-, GABA-, and glycine-activated currents. Visual Neuroscience 21, 181–188.Google Scholar