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Receptor targets of amacrine cells

Published online by Cambridge University Press:  06 February 2012

CHI ZHANG
Affiliation:
Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY 40202
MAUREEN A. McCALL*
Affiliation:
Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY 40202 Department of Ophthalmology and Visual Sciences, University of Louisville, Louisville, KY 40202
*
*Address correspondence and reprint requests to: Dr. Maureen A. McCall, Department of Ophthalmology and Visual Sciences, University of Louisville, Louisville, KY 40202. E-mail: [email protected]

Abstract

Amacrine cells are a morphologically and functionally diverse group of inhibitory interneurons. Morphologically, they have been divided into approximately 30 types. Although this diversity is probably important to the fine structure and function of the retinal circuit, the amacrine cells have been more generally divided into two subclasses. Glycinergic narrow-field amacrine cells have dendrites that ramify close to their somas, cross the sublaminae of the inner plexiform layer, and create cross talk between its parallel ON and OFF pathways. GABAergic wide-field amacrine cells have dendrites that stretch long distances from their soma but ramify narrowly within an inner plexiform layer sublamina. These wide-field cells are thought to mediate inhibition within a sublamina and thus within the ON or OFF pathway. The postsynaptic targets of all amacrine cell types include bipolar, ganglion, and other amacrine cells. Almost all amacrine cells use GABA or glycine as their primary neurotransmitter, and their postsynaptic receptor targets include the most common GABAA, GABAC, and glycine subunit receptor configurations. This review addresses the diversity of amacrine cells, the postsynaptic receptors on their target cells in the inner plexiform layer of the retina, and some of the inhibitory mechanisms that arise as a result. When possible, the effects of GABAergic and glycinergic inputs on the visually evoked responses of their postsynaptic targets are discussed.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2012

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References

Amin, J. & Weiss, D.S. (1994). Homomeric rho 1 GABA channels: Activation properties and domains. Receptors Channels 2, 227236.Google Scholar
Anderson, J.R., Jones, B.W., Watt, C.B., Shaw, M.V., Yang, J.H., Demill, D., Lauritzen, J.S., Lin, Y., Rapp, K.D., Mastronarde, D., Koshevoy, P., Grimm, B., Tasdizen, T., Whitaker, R. & Marc, R.E. (2011). Exploring the retinal connectome. Molecular Vision 17, 355379.Google Scholar
Badea, T.C. & Nathans, J. (2004). Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. The Journal of Comparative Neurology 480, 331351.Google Scholar
Beaudoin, D.L., Borghuis, B.G. & Demb, J.B. (2007). Cellular basis for contrast gain control over the receptive field center of mammalian retinal ganglion cells. The Journal of Neuroscience 27, 26362645.CrossRefGoogle ScholarPubMed
Benke, D., Michel, C. & Mohler, H. (2002). Structure of GABAB receptors in rat retina. Journal of Receptor and Signal Transduction Research 22, 253266.Google Scholar
Berson, D.M., Isayama, T. & Pu, M. (1999). The Eta ganglion cell type of cat retina. The Journal of Comparative Neurology 408, 204219.Google Scholar
Berson, D.M., Pu, M. & Famiglietti, E.V. (1998). The zeta cell: A new ganglion cell type in cat retina. The Journal of Comparative Neurology 399, 269288.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711725.Google Scholar
Bloomfield, S.A. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 75, 18781893.CrossRefGoogle ScholarPubMed
Bolz, J., Frumkes, T., Voigt, T. & Wässle, H. (1985 a). Action and localization of gamma-aminobutyric acid in the cat retina. The Journal of Physiology 362, 369393.CrossRefGoogle ScholarPubMed
Bolz, J., Thier, P., Voigt, T. & Wässle, H. (1985 b). Action and localization of glycine and taurine in the cat retina. The Journal of Physiology 362, 395413.Google Scholar
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of all-amacrine cells in a slice preparation of the rat retina. The Journal of Neuroscience 13, 28742888.Google Scholar
Brecha, N., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the United States of America 85, 61876191.Google Scholar
Breuninger, T., Puller, C., Haverkamp, S. & Euler, T. (2011). Chromatic bipolar cell pathways in the mouse retina. The Journal of Neuroscience 31, 65046517.Google Scholar
Briggman, K.L., Helmstaedter, M. & Denk, W. (2011). Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183188.CrossRefGoogle ScholarPubMed
Caldwell, J.H. & Daw, N.W. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Changes in centre surround receptive fields. The Journal of Physiology 276, 299310.Google Scholar
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Lateral interactions for cells with more complex receptive fields. The Journal of Physiology 276, 277298.Google Scholar
Cascio, M. (2006). Modulating inhibitory ligand-gated ion channels. American Association of Pharmaceutical Scientists Journal 8, E353E361.Google ScholarPubMed
Casini, G., Catalani, E., Dal, M.M. & Bagnoli, P. (2005). Functional aspects of the somatostatinergic system in the retina and the potential therapeutic role of somatostatin in retinal disease. Histology and Histopathology 20, 615632.Google ScholarPubMed
Chavez, A.E. & Diamond, J.S. (2008). Diverse mechanisms underlie glycinergic feedback transmission onto rod bipolar cells in rat retina. The Journal of Neuroscience 28, 79197928.Google Scholar
Chavez, A.E., Grimes, W.N. & Diamond, J.S. (2010). Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina. The Journal of Neuroscience 30, 23302339.Google Scholar
Chavez, A.E., Singer, J.H. & Diamond, J.S. (2006). Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443, 705708.Google Scholar
Chebib, M. (2004). GABAC receptor ion channels. Clinical and Experimental Pharmacology and Physiology 31, 800804.Google Scholar
Chen, X., Hsueh, H.A., Greenberg, K. & Werblin, F.S. (2010). Three forms of spatial temporal feedforward inhibition are common to different ganglion cell types in rabbit retina. Journal of Neurophysiology 103, 26182632.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. The Journal of Comparative Neurology 332, 421432.CrossRefGoogle ScholarPubMed
Contini, M., Lin, B., Kobayashi, K., Okano, H., Masland, R.H. & Raviola, E. (2010). Synaptic input of ON-bipolar cells onto the dopaminergic neurons of the mouse retina. The Journal of Comparative Neurology 518, 20352050.Google Scholar
Contini, M. & Raviola, E. (2003). GABAergic synapses made by a retinal dopaminergic neuron. Proceedings of the National Academy of Sciences of the United States of America 100, 13581363.Google Scholar
Coombs, J., van der List, D., Wang, G.Y. & Chalupa, L.M. (2006). Morphological properties of mouse retinal ganglion cells. Neuroscience 140, 123136.Google Scholar
D’Angelo, I. & Brecha, N.C. (2004). Y2 receptor expression and inhibition of voltage-dependent Ca2+ influx into rod bipolar cell terminals. Neuroscience 125, 10391049.Google Scholar
Demb, J.B. (2007). Cellular mechanisms for direction selectivity in the retina. Neuron 55, 179186.CrossRefGoogle ScholarPubMed
Demb, J.B. (2008). Functional circuitry of visual adaptation in the retina. Journal of Physiology 586(Pt 18), 43774384.Google Scholar
de Vries, S.E., Baccus, S.A. & Meister, M. (2011). The projective field of a retinal amacrine cell. The Journal of Neuroscience 31, 85958604.Google Scholar
DeVries, S.H. & Baylor, D.A. (1995). An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proceedings of the National Academy of Sciences of the United States of America 92, 1065810662.Google Scholar
Dong, C.J. & Hare, W.A. (2003). Temporal modulation of scotopic visual signals by A17 amacrine cells in mammalian retina in vivo. Journal of Neurophysiology 89, 21592166.Google Scholar
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 21712180.Google Scholar
Dowling, J.E. & Ehinger, B. (1978). Synaptic organization of the dopaminergic neurons in the rabbit retina. The Journal of Comparative Neurology 180, 203220.Google Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2006). Receptor and transmitter release properties set the time course of retinal inhibition. The Journal of Neuroscience 26, 94139425.Google Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2010). Interneuron circuits tune inhibition in retinal bipolar cells. Journal of Neurophysiology 103, 2537.Google Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2011). Multiple pathways of inhibition shape bipolar cell responses in the retina. Visual Neuroscience 28, 95108.CrossRefGoogle ScholarPubMed
Eggers, E.D., McCall, M.A. & Lukasiewicz, P.D. (2007). Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. The Journal of Physiology 582, 569582.Google Scholar
Ehinger, B. & Floren, I. (1976). Indoleamine-accumulating neurons in the retina of rabbit, cat and goldfish. Cell and Tissue Research 175, 3748.CrossRefGoogle Scholar
Ellias, S.A. & Stevens, J.K. (1980). The dendritic varicosity: A mechanism for electrically isolating the dendrites of cat retinal amacrine cells? Brain Research 196, 365372.Google Scholar
Elstrott, J. & Feller, M.B. (2009). Vision and the establishment of direction-selectivity: A tale of two circuits. Current Opinion in Neurobiology 9, 293297.CrossRefGoogle Scholar
Enz, R. (2001). GABA(C) receptors: A molecular view. Biological Chemistry 382, 11111122.Google Scholar
Enz, R., Brandstatter, J.H., Hartveit, E., Wässle, H. & Bormann, J. (1995). Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. The European Journal of Neuroscience 7, 14951501.Google Scholar
Enz, R. & Cutting, G.R. (1999). GABAC receptor rho subunits are heterogeneously expressed in the human CNS and form homo- and heterooligomers with distinct physical properties. The European Journal of Neuroscience 11, 4150.Google Scholar
Euler, T. & Wässle, H. (1998). Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. Journal of Neurophysiology 79, 13841395.CrossRefGoogle Scholar
Famiglietti, E.V. Jr. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138144.CrossRefGoogle ScholarPubMed
Farrant, M. & Nusser, Z. (2005). Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nature Reviews. Neuroscience 6, 215229.Google Scholar
Feigenspan, A. & Bormann, J. (1994). Differential pharmacology of GABAA and GABAC receptors on rat retinal bipolar cells. European Journal of Pharmacology 288, 97104.Google Scholar
Feigenspan, A., Gustincich, S. & Raviola, E. (2000). Pharmacology of GABA(A) receptors of retinal dopaminergic neurons. Journal of Neurophysiology 84, 16971707.Google Scholar
Fletcher, E.L., Koulen, P. & Wässle, H. (1998). GABAA and GABAC receptors on mammalian rod bipolar cells. The Journal of Comparative Neurology 396, 351365.Google Scholar
Fletcher, E.L. & Wässle, H. (1999). Indoleamine-accumulating amacrine cells are presynaptic to rod bipolar cells through GABA(C) receptors. The Journal of Comparative Neurology 413, 155167.Google Scholar
Flores-Herr, N., Protti, D.A. & Wässle, H. (2001). Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. The Journal of Neuroscience 21, 48524863.Google Scholar
Frech, M.J. & Backus, K.H. (2004). Characterization of inhibitory postsynaptic currents in rod bipolar cells of the mouse retina. Visual Neuroscience 21, 645652.Google Scholar
Frech, M.J., Perez-Leon, J., Wässle, H. & Backus, K.H. (2001). Characterization of the spontaneous synaptic activity of amacrine cells in the mouse retina. Journal of Neurophysiology 86, 16321643.Google Scholar
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. The Journal of Comparative Neurology 266, 445455.Google Scholar
Freed, M.A., Smith, R.G. & Sterling, P. (2003). Timing of quantal release from the retinal bipolar terminal is regulated by a feedback circuit. Neuron 38, 89101.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. The Journal of Neuroscience 8, 23032320.Google Scholar
Gallagher, S.K., Witkovsky, P., Roux, M.J., Low, M.J., Otero-Corchon, V., Hentges, S.T. & Vigh, J. (2010). beta-Endorphin expression in the mouse retina. The Journal of Comparative Neurology 518, 31303148.Google Scholar
Ghosh, K.K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wässle, H. (2004). Types of bipolar cells in the mouse retina. The Journal of Comparative Neurology 469, 7082.Google Scholar
Gill, S.B., Veruki, M.L. & Hartveit, E. (2006). Functional properties of spontaneous IPSCs and glycine receptors in rod amacrine (AII) cells in the rat retina. The Journal of Physiology 575, 739759.Google Scholar
Gillette, M.A. & Dacheux, R.F. (1995). GABA- and glycine-activated currents in the rod bipolar cell of the rabbit retina. Journal of Neurophysiology 74, 856875.Google Scholar
Greferath, U., Grünert, U., Fritschy, J.M., Stephenson, A., Mohler, H. & Wässle, H. (1995). GABAA receptor subunits have differential distributions in the rat retina: In situ hybridization and immunohistochemistry. The Journal of Comparative Neurology 353, 553571.Google Scholar
Grimes, W.N., Li, W., Chavez, A.E. & Diamond, J.S. (2009). BK channels modulate pre- and postsynaptic signaling at reciprocal synapses in retina. Nature Neuroscience 12, 585592.Google Scholar
Grimes, W.N., Zhang, J., Graydon, C.W., Kachar, B. & Diamond, J.S. (2010). Retinal parallel processors: More than 100 independent microcircuits operate within a single interneuron. Neuron 65, 873885.Google Scholar
Grünert, U. (1999). Distribution of GABAA and glycine receptors in the mammalian retina. Clinical and Experimental Pharmacology and Physiology 26, 941944.Google Scholar
Grünert, U. (2000). Distribution of GABA and glycine receptors on bipolar and ganglion cells in the mammalian retina. Microscopy Research and Technique 50, 130140.Google Scholar
Grünert, U. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. The Journal of Comparative Neurology 335, 523537.Google Scholar
Gustincich, S., Feigenspan, A., Sieghart, W. & Raviola, E. (1999). Composition of the GABA(A) receptors of retinal dopaminergic neurons. The Journal of Neuroscience 19, 78127822.Google Scholar
Gustincich, S., Feigenspan, A., Wu, D.K., Koopman, L.J. & Raviola, E. (1997). Control of dopamine release in the retina: A transgenic approach to neural networks. Neuron 18, 723736.Google Scholar
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 29232936.Google Scholar
Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K.W. & Berson, D.M. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. The Journal of Comparative Neurology 497, 326349.Google Scholar
Haverkamp, S., Müller, U., Harvey, K., Harvey, R.J., Betz, H. & Wässle, H. (2003). Diversity of glycine receptors in the mouse retina: Localization of the alpha3 subunit. The Journal of Comparative Neurology 465, 524539.Google Scholar
Haverkamp, S., Muller, U., Zeilhofer, H.U., Harvey, R.J. & Wässle, H. (2004). Diversity of glycine receptors in the mouse retina: Localization of the alpha2 subunit. The Journal of Comparative Neurology 477, 399411.Google Scholar
Heinze, L., Harvey, R.J., Haverkamp, S. & Wässle, H. (2007). Diversity of glycine receptors in the mouse retina: Localization of the alpha4 subunit. The Journal of Comparative Neurology 500, 693707.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. The Journal of Comparative Neurology 273, 473487.Google Scholar
Hermann, R., Heflin, S.J., Hammond, T., Lee, B., Wang, J., Gainetdinov, R.R., Caron, M.G., Eggers, E.D., Frishman, L.J., McCall, M.A. & Arshavsky, V.Y. (2011). Rod vision is controlled by dopamine-dependent sensitization of rod bipolar cells by GABA. Neuron 72, 101110.Google Scholar
Holmgren-Taylor, I. (1982). Electron microscopical observations on the indoleamine-accumulating neurons and their synaptic connections in the retina of the cat. The Journal of Comparative Neurology 208, 144156.Google Scholar
Hou, M., Duan, L. & Slaughter, M.M. (2008). Synaptic inhibition by glycine acting at a metabotropic receptor in tiger salamander retina. The Journal of Physiology 586, 29132926.Google Scholar
Hughes, A. & Wieniawa-Narkiewicz, E. (1980). A newly identified population of presumptive microneurones in the cat retinal ganglion cell layer. Nature 284, 468470.Google Scholar
Isayama, T., Berson, D.M. & Pu, M. (2000). Theta ganglion cell type of cat retina. The Journal of Comparative Neurology 417, 3248.Google Scholar
Ivanova, E., Muller, U. & Wässle, H. (2006). Characterization of the glycinergic input to bipolar cells of the mouse retina. The European Journal of Neuroscience 23, 350364.Google Scholar
Jarsky, T., Cembrowski, M., Logan, S.M., Kath, W.L., Riecke, H., Demb, J.B. & Singer, J.H. (2011). A synaptic mechanism for retinal adaptation to luminance and contrast. The Journal of Neuroscience 27, 1100311015.CrossRefGoogle Scholar
Jeon, C.J., Strettoi, E. & Masland, R.H. (1998). The major cell populations of the mouse retina. The Journal of Neuroscience 18, 89368946.Google Scholar
Jia, F., Goldstein, P.A. & Harrison, N.L. (2009). The modulation of synaptic GABA(A) receptors in the thalamus by eszopiclone and zolpidem. The Journal of Pharmacology and Experimental Therapeutics 328, 10001006.Google Scholar
Kim, S.A., Jung, C.K., Kang, T.H., Jeon, J.H., Cha, J., Kim, I.B. & Chun, M.H. (2010). Synaptic connections of calbindin-immunoreactive cone bipolar cells in the inner plexiform layer of rabbit retina. Cell and Tissue Research 339, 311320.Google Scholar
Kingsmore, S.F., Giros, B., Suh, D., Bieniarz, M., Caron, M.G. & Seldin, M.F. (1994). Glycine receptor beta-subunit gene mutation in spastic mouse associated with LINE-1 element insertion. Nature Genetics 7, 136141.Google Scholar
Kirby, A.W. & Enroth-Cugell, C. (1976). The involvement of gamma-aminobutyric acid in the organization of cat retinal ganglion cell receptive fields. A study with picrotoxin and bicuculline. The Journal of General Physiology 68, 465484.Google Scholar
Kirby, A.W. & Schweitzer-Tong, D.E. (1981). GABA-antagonists and spatial summation in Y-type cat retinal ganglion cells. The Journal of Physiology 312, 335344.Google Scholar
Knop, G.C., Feigenspan, A., Weiler, R. & Dedek, K. (2011). Inputs underlying the ON-OFF light responses of type 2 wide-field amacrine cells in TH::GFP mice. The Journal of Neuroscience 31, 47804791.Google Scholar
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295329.Google Scholar
Kolb, H. (1997). Amacrine cells of the mammalian retina: Neurocircuitry and functional roles. Eye 11(Part 6), 904923.Google Scholar
Kolb, H., Cuenca, N. & Dekorver, L. (1991). Postembedding immunocytochemistry for GABA and glycine reveals the synaptic relationships of the dopaminergic amacrine cell of the cat retina. The Journal of Comparative Neurology 310, 267284.Google Scholar
Kolb, H., Cuenca, N., Wang, H.H. & Dekorver, L. (1990). The synaptic organization of the dopaminergic amacrine cell in the cat retina. Journal of Neurocytology 19, 343366.Google Scholar
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301312.Google Scholar
Kolb, H. & Nelson, R. (1993). OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. The Journal of Comparative Neurology 329, 85110.Google Scholar
Kolb, H. & Nelson, R. (1996). Hyperpolarizing, small-field, amacrine cells in cone pathways of cat retina. The Journal of Comparative Neurology 371, 415436.Google Scholar
Koontz, M.A. & Hendrickson, A.E. (1987). Stratified distribution of synapses in the inner plexiform layer of primate retina. The Journal of Comparative Neurology 263, 581592.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, 605617.Google Scholar
Korpi, E.R., Gruender, G. & Luddens, H. (2002). Drug interactions at GABAA receptors. Progress in Neurobiology 67, 113159.Google Scholar
Koulen, P., Brandstatter, J.H., Enz, R., Bormann, J. & Wässle, H. (1998 a). Synaptic clustering of GABA(C) receptor rho-subunits in the rat retina. The European Journal of Neuroscience 10, 115127.Google Scholar
Koulen, P., Malitschek, B., Kuhn, R., Bettler, B., Wässle, H. & Brandstatter, J.H. (1998 b). Presynaptic and postsynaptic localization of GABA(B) receptors in neurons of the rat retina. The European Journal of Neuroscience 10, 14461456.Google Scholar
Koulen, P., Sassoe-Pognetto, M., Grünert, U. & Wässle, H. (1996 a). Selective clustering of GABA(A) and glycine receptors in the mammalian retina. The Journal of Neuroscience 16, 21272140.Google Scholar
Lin, B. & Masland, R.H. (2006). Populations of wide-field amacrine cells in the mouse retina. The Journal of Comparative Neurology 499, 797809.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D., Eggers, E.D., Sagdullaev, B.T. & McCall, M.A. (2004). GABAC receptor-mediated inhibition in the retina. Vision Research 44, 32893296.Google Scholar
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. The Journal of Neuroscience 14, 12131223.CrossRefGoogle ScholarPubMed
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. The Journal of Comparative Neurology 413, 305326.Google Scholar
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971982.Google Scholar
Majumdar, S., Heinze, L., Haverkamp, S., Ivanova, E. & Wässle, H. (2007). Glycine receptors of A-type ganglion cells of the mouse retina. Visual Neuroscience 24, 471487.Google Scholar
Majumdar, S., Weiss, J. & Wässle, H. (2009). Glycinergic input of widefield, displaced amacrine cells of the mouse retina. The Journal of Physiology 587, 38313849.Google Scholar
Manookin, M.B., Beaudoin, D.L., Ernst, Z.R., Flagel, L.J. & Demb, J.B. (2008). Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. The Journal of Neuroscience 28, 41364150.Google Scholar
Masland, R.H. (1988). Amacrine cells. Trends in Neurosciences 11, 405410.Google Scholar
Masland, R.H. (2001). Neuronal diversity in the retina. Current Opinion in Neurobiology 11, 431436.Google Scholar
Masland, R.H. & Livingstone, C.J. (1976). Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. Journal of Neurophysiology 39, 12101219.Google Scholar
Matsui, K., Hasegawa, J. & Tachibana, M. (2001). Modulation of excitatory synaptic transmission by GABA(C) receptor-mediated feedback in the mouse inner retina. Journal of Neurophysiology 86, 22852298.Google Scholar
McCall, M.A., Lukasiewicz, P.D., Gregg, R.G. & Peachey, N.S. (2002). Elimination of the rho1 subunit abolishes GABA(C) receptor expression and alters visual processing in the mouse retina. The Journal of Neuroscience 22, 41634174.Google Scholar
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. The Journal of Neuroscience 4, 29202938.Google Scholar
McGuire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. The Journal of Neuroscience 6, 907918.Google Scholar
Menger, N., Pow, D.V. & Wässle, H. (1998). Glycinergic amacrine cells of the rat retina. The Journal of Comparative Neurology 401, 3446.Google Scholar
Menger, N. & Wässle, H. (2000). Morphological and physiological properties of the A17 amacrine cell of the rat retina. Visual Neuroscience 17, 769780.Google Scholar
Merighi, A., Raviola, E. & Dacheux, R.F. (1996). Connections of two types of flat cone bipolars in the rabbit retina. The Journal of Comparative Neurology 371, 164178.Google Scholar
Mitrofanis, J., Vigny, A. & Stone, J. (1988). Distribution of catecholaminergic cells in the retina of the rat, guinea pig, cat, and rabbit: Independence from ganglion cell distribution. The Journal of Comparative Neurology 267, 114.Google Scholar
Molnar, A., Hsueh, H.A., Roska, B. & Werblin, F.S. (2009). Crossover inhibition in the retina: Circuitry that compensates for nonlinear rectifying synaptic transmission. Journal of Computational Neuroscience 27, 569590.Google Scholar
Mohler, H., Luscher, B., Fritschy, J.M., Benke, D., Benson, J. & Rudolph, U. (1998). GABA(A)-receptor assembly in vivo: Lessons from subunit mutant mice. Life Sciences 62, 16111615.Google Scholar
Molnar, A. & Werblin, F. (2007). Inhibitory feedback shapes bipolar cell responses in the rabbit retina. Journal of Neurophysiology 98, 34233435.Google Scholar
Morkve, S.H. & Hartveit, E. (2009). Properties of glycine receptors underlying synaptic currents in presynaptic axon terminals of rod bipolar cells in the rat retina. The Journal of Physiology 587, 38133830.Google Scholar
Mozrzymas, J.W., Barberis, A. & Vicini, S. (2007). GABAergic currents in RT and VB thalamic nuclei follow kinetic pattern of α3- and α1-subunit-containing GABAA receptors. The European Journal of Neuroscience 26, 657665.Google Scholar
Munch, T.A., da Silveira, R.A., Siegert, S., Viney, T.J., Awatramani, G.B. & Roska, B. (2009). Approach sensitivity in the retina processed by a multifunctional neural circuit. Nature Neuroscience 12, 13081316.Google Scholar
Nakamura, T., Tokunaga, F. & Yoshizawa, T. (1978). Isolation of rod early receptor potential from frog retina. Vision Research 18, 861863.Google Scholar
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592614.Google Scholar
Nguyen-Legros, J. (1988). Functional neuroarchitecture of the retina: Hypothesis on the dysfunction of retinal dopaminergic circuitry in Parkinson’s disease. Surgical and Radiologic Anatomy 10, 137144.Google Scholar
Nobles, R.D., Zhang, C., Muller, U., Betz, H. & McCall, M.A. (2012). Selective glycine receptor alpha 2 subunit control of crossover inhibition between the on and off retinal pathways. (The Journal of Neuroscience, in press).Google Scholar
Nusser, Z. (2009). Variability in the subcellular distribution of ion channels increases neuronal diversity. Trends in Neurosciences 32, 267274.Google Scholar
Nusser, Z., Sieghart, W. & Somogyi, P. (1998). Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. The Journal of Neuroscience 18, 16931703.Google Scholar
O’Brien, B.J., Richardson, R.C. & Berson, D.M. (2003). Inhibitory network properties shaping the light evoked responses of cat alpha retinal ganglion cells. Visual Neuroscience 20, 351361.Google Scholar
O’Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the United States of America 86, 34143418.Google Scholar
Olsen, R.W. & Sieghart, W. (2009). GABA A receptors: Subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141148.Google Scholar
Owczarzak, M.T. & Pourcho, R.G. (1999). Transmitter-specific input to OFF-alpha ganglion cells in the cat retina. The Anatomical Record 255, 363373.Google Scholar
Padgett, C.L. & Slesinger, P.A. (2010). GABAB receptor coupling to G-proteins and ion channels. Advances in Pharmacology 58, 123147.Google Scholar
Perez de Sevilla Muller, L., Shelley, J. & Weiler, R. (2007). Displaced amacrine cells of the mouse retina. The Journal of Comparative Neurology 505, 177189.Google Scholar
Perry, V.H. & Walker, M. (1980). Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat. Proceedings of the Royal Society of London. Series B, Biological Sciences 208, 415431.Google Scholar
Pignatelli, V. & Strettoi, E. (2004). Bipolar cells of the mouse retina: A gene gun, morphological study. The Journal of Comparative Neurology 476, 254266.Google Scholar
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 Scholar
Pourcho, R.G. (1980). Uptake of [3H]glycine and [3H]GABA by amacrine cells in the cat retina. Brain Research 198, 3346.Google Scholar
Pourcho, R.G. (1982). Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101109.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, (3H)muscimol: A combined Golgi and autoradiographic study. The Journal of Comparative Neurology 219, 2535.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. The Journal of Comparative Neurology 233, 473480.Google Scholar
Pourcho, R.G. & Osman, K. (1986). Cytochemical identification of cholinergic amacrine cells in cat retina. The Journal of Comparative Neurology 247, 497504.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1991 a). Glycine receptor immunoreactivity is localized at amacrine synapses in cat retina. Visual Neuroscience 7, 611618.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1991 b). Connectivity of glycine immunoreactive amacrine cells in the cat retina. The Journal of Comparative Neurology 307, 549561.Google Scholar
Protti, D.A., Flores-Herr, N., Li, W., Massey, S.C. & Wässle, H. (2005). Light signaling in scotopic conditions in the rabbit, mouse and rat retina: A physiological and anatomical study. Journal of Neurophysiology 93, 34793488.Google Scholar
Protti, D.A., Gerschenfeld, H.M. & Llano, I. (1997). GABAergic and glycinergic IPSCs in ganglion cells of rat retinal slices. The Journal of Neuroscience 17, 60756085.Google Scholar
Protti, D.A. & Llano, I. (1998). Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. The Journal of Neuroscience 18, 37153724.Google Scholar
Puller, C. & Haverkamp, S. (2011). Bipolar cell pathways for color vision in non-primate dichromats. Visual Neuroscience 28, 5160.Google Scholar
Puopolo, M., Hochstetler, S.E., Gustincich, S., Wightman, R.M. & Raviola, E. (2001). Extrasynaptic release of dopamine in a retinal neuron: Activity dependence and transmitter modulation. Neuron 30, 211225.Google Scholar
Qian, H. & Ripps, H. (1999). Response kinetics and pharmacological properties of heteromeric receptors formed by coassembly of GABA rho- and gamma 2-subunits. Proceedings of the Royal Society of London. Series B, Biological Sciences 266, 24192425.Google Scholar
Raviola, E. & Dacheux, R.F. (1987). Excitatory dyad synapse in rabbit retina. Proceedings of the National Academy of Sciences of the United States of America 84, 73247328.Google Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P. & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. The Journal of Neuroscience 22, 38313843.Google Scholar
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior and Evolution 23, 121164.Google Scholar
Roska, B., Molnar, A. & Werblin, F.S. (2006). Parallel processing in retinal ganglion cells: How integration of space-time patterns of excitation and inhibition form the spiking output. Journal of Neurophysiology 95, 38103822.Google Scholar
Roska, B., Nemeth, E. & Werblin, F.S. (1998). Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. The Journal of Neuroscience 18, 34513459.Google Scholar
Rotolo, T.C. & Dacheux, R.F. (2003 a). Two neuropharmacological types of rabbit ON-alpha ganglion cells express GABAC receptors. Visual Neuroscience 20, 373384.Google Scholar
Rotolo, T.C. & Dacheux, R.F. (2003 b). Evidence for glycine, GABAA, and GABAB receptors on rabbit OFF-alpha ganglion cells. Visual Neuroscience 20, 285296.Google Scholar
Rowe, M.H. & Stone, J. (1977). Naming of neurones. Classification and naming of cat retinal ganglion cells. Brain, Behavior and Evolution 14, 185216.Google Scholar
Russell, T.L. & Werblin, F.S. (2010). Retinal synaptic pathways underlying the response of the rabbit local edge detector. Journal of Neurophysiology 103, 27572769.Google Scholar
Sagdullaev, B.T., McCall, M.A. & Lukasiewicz, P.D. (2006). Presynaptic inhibition modulates spillover, creating distinct dynamic response ranges of sensory output. Neuron 50, 923935.Google Scholar
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. The Journal of Neuroscience 6, 33313347.Google Scholar
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connections of indoleamine-accumulating cells in the rabbit retina. The Journal of Comparative Neurology 283, 303313.Google Scholar
Sassoe-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the alpha 1 subunit of the glycine receptor. The Journal of Neuroscience 14, 51315146.Google Scholar
Schlicker, K., McCall, M.A. & Schmidt, M. (2009). GABAC receptor-mediated inhibition is altered but not eliminated in the superior colliculus of GABAC rho1 knockout mice. Journal of Neurophysiology 101, 29742983.Google Scholar
Schofield, C.M. & Huguenard, J.R. (2007) GABA affinity shapes IPSCs in thalamic nuclei. The Journal of Neuroscience 27, 79547962.Google Scholar
Shields, C.R., Tran, M.N., Wong, R.O. & Lukasiewicz, P.D. (2000). Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. The Journal of Neuroscience 20, 26732682.Google Scholar
Siegert, S., Scherf, B.G., Del, P.K., Didkovsky, N., Heintz, N. & Roska, B. (2009). Genetic address book for retinal cell types. Nature Neuroscience 12, 11971204.Google Scholar
Sieghart, W. & Sperk, G. (2002). Subunit composition, distribution and function of GABA(A) receptor subtypes. Current Topics in Medicinal Chemistry 2, 795816.Google Scholar
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. The Journal of Neuroscience 23, 1092310933.Google Scholar
Song, Y. & Slaughter, M.M. (2010). GABA(B) receptor feedback regulation of bipolar cell transmitter release. The Journal of Physiology 588, 49374949.Google Scholar
Soucy, E., Wang, Y., Nirenberg, S., Nathans, J. & Meister, M. (1998). A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481493.Google Scholar
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. The Journal of Neuroscience 8, 623642.Google Scholar
Sterling, P. & Lampson, L.A. (1986). Molecular specificity of defined types of amacrine synapse in cat retina. The Journal of Neuroscience 6, 13141324.Google Scholar
Stone, C. & Pinto, L.H. (1992). Receptive field organization of retinal ganglion cells in the spastic mutant mouse. The Journal of Physiology 456, 125142.Google Scholar
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. The Journal of Comparative Neurology 295, 449466.Google Scholar
Strettoi, E., Dacheux, R.F. & Raviola, E. (1994). Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. The Journal of Comparative Neurology 347, 139149.Google Scholar
Strettoi, E., Novelli, E., Mazzoni, F., Barone, I. & Damiani, D. (2010). Complexity of retinal cone bipolar cells. Progress in Retinal and Eye Research 29, 272283.Google Scholar
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. The Journal of Comparative Neurology 325, 152168.Google Scholar
Sun, W., Li, N. & He, S. (2002). Large-scale morphological survey of rat retinal ganglion cells. Visual Neuroscience 19, 483493.Google Scholar
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297305.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 of London. Series B, Biological Sciences 223, 101119.Google Scholar
Tian, N., Hwang, T.N. & Copenhagen, D.R. (1998). Analysis of excitatory and inhibitory spontaneous synaptic activity in mouse retinal ganglion cells. Journal of Neurophysiology 80, 13271340.Google Scholar
Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. (2001). Microcircuits for night vision in mouse retina. The Journal of Neuroscience 21, 86168623.Google Scholar
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444446.Google Scholar
Vaney, D.I., Nelson, J.C. & Pow, D.V. (1998). Neurotransmitter coupling through gap junctions in the retina. The Journal of Neuroscience 18, 1059410602.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369373.Google Scholar
van Wyk, M., Wässle, H. & Taylor, W.R. (2009). Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Visual Neuroscience 26, 297308.Google Scholar
Veruki, M.L., Gill, S.B. & Hartveit, E. (2007). Spontaneous IPSCs and glycine receptors with slow kinetics in wide-field amacrine cells in the mature rat retina. The Journal of Physiology 581, 203219.Google Scholar
Viney, T.J., Balint, K., Hillier, D., Siegert, S., Boldogkoi, Z., Enquist, L.W., Meister, M., Cepko, C.L. & Roska, B. (2007). Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Current Biology 17, 981988.Google Scholar
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. The Journal of Comparative Neurology 248, 1935.Google Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of A II amacrine cells in mammalian retina. The Journal of Neuroscience 7, 41154128.Google Scholar
Volgyi, B., Xin, D. & Bloomfield, S.A. (2002). Feedback inhibition in the inner plexiform layer underlies the surround-mediated responses of AII amacrine cells in the mammalian retina. The Journal of Physiology 539, 603614.Google Scholar
Wafford, K.A., Macaulay, A.J., Fradley, R., O’Meara, G.F., Reynolds, D.S. & Rosahl, T.W. (2004). Differentiating the role of γ-aminobutyric acid type A (GABAA) receptor subtypes. Biochemical Society Transactions 32(Pt 3), 553556.Google Scholar
Ward, M.M. & Fletcher, E.L. (2009). Subsets of retinal neurons and glia express P2Y1 receptors. Neuroscience 160, 555566.Google Scholar
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews. Neuroscience 5, 747757.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.Google Scholar
Wässle, H. & Chun, M.H. (1988). Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. The Journal of Neuroscience 8, 33833394.Google Scholar
Wässle, H., Chun, M.H. & Muller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. The Journal of Comparative Neurology 265, 391408.Google Scholar
Wässle, H., Heinze, L., Ivanova, E., Majumdar, S., Weiss, J., Harvey, R.J. & Haverkamp, S. (2009). Glycinergic transmission in the Mammalian retina. Frontiers in Molecular Neuroscience 2, 6.Google Scholar
Wässle, H., Koulen, P., Brandstatter, J.H., Fletcher, E.L. & Becker, C.M. (1998). Glycine and GABA receptors in the mammalian retina. Vision Research 38, 14111430.Google Scholar
Wässle, H., Schafer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. The Journal of Neuroscience 6, 594604.Google Scholar
Watanabe, M., Fukuda, Y., Hsiao, C.F. & Ito, H. (1985). Electron microscopic analysis of amacrine and bipolar cell inputs on Y-, X-, and W-cells in the cat retina. Brain Research 358, 229240.Google Scholar
Webb, T.I. & Lynch, J.W. (2007). Molecular pharmacology of the glycine receptor chloride channel. Curr Pharm Des. 2007; 13(23), 23502367.Google Scholar
Weber, A.J., McCall, M.A. & Stanford, L.R. (1991). Synaptic inputs to physiologically identified retinal X-cells in the cat. The Journal of Comparative Neurology 314, 350366.Google Scholar
Weber, A.J. & Stanford, L.R. (1994). Synaptology of physiologically identified ganglion cells in the cat retina: A comparison of retinal X- and Y-cells. The Journal of Comparative Neurology 343, 483499.Google Scholar
Wegelius, K., Pasternack, M., Hiltunen, J.O., Rivera, C., Kaila, K., Saarma, M. & Reeben, M. (1998). Distribution of GABA receptor rho subunit transcripts in the rat brain. The European Journal of Neuroscience 10, 350357.Google Scholar
Wei, W., Hamby, A.M., Zhou, K. & Feller, M.B. (2011). Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469, 402406.Google Scholar
Weiss, J., O’Sullivan, G.A., Heinze, L., Chen, H.X., Betz, H. & Wässle, H. (2008). Glycinergic input of small-field amacrine cells in the retinas of wildtype and glycine receptor deficient mice. Molecular and Cellular Neurosciences 37, 4055.Google Scholar
Werblin, F.S. (2010). Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission. Visual Neuroscience 27, 18.Google Scholar
Whiting, P.J., Bonnert, T.P., McKernan, R.M., Farrar, S., Le Bourdellès, B.B., Heavens, R.P., Smith, D.W., Hewson, L., Rigby, M.R., Sirinathsinghji, D.J., Thompson, S.A. & Wafford, K.A. (1999). Molecular and functional diversity of the expanding GABA-A receptor gene family. Annals of the New York Academy of Sciences 868, 645653.Google Scholar
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 1740.Google Scholar
Wotring, V.E., Chang, Y. & Weiss, D.S. (1999). Permeability and single channel conductance of human homomeric rho1 GABAC receptors. The Journal of Physiology 521(Pt 2), 327336.Google Scholar
Wulle, I. & Schnitzer, J. (1989). Distribution and morphology of tyrosine hydroxylase-immunoreactive neurons in the developing mouse retina. Brain Research Developmental Brain Research 48, 5972.Google Scholar
Xin, D. & Bloomfield, S.A. (1999). Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Visual Neuroscience 16, 653665.Google Scholar
Yang, X.L. (2004). Characterization of receptors for glutamate and GABA in retinal neurons. Progress in Neurobiology 73, 127150.Google Scholar
Yazulla, S. (2008). Endocannabinoids in the retina: From marijuana to neuroprotection. Progress in Retinal and Eye Research 27, 501526.Google Scholar
Yazulla, S., Studholme, K.M. & Pinto, L.H. (1997). Differences in the retinal GABA system among control, spastic mutant and retinal degeneration mutant mice. Vision Research 37, 34713482.Google Scholar
Zhang, F., Gradinaru, V., Adamantidis, A.R., Durand, R., Airan, R.D., de Lecea, L. & Deisseroth, K. (2010). Optogenetic interrogation of neural circuits: Technology for probing mammalian brain structures. Nature Protocols 5, 439456.Google Scholar
Zhang, J., Jung, C.S. & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553563.Google Scholar
Zhang, J., Li, W., Trexler, E.B. & Massey, S.C. (2002). Confocal analysis of reciprocal feedback at rod bipolar terminals in the rabbit retina. The Journal of Neuroscience 22, 1087110882.Google Scholar
Zhang, D.Q., Stone, J.F., Zhou, T., Ohta, H. & McMahon, D.G. (2004). Characterization of genetically labeled catecholamine neurons in the mouse retina. Neuroreport 15, 17611765.Google Scholar
Zhou, C. & Dacheux, R.F. (2004). All amacrine cells in the rabbit retina possess AMPA-, NMDA-, GABA-, and glycine-activated currents. Visual Neuroscience 21, 181188.Google Scholar
Zhou, C. & Dacheux, R.F. (2005). Glycine- and GABA-activated inhibitory currents on axon terminals of rabbit cone bipolar cells. Visual Neuroscience 22, 759767.Google Scholar
Zhou, Z.J. & Lee, S. (2008). Synaptic physiology of direction selectivity in the retina. The Journal of Physiology 586, 43714376.Google Scholar
Zucker, C. & Yazulla, S. (1982). Localization of synaptic and nonsynaptic nicotinic-acetylcholine receptors in the goldfish retina. The Journal of Comparative Neurology 204, 188195.Google Scholar