Skip to main content
×
×
Home

Intrinsic properties and functional circuitry of the AII amacrine cell

  • JONATHAN B. DEMB (a1) and JOSHUA H. SINGER (a2)
Abstract

Amacrine cells represent the most diverse class of retinal neuron, comprising dozens of distinct cell types. Each type exhibits a unique morphology and generates specific visual computations through its synapses with a subset of excitatory interneurons (bipolar cells), other amacrine cells, and output neurons (ganglion cells). Here, we review the intrinsic and network properties that underlie the function of the most common amacrine cell in the mammalian retina, the AII amacrine cell. The AII connects rod and cone photoreceptor pathways, forming an essential link in the circuit for rod-mediated (scotopic) vision. As such, the AII has become known as the rod–amacrine cell. We, however, now understand that AII function extends to cone-mediated (photopic) vision, and AII function in scotopic and photopic conditions utilizes the same underlying circuit: AIIs are electrically coupled to each other and to the terminals of some types of ON cone bipolar cells. The direction of signal flow, however, varies with illumination. Under photopic conditions, the AII network constitutes a crossover inhibition pathway that allows ON signals to inhibit OFF ganglion cells and contributes to motion sensitivity in certain ganglion cell types. We discuss how the AII’s combination of intrinsic and network properties accounts for its unique role in visual processing.

Copyright
Corresponding author
*Address correspondence and reprint requests to: Jonathan B. Demb. E-mail: jonathan.demb@yale.edu or Joshua H. Singer. E-mail: jhsinger@umd.edu
References
Hide All
Alpern, M. (1965). Rod-cone independence in the after-flash effect. The Journal of Physiology 176, 462472.
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.
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Dark adaptation, absolute threshold and Purkinje shift in single units of the cat’s retina. The Journal of Physiology 137, 327337.
Barlow, H.B., Levick, W.R. & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl. 3), 87101.
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. The Journal of Physiology 357, 575607.
Beaudoin, D.L., Manookin, M.B. & Demb, J.B. (2008). Distinct expressions of contrast gain control in parallel synaptic pathways converging on a retinal ganglion cell. The Journal of Physiology 586, 54875502.
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal & Eye Research 20, 351384.
Bloomfield, S.A. & Xin, D. (2000). Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. The Journal of Physiology 523(Pt 3), 771783.
Bloomfield, S.A., Xin, D. & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565576.
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.
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 255, 105.
Boycott, B.B. & Kolb, H. (1973). The connections between bipolar cells and photoreceptors in the retina of the domestic cat. The Journal of Comparative Neurology 148, 91114.
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.
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.
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurons in the cat’s retina and lateral geniculate nucleus. The Journal of Physiology 217, 473496.
Cohen, E.D. (1998). Interactions of inhibition and excitation in the light-evoked currents of X type retinal ganglion cells. Journal of Neurophysiology 80, 29752990.
Cohen, E.D. & Miller, R.F. (1999). The network-selective actions of quinoxalines on the neurocircuitry operations of the rabbit retina. Brain Research 831, 206228.
Cohen, E. & Sterling, P. (1990). Convergence and divergence of cones onto bipolar cells in the central area of cat retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 330, 323328.
Crook, J.D., Davenport, C.M., Peterson, B.B., Packer, O.S., Detwiler, P.B. & Dacey, D.M. (2009). Parallel ON and OFF cone bipolar inputs establish spatially coextensive receptive field structure of blue-yellow ganglion cells in primate retina. The Journal of Neuroscience 29, 83728387.
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. The Journal of Neuroscience 6, 331345.
Deans, M.R., Völgyi, B., Goodenough, D.A., Bloomfield, S.A. & Paul, D.L. (2002). Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703712.
Dedek, K., Schultz, K., Pieper, M., Dirks, P., Maxeiner, S., Willecke, K., Weiler, R. & Janssen-Bienhold, U. (2006). Localization of heterotypic gap junctions composed of connexin45 and connexin36 in the rod pathway of the mouse retina. The European Journal of Neuroscience 24, 16751686.
Demb, J.B., Zaghloul, K., Haarsma, L. & Sterling, P. (2001 a). Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. The Journal of Neuroscience 21, 74477454.
Demb, J.B., Zaghloul, K. & Sterling, P. (2001 b). Cellular basis for the response to second-order motion cues in Y retinal ganglion cells. Neuron 32, 711721.
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.
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London. Series B, Biological Sciences 166, 80111.
Dunn, F.A., Doan, T., Sampath, A.P. & Rieke, F. (2006). Controlling the gain of rod-mediated signals in the Mammalian retina. The Journal of Neuroscience 26, 39593970.
Famiglietti, E.V. Jr. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293300.
Feigenspan, A., Teubner, B., Willecke, K. & Weiler, R. (2001). Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina. The Journal of Neuroscience 21, 230239.
Field, G.D., Greschner, M., Gauthier, J.L., Rangel, C., Shlens, J., Sher, A., Marshak, D.W., Litke, A.M. & Chichilnisky, E.J. (2009). High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina. Nature Neuroscience 12, 11591164.
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773785.
Field, G.D., Sampath, A.P. & Rieke, F. (2005). Retinal processing near absolute threshold: From behavior to mechanism. Annual Review of Physiology 67, 491514.
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.
Gouras, P. & Link, K. (1966). Rod and cone interaction in dark-adapted monkey ganglion cells. The Journal of Physiology 184, 499510.
Hack, I., Peichl, L. & Brandstatter, J.H. (1999). An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proceedings of the National Academy of Sciences of the United States of America 96, 1413014135.
Hampson, E.C., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. The Journal of Neuroscience 12, 49114922.
Han, Y. & Massey, S.C. (2005). Electrical synapses in retinal ON cone bipolar cells: Subtype-specific expression of connexins. Proceedings of the National Academy of Sciences of the United States of America 102, 1331313318.
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 29232936.
Hecht, S., Shlaer, S. & Pirenne, M.H. (1942). Energy, quanta, and vision. The Journal of General Physiology 25, 819840.
Hochstein, S. & Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. The Journal of Physiology 262, 265284.
Jacoby, R.A. & Marshak, D.W. (2000). Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina. The Journal of Comparative Neurology 416, 1929.
Jarsky, T., Tian, M. & Singer, J.H. (2010). Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. The Journal of Neuroscience 30, 1188511895.
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 & Tissue Research 339, 311320.
Kim, I.B., Park, M.R., Kang, T.H., Kim, H.J., Lee, E.J., Ahn, M.D. & Chun, M.H. (2005). Synaptic connections of cone bipolar cells that express the neurokinin 1 receptor in the rabbit retina. Cell & Tissue Research 321, 18.
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 258, 22.
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 4749.
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301312.
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.
Kothmann, W.W., Massey, S.C. & O’Brien, J. (2009). Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. The Journal of Neuroscience 29, 1490314911.
Lamb, T.D. (2009). Evolution of vertebrate retinal photoreception. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 23.
Lamb, T.D. & Simon, E.J. (1976). The relation between intercellular coupling and electrical noise in turtle photoreceptors. The Journal of Physiology 263, 257286.
Lee, B.B., Smith, V.C., Pokorny, J. & Kremers, J. (1997). Rod inputs to macaque ganglion cells. Vision Research 37, 28132828.
Li, W., Keung, J.W. & Massey, S.C. (2004). Direct synaptic connections between rods and OFF cone bipolar cells in the rabbit retina. The Journal of Comparative Neurology 474, 112.
Liang, Z. & Freed, M.A. (2010). The ON pathway rectifies the OFF pathway of the mammalian retina. The Journal of Neuroscience 30, 55335543.
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.
Manookin, M.B. & Demb, J.B. (2006). Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50, 453464.
Margolis, D.J. & Detwiler, P.B. (2007). Different mechanisms generate maintained activity in ON and OFF retinal ganglion cells. The Journal of Neuroscience 27, 59946005.
Massey, S.C. & Mills, S.L. (1996). A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. The Journal of Comparative Neurology 366, 1533.
Massey, S.C. & Mills, S.L. (1999). Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina. Visual Neuroscience 16, 11811189.
Mastronarde, D.N. (1983). Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. Journal of Neurophysiology 49, 325349.
Maxeiner, S., Dedek, K., Janssen-Bienhold, U., AmmerMüller, J., Brune, H., Kirsch, T., Pieper, M., Degen, J., Kruger, O., Willecke, K. & Weiler, R. (2005). Deletion of connexin45 in mouse retinal neurons disrupts the rod/cone signaling pathway between AII amacrine and ON cone bipolar cells and leads to impaired visual transmission. The Journal of Neuroscience 25, 566576.
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. The Journal of Neuroscience 4, 29202938.
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.
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734737.
Mills, S.L., O’Brien, J.J., Li, W., O’Brien, J. & Massey, S.C. (2001). Rod pathways in the mammalian retina use connexin 36. The Journal of Comparative Neurology 436, 336350.
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 37, 569590.
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 16571672.
Münch, 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.
Murphy, G.J. & Rieke, F. (2006). Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52, 511524.
Murphy, G.J. & Rieke, F. (2008). Signals and noise in an inhibitory interneuron diverge to control activity in nearby retinal ganglion cells. Nature Neuroscience 11, 318326.
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. The Journal of Comparative Neurology 172, 109135.
Nelson, R. (1982). AII amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928947.
Neve, K.A., Seamans, J.K. & Trantham-Davidson, H. (2004). Dopamine receptor signaling. Journal of Receptor and Signal Transduction Research 24, 165205.
Nguyen-Legros, J., Simon, A., Caille, I. & Bloch, B. (1997). Immunocytochemical localization of dopamine D1 receptors in the retina of mammals. Visual Neuroscience 14, 545551.
Owczarzak, M.T. & Pourcho, R.G. (1999). Transmitter-specific input to OFF-alpha ganglion cells in the cat retina. The Anatomical Record 255, 363373.
Pang, J.J., Abd-El-Barr, M.M., Gao, F., Bramblett, D.E., Paul, D.L. & Wu, S.M. (2007). Relative contributions of rod and cone bipolar cell inputs to AII amacrine cell light response in the mouse retina. The Journal of Physiology 580, 397410.
Pang, J.J., Gao, F. & Wu, S.M. (2004). Light-evoked current responses in rod bipolar cells, cone depolarizing bipolar cells and AII amacrine cells in dark-adapted mouse retina. The Journal of Physiology 558, 897912.
Partida, G.J., Lee, S.C., Haft-Candell, L., Nichols, G.S. & Ishida, A.T. (2004). DARPP-32-like immunoreactivity in AII amacrine cells of rat retina. The Journal of Comparative Neurology 480, 251263.
Petrides, A. & Trexler, E.B. (2008). Differential output of the high-sensitivity rod photoreceptor: AII amacrine pathway. The Journal of Comparative Neurology 507, 16531662.
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.
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.
Purpura, K., Kaplan, E. & Shapley, R.M. (1988). Background light and the contrast gain of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the United States of America 85, 45344537.
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.
Raviola, E. & Gilula, N.B. (1973). Gap junctions between photoreceptor cells in the vertebrate retina. Proceedings of the National Academy of Sciences of the United States of America 70, 16771681.
Rosenberg, A., Husson, T.R. & Issa, N.P. (2010). Subcortical representation of non-Fourier image features. The Journal of Neuroscience 30, 19851993.
Sakitt, B. (1972). Counting every quantum. The Journal of Physiology 223, 131150.
Sampath, A.P. & Rieke, F. (2004). Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41, 431443.
Schorderet, M. & Nowak, J.Z. (1990). Retinal dopamine D1 and D2 receptors: Characterization by binding or pharmacological studies and physiological functions. Cellular and Molecular Neurobiology 10, 303325.
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 10531056.
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.
Singer, J.H., Lassova, L., Vardi, N. & Diamond, J.S. (2004). Coordinated multivesicular release at a mammalian ribbon synapse. Nature Neuroscience 7, 826833.
Smith, R.G., Freed, M.A. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod-cone network. The Journal of Neuroscience 6, 35053517.
Smith, R.G. & Vardi, N. (1995). Simulation of the AII amacrine cell of mammalian retina: Functional consequences of electrical coupling and regenerative membrane properties. Visual Neuroscience 12, 851860.
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.
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.
Stiles, W.S. (1959). Color vision: The approach through increment-threshold sensitivity. Proceedings of the National Academy of Sciences of the United States of America 45, 14.
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.
Strettoi, E. & Masland, R.H. (1996). The number of unidentified amacrine cells in the mammalian retina. Proceedings of the National Academy of Sciences of the United States of America 93, 1490614911.
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.
Svenningsson, P., Nishi, A., Fisone, G., Girault, J.A., Nairn, A.C. & Greengard, P. (2004). DARPP-32: An integrator of neurotransmission. Annual Review of Pharmacology and Toxicology 44, 269296.
Tessier-Lavigne, M. & Attwell, D. (1988). The effect of photoreceptor coupling and synapse nonlinearity on signal:noise ratio in early visual processing. Proceedings of the Royal Society of London. Series B, Biological Sciences 234, 171197.
Tian, M., Jarsky, T., Murphy, G.J., Rieke, F. & Singer, J.H. (2010). Voltage-gated Na channels in AII amacrine cells accelerate scotopic light responses mediated by the rod bipolar cell pathway. The Journal of Neuroscience 30, 46504659.
Trexler, E.B., Li, W. & Massey, S.C. (2005). Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. Journal of Neurophysiology 93, 14761485.
Tsukamoto, Y., Morigiwa, K., Ishii, M., Takao, M., Iwatsuki, K., Nakanishi, S. & Fukuda, Y. (2007). A novel connection between rods and ON cone bipolar cells revealed by ectopic metabotropic glutamate receptor 7 (mGluR7) in mGluR6-deficient mouse retinas. The Journal of Neuroscience 27, 62616267.
Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. (2001). Microcircuits for night vision in mouse retina. The Journal of Neuroscience 21, 86168623.
Urschel, S., Hoher, T., Schubert, T., Alev, C., Sohl, G., Worsdorfer, P., Asahara, T., Dermietzel, R., Weiler, R. & Willecke, K. (2006). Protein kinase A-mediated phosphorylation of connexin36 in mouse retina results in decreased gap junctional communication between AII amacrine cells. The Journal of Biological Chemistry 281, 3316333171.
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187190.
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991). Rod-signal interneurons in the rabbit retina: 2. AII amacrine cells. The Journal of Comparative Neurology 310, 154169.
Vaney, D.I., Nelson, J.C. & Pow, D.V. (1998). Neurotransmitter coupling through gap junctions in the retina. The Journal of Neuroscience 18, 1059410602.
Vardi, N. & Smith, R.G. (1996). The AII amacrine network: Coupling can increase correlated activity. Vision Research 36, 37433757.
van Rossum, M.C. & Smith, R.G. (1998). Noise removal at the rod synapse of mammalian retina. Visual Neuroscience 15, 809821.
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.
Veruki, M.L. & Hartveit, E. (2002 a). AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33, 935946.
Veruki, M.L. & Hartveit, E. (2002 b). Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. The Journal of Neuroscience 22, 1055810566.
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. The Journal of Physiology 549, 759774.
Veruki, M.L., Oltedal, L. & Hartveit, E. (2008). Electrical synapses between AII amacrine cells: Dynamic range and functional consequences of variation in junctional conductance. Journal of Neurophysiology 100, 33053322.
Veruki, M.L. & Wässle, H. (1996). Immunohistochemical localization of dopamine D1 receptors in rat retina. The European Journal of Neuroscience 8, 22862297.
Völgyi, B., Deans, M.R., Paul, D.L. & Bloomfield, S.A. (2004). Convergence and segregation of the multiple rod pathways in mammalian retina. The Journal of Neuroscience 24, 1118211192.
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. The Journal of Comparative Neurology 361, 537551.
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.
Werblin, F.S. (2010). Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission. Visual Neuroscience 27, 18.
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 1740.
Witkovsky, P., Svenningsson, P., Yan, L., Bateup, H. & Silver, R. (2007). Cellular localization and function of DARPP-32 in the rodent retina. The European Journal of Neuroscience 25, 32333242.
Xia, X.B. & Mills, S.L. (2004). Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina. Visual Neuroscience 21, 791805.
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.
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. The Journal of Comparative Neurology 310, 139153.
Zaghloul, K.A., Boahen, K. & Demb, J.B. (2003). Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. The Journal of Neuroscience 23, 26452654.
Zhang, J., Li, W., Hoshi, H., Mills, S.L. & Massey, S.C. (2005). Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina. Visual Neuroscience 22, 535549.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed