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Amacrine cell-mediated input to bipolar cells: Variations on a common mechanistic theme

Published online by Cambridge University Press:  06 February 2012

WILLIAM N. GRIMES
WILLIAM N. GRIMES*
Affiliation:
Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, Washington
*
†Address correspondence and reprint requests to: William N. Grimes, Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195. E-mail: [email protected]
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Abstract

Feedback is a ubiquitous feature of neural circuits in the mammalian central nervous system (CNS). Analogous to pure electronic circuits, neuronal feedback provides either a positive or negative influence on the output of upstream components/neurons. Although the particulars (i.e., connectivity, physiological encoding/processing/signaling) of circuits in higher areas of the brain are often unclear, the inner retina proves an excellent model for studying both the anatomy and physiology of feedback circuits within the functional context of visual processing. Inner retinal feedback to bipolar cells is almost entirely mediated by a single class of interneurons, the amacrine cells. Although this might sound like a simple circuit arrangement with an equally simple function, anatomical, molecular, and functional evidence suggest that amacrine cells represent an extremely diverse class of CNS interneurons that contribute to a variety of retinal processes. In this review, I classify the amacrine cells according to their anatomical output synapses and target cell(s) (i.e., bipolar cells, ganglion cells, and/or amacrine cells) and discuss specifically our current understandings of amacrine cell-mediated feedback and output to bipolar cells on the synaptic, cellular, and circuit levels, while drawing connections to visual processing.

Keywords

RetinaSynapseInterneuronInhibitionFeedbackDendritic integrationGap junctions
Type
Review Article
Information
Visual Neuroscience , Volume 29 , Issue 1 , January 2012 , pp. 41 - 49
Copyright
Copyright © Cambridge University Press 2012

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References

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, 355–379.Google ScholarPubMed
Baccus, S.A. (2007). Timing and computation in inner retinal circuitry. Annual Review of Physiology 69, 271–290.CrossRefGoogle ScholarPubMed
Baccus, S.A., Olveczky, B.P., Manu, M. & Meister, M. (2008). A retinal circuit that computes object motion. The Journal of Neuroscience 28, 6807–6817.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Volgyi, B. (2007). Response properties of a unique subtype of wide-field amacrine cell in the rabbit retina. Visual Neuroscience 24, 459–469.CrossRefGoogle ScholarPubMed
Briggman, K.L., Helmstaedter, M. & Denk, W. (2011). Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188.CrossRefGoogle ScholarPubMed
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, 277–298.CrossRefGoogle 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, 7919–7928.CrossRefGoogle ScholarPubMed
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, 2330–2339.CrossRefGoogle ScholarPubMed
Chavez, A.E., Singer, J.H. & Diamond, J.S. (2006). Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443, 705–708.CrossRefGoogle ScholarPubMed
Cohen, E.D. (2001). Voltage-gated calcium and sodium currents of starburst amacrine cells in the rabbit retina. Visual Neuroscience 18, 799–809.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. The Journal of Comparative Neurology 315, 287–302.CrossRefGoogle ScholarPubMed
Cuenca, N., De Juan, J. & Kolb, H. (1995). Substance P-immunoreactive neurons in the human retina. The Journal of Comparative Neurology 356, 491–504.CrossRefGoogle ScholarPubMed
Cuenca, N. & Kolb, H. (1998). Circuitry and role of substance P-immunoreactive neurons in the primate retina. The Journal of Comparative Neurology 393, 439–456.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Glutamate, GABA, and glycine in the human retina: An immunocytochemical investigation. The Journal of Comparative Neurology 311, 483–494.CrossRefGoogle ScholarPubMed
Deans, M.R., Volgyi, 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, 703–712.CrossRefGoogle ScholarPubMed
Denk, W. & Horstmann, H. (2004). Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biology 2, e329.CrossRefGoogle ScholarPubMed
DeVries, S.H. (1999). Correlated firing in rabbit retinal ganglion cells. Journal of Neurophysiology 81, 908–920.CrossRefGoogle ScholarPubMed
Dick, E. & Lowry, O.H. (1984). Distribution of glycine, gamma-aminobutyric acid, glutamate decarboxylase, and gamma-aminobutyric acid transaminase in rabbit and mudpuppy retinas. Journal of Neurochemistry 42, 1274–1280.CrossRefGoogle ScholarPubMed
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, 2159–2166.CrossRefGoogle ScholarPubMed
Eggers, E.D. & Lukasiewicz, P.D. (2006). GABA(A), GABA(C) and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. The Journal of Physiology 572, 215–225.CrossRefGoogle Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2010). Interneuron circuits tune inhibition in retinal bipolar cells. Journal of Neurophysiology 103, 25–37.CrossRefGoogle ScholarPubMed
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.CrossRefGoogle ScholarPubMed
Euler, T. & Wassle, 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, 1384–1395.CrossRefGoogle Scholar
Famiglietti, E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. The Journal of Comparative Neurology 309, 40–70.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2005). Synaptic organization of complex ganglion cells in rabbit retina: Type and arrangement of inputs to directionally selective and local-edge-detector cells. The Journal of Comparative Neurology 484, 357–391.CrossRefGoogle ScholarPubMed
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, 89–101.CrossRefGoogle ScholarPubMed
Fried, S.I., Munch, T.A. & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle ScholarPubMed
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, 585–592.CrossRefGoogle ScholarPubMed
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, 873–885.CrossRefGoogle ScholarPubMed
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 2923–2936.CrossRefGoogle ScholarPubMed
Hausselt, S.E., Euler, T., Detwiler, P.B. & Denk, W. (2007). A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biology 5, e185.CrossRefGoogle ScholarPubMed
Helmstaedter, M., Briggman, K.L. & Denk, W. (2008). 3D structural imaging of the brain with photons and electrons. Current Opinion in Neurobiology 18, 633–641.CrossRefGoogle ScholarPubMed
Hsueh, H.A., Molnar, A. & Werblin, F.S. (2008). Amacrine-to-amacrine cell inhibition in the rabbit retina. Journal of Neurophysiology 100, 2077–2088.CrossRefGoogle ScholarPubMed
Ivanova, E., Muller, U. & Wassle, H. (2006). Characterization of the glycinergic input to bipolar cells of the mouse retina. The European journal of Neuroscience 23, 350–364.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
Lee, S., Kim, K. & Zhou, Z.J. (2010). Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68, 1159–1172.CrossRefGoogle ScholarPubMed
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971–982.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, 305–326.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
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, 4136–4150.CrossRefGoogle ScholarPubMed
Masland, R.H. (1988). Amacrine cells. Trends in Neurosciences 11, 405–410.CrossRefGoogle ScholarPubMed
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, 569–590.CrossRefGoogle ScholarPubMed
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, 3813–3830.CrossRefGoogle ScholarPubMed
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, 1308–1316.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1984). Amacrine cells in scotopic vision. Ophthalmic Research 16, 21–26.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.CrossRefGoogle ScholarPubMed
Oesch, N. & Diamond, J. (2009). A night vision neuron gets a day job. Nature Neuroscience 12, 1209–1211.CrossRefGoogle ScholarPubMed
Oesch, N.W., Kothmann, W.W. & Diamond, J.S. (2011). Illuminating synapses and circuitry in the retina. Current Opinion in Neurobiology 21, 238–244.CrossRefGoogle ScholarPubMed
Oesch, N.W. & Taylor, W.R. (2010). Tetrodotoxin-resistant sodium channels contribute to directional responses in starburst amacrine cells. PLoS One 5, e12447.CrossRefGoogle ScholarPubMed
Oheim, M., Kirchhoff, F. & Stuhmer, W. (2006). Calcium microdomains in regulated exocytosis. Cell Calcium 40, 423–439.CrossRefGoogle ScholarPubMed
Parekh, A.B. (2008). Ca2+ microdomains near plasma membrane Ca2+ channels: Impact on cell function. The Journal of Physiology 586, 3043–3054.CrossRefGoogle ScholarPubMed
Pourcho, R.G. (1980). Uptake of [3H]glycine and [3H]GABA by amacrine cells in the cat retina. Brain Research 198, 33–46.CrossRefGoogle ScholarPubMed
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, 25–35.CrossRefGoogle ScholarPubMed
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, 473–480.CrossRefGoogle ScholarPubMed
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, 3451–3459.CrossRefGoogle ScholarPubMed
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.CrossRefGoogle ScholarPubMed
Shields, C.R. & Lukasiewicz, P.D. (2003). Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. Journal of Neurophysiology 89, 2449–2458.CrossRefGoogle ScholarPubMed
Sterling, P. & Lampson, L.A. (1986). Molecular specificity of defined types of amacrine synapse in cat retina. The Journal of Neuroscience 6, 1314–1324.CrossRefGoogle ScholarPubMed
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, 14906–14911.CrossRefGoogle ScholarPubMed
Suzuki, S., Tachibana, M. & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. The Journal of Physiology 421, 645–662.CrossRefGoogle ScholarPubMed
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, 4650–4659.CrossRefGoogle ScholarPubMed
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, 1476–1485.CrossRefGoogle ScholarPubMed
Trong, P.K. & Rieke, F. (2008). Origin of correlated activity between parasol retinal ganglion cells. Nature Neuroscience 11, 1343–1351.CrossRefGoogle ScholarPubMed
Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. (2001). Microcircuits for night vision in mouse retina. The Journal of Neuroscience 21, 8616–8623.CrossRefGoogle ScholarPubMed
Vardi, N. & Smith, R.G. (1996). The AII amacrine network: Coupling can increase correlated activity. Vision Research 36, 3743–3757.CrossRefGoogle ScholarPubMed
Velte, T.J. & Miller, R.F. (1997). Spiking and nonspiking models of starburst amacrine cells in the rabbit retina. Visual Neuroscience 14, 1073–1088.CrossRefGoogle ScholarPubMed
Venkataramani, S. & Taylor, W.R. (2010). Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition. The Journal of Neuroscience 30, 15664–15676.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Hartveit, E. (2002). Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. The Journal of Neuroscience 22, 10558–10566.CrossRefGoogle ScholarPubMed
Werblin, F.S. (2010). Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission. Visual Neuroscience 27, 1–8.CrossRefGoogle ScholarPubMed
Zaghloul, K.A., Manookin, M.B., Borghuis, B.G., Boahen, K. & Demb, J.B. (2007). Functional circuitry for peripheral suppression in Mammalian Y-type retinal ganglion cells. Journal of Neurophysiology 97, 4327–4340.CrossRefGoogle ScholarPubMed