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The role of starburst amacrine cells in visual signal processing

Published online by Cambridge University Press:  06 February 2012

W.R. TAYLOR  and
R.G. SMITH
W.R. TAYLOR*
Affiliation:
Department of Ophthalmology, Casey Eye Institute, Oregon Health & Science University, Portland, Oregon
R.G. SMITH
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania
*
*Address correspondence and reprint requests to: W.R. Taylor, Department of Ophthalmology, Casey Eye Institute, Oregon Health & Science University, 3375 SW Terwillger Blvd, Portland, OR 97239. E-mail: taylorw@ohsu.edu
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Abstract

Starburst amacrine cells (SBACs) within the adult mammalian retina provide the critical inhibition that underlies the receptive field properties of direction-selective ganglion cells (DSGCs). The SBACs generate direction-selective output of GABA that differentially inhibits the DSGCs. We review the biophysical mechanisms that produce directional GABA release from SBACs and test a network model that predicts the effects of reciprocal inhibition between adjacent SBACs. The results of the model simulations suggest that reciprocal inhibitory connections between closely spaced SBACs should be spatially selective, while connections between more widely spaced cells could be indiscriminate. SBACs were initially identified as cholinergic neurons and were subsequently shown to contain release both acetylcholine and GABA. While the role of the GABAergic transmission is well established, the role of the cholinergic transmission remains unclear.

Keywords

RetinaVisual systemDirection selectivityComputational modelGabaergic inhibition
Type
Review Article
Information
Visual Neuroscience , Volume 29 , Issue 1 , January 2012 , pp. 73 - 81
Copyright
Copyright © Cambridge University Press 2012

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References

Amthor, F.R., Keyser, K.T. & Dmitrieva, N.A. (2002). Effects of the destruction of starburst-cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity. Visual Neuroscience 19, 495–509.Google Scholar
Ariel, M. & Daw, N.W. (1982). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. The Journal of Physiology 324, 135–160.CrossRefGoogle ScholarPubMed
Attwell, D. & Wilson, M. (1983). The spatial frequency sensitivity of bipolar cells. Biological Cybernetics 47, 131–140.CrossRefGoogle ScholarPubMed
Auferkorte, O.N., Kaushalya, S.K., Reddy, S., Euler, T. & Haverkamp, S. (2011). Inhibitory neurotransmitter receptors in the retinal circuitry which detects direction of motion. Invest. Ophthalmol. Vis. Sci., ARVO E-Abstract 3033.Google Scholar
Baldridge, W.H. (1996). Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina. The Journal of Neuroscience 16, 5060–5072.CrossRefGoogle ScholarPubMed
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Rabbit retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. The Journal of Physiology 173, 377–407.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit’s retina. The Journal of Physiology 178, 477–504.Google Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.CrossRefGoogle ScholarPubMed
Borst, A., Haag, J. & Reiff, D.F. (2010). Fly motion vision. Annual Review of Neuroscience 33, 49–70.CrossRefGoogle ScholarPubMed
Brandon, C. (1987 a). Cholinergic neurons in the rabbit retina: Immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Research 401, 385–391.CrossRefGoogle ScholarPubMed
Brandon, C. (1987 b). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.CrossRefGoogle ScholarPubMed
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, 6187–6191.Google Scholar
Briggman, K.L., Helmstaedter, M. & Denk, W. (2011). Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188.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, 277–298.CrossRefGoogle ScholarPubMed
Chiao, C.C. & Masland, R.H. (2002). Starburst cells nondirectionally facilitate the responses of direction-selective retinal ganglion cells. The Journal of Neuroscience 22, 10509–10513.CrossRefGoogle ScholarPubMed
Dacheux, R.F., Chimento, M.F. & Amthor, F.R. (2003). Synaptic input to the on-off directionally selective ganglion cell in the rabbit retina. The Journal of Comparative Neurology 456, 267–278.CrossRefGoogle Scholar
Enciso, G.A., Rempe, M., Dmitriev, A.V., Gavrikov, K.E., Terman, D. & Mangel, S.C. (2010). A model of direction selectivity in the starburst amacrine cell network. Journal of Computational Neuroscience 28, 567–578.Google Scholar
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.CrossRefGoogle ScholarPubMed
Famiglietti, E.V.J. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138–144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404–408.Google 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. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.CrossRefGoogle ScholarPubMed
Feller, M.B., Wellis, D.P., Stellwagen, D., Werblin, F.S. & Shatz, C.J. (1996). Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272, 1182–1187.Google Scholar
Fried, S.I., Münch, T.A. & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle ScholarPubMed
Fried, S.I., Münch, T.A. & Werblin, F.S. (2005). Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46, 117–127.CrossRefGoogle ScholarPubMed
Gavrikov, K.E., Dmitriev, A.V., Keyser, K.T. & Mangel, S.C. (2003). Cation–chloride cotransporters mediate neural computation in the retina. Proceedings of the National Academy of Sciences of the United States of America 100, 16047–16052.Google Scholar
Gavrikov, K.E., Nilson, J.E., Dmitriev, A.V., Zucker, C.L. & Mangel, S.C. (2006). Dendritic compartmentalization of chloride cotransporters underlies directional responses of starburst amacrine cells in retina. Proceedings of the National Academy of Sciences of the United States of America 103, 18793–18798.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (2007). Robust directional computation in on-off directionally selective ganglion cells of rabbit retina. Visual Neuroscience 24, 647–661.CrossRefGoogle ScholarPubMed
Grzywacz, N.M., Amthor, F.R. & Merwine, D.K. (1998). Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit. The Journal of Physiology 512, 575–581.Google Scholar
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
Hayden, S.A., Mills, J.W. & Masland, R.M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science 210, 435–437.CrossRefGoogle ScholarPubMed
Hughes, A. & Vaney, D.I. (1980). Coronate cells: Displaced amacrines of the rabbit retina? The Journal of Comparative Neurology 189, 169–189.CrossRefGoogle ScholarPubMed
Jeon, C.J., Kong, J.H., Strettoi, E., Rockhill, R., Stasheff, S.F. & Masland, R.H. (2002). Pattern of synaptic excitation and inhibition upon direction-selective retinal ganglion cells. Journal of Comparative Neurology 449, 195–205.CrossRefGoogle ScholarPubMed
Jeon, C.J., Strettoi, E. & Masland, R.H. (1998). The major cell populations of the mouse retina. The Journal of Neuroscience 18, 8936–8946.CrossRefGoogle ScholarPubMed
Kao, Y.H. & Sterling, P. (2006). Displaced GAD65 amacrine cells of the guinea pig retina are morphologically diverse. Vis Neurosci 23, 931–939.Google Scholar
Kittila, C.A. & Massey, S.C. (1997). Pharmacology of directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 77, 675–689.Google Scholar
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
Lee, S. & Zhou, Z.J. (2006). The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787–799.Google Scholar
Liang, Z. & Freed, M.A. (2010). The ON pathway rectifies the OFF pathway of the mammalian retina. The Journal of Neuroscience 30, 5533–5543.CrossRefGoogle ScholarPubMed
Lipin, M.Y., Smith, R.G. & Taylor, W.R. (2010). Maximizing contrast resolution in the outer retina of mammals. Biological Cybernetics 103, 57–77.Google Scholar
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
Masland, R.H. & Ames, A. III (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
Massey, S.C. & Redburn, D.A. (1982). A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. The Journal of Neuroscience 2, 1633–1643.Google Scholar
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.CrossRefGoogle ScholarPubMed
Miller, R.F. & Bloomfield, S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Sciences of the United States of America 80, 3069–3073.CrossRefGoogle ScholarPubMed
Münch, T.A. & Werblin, F.S. (2006). Symmetric interactions within a homogeneous starburst cell network can lead to robust asymmetries in dendrites of starburst amacrine cells. Journal of Neurophysiology 96, 471–477.CrossRefGoogle ScholarPubMed
Oesch, N., Euler, T. & Taylor, W.R. (2005). Direction-selective dendritic action potentials in rabbit retina. Neuron 47, 739–750.Google Scholar
Oesch, N.W. & Taylor, W.R. (2010). Tetrodotoxin-resistant sodium channels contribute to directional responses in starburst amacrine cells. PLoS One 5, e12447.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, 3414–3418.Google Scholar
Perry, V.H. & Walker, M. (1980). Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat. Proc R Soc Lond B Biol Sci 208, 415–431.Google ScholarPubMed
Peters, B.N. & Masland, R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469–480.Google Scholar
Poznanski, R.R. (2010). Cellular inhibitory behavior underlying the formation of retinal direction selectivity in the starburst network. Journal of Integrative Neuroscience 9, 299–335.CrossRefGoogle ScholarPubMed
Priebe, N.J. & Ferster, D. (2008). Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57, 482–497.CrossRefGoogle ScholarPubMed
Schachter, M.J., Oesch, N., Smith, R.G. & Taylor, W.R. (2010). Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell. PLoS Computational Biology 6, e1000899.Google Scholar
Srinivasan, M.V., Laughlin, S.B. & Dubs, A. (1982). Predictive coding: A fresh view of inhibition in the retina. Proceedings of the Royal Society of London. Series B, Biological Sciences 216, 427–459.Google ScholarPubMed
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, 101–119.Google Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. The Journal of Neuroscience 22, 7712–7720.Google Scholar
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. The European Journal of Neuroscience 7, 2308–2321.Google Scholar
Torre, V. & Poggio, T. (1978). A synaptic mechanism possibly underlying directional selectivity to motion. Proceedings of the Royal Society of London. Series B: Biological Sciences 202, 409–416.Google Scholar
Tukker, J.J., Taylor, W.R. & Smith, R.G. (2004). Direction selectivity in a model of the starburst amacrine cell. Visual Neuroscience 21, 611–625.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society of London. Series B, Biological Sciences 220, 501–508.Google ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 49–100. Oxford: Pergamon Press.Google Scholar
Vaney, D.I., Collin, S.P. & Young, H.M. (1989). Dendritic relationships between cholinergic amacrine cells and direction-selective ganglion cells. In Neurobiology of the inner retina, ed. Weiler, R. & Osborne, N.N., pp. 157–168. Berlin, Germany: Springer.Google Scholar
Vaney, D.I., Peichi, L. & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. The Journal of Comparative Neurology 199, 373–391.Google Scholar
Vaney, D.I. & Pow, D.V. (2000). The dendritic architecture of the cholinergic plexus in the rabbit retina: Selective labeling by glycine accumulation in the presence of sarcosine. The Journal of Comparative Neurology 421, 1–13.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.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.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, 402–406.Google Scholar
Wyatt, H.J. & Daw, N.W. (1975). Directionally sensitive ganglion cells in the rabbit retina: Specificity for stimulus direction, size, and speed. Journal of Neurophysiology 38, 613–626.Google Scholar
Yamada, E.S., Dmitrieva, N., Keyser, K.T., Lindstrom, J.M., Hersh, L.B. & Marshak, D.W. (2003). Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. The Journal of Comparative Neurology 461, 76–90.Google Scholar
Yonehara, K., Balint, K., Noda, M., Nagel, G., Bamberg, E. & Roska, B. (2011). Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469, 407–410.CrossRefGoogle ScholarPubMed
Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I. & Nakanishi, S. (2001). A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780.Google Scholar
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, 2645–2654.CrossRefGoogle ScholarPubMed
Zhou, Z.J. (1998). Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. The Journal of Neuroscience 18, 4155–4165.Google Scholar
Zhou, Z.J. & Lee, S. (2008). Synaptic physiology of direction selectivity in the retina. The Journal of Physiology 586, 4371–4376.Google Scholar