The role of starburst amacrine cells in visual signal processing

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.

[1]  J. Mills,et al.  Acetylcholine synthesis by displaced amacrine cells. , 1980, Science.

[2]  Christopher Brandon,et al.  Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity , 1987, Brain Research.

[3]  Robert G. Smith,et al.  Maximizing contrast resolution in the outer retina of mammals , 2010, Biological Cybernetics.

[4]  R. R. Poznanski.  Cellular inhibitory behavior underlying the formation of retinal direction selectivity in the starburst network. , 2010, Journal of integrative neuroscience.

[5]  F. Werblin,et al.  Symmetric interactions within a homogeneous starburst cell network can lead to robust asymmetries in dendrites of starburst amacrine cells. , 2006, Journal of neurophysiology.

[6]  V. Perry,et al.  Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  P. Detwiler,et al.  Directionally selective calcium signals in dendrites of starburst amacrine cells , 2002, Nature.

[8]  D. I. Vaney,et al.  Chapter 2 The mosaic of amacrine cells in the mammalian retina , 1990 .

[9]  Germán A. Enciso,et al.  A model of direction selectivity in the starburst amacrine cell network , 2010, Journal of Computational Neuroscience.

[10]  A. Borst,et al.  Fly motion vision. , 2010, Annual review of neuroscience.

[11]  F. Amthor,et al.  Effects of the destruction of starburst-cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity , 2002, Visual Neuroscience.

[12]  P. Sterling,et al.  Displaced GAD65 amacrine cells of the guinea pig retina are morphologically diverse , 2006, Visual Neuroscience.

[13]  E. V. Famiglietti,et al.  Immunocytochemical staining of cholinergic amacrine cells in rabbit retina , 1987, Brain Research.

[14]  W. Baldridge.  Optical Recordings of the Effects of Cholinergic Ligands on Neurons in the Ganglion Cell Layer of Mammalian Retina , 1996, The Journal of Neuroscience.

[15]  R. Masland,et al.  The shapes and numbers of amacrine cells: Matching of photofilled with Golgi‐stained cells in the rabbit retina and comparison with other mammalian species , 1999, The Journal of comparative neurology.

[16]  R. Masland,et al.  Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Nicholas J. Priebe,et al.  Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex , 2008, Neuron.

[18]  T. Velte,et al.  Spiking and nonspiking models of starburst amacrine cells in the rabbit retina , 1997, Visual Neuroscience.

[19]  F. Werblin,et al.  Directional Selectivity Is Formed at Multiple Levels by Laterally Offset Inhibition in the Rabbit Retina , 2005, Neuron.

[20]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[21]  S. Massey,et al.  Pharmacology of directionally selective ganglion cells in the rabbit retina. , 1997, Journal of neurophysiology.

[22]  Andrey V Dmitriev,et al.  Dendritic compartmentalization of chloride cotransporters underlies directional responses of starburst amacrine cells in retina , 2006, Proceedings of the National Academy of Sciences.

[23]  Seunghoon Lee,et al.  Synaptic physiology of direction selectivity in the retina , 2008, The Journal of physiology.

[24]  Richard H. Masland,et al.  Starburst Cells Nondirectionally Facilitate the Responses of Direction-Selective Retinal Ganglion Cells , 2002, The Journal of Neuroscience.

[25]  R. Masland,et al.  The Major Cell Populations of the Mouse Retina , 1998, The Journal of Neuroscience.

[26]  R H Masland,et al.  The shape and arrangement of the cholinergic neurons in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  S. Bloomfield,et al.  Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. , 1992, Journal of neurophysiology.

[28]  N. Daw,et al.  Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed. , 1975, Journal of neurophysiology.

[29]  M. Tachibana,et al.  A Key Role of Starburst Amacrine Cells in Originating Retinal Directional Selectivity and Optokinetic Eye Movement , 2001, Neuron.

[30]  George E. P. Box,et al.  The Royal Society of London , 2013 .

[31]  Z. J. Zhou,et al.  Direct Participation of Starburst Amacrine Cells in Spontaneous Rhythmic Activities in the Developing Mammalian Retina , 1998, The Journal of Neuroscience.

[32]  Frank S. Werblin,et al.  Mechanisms and circuitry underlying directional selectivity in the retina , 2002, Nature.

[33]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  H. Barlow,et al.  Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit , 1964, The Journal of physiology.

[35]  P. Detwiler,et al.  A Dendrite-Autonomous Mechanism for Direction Selectivity in Retinal Starburst Amacrine Cells , 2007, PLoS biology.

[36]  H. Young,et al.  GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina , 1988, Brain Research.

[37]  A. Hughes,et al.  Coronate cells: Displaced amacrines of the rabbit retina? , 1980, The Journal of comparative neurology.

[38]  S. Bloomfield,et al.  Electroanatomy of a unique amacrine cell in the rabbit retina. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Michael J. Schachter,et al.  Dendritic Spikes Amplify the Synaptic Signal to Enhance Detection of Motion in a Simulation of the Direction-Selective Ganglion Cell , 2010, PLoS Comput. Biol..

[40]  Nicholas W. Oesch,et al.  Tetrodotoxin-Resistant Sodium Channels Contribute to Directional Responses in Starburst Amacrine Cells , 2010, PloS one.

[41]  Zhou Zj,et al.  Direct Participation of Starburst Amacrine Cells in Spontaneous Rhythmic Activities in the Developing Mammalian Retina , 1998 .

[42]  J. Caldwell,et al.  Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. , 1978, The Journal of physiology.

[43]  D. I. Vaney,et al.  ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  Zhiyin Liang,et al.  The ON Pathway Rectifies the OFF Pathway of the Mammalian Retina , 2010, The Journal of Neuroscience.

[45]  Shaun P. Collin,et al.  Dendritic Relationships between Cholinergic Amacrine Cells and Direction-Selective Retinal Ganglion Cells , 1989 .

[46]  Martin Wilson,et al.  The spatial frequency sensitivity of bipolar cells , 2004, Biological Cybernetics.

[47]  Neville N. Osborne,et al.  Neurobiology of the Inner Retina , 1989, NATO ASI Series.

[48]  Kevin L. Briggman,et al.  Wiring specificity in the direction-selectivity circuit of the retina , 2011, Nature.

[49]  D. Pow,et al.  The dendritic architecture of the cholinergic plexus in the rabbit retina: Selective labeling by glycine accumulation in the presence of sarcosine , 2000, The Journal of comparative neurology.

[50]  Botond Roska,et al.  Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit , 2011, Nature.

[51]  K. Keyser,et al.  Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas , 2003, The Journal of comparative neurology.

[52]  E. V. Famiglietti,et al.  Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction , 1991, The Journal of comparative neurology.

[53]  E. V. Famiglietti,et al.  ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina , 1983, Brain Research.

[54]  N M Grzywacz,et al.  Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit , 1998, The Journal of physiology.

[55]  F. Amthor,et al.  Robust directional computation in on-off directionally selective ganglion cells of rabbit retina , 2007, Visual Neuroscience.

[56]  F. Werblin,et al.  Requirement for Cholinergic Synaptic Transmission in the Propagation of Spontaneous Retinal Waves , 1996, Science.

[57]  W. R. Taylor,et al.  Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina , 2002, The Journal of Neuroscience.

[58]  F. Amthor,et al.  Synaptic input to the on–off directionally selective ganglion cell in the rabbit retina , 2003, The Journal of comparative neurology.

[59]  J. J. Tukker,et al.  Direction selectivity in a model of the starburst amacrine cell , 2004, Visual Neuroscience.

[60]  M. Ariel,et al.  Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells , 1982, The Journal of physiology.

[61]  Seunghoon Lee,et al.  The Synaptic Mechanism of Direction Selectivity in Distal Processes of Starburst Amacrine Cells , 2006, Neuron.

[62]  R. Masland,et al.  Responses to light of starburst amacrine cells. , 1996, Journal of neurophysiology.

[63]  T. Poggio,et al.  A synaptic mechanism possibly underlying directional selectivity to motion , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[64]  H. Wässle,et al.  Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[65]  J. B. Demb,et al.  Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities , 2003, The Journal of Neuroscience.

[66]  E. Famiglietti.  Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells , 1987, Brain Research.

[67]  Seunghoon Lee,et al.  Role of ACh-GABA Cotransmission in Detecting Image Motion and Motion Direction , 2010, Neuron.

[68]  R H Masland,et al.  Responses to acetylcholine of ganglion cells in an isolated mammalian retina. , 1976, Journal of neurophysiology.

[69]  Marla B. Feller,et al.  Development of asymmetric inhibition underlying direction selectivity in the retina , 2011, Nature.

[70]  H. Wässle,et al.  Receptive Field Properties of Starburst Cholinergic Amacrine Cells in the Rabbit Retina , 1995, The European journal of neuroscience.

[71]  B. Boycott,et al.  Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina , 1981, The Journal of comparative neurology.

[72]  C. Brandon.  Cholinergic neurons in the rabbit retina: immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons , 1987, Brain Research.

[73]  S. Mangel,et al.  Cation–chloride cotransporters mediate neural computation in the retina , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[74]  Enrica Strettoi,et al.  Pattern of synaptic excitation and inhibition upon direction‐selective retinal ganglion cells , 2002, The Journal of comparative neurology.

[75]  Nicholas Oesch,et al.  Direction-Selective Dendritic Action Potentials in Rabbit Retina , 2005, Neuron.

[76]  S. Massey,et al.  A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  T. Millar,et al.  Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells , 1987, Neuroscience Letters.