Symmetric interactions within a homogeneous starburst cell network can lead to robust asymmetries in dendrites of starburst amacrine cells.

Starburst amacrine cells in the mammalian retina respond asymmetrically to movement along their dendrites; centrifugal movement elicits stronger responses in each dendrite than centripetal movement. It has been suggested that the asymmetrical response can be attributed to intrinsic properties of the processes themselves. But starburst cells are known to release and have receptors for both GABA and acetylcholine. We tested whether interactions within the starburst cell network can contribute to their directional response properties. In a computational model of interacting starburst amacrine cells, we simulated the response of individual dendrites to moving light stimuli. By setting the model parameters for "synaptic connection strength" (cs) to positive or negative values, overlapping starburst dendrites could either excite or inhibit each other. For some values of cs, we observed a very robust inward/outward asymmetry of the starburst dendrites consistent with the reported physiological findings. This is the case, for example, if a starburst cell receives inhibition from other starburst cells located in its surround. For other values of cs, individual dendrites can respond best either to inward movement or respond symmetrically. A properly wired network of starburst cells can therefore account for the experimentally observed asymmetry of their response to movement, independent of any internal biophysical or biochemical properties of starburst cell dendrites.

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

[2]  E. V. Famiglietti,et al.  On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells , 1983, Vision Research.

[3]  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.

[4]  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.

[5]  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.

[6]  D. O'Malley,et al.  Co-release of acetylcholine and GABA by the starburst amacrine cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  GABA inhibits ACh release from the rabbit retina: a direct effect or feedback to bipolar cells? , 1992, Visual neuroscience.

[8]  N. Grzywacz,et al.  A model of the directional selectivity circuit in retina: transformations by neurons singly and in concert , 1992 .

[9]  Joel L. Davis,et al.  Single neuron computation , 1992 .

[10]  G. Fain,et al.  Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  M. Neal,et al.  Baclofen enhancement of acetylcholine release from amacrine cells in the rabbit retina by reduction of glycinergic inhibition. , 1995, The Journal of physiology.

[12]  H Barlow,et al.  Intraneuronal information processing, directional selectivity and memory for spatio-temporal sequences. , 1996, Network.

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

[14]  K. Johansson,et al.  Correlations between cholinergic neurons and muscarinic m2 receptors in the rat retina , 1998, Neuroreport.

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

[16]  Marla B Feller,et al.  The role of nAChR-mediated spontaneous retinal activity in visual system development. , 2002, Journal of neurobiology.

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

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

[19]  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.

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

[21]  Seunghoon Lee,et al.  A Developmental Switch in the Excitability and Function of the Starburst Network in the Mammalian Retina , 2004, Neuron.

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

[23]  Compartmental Localization Of GABAB Receptors On Starburst Amacrine Cell Dendrites In The Rabbit Retina , 2004 .

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

[25]  Directionally Asymmetric Synaptic Inputs to Starburst Amacrine Cell Dendrites During Light Stimulation , 2005 .