Directionally selective calcium signals in dendrites of starburst amacrine cells

The detection of image motion is fundamental to vision. In many species, unique classes of retinal ganglion cells selectively respond to visual stimuli that move in specific directions. It is not known which retinal cell first performs the neural computations that give rise to directional selectivity in the ganglion cell. A prominent candidate has been an interneuron called the ‘starburst amacrine cell’. Using two-photon optical recordings of intracellular calcium concentration, here we find that individual dendritic branches of starburst cells act as independent computation modules. Dendritic calcium signals, but not somatic membrane voltage, are directionally selective for stimuli that move centrifugally from the cell soma. This demonstrates that direction selectivity is computed locally in dendritic branches at a stage before ganglion cells.

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

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

[3]  F. Dodge,et al.  Co‐operative action of calcium ions in transmitter release at the neuromuscular junction , 1967, The Journal of physiology.

[4]  H. J. Wyatt,et al.  Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. , 1976, Science.

[5]  R H Masland,et al.  Autoradiographic identification of acetylcholine in the rabbit retina , 1979, The Journal of cell biology.

[6]  M. Ariel,et al.  Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells , 1982, The Journal of physiology.

[7]  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.

[8]  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.

[9]  R H Masland,et al.  Acetylcholine-synthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  R. Masland,et al.  The functions of acetylcholine in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[11]  E. A. Schwartz,et al.  Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. , 1987, Science.

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

[13]  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.

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

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

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

[17]  A. Borst,et al.  Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[18]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

[19]  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.

[20]  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.

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

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

[23]  R R Poznanski,et al.  Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology , 1992, Bulletin of mathematical biology.

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

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

[26]  In vivo staining of oligodendroglia in the rabbit retina , 1994, Glia.

[27]  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.

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

[29]  S A Lipton,et al.  Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[31]  N M Grzywacz,et al.  Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit's retinal directional selectivity? , 1997, Visual Neuroscience.

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

[33]  Richard H. Masland,et al.  Retinal direction selectivity after targeted laser ablation of starburst amacrine cells , 1997, Nature.

[34]  S. Massey,et al.  Contributions of GABAA receptors and GABAC receptors to acetylcholine release and directional selectivity in the rabbit retina , 1997, Visual Neuroscience.

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

[36]  H. Wässle,et al.  Glycine and GABA receptors in the mammalian retina , 1998, Vision Research.

[37]  Idan Segev,et al.  Dendritic processing , 1998 .

[38]  Complementary roles of two excitatory pathways in retinal directional selectivity. , 1998, Visual neuroscience.

[39]  P. Detwiler,et al.  Optical recording of light-evoked calcium signals in the functionally intact retina. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Dendritic computation of direction selectivity by retinal ganglion cells. , 2000, Science.

[41]  R. Masland,et al.  Amacrine, ganglion, and displaced amacrine cells in the rabbit retina express nicotinic acetylcholine receptors , 2000, Visual Neuroscience.

[42]  N. Staff,et al.  Structure and functional connections of presynaptic terminals in the vertebrate retina revealed by activity‐dependent dyes and confocal microscopy , 2001, The Journal of comparative neurology.

[43]  Thomas Euler,et al.  Dendritic processing , 2001, Current Opinion in Neurobiology.

[44]  Lyle J. Borg-Graham,et al.  The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell , 2001, Nature Neuroscience.

[45]  J. Zanker,et al.  Motion vision : computational, neural, and ecological constraints , 2001 .

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