Spikes and ribbon synapses in early vision

Image processing begins in the retina, where neurons respond with graded voltage changes that must be converted into spikes. This conversion from 'analog' to 'digital' coding is a fundamental transformation carried out by the visual system, but the mechanisms are still not well understood. Recent work demonstrates that, in vertebrates, graded-to-spiking conversion of the visual signal begins in the axonal system of bipolar cells (BCs), which transmit visual information through ribbon-type synapses specialized for responding to graded voltage signals. Here, we explore the evidence for and against the idea that ribbon synapses also transmit digital information. We then discuss the potential costs and benefits of digitization at different stages of visual pathways in vertebrates and invertebrates.

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

[2]  L. Lagnado,et al.  Two Actions of Calcium Regulate the Supply of Releasable Vesicles at the Ribbon Synapse of Retinal Bipolar Cells , 1999, The Journal of Neuroscience.

[3]  Richard H Masland,et al.  Processing and encoding of visual information in the retina , 1996, Current Opinion in Neurobiology.

[4]  Zhuo-Hua Pan,et al.  Two types of cone bipolar cells express voltage-gated Na+ channels in the rat retina , 2008, Visual Neuroscience.

[5]  R. Heidelberger,et al.  Mechanisms contributing to tonic release at the cone photoreceptor ribbon synapse. , 2008, Journal of neurophysiology.

[6]  W. Almers,et al.  Imaging Calcium Entry Sites and Ribbon Structures in Two Presynaptic Cells , 2003, The Journal of Neuroscience.

[7]  E J Chichilnisky,et al.  Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type , 2007, The Journal of Neuroscience.

[8]  Thomas Euler,et al.  OFF bipolar cells express distinct types of dendritic glutamate receptors in the mouse retina , 2013, Neuroscience.

[9]  I. Meinertzhagen,et al.  Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster , 1991, The Journal of comparative neurology.

[10]  Matti Weckström,et al.  Large Functional Variability in Cockroach Photoreceptors: Optimization to Low Light Levels , 2006, The Journal of Neuroscience.

[11]  P. Simmons Signal processing in a simple visual system: The locust ocellar system and its synapses , 2002, Microscopy research and technique.

[12]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[13]  G. Matthews,et al.  Calcium action potentials in retinal bipolar neurons , 1998, Visual Neuroscience.

[14]  G. Fain,et al.  Calcium spikes in toad rods. , 1980, The Journal of physiology.

[15]  Z. Pan,et al.  Voltage-dependent Na(+) currents in mammalian retinal cone bipolar cells. , 2000, Journal of neurophysiology.

[16]  Xiong-Li Yang,et al.  Retinal bipolar cells , 1999 .

[17]  I. Meinertzhagen,et al.  Quantitative features of synapse formation in the fly's visual system. I. The presynaptic photoreceptor terminal , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  A. Berntson,et al.  The unitary event amplitude of mouse retinal on-cone bipolar cells , 2003, Visual Neuroscience.

[20]  J. Diamond,et al.  Vesicle depletion and synaptic depression at a mammalian ribbon synapse. , 2006, Journal of neurophysiology.

[21]  Shannon Saszik,et al.  A Mammalian Retinal Bipolar Cell Uses Both Graded Changes in Membrane Voltage and All-or-Nothing Na+ Spikes to Encode Light , 2012, The Journal of Neuroscience.

[22]  M. Egelhaaf Fly Vision: Neural Mechanisms of Motion Computation , 2008, Current Biology.

[23]  T. Ichinose,et al.  Sodium Channels in Transient Retinal Bipolar Cells Enhance Visual Responses in Ganglion Cells , 2005, The Journal of Neuroscience.

[24]  F. Werblin,et al.  Vertical interactions across ten parallel, stacked representations in the mammalian retina , 2001, Nature.

[25]  J. B. Demb,et al.  Functional Circuitry of the Retinal Ganglion Cell's Nonlinear Receptive Field , 1999, The Journal of Neuroscience.

[26]  K. Rábl,et al.  Kinetics of Exocytosis Is Faster in Cones Than in Rods , 2005, The Journal of Neuroscience.

[27]  M. Bethge,et al.  Spikes in Mammalian Bipolar Cells Support Temporal Layering of the Inner Retina , 2013, Current Biology.

[28]  Gary Matthews,et al.  The diverse roles of ribbon synapses in sensory neurotransmission , 2010, Nature Reviews Neuroscience.

[29]  F. Baumann Slow and Spike Potentials Recorded from Retinula Cells of the Honeybee Drone in Response to Light , 1968, The Journal of general physiology.

[30]  Alexander Egner,et al.  Tuning of synapse number, structure and function in the cochlea , 2009, Nature Neuroscience.

[31]  E. A. Schwartz,et al.  Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina , 1999, Nature.

[32]  Gordon L. Fain,et al.  Phototransduction and the Evolution of Photoreceptors , 2010, Current Biology.

[33]  P A Fuchs,et al.  Mechanisms of hair cell tuning. , 1999, Annual review of physiology.

[34]  F. Rieke,et al.  Nonlinear Signal Transfer from Mouse Rods to Bipolar Cells and Implications for Visual Sensitivity , 2002, Neuron.

[35]  Tim Gollisch,et al.  Eye Smarter than Scientists Believed: Neural Computations in Circuits of the Retina , 2010, Neuron.

[36]  W. M. Roberts,et al.  Spikes and Membrane Potential Oscillations in Hair Cells Generate Periodic Afferent Activity in the Frog Sacculus , 2009, The Journal of Neuroscience.

[37]  M.,et al.  Graded Responses and Spiking Properties of Identified First-Order Visual Interneurons of the Fly Compound Eye , 2002 .

[38]  N. Vardi,et al.  Coordinated multivesicular release at a mammalian ribbon synapse , 2004, Nature Neuroscience.

[39]  J. Brandstätter,et al.  Ribbon synapses of the retina , 2006, Cell and Tissue Research.

[40]  R. O. Uusitalo,et al.  Potentiation in the first visual synapse of the fly compound eye. , 2000, Journal of neurophysiology.

[41]  R. Hardie,et al.  The Drosophila SK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network , 2011, The Journal of Neuroscience.

[42]  J. Eilbeck,et al.  Membrane conductances involved in amplification of small signals by sodium channels in photoreceptors of drone honey bee. , 1992, The Journal of physiology.

[43]  M. Horiguchi,et al.  Na+ Action Potentials in Human Photoreceptors , 2001, Neuron.

[44]  R. Frolov,et al.  Signal coding in cockroach photoreceptors is tuned to dim environments. , 2012, Journal of neurophysiology.

[45]  A. Hudspeth,et al.  Efferent Control of the Electrical and Mechanical Properties of Hair Cells in the Bullfrog's Sacculus , 2010, PloS one.

[46]  Eric J. Warrant,et al.  Ocellar adaptations for dim light vision in a nocturnal bee , 2011, Journal of Experimental Biology.

[47]  F. Esposti,et al.  Spikes in Retinal Bipolar Cells Phase-Lock to Visual Stimuli with Millisecond Precision , 2011, Current Biology.

[48]  Norbert Babai,et al.  Vesicle pool size at the salamander cone ribbon synapse. , 2010, Journal of neurophysiology.

[49]  D. Baylor,et al.  Electrical responses of single cones in the retina of the turtle , 1970, The Journal of physiology.

[50]  W. M. Roberts,et al.  Frequency selectivity of synaptic exocytosis in frog saccular hair cells. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D. Furness,et al.  Auditory Hair Cell-Afferent Fiber Synapses Are Specialized to Operate at Their Best Frequencies , 2005, Neuron.

[52]  Peter Sterling,et al.  Encoding Light Intensity by the Cone Photoreceptor Synapse , 2005, Neuron.

[53]  G. Matthews,et al.  Ultrafast Exocytosis Elicited by Calcium Current in Synaptic Terminals of Retinal Bipolar Neurons , 1996, Neuron.

[54]  J. Sanes,et al.  The most numerous ganglion cell type of the mouse retina is a selective feature detector , 2012, Proceedings of the National Academy of Sciences.

[55]  S. DeVries,et al.  Bipolar Cells Use Kainate and AMPA Receptors to Filter Visual Information into Separate Channels , 2000, Neuron.

[56]  L. Lagnado,et al.  High Mobility of Vesicles Supports Continuous Exocytosis at a Ribbon Synapse , 2004, Current Biology.

[57]  D. Baylor,et al.  Visual transduction in cones of the monkey Macaca fascicularis. , 1990, The Journal of physiology.

[58]  A. S. French,et al.  Information processing by graded-potential transmission through tonically active synapses , 1996, Trends in Neurosciences.

[59]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[60]  G. Matthews,et al.  Voltage-Dependent Sodium Channels Are Expressed in Nonspiking Retinal Bipolar Neurons , 2001, The Journal of Neuroscience.

[61]  Nicolas Flores-Herr,et al.  Light Evokes Ca2+ Spikes in the Axon Terminal of a Retinal Bipolar Cell , 2000, Neuron.

[62]  A. V. Maricq,et al.  Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors , 1988, Neuron.

[63]  Fred Rieke,et al.  The spatial structure of a nonlinear receptive field , 2012, Nature Neuroscience.

[64]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[65]  M. Palmer Characterisation of bipolar cell synaptic transmission in goldfish retina using paired recordings , 2010, The Journal of physiology.

[66]  G. Matthews,et al.  Evidence That Vesicles on the Synaptic Ribbon of Retinal Bipolar Neurons Can Be Rapidly Released , 1996, Neuron.

[67]  Skyler L Jackman,et al.  Role of the synaptic ribbon in transmitting the cone light response , 2009, Nature Neuroscience.

[68]  K. Rábl,et al.  A Highly Ca2+-Sensitive Pool of Vesicles Contributes to Linearity at the Rod Photoreceptor Ribbon Synapse , 2004, Neuron.

[69]  Peter Sterling,et al.  Structure and function of ribbon synapses , 2005, Trends in Neurosciences.

[70]  L. Lagnado,et al.  Exocytosis at the Ribbon Synapse of Retinal Bipolar Cells Studied in Patches of Presynaptic Membrane , 2003, The Journal of Neuroscience.

[71]  I. Meinertzhagen,et al.  Development and structure of synaptic contacts in Drosophila. , 2006, Seminars in cell & developmental biology.

[72]  S. Laughlin,et al.  The rate of information transfer at graded-potential synapses , 1996, Nature.

[73]  S. Laughlin,et al.  Membrane parameters, signal transmission, and the design of a graded potential neuron , 1990, Journal of Comparative Physiology A.

[74]  N. Strausfeld,et al.  Visual Motion-Detection Circuits in Flies: Parallel Direction- and Non-Direction-Sensitive Pathways between the Medulla and Lobula Plate , 1996, The Journal of Neuroscience.

[75]  E. A. Schwartz,et al.  Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. , 1996, The Journal of physiology.

[76]  H. V. Gersdorff,et al.  Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals , 1994, Nature.

[77]  Thomas Euler,et al.  Light-Driven Calcium Signals in Mouse Cone Photoreceptors , 2012, The Journal of Neuroscience.

[78]  R. Fettiplace,et al.  Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells , 1995, Neuron.

[79]  Stuart L. Johnson,et al.  Sodium and calcium currents shape action potentials in immature mouse inner hair cells , 2003, The Journal of physiology.

[80]  T. Moser,et al.  Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Aziz El-Amraoui,et al.  The auditory hair cell ribbon synapse: from assembly to function. , 2012, Annual review of neuroscience.

[82]  F. Esposti,et al.  In vivo evidence that retinal bipolar cells generate spikes modulated by light , 2011, Nature Neuroscience.

[83]  L. Lagnado,et al.  Electrical resonance and Ca2+ influx in the synaptic terminal of depolarizing bipolar cells from the Goldfish retina , 1997, The Journal of physiology.

[84]  Wei Li,et al.  Parallel Processing in Two Transmitter Microenvironments at the Cone Photoreceptor Synapse , 2006, Neuron.

[85]  M. Palmer Modulation of Ca2+‐activated K+ currents and Ca2+‐dependent action potentials by exocytosis in goldfish bipolar cell terminals , 2006, The Journal of physiology.

[86]  G. Awatramani,et al.  Origin of Transient and Sustained Responses in Ganglion Cells of the Retina , 2000, The Journal of Neuroscience.

[87]  Martin Egelhaaf,et al.  Neural Coding with Graded Membrane Potential Changes and Spikes , 2001, Journal of Computational Neuroscience.

[88]  Roger C. Hardie,et al.  Feedback Network Controls Photoreceptor Output at the Layer of First Visual Synapses in Drosophila , 2006, The Journal of general physiology.

[89]  Simon B. Laughlin,et al.  Presynaptic enhancement of signal transients in photoreceptor terminals in the compound eye , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[90]  Zhuo-Hua Pan,et al.  Heterogeneous expression of voltage-dependent Na+ and K+ channels in mammalian retinal bipolar cells , 2005, Visual Neuroscience.

[91]  R. Masland The Neuronal Organization of the Retina , 2012, Neuron.

[92]  A. Borst,et al.  Neural networks in the cockpit of the fly , 2002, Journal of Comparative Physiology A.

[93]  G. Matthews,et al.  The Role of Ribbons at Sensory Synapses , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[94]  M. Egelhaaf,et al.  Precise timing in fly motion vision is mediated by fast components of combined graded and spike signals , 2009, Neuroscience.

[95]  P. Simmons,et al.  Sparse but specific temporal coding by spikes in an insect sensory-motor ocellar pathway , 2010, Journal of Experimental Biology.

[96]  M H Ellisman,et al.  Synaptic Vesicle Populations in Saccular Hair Cells Reconstructed by Electron Tomography , 1999, The Journal of Neuroscience.

[97]  Richard H. Masland,et al.  Receptive Field Microstructure and Dendritic Geometry of Retinal Ganglion Cells , 2000, Neuron.

[98]  W. Thoreson,et al.  The dynamic architecture of photoreceptor ribbon synapses: Cytoskeletal, extracellular matrix, and intramembrane proteins , 2011, Visual Neuroscience.

[99]  H. Ichinose,et al.  Suppression by an h current of spontaneous Na+ action potentials in human cone and rod photoreceptors. , 2005, Investigative ophthalmology & visual science.

[100]  Wallace B. Thoreson,et al.  Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones , 2007, Molecular Neurobiology.

[101]  L. Lagnado,et al.  Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[102]  Stuart L. Johnson,et al.  Elementary properties of CaV1.3 Ca2+ channels expressed in mouse cochlear inner hair cells , 2009, The Journal of physiology.

[103]  Tobias Moser,et al.  Hair cell ribbon synapses , 2006, Cell and Tissue Research.

[104]  M. Tachibana,et al.  Ca2+-activated K+ current at presynaptic terminals of goldfish retinal bipolar cells , 1997, Neuroscience Research.

[105]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[106]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[107]  T. Parsons,et al.  Structure and Function of the Hair Cell Ribbon Synapse , 2006, The Journal of Membrane Biology.