Cone photoreceptor contributions to noise and correlations in the retinal output

Transduction and synaptic noise generated in retinal cone photoreceptors determine the fidelity with which light inputs are encoded, and the readout of cone signals by downstream circuits determines whether this fidelity is used for vision. We examined the effect of cone noise on visual signals by measuring its contribution to correlated noise in primate retinal ganglion cells. Correlated noise was strong in the responses of dissimilar cell types with shared cone inputs. The dynamics of cone noise could account for rapid correlations in ganglion cell activity, and the extent of shared cone input could explain correlation strength. Furthermore, correlated noise limited the fidelity with which visual signals were encoded by populations of ganglion cells. Thus, a simple picture emerges: cone noise, traversing the retina through diverse pathways, accounts for most of the noise and correlations in the retinal output and constrains how higher centers exploit signals carried by parallel visual pathways.

[1]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

[2]  S. Bloomfield,et al.  Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. , 2003, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Peter Sterling,et al.  Different types of ganglion cell share a synaptic pattern , 2008, The Journal of comparative neurology.

[4]  K. Yau,et al.  Quantal noise from human red cone pigment , 2008, Nature Neuroscience.

[5]  Iman H. Brivanlou,et al.  Mechanisms of Concerted Firing among Retinal Ganglion Cells , 1998, Neuron.

[6]  S. Bloomfield,et al.  Gap Junctional Coupling Underlies the Short-Latency Spike Synchrony of Retinal α Ganglion Cells , 2003, The Journal of Neuroscience.

[7]  Peter Sterling,et al.  Parallel Circuits from Cones to the On‐Beta Ganglion Cell , 1992, The European journal of neuroscience.

[8]  J. L. Schnapf,et al.  The Photovoltage of Macaque Cone Photoreceptors: Adaptation, Noise, and Kinetics , 1999, The Journal of Neuroscience.

[9]  D. Mastronarde.  Correlated firing of retinal ganglion cells , 1989, Trends in Neurosciences.

[10]  H. Barlow.  Retinal noise and absolute threshold. , 1956, Journal of the Optical Society of America.

[11]  Peter Sterling,et al.  Loss of Sensitivity in an Analog Neural Circuit , 2009, The Journal of Neuroscience.

[12]  D. Dacey,et al.  Colour coding in the primate retina: diverse cell types and cone-specific circuitry , 2003, Current Opinion in Neurobiology.

[13]  Kristian Donner,et al.  Noise and the absolute thresholds of cone and rod vision , 1992, Vision Research.

[14]  T. Lamb,et al.  Analysis of electrical noise in turtle cones , 1977, The Journal of physiology.

[15]  Michael P Stryker,et al.  Intrinsic ON Responses of the Retinal OFF Pathway Are Suppressed by the ON Pathway , 2006, The Journal of Neuroscience.

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

[17]  Jonathon Shlens,et al.  Synchronized firing in the retina , 2008, Current Opinion in Neurobiology.

[18]  D. Tranchina,et al.  Multiple Steps of Phosphorylation of Activated Rhodopsin Can Account for the Reproducibility of Vertebrate Rod Single-photon Responses , 2003, The Journal of general physiology.

[19]  G D Field,et al.  Information processing in the primate retina: circuitry and coding. , 2007, Annual review of neuroscience.

[20]  H. Barlow,et al.  Purkinje Shift and Retinal Noise , 1957, Nature.

[21]  O. Braddick.  Visual hyperacuity. , 1984, Nature.

[22]  D. Dacey,et al.  A coupled network for parasol but not midget ganglion cells in the primate retina , 1992, Visual Neuroscience.

[23]  Jonathon Shlens,et al.  Uniform Signal Redundancy of Parasol and Midget Ganglion Cells in Primate Retina , 2009, The Journal of Neuroscience.

[24]  M. Slaughter,et al.  2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. , 1981, Science.

[25]  J. Mollon,et al.  A reduction in stimulus duration can improve wavelength discriminations mediated by short-wave cones , 1992, Vision Research.

[26]  D. Mastronarde.  Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. , 1983, Journal of neurophysiology.

[27]  T. M. Esdaille,et al.  Dark Light, Rod Saturation, and the Absolute and Incremental Sensitivity of Mouse Cone Vision , 2010, The Journal of Neuroscience.

[28]  Paul R. Martin,et al.  Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus , 1996, The Journal of comparative neurology.

[29]  William Bialek,et al.  Reading a Neural Code , 1991, NIPS.

[30]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

[31]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[33]  M. Meister.  Multineuronal codes in retinal signaling. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Baylor,et al.  Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina , 1977, The Journal of physiology.

[35]  F. Rieke,et al.  Origin of correlated activity between parasol retinal ganglion cells , 2008, Nature Neuroscience.

[36]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[37]  B. Boycott,et al.  Morphological Classification of Bipolar Cells of the Primate Retina , 1991, The European journal of neuroscience.

[38]  A. Aho,et al.  Retinal noise, the performance of retinal ganglion cells, and visual sensitivity in the dark-adapted frog. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[39]  D. I. Vaney,et al.  Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin , 1991, Neuroscience Letters.

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

[41]  Jonathon Shlens,et al.  Spatial Properties and Functional Organization of Small Bistratified Ganglion Cells in Primate Retina , 2007, The Journal of Neuroscience.

[42]  Pamela Reinagel,et al.  Decoding visual information from a population of retinal ganglion cells. , 1997, Journal of neurophysiology.

[43]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[44]  D. Mastronarde.  Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. , 1983, Journal of neurophysiology.

[45]  Y. Kurosawa,et al.  Dendrodendritic Electrical Synapses between Mammalian Retinal Ganglion Cells , 2004, The Journal of Neuroscience.

[46]  Michael J. Berry,et al.  Redundancy in the Population Code of the Retina , 2005, Neuron.

[47]  F. Rieke,et al.  Retinal processing near absolute threshold: from behavior to mechanism. , 2005, Annual review of physiology.

[48]  F. Rieke,et al.  Light adaptation in cone vision involves switching between receptor and post-receptor sites , 2007, Nature.

[49]  S. DeVries.  Correlated firing in rabbit retinal ganglion cells. , 1999, Journal of neurophysiology.

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