Rapid Neural Coding in the Retina with Relative Spike Latencies

Natural vision is a highly dynamic process. Frequent body, head, and eye movements constantly bring new images onto the retina for brief periods, challenging our understanding of the neural code for vision. We report that certain retinal ganglion cells encode the spatial structure of a briefly presented image in the relative timing of their first spikes. This code is found to be largely invariant to stimulus contrast and robust to noisy fluctuations in response latencies. Mechanistically, the observed response characteristics result from different kinetics in two retinal pathways (“ON” and “OFF”) that converge onto ganglion cells. This mechanism allows the retina to rapidly and reliably transmit new spatial information with the very first spikes emitted by a neural population.

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

[2]  F. M. D. Monasterio Properties of ganglion cells with atypical receptive-field organization in retina of macaques. , 1978 .

[3]  R. Shapley,et al.  The nonlinear pathway of Y ganglion cells in the cat retina , 1979, The Journal of general physiology.

[4]  J. Ashmore,et al.  Different postsynaptic events in two types of retinal bipolar cell , 1980, Nature.

[5]  W. Press,et al.  Numerical Recipes: The Art of Scientific Computing , 1987 .

[6]  F. Amthor,et al.  Morphologies of rabbit retinal ganglion cells with complex receptive fields , 1989, The Journal of comparative neurology.

[7]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[8]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

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

[10]  W. G. Owen,et al.  Receptive field of the retinal bipolar cell: a pharmacological study in the tiger salamander. , 1996, Journal of neurophysiology.

[11]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[12]  D. A. Burkhardt,et al.  Responses of ganglion cells to contrast steps in the light-adapted retina of the tiger salamander , 1998, Visual Neuroscience.

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

[14]  M. Land Motion and vision: why animals move their eyes , 1999, Journal of Comparative Physiology A.

[15]  R. Reid,et al.  Synaptic Interactions between Thalamic Inputs to Simple Cells in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[16]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

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

[18]  F. Mechler,et al.  Temporal coding of contrast in primary visual cortex: when, what, and why. , 2001, Journal of neurophysiology.

[19]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[20]  J. B. Demb,et al.  Bipolar Cells Contribute to Nonlinear Spatial Summation in the Brisk-Transient (Y) Ganglion Cell in Mammalian Retina , 2001, The Journal of Neuroscience.

[21]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

[22]  M. Meister,et al.  Fast and Slow Contrast Adaptation in Retinal Circuitry , 2002, Neuron.

[23]  F. Werblin,et al.  Rapid global shifts in natural scenes block spiking in specific ganglion cell types , 2003, Nature Neuroscience.

[24]  R. Reid,et al.  Efficacy of Retinal Spikes in Driving Cortical Responses , 2003, The Journal of Neuroscience.

[25]  R. Freeman,et al.  Stereoscopic depth processing in the visual cortex: a coarse-to-fine mechanism , 2003, Nature Neuroscience.

[26]  E. Chichilnisky,et al.  Precision of spike trains in primate retinal ganglion cells. , 2004, Journal of neurophysiology.

[27]  Xiong-Li Yang Characterization of receptors for glutamate and GABA in retinal neurons , 2004, Progress in Neurobiology.

[28]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[29]  Nathaniel B Sawtell,et al.  From sparks to spikes: information processing in the electrosensory systems of fish , 2005, Current Opinion in Neurobiology.

[30]  J. van Loon Network , 2006 .

[31]  M. Greschner,et al.  Complex spike-event pattern of transient ON-OFF retinal ganglion cells. , 2006, Journal of neurophysiology.

[32]  L. Chalupa,et al.  Morphological properties of mouse retinal ganglion cells during postnatal development , 2007, The Journal of comparative neurology.

[33]  Eric D Young,et al.  First-spike latency information in single neurons increases when referenced to population onset , 2007, Proceedings of the National Academy of Sciences.

[34]  Saskia E. J. de Vries,et al.  Retinal Ganglion Cells Can Rapidly Change Polarity from Off to On , 2007, PLoS biology.

[35]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.