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The Journal of Neuroscience, March 19, 2008, 28(12):3178-3189; doi:10.1523/JNEUROSCI.5259-07.2008

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Behavioral/Systems/Cognitive
Design of a Neuronal Array

Bart G. Borghuis,¹ Charles P. Ratliff,² Robert G. Smith,¹ Peter Sterling,¹ and Vijay Balasubramanian^2,3

Departments of ¹Neuroscience and ²Physics and Astronomy, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6396, and ³School of Natural Sciences, Institute for Advanced Study, Princeton, New Jersey 08540

Correspondence should be addressed to Bart G. Borghuis, Department of Neuroscience, 123 Anatomy/Chemistry Building, University of Pennsylvania, Philadelphia, PA 19104. Email: bart{at}retina.anatomy.upenn.edu

Retinal ganglion cells of a given type overlap their dendritic fields such that every point in space is covered by three to four cells. We investigated what function is served by such extensive overlap. Recording from pairs of ON or OFF brisk-transient ganglion cells at photopic intensities, we confirmed that this overlap causes the Gaussian receptive field centers to be spaced at 2 SDs (). This, together with response nonlinearities and variability, was just sufficient to provide an ideal observer with uniform contrast sensitivity across the retina for both threshold and suprathreshold stimuli. We hypothesized that overlap might maximize the information represented from natural images, thereby optimizing retinal performance for many tasks. Indeed, tested with natural images (which contain statistical correlations), a model ganglion cell array maximized information represented in its population responses with 2 spacing, i.e., the overlap observed in the retina. Yet, tested with white noise (which lacks statistical correlations), an array maximized its information by minimizing overlap. In both cases, optimal overlap balanced greater signal-to-noise ratio (from larger receptive fields) against greater redundancy (because of larger receptive field overlap). Thus, dendritic overlap improves vision by taking optimal advantage of the statistical correlations of natural scenes.

Key words: retina; ganglion cell; paired recording; contrast sensitivity; ideal observer; natural scenes; optimal coding

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Received July 23, 2007; revised Feb. 7, 2008; accepted Feb. 7, 2008.

Correspondence should be addressed to Bart G. Borghuis, Department of Neuroscience, 123 Anatomy/Chemistry Building, University of Pennsylvania, Philadelphia, PA 19104. Email: bart{at}retina.anatomy.upenn.edu

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