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Featured ArticleArticles, Behavioral/Systems/Cognitive

The Structure of Multi-Neuron Firing Patterns in Primate Retina

Jonathon Shlens, Greg D. Field, Jeffrey L. Gauthier, Matthew I. Grivich, Dumitru Petrusca, Alexander Sher, Alan M. Litke and E. J. Chichilnisky
Journal of Neuroscience 9 August 2006, 26 (32) 8254-8266; https://doi.org/10.1523/JNEUROSCI.1282-06.2006
Jonathon Shlens
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Greg D. Field
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Jeffrey L. Gauthier
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Matthew I. Grivich
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Dumitru Petrusca
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Alexander Sher
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Alan M. Litke
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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E. J. Chichilnisky
1Department of Systems Neurobiology, The Salk Institute, La Jolla, California 92037, and 2Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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This article has a correction. Please see:

  • Correction for Jonathon et al., The Structure of Multi-Neuron Firing Patterns in Primate Retina - January 30, 2008

Abstract

Current understanding of many neural circuits is limited by our ability to explore the vast number of potential interactions between different cells. We present a new approach that dramatically reduces the complexity of this problem. Large-scale multi-electrode recordings were used to measure electrical activity in nearly complete, regularly spaced mosaics of several hundred ON and OFF parasol retinal ganglion cells in macaque monkey retina. Parasol cells exhibited substantial pairwise correlations, as has been observed in other species, indicating functional connectivity. However, pairwise measurements alone are insufficient to determine the prevalence of multi-neuron firing patterns, which would be predicted from widely diverging common inputs and have been hypothesized to convey distinct visual messages to the brain. The number of possible multi-neuron firing patterns is far too large to study exhaustively, but this problem may be circumvented if two simple rules of connectivity can be established: (1) multi-cell firing patterns arise from multiple pairwise interactions, and (2) interactions are limited to adjacent cells in the mosaic. Using maximum entropy methods from statistical mechanics, we show that pairwise and adjacent interactions accurately accounted for the structure and prevalence of multi-neuron firing patterns, explaining ∼98% of the departures from statistical independence in parasol cells and ∼99% of the departures that were reproducible in repeated measurements. This approach provides a way to define limits on the complexity of network interactions and thus may be relevant for probing the function of many neural circuits.

  • vision
  • information theory
  • correlated variability
  • neural coding
  • synchrony
  • retinal ganglion cell
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The Journal of Neuroscience: 26 (32)
Journal of Neuroscience
Vol. 26, Issue 32
9 Aug 2006
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The Structure of Multi-Neuron Firing Patterns in Primate Retina
Jonathon Shlens, Greg D. Field, Jeffrey L. Gauthier, Matthew I. Grivich, Dumitru Petrusca, Alexander Sher, Alan M. Litke, E. J. Chichilnisky
Journal of Neuroscience 9 August 2006, 26 (32) 8254-8266; DOI: 10.1523/JNEUROSCI.1282-06.2006

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The Structure of Multi-Neuron Firing Patterns in Primate Retina
Jonathon Shlens, Greg D. Field, Jeffrey L. Gauthier, Matthew I. Grivich, Dumitru Petrusca, Alexander Sher, Alan M. Litke, E. J. Chichilnisky
Journal of Neuroscience 9 August 2006, 26 (32) 8254-8266; DOI: 10.1523/JNEUROSCI.1282-06.2006
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Keywords

  • vision
  • information theory
  • correlated variability
  • neural coding
  • synchrony
  • retinal ganglion cell

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