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Research ArticleNew Research, Sensory and Motor Systems

Rank Order Coding: a Retinal Information Decoding Strategy Revealed by Large-Scale Multielectrode Array Retinal Recordings

Geoffrey Portelli, John M. Barrett, Gerrit Hilgen, Timothée Masquelier, Alessandro Maccione, Stefano Di Marco, Luca Berdondini, Pierre Kornprobst and Evelyne Sernagor
eNeuro 12 May 2016, 3 (3) ENEURO.0134-15.2016; DOI: https://doi.org/10.1523/ENEURO.0134-15.2016
Geoffrey Portelli
1Biovision Team, Inria Sophia Antipolis Méditerranée, FR-06902, Sophia Antipolis, France
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John M. Barrett
2Faculty of Medical Sciences, Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne NE2 4HH, United Kingdom
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Gerrit Hilgen
2Faculty of Medical Sciences, Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne NE2 4HH, United Kingdom
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Timothée Masquelier
3 INSERM, U968, Paris, F-75012, France
4Sorbonne Universités, UPMC Univ Paris 06, UMR S 968, Institut de la Vision, Paris, F-75012, France
5 CNRS, UMR 7210, Paris, F-75012, France
6Present address: CERCO UMR 5549, CNRS – Université de Toulouse, F-31300, France
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Alessandro Maccione
7NetS3 Laboratory, Neuroscience and Brain Technologies Dpt., Istituto Italiano di Tecnologia, Genova, Italy.
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Stefano Di Marco
7NetS3 Laboratory, Neuroscience and Brain Technologies Dpt., Istituto Italiano di Tecnologia, Genova, Italy.
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Luca Berdondini
7NetS3 Laboratory, Neuroscience and Brain Technologies Dpt., Istituto Italiano di Tecnologia, Genova, Italy.
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Pierre Kornprobst
1Biovision Team, Inria Sophia Antipolis Méditerranée, FR-06902, Sophia Antipolis, France
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Evelyne Sernagor
2Faculty of Medical Sciences, Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne NE2 4HH, United Kingdom
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Abstract

How a population of retinal ganglion cells (RGCs) encodes the visual scene remains an open question. Going beyond individual RGC coding strategies, results in salamander suggest that the relative latencies of a RGC pair encode spatial information. Thus, a population code based on this concerted spiking could be a powerful mechanism to transmit visual information rapidly and efficiently. Here, we tested this hypothesis in mouse by recording simultaneous light-evoked responses from hundreds of RGCs, at pan-retinal level, using a new generation of large-scale, high-density multielectrode array consisting of 4096 electrodes. Interestingly, we did not find any RGCs exhibiting a clear latency tuning to the stimuli, suggesting that in mouse, individual RGC pairs may not provide sufficient information. We show that a significant amount of information is encoded synergistically in the concerted spiking of large RGC populations. Thus, the RGC population response described with relative activities, or ranks, provides more relevant information than classical independent spike count- or latency- based codes. In particular, we report for the first time that when considering the relative activities across the whole population, the wave of first stimulus-evoked spikes is an accurate indicator of stimulus content. We show that this coding strategy coexists with classical neural codes, and that it is more efficient and faster. Overall, these novel observations suggest that already at the level of the retina, concerted spiking provides a reliable and fast strategy to rapidly transmit new visual scenes.

  • ganglion cells
  • multielectrode array
  • population coding
  • rank order coding
  • retina

Footnotes

  • ↵1 The authors report no conflict of interest.

  • ↵3 This work was supported by the 7th Framework Program for Research of the European Commission [Grant agreement 600847: RENVISION, project of the Future and Emerging Technologies (FET) program Neuro-bio-inspired systems FET-Proactive Initiative] and the Wellcome Trust (grant 096975/Z/11/Z). We thank Bruno Cessac and Matthias Hennig for their insightful discussions and the two reviewers who helped to improve the paper.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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eneuro: 3 (3)
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May/June 2016
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Rank Order Coding: a Retinal Information Decoding Strategy Revealed by Large-Scale Multielectrode Array Retinal Recordings
Geoffrey Portelli, John M. Barrett, Gerrit Hilgen, Timothée Masquelier, Alessandro Maccione, Stefano Di Marco, Luca Berdondini, Pierre Kornprobst, Evelyne Sernagor
eNeuro 12 May 2016, 3 (3) ENEURO.0134-15.2016; DOI: 10.1523/ENEURO.0134-15.2016

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Rank Order Coding: a Retinal Information Decoding Strategy Revealed by Large-Scale Multielectrode Array Retinal Recordings
Geoffrey Portelli, John M. Barrett, Gerrit Hilgen, Timothée Masquelier, Alessandro Maccione, Stefano Di Marco, Luca Berdondini, Pierre Kornprobst, Evelyne Sernagor
eNeuro 12 May 2016, 3 (3) ENEURO.0134-15.2016; DOI: 10.1523/ENEURO.0134-15.2016
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Keywords

  • ganglion cells
  • multielectrode array
  • population coding
  • rank order coding
  • retina

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