Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes

  1. Juyue Chen
  2. Holly B Mandel
  3. James E Fitzgerald  Is a corresponding author
  4. Damon A Clark  Is a corresponding author
  1. Yale University, United States
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

Animals detect motion using a variety of visual cues that reflect regularities in the natural world. Experiments in animals across phyla have shown that motion percepts incorporate both pairwise and triplet spatiotemporal correlations that could theoretically benefit motion computation. However, it remains unclear how visual systems assemble these cues to build accurate motion estimates. Here we used systematic behavioral measurements of fruit fly motion perception to show how flies combine local pairwise and triplet correlations to reduce variability in motion estimates across natural scenes. By generating synthetic images with statistics controlled by maximum entropy distributions, we show that the triplet correlations are useful only when images have light-dark asymmetries that mimic natural ones. This suggests that asymmetric ON-OFF processing is tuned to the particular statistics of natural scenes. Since all animals encounter the world's light-dark asymmetries, many visual systems are likely to use asymmetric ON-OFF processing to improve motion estimation.

Data availability

All data and code to reproduce figures here are available at:https://github.com/ClarkLabCode/ThirdOrderKernelCodeData is also available on Dryad under https://doi.org/10.5061/dryad.7jm87bt

The following data sets were generated

Article and author information

Author details

  1. Juyue Chen

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Holly B Mandel

    Department of Molecular, Cellular, Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. James E Fitzgerald

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    fitzgeraldj@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
  4. Damon A Clark

    Department of Molecular, Cellular, Developmental Biology, Yale University, New Haven, United States
    For correspondence
    damon.clark@yale.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8487-700X

Funding

National Institutes of Health (R01EY026555)

  • Juyue Chen
  • Damon A Clark

National Science Foundation (IOS1558103)

  • Juyue Chen
  • Damon A Clark

Chicago Community Trust (Searle Scholar Award)

  • Holly B Mandel
  • Damon A Clark

Howard Hughes Medical Institute

  • James E Fitzgerald

Alfred P. Sloan Foundation (Research Fellowship)

  • Damon A Clark

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Stephanie Palmer, University of Chicago, United States

Publication history

  1. Received: April 10, 2019
  2. Accepted: October 12, 2019
  3. Accepted Manuscript published: October 15, 2019 (version 1)
  4. Version of Record published: November 29, 2019 (version 2)
  5. Version of Record updated: December 5, 2019 (version 3)

Copyright

© 2019, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Juyue Chen
  2. Holly B Mandel
  3. James E Fitzgerald
  4. Damon A Clark
(2019)
Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes
eLife 8:e47579.
https://doi.org/10.7554/eLife.47579

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