Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

  1. Maxwell H Turner  Is a corresponding author
  2. Gregory William Schwartz
  3. Fred Rieke
  1. University of Washington, United States
  2. Northwestern University, United States

Abstract

Antagonistic receptive field surrounds are a near-universal property of early sensory processing. A key assumption in many models for retinal ganglion cell encoding is that receptive field surrounds are added only to the fully formed center signal. But anatomical and functional observations indicate that surrounds are added before the summation of signals across receptive field subunits that creates the center. Here, we show that in the macaque monkey retina this receptive field architecture has an important consequence for spatial contrast encoding: the surround can control sensitivity to fine spatial structure by changing the way the center integrates visual information over space. The impact of the surround is particularly prominent when center and surround signals are correlated, as they are in natural stimuli. This effect of the surround differs substantially from classic center-surround models and raises the possibility that the surround plays unappreciated roles in shaping ganglion cell sensitivity to natural inputs.

Data availability

We have made all the data in the study freely available. Source data files have been provided for Figures 2, 3, 4 and 7, and example code to demonstrate how to pull out and plot the data is provided as Source code file 1.

Article and author information

Author details

  1. Maxwell H Turner

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    mhturner@stanford.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4164-9995
  2. Gregory William Schwartz

    Department of Ophthalmology, Northwestern University, Chicago, United States
    Competing interests
    No competing interests declared.
  3. Fred Rieke

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    Fred Rieke, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1052-2609

Funding

National Eye Institute (F31-EY026288)

  • Maxwell H Turner

National Eye Institute (EY11850)

  • Fred Rieke

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

Ethics

Animal experimentation: Tissue was obtained via the tissue distribution program at the Washington National Primate Research Center. All animal procedures were performed in accordance with IACUC protocols at the University of Washington (IACUC protocol number 4277-01).

Reviewing Editor

  1. Andrew J. King, University of Oxford, United Kingdom

Publication history

  1. Received: June 2, 2018
  2. Accepted: August 29, 2018
  3. Accepted Manuscript published: September 6, 2018 (version 1)
  4. Version of Record published: October 12, 2018 (version 2)

Copyright

© 2018, Turner 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. Maxwell H Turner
  2. Gregory William Schwartz
  3. Fred Rieke
(2018)
Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina
eLife 7:e38841.
https://doi.org/10.7554/eLife.38841

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