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

Abstract
Data availability
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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

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.

"This ORCID iD identifies the author of this article:" 0000-0002-4164-9995
Gregory William Schwartz

Department of Ophthalmology, Northwestern University, Chicago, United States

Competing interests
No competing interests declared.
Fred Rieke

Department of Physiology and Biophysics, University of Washington, Seattle, United States

Competing interests
Fred Rieke, Reviewing editor, eLife.

"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).

Copyright

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.