A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates

Abstract
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Abstract

Visual perception across a broad range of light levels is shaped by interactions between rod- and cone-mediated signals. Because responses of retinal ganglion cells, the output cells of the retina, depend on signals from both rod and cone photoreceptors, interactions occurring in retinal circuits provide an opportunity to link the mechanistic operation of parallel pathways and perception. Here we show that rod- and cone-mediated responses interact nonlinearly to control the responses of primate retinal ganglion cells; these nonlinear interactions, surprisingly, were asymmetric, with rod responses strongly suppressing subsequent cone responses but not vice-versa. Human psychophysical experiments revealed a similar perceptual asymmetry. Nonlinear interactions in the retinal output cells were well-predicted by linear summation of kinetically-distinct rod- and cone-mediated signals followed by a synaptic nonlinearity. These experiments thus reveal how a simple mechanism controlling interactions between parallel pathways shapes circuit outputs and perception.

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Author details

William N Grimes

Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.
Logan R Graves

Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.
Mathew T Summers

Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, United States

Competing interests
The authors declare that no competing interests exist.
Fred Rieke

Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, United States

For correspondence
rieke@u.washington.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: We obtained primate retinas (Macaca fascicularis, Macaca nemestrina and Macaca mulatta of either sex, ages 3-19 years) through the Tissue Distribution Program of the Regional Primate Research Center. All protocols were approved by the Institutional Animal Care and Use Committee at the University of Washington (protocol 4140-01).

Human subjects: The experimental protocol was approved by the Institutional Review Board of the University of Washington (protocol 16934) and was in accordance with the Declaration of Helsinki. All subjects gave informed consent in writing before participating in the experiment.

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.