Adaptation in cone photoreceptors contributes to an unexpected insensitivity of primate On parasol retinal ganglion cells to spatial structure in natural images
Abstract
Neural circuits are constructed from nonlinear building blocks, and not surprisingly overall circuit behavior is often strongly nonlinear. But neural circuits can also behave near linearly, and some circuits shift from linear to nonlinear behavior depending on stimulus conditions. Such control of nonlinear circuit behavior is fundamental to neural computation. Here, we study a surprising stimulus dependence of the responses of macaque On (but not Off) parasol retinal ganglion cells: these cells respond nonlinearly to spatial structure in some stimuli but near-linearly to spatial structure in others, including natural inputs. We show that these differences in the linearity of the integration of spatial inputs can be explained by a shift in the balance of excitatory and inhibitory synaptic inputs that originates at least partially from adaptation in the cone photoreceptors. More generally, this highlights how subtle asymmetries in signaling - here in the cone signals - can qualitatively alter circuit computation.
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Source data for Figures 2, 3, 5, and 7 is provided.
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Funding
National Institutes of Health (EY028542)
- Fred Rieke
National Institutes of Health (F31-EY026288)
- Maxwell H Turner
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Experiments were performed on primate retina obtained through the Tissue Distribution Program of the University of Washington's Regional Primate Research Center. Recordings were made from retinas from Macaca fascicularis, Macaca nemestrina, and Macaca mulatta of both sexes, aged 2 through 20 years. All use of primate tissue was in accordance with the University of Washington Institutional Animal Care and Use Committee (protocol 4140-01).
Copyright
© 2022, Yu 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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