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Published November 2013 | Published + Supplemental Material
Journal Article Open

Dynamical Adaptation in Photoreceptors

Abstract

Adaptation is at the heart of sensation and nowhere is it more salient than in early visual processing. Light adaptation in photoreceptors is doubly dynamical: it depends upon the temporal structure of the input and it affects the temporal structure of the response. We introduce a non-linear dynamical adaptation model of photoreceptors. It is simple enough that it can be solved exactly and simulated with ease; analytical and numerical approaches combined provide both intuition on the behavior of dynamical adaptation and quantitative results to be compared with data. Yet the model is rich enough to capture intricate phenomenology. First, we show that it reproduces the known phenomenology of light response and short-term adaptation. Second, we present new recordings and demonstrate that the model reproduces cone response with great precision. Third, we derive a number of predictions on the response of photoreceptors to sophisticated stimuli such as periodic inputs, various forms of flickering inputs, and natural inputs. In particular, we demonstrate that photoreceptors undergo rapid adaptation of response gain and time scale, over ∼ 300 ms—i. e., over the time scale of the response itself—and we confirm this prediction with data. For natural inputs, this fast adaptation can modulate the response gain more than tenfold and is hence physiologically relevant.

Additional Information

© 2013 Clark et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received May 20, 2011; Accepted September 3, 2013; Published November 14, 2013. We acknowledge Stephen Baccus, Michael J. Berry II, Tom Clandinin, Vincent Hakim, and Simon Laughlin for helpful discussions and comments on the manuscript. We thank Stephen Baccus for the salamander cone cell recordings. Author Contributions: Conceived and designed the experiments: DAC MM RAdS. Analyzed the data: DAC RB MM RAdS. Wrote the paper: DAC MM RAdS. This work was supported by the Jane Coffin Childs Fund and a CNRS postdoctoral fellowship (DAC), the Ecole Polytechnique (RB), a grant from the NIH (MM), and the CNRS though UMR 8550, the Université Pierre et Marie Curie, and the Université Denis Diderot (RAdS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have declared that no competing interests exist.

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