Nonlinear receptive fields evoke redundant retinal coding of natural scenes

The role of the vertebrate retina in early vision is generally described by the efficient coding hypothesis<sup>1,2</sup>, which predicts that the retina reduces the redundancy inherent in natural scenes<sup>3</sup> by discarding spatiotemporal correlations while preserving stimulus information<sup>4</sup>. It is unclear, however, whether the predicted decorrelation and redundancy reduction in the activity of ganglion cells, the retina's output neurons, hold under gaze shifts, which dominate the dynamics of the natural visual input<sup>5</sup>. We show here that species-specific gaze patterns in natural stimuli can drive correlated spiking responses both in and across distinct types of ganglion cells in marmoset as well as mouse retina. These concerted responses disrupt redundancy reduction to signal fixation periods with locally high spatial contrast. Model-based analyses of ganglion cell responses to natural stimuli show that the observed response correlations follow from nonlinear pooling of ganglion cell inputs. Our results indicate cell-type-specific deviations from efficient coding in retinal processing of natural gaze shifts.

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Journal
Nature
Published
2024-11-20
DOI
https://doi.org/10.1038/s41586-024-08212-3
Citations
12
Primary Topic
Retinal Development and Disorders
Type
article
Field-Weighted Citation Impact
2.81
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article

Nonlinear receptive fields evoke redundant retinal coding of natural scenes

Matthias Mietsch, Sören J. Zapp, Mohammad H. Khani, Dimokratis Karamanlis et al.
12 citations
Nature
Retinal Development and Disorders
2.81
article

Nonlinear receptive fields evoke redundant retinal coding of natural scenes

Matthias Mietsch, Sören J. Zapp, Mohammad H. Khani, Dimokratis Karamanlis, Tim Gollisch, Helene M. Schreyer
article en
12 citations

Abstract

The role of the vertebrate retina in early vision is generally described by the efficient coding hypothesis<sup>1,2</sup>, which predicts that the retina reduces the redundancy inherent in natural scenes<sup>3</sup> by discarding spatiotemporal correlations while preserving stimulus information<sup>4</sup>. It is unclear, however, whether the predicted decorrelation and redundancy reduction in the activity of ganglion cells, the retina's output neurons, hold under gaze shifts, which dominate the dynamics of the natural visual input<sup>5</sup>. We show here that species-specific gaze patterns in natural stimuli can drive correlated spiking responses both in and across distinct types of ganglion cells in marmoset as well as mouse retina. These concerted responses disrupt redundancy reduction to signal fixation periods with locally high spatial contrast. Model-based analyses of ganglion cell responses to natural stimuli show that the observed response correlations follow from nonlinear pooling of ganglion cell inputs. Our results indicate cell-type-specific deviations from efficient coding in retinal processing of natural gaze shifts.

NatureVol. 637(8045)
German Primate Center (DE), Bernstein Center for Computational Neuroscience Göttingen (DE), University Hospital of Geneva (CH), Universitätsmedizin Göttingen (DE), German Centre for Cardiovascular Research (DE), Institute of Molecular and Clinical Ophthalmology Basel (CH), University of Göttingen (DE)
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Retinal Development and Disorders
2.81
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Nonlinear receptive fields evoke redundant retinal coding of natural scenes — Matthias Mietsch, Sören J. Zapp, et al. · Nature (2024) | TGRS Research Map | TGRS