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Distinct Inhibitory Pathways Control Velocity and Directional Tuning in the Retina

Mathew T. Summers, Marla B. Feller
doi: https://doi.org/10.1101/2022.01.13.476257
Mathew T. Summers
1Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA
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Marla B. Feller
1Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA
2Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA
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  • For correspondence: mfeller@berkeley.edu
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Summary

The sensory periphery is responsible for detecting ethologically relevant features of the external world, using compact, predominantly feedforward circuits. Visual motion is a particularly prevalent sensory feature, the presence of which can be a signal to enact diverse behaviors ranging from gaze stabilization reflexes, to predator avoidance or prey capture. To understand how the retina constructs the distinct neural representations required for these diverse behaviors, we investigated two circuits responsible for encoding different aspects of image motion: ON and ON-OFF direction selective ganglion cells (DSGCs). Using a combination of 2-photon targeted whole cell electrophysiology, pharmacology, and conditional knockout mice, we show that distinct inhibitory pathways independently control tuning for motion velocity and motion direction in these two cell types. We further employ dynamic clamp and numerical modeling techniques to show that asymmetric inhibition provides a velocity-invariant mechanism of directional tuning, despite the strong velocity dependence of classical models of direction selectivity. We therefore demonstrate that invariant representations of motion features by inhibitory interneurons act as computational building blocks to construct distinct, behaviorally relevant signals at the earliest stages of the visual system.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 17, 2022.
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Distinct Inhibitory Pathways Control Velocity and Directional Tuning in the Retina
Mathew T. Summers, Marla B. Feller
bioRxiv 2022.01.13.476257; doi: https://doi.org/10.1101/2022.01.13.476257
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Distinct Inhibitory Pathways Control Velocity and Directional Tuning in the Retina
Mathew T. Summers, Marla B. Feller
bioRxiv 2022.01.13.476257; doi: https://doi.org/10.1101/2022.01.13.476257

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