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A GPCR negative feedback loop underlies efficient coding of external stimuli

Rotem Ruach, Shai Yellinek, Eyal Itskovits, View ORCID ProfileAlon Zaslaver
doi: https://doi.org/10.1101/2020.12.14.422627
Rotem Ruach
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University, Jerusalem 9190401, Israel
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Shai Yellinek
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University, Jerusalem 9190401, Israel
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Eyal Itskovits
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University, Jerusalem 9190401, Israel
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Alon Zaslaver
Department of Genetics, Silberman Institute of Life Science, Edmond J. Safra Campus, The Hebrew University, Jerusalem 9190401, Israel
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  • ORCID record for Alon Zaslaver
  • For correspondence: alonzas@mail.huji.ac.il
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Abstract

Efficient navigation based on chemical cues is an essential feature shared by all animals. These cues may be encountered in complex spatio-temporal patterns and with orders of magnitude varying intensities. Nevertheless, sensory neurons accurately extract the relevant information from such perplexing signals. Here, we show how a single sensory neuron in C. elegans worms can cell-autonomously encode complex stimulus patterns composed of instantaneous sharp changes and of slowly-changing continuous gradients. This encoding relies on a simple negative feedback in the GPCR signaling pathway in which TAX-6/Calcineurin plays a key role in mediating the feedback inhibition. Crucially, this negative feedback pathway supports several important coding features that underlie an efficient navigation strategy, including exact adaptation and adaptation to the magnitude of the gradient’s first derivative. A simple mathematical model accurately captured the fine neural dynamics of both wt and tax-6 mutant animals, further highlighting how the calcium-dependent activity of TAX-6/Calcineurin dictates GPCR inhibition and response dynamics. As GPCRs are ubiquitously expressed in all sensory neurons, this mechanism may be a universal solution for efficient cell-autonomous coding of external stimuli.

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. It is made available under a CC-BY-NC 4.0 International license.
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Posted December 14, 2020.
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A GPCR negative feedback loop underlies efficient coding of external stimuli
Rotem Ruach, Shai Yellinek, Eyal Itskovits, Alon Zaslaver
bioRxiv 2020.12.14.422627; doi: https://doi.org/10.1101/2020.12.14.422627
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A GPCR negative feedback loop underlies efficient coding of external stimuli
Rotem Ruach, Shai Yellinek, Eyal Itskovits, Alon Zaslaver
bioRxiv 2020.12.14.422627; doi: https://doi.org/10.1101/2020.12.14.422627

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