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A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli

Efficient navigation based on chemical cues is an essential feature shared by all animals. These cues may be encountered in complex spatiotemporal patterns and with orders of magnitude varying intensities. Nevertheless, sensory neurons accurately extract the relevant information from such perplexing...

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Autores principales: Ruach, Rotem, Yellinek, Shai, Itskovits, Eyal, Deshe, Noa, Eliezer, Yifat, Bokman, Eduard, Zaslaver, Alon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9476886/
https://www.ncbi.nlm.nih.gov/pubmed/36106925
http://dx.doi.org/10.15252/msb.202110514
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author Ruach, Rotem
Yellinek, Shai
Itskovits, Eyal
Deshe, Noa
Eliezer, Yifat
Bokman, Eduard
Zaslaver, Alon
author_facet Ruach, Rotem
Yellinek, Shai
Itskovits, Eyal
Deshe, Noa
Eliezer, Yifat
Bokman, Eduard
Zaslaver, Alon
author_sort Ruach, Rotem
collection PubMed
description Efficient navigation based on chemical cues is an essential feature shared by all animals. These cues may be encountered in complex spatiotemporal 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 Caenorhabditis elegans animals 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 G‐protein‐coupled receptor (GPCR) signaling pathway in which TAX‐6/Calcineurin plays a key role in mediating the feedback inhibition. This negative feedback 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 explains the fine neural dynamics of both wild‐type 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 general solution for efficient cell‐autonomous coding of external stimuli.
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spelling pubmed-94768862022-09-21 A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli Ruach, Rotem Yellinek, Shai Itskovits, Eyal Deshe, Noa Eliezer, Yifat Bokman, Eduard Zaslaver, Alon Mol Syst Biol Articles Efficient navigation based on chemical cues is an essential feature shared by all animals. These cues may be encountered in complex spatiotemporal 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 Caenorhabditis elegans animals 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 G‐protein‐coupled receptor (GPCR) signaling pathway in which TAX‐6/Calcineurin plays a key role in mediating the feedback inhibition. This negative feedback 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 explains the fine neural dynamics of both wild‐type 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 general solution for efficient cell‐autonomous coding of external stimuli. John Wiley and Sons Inc. 2022-09-15 /pmc/articles/PMC9476886/ /pubmed/36106925 http://dx.doi.org/10.15252/msb.202110514 Text en © 2022 The Authors. Published under the terms of the CC BY 4.0 license. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Ruach, Rotem
Yellinek, Shai
Itskovits, Eyal
Deshe, Noa
Eliezer, Yifat
Bokman, Eduard
Zaslaver, Alon
A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli
title A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli
title_full A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli
title_fullStr A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli
title_full_unstemmed A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli
title_short A negative feedback loop in the GPCR pathway underlies efficient coding of external stimuli
title_sort negative feedback loop in the gpcr pathway underlies efficient coding of external stimuli
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9476886/
https://www.ncbi.nlm.nih.gov/pubmed/36106925
http://dx.doi.org/10.15252/msb.202110514
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