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Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation
A conventional understanding of perception assigns sensory organs the role of capturing the environment. Better sensors result in more accurate encoding of stimuli, allowing for cognitive processing downstream. Here we show that plasticity in sensory neurons mediates a behavioral switch in C. elegan...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8429449/ https://www.ncbi.nlm.nih.gov/pubmed/34504291 http://dx.doi.org/10.1038/s42003-021-02561-9 |
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author | Dekkers, Martijn P. J. Salfelder, Felix Sanders, Tom Umuerri, Oluwatoroti Cohen, Netta Jansen, Gert |
author_facet | Dekkers, Martijn P. J. Salfelder, Felix Sanders, Tom Umuerri, Oluwatoroti Cohen, Netta Jansen, Gert |
author_sort | Dekkers, Martijn P. J. |
collection | PubMed |
description | A conventional understanding of perception assigns sensory organs the role of capturing the environment. Better sensors result in more accurate encoding of stimuli, allowing for cognitive processing downstream. Here we show that plasticity in sensory neurons mediates a behavioral switch in C. elegans between attraction to NaCl in naïve animals and avoidance of NaCl in preconditioned animals, called gustatory plasticity. Ca(2+) imaging in ASE and ASH NaCl sensing neurons reveals multiple cell-autonomous and distributed circuit adaptation mechanisms. A computational model quantitatively accounts for observed behaviors and reveals roles for sensory neurons in the control and modulation of motor behaviors, decision making and navigational strategy. Sensory adaptation dynamically alters the encoding of the environment. Rather than encoding the stimulus directly, therefore, we propose that these C. elegans sensors dynamically encode a context-dependent value of the stimulus. Our results demonstrate how adaptive sensory computation can directly control an animal’s behavioral state. |
format | Online Article Text |
id | pubmed-8429449 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-84294492021-09-22 Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation Dekkers, Martijn P. J. Salfelder, Felix Sanders, Tom Umuerri, Oluwatoroti Cohen, Netta Jansen, Gert Commun Biol Article A conventional understanding of perception assigns sensory organs the role of capturing the environment. Better sensors result in more accurate encoding of stimuli, allowing for cognitive processing downstream. Here we show that plasticity in sensory neurons mediates a behavioral switch in C. elegans between attraction to NaCl in naïve animals and avoidance of NaCl in preconditioned animals, called gustatory plasticity. Ca(2+) imaging in ASE and ASH NaCl sensing neurons reveals multiple cell-autonomous and distributed circuit adaptation mechanisms. A computational model quantitatively accounts for observed behaviors and reveals roles for sensory neurons in the control and modulation of motor behaviors, decision making and navigational strategy. Sensory adaptation dynamically alters the encoding of the environment. Rather than encoding the stimulus directly, therefore, we propose that these C. elegans sensors dynamically encode a context-dependent value of the stimulus. Our results demonstrate how adaptive sensory computation can directly control an animal’s behavioral state. Nature Publishing Group UK 2021-09-09 /pmc/articles/PMC8429449/ /pubmed/34504291 http://dx.doi.org/10.1038/s42003-021-02561-9 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Dekkers, Martijn P. J. Salfelder, Felix Sanders, Tom Umuerri, Oluwatoroti Cohen, Netta Jansen, Gert Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation |
title | Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation |
title_full | Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation |
title_fullStr | Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation |
title_full_unstemmed | Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation |
title_short | Plasticity in gustatory and nociceptive neurons controls decision making in C. elegans salt navigation |
title_sort | plasticity in gustatory and nociceptive neurons controls decision making in c. elegans salt navigation |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8429449/ https://www.ncbi.nlm.nih.gov/pubmed/34504291 http://dx.doi.org/10.1038/s42003-021-02561-9 |
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