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Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron

How neurons are capable of decoding stimulus intensity and translate this information into complex behavioral outputs is poorly defined. Here, we demonstrate that the C. elegans interneuron AIB regulates two types of behaviors: reversal initiation and feeding suppression in response to different con...

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Autores principales: Zou, Wenjuan, Fu, Jiajun, Zhang, Haining, Du, Kang, Huang, Wenming, Yu, Junwei, Li, Shitian, Fan, Yuedan, Baylis, Howard A., Gao, Shangbang, Xiao, Rui, Ji, Wei, Kang, Lijun, Xu, Tao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6193023/
https://www.ncbi.nlm.nih.gov/pubmed/30333484
http://dx.doi.org/10.1038/s41467-018-06819-5
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author Zou, Wenjuan
Fu, Jiajun
Zhang, Haining
Du, Kang
Huang, Wenming
Yu, Junwei
Li, Shitian
Fan, Yuedan
Baylis, Howard A.
Gao, Shangbang
Xiao, Rui
Ji, Wei
Kang, Lijun
Xu, Tao
author_facet Zou, Wenjuan
Fu, Jiajun
Zhang, Haining
Du, Kang
Huang, Wenming
Yu, Junwei
Li, Shitian
Fan, Yuedan
Baylis, Howard A.
Gao, Shangbang
Xiao, Rui
Ji, Wei
Kang, Lijun
Xu, Tao
author_sort Zou, Wenjuan
collection PubMed
description How neurons are capable of decoding stimulus intensity and translate this information into complex behavioral outputs is poorly defined. Here, we demonstrate that the C. elegans interneuron AIB regulates two types of behaviors: reversal initiation and feeding suppression in response to different concentrations of quinine. Low concentrations of quinine are decoded in AIB by a low-threshold, fast-inactivation glutamate receptor GLR-1 and translated into reversal initiation. In contrast, high concentrations of quinine are decoded by a high-threshold, slow-inactivation glutamate receptor GLR-5 in AIB. After activation, GLR-5 evokes sustained Ca(2+) release from the inositol 1,4,5-trisphosphate (IP(3))-sensitive Ca(2+) stores and triggers neuropeptide secretion, which in turn activates the downstream neuron RIM and inhibits feeding. Our results reveal that distinct signal patterns in a single interneuron AIB can encode differential behavioral outputs depending on the stimulus intensity, thus highlighting the importance of functional mapping of information propagation at the single-neuron level during connectome construction.
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spelling pubmed-61930232018-10-19 Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron Zou, Wenjuan Fu, Jiajun Zhang, Haining Du, Kang Huang, Wenming Yu, Junwei Li, Shitian Fan, Yuedan Baylis, Howard A. Gao, Shangbang Xiao, Rui Ji, Wei Kang, Lijun Xu, Tao Nat Commun Article How neurons are capable of decoding stimulus intensity and translate this information into complex behavioral outputs is poorly defined. Here, we demonstrate that the C. elegans interneuron AIB regulates two types of behaviors: reversal initiation and feeding suppression in response to different concentrations of quinine. Low concentrations of quinine are decoded in AIB by a low-threshold, fast-inactivation glutamate receptor GLR-1 and translated into reversal initiation. In contrast, high concentrations of quinine are decoded by a high-threshold, slow-inactivation glutamate receptor GLR-5 in AIB. After activation, GLR-5 evokes sustained Ca(2+) release from the inositol 1,4,5-trisphosphate (IP(3))-sensitive Ca(2+) stores and triggers neuropeptide secretion, which in turn activates the downstream neuron RIM and inhibits feeding. Our results reveal that distinct signal patterns in a single interneuron AIB can encode differential behavioral outputs depending on the stimulus intensity, thus highlighting the importance of functional mapping of information propagation at the single-neuron level during connectome construction. Nature Publishing Group UK 2018-10-17 /pmc/articles/PMC6193023/ /pubmed/30333484 http://dx.doi.org/10.1038/s41467-018-06819-5 Text en © The Author(s) 2018 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/.
spellingShingle Article
Zou, Wenjuan
Fu, Jiajun
Zhang, Haining
Du, Kang
Huang, Wenming
Yu, Junwei
Li, Shitian
Fan, Yuedan
Baylis, Howard A.
Gao, Shangbang
Xiao, Rui
Ji, Wei
Kang, Lijun
Xu, Tao
Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
title Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
title_full Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
title_fullStr Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
title_full_unstemmed Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
title_short Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
title_sort decoding the intensity of sensory input by two glutamate receptors in one c. elegans interneuron
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6193023/
https://www.ncbi.nlm.nih.gov/pubmed/30333484
http://dx.doi.org/10.1038/s41467-018-06819-5
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