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Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans

BACKGROUND: Under experimental conditions, virtually all behaviors of Caenorhabditis elegans are achieved by combinations of simple locomotion, including forward, reversal movement, turning by deep body bending, and gradual shallow turning. To study how worms regulate these locomotion in response to...

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Autores principales: Wakabayashi, Tokumitsu, Sakata, Kazumi, Togashi, Takuya, Itoi, Hiroaki, Shinohe, Sayaka, Watanabe, Miwa, Shingai, Ryuzo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4653917/
https://www.ncbi.nlm.nih.gov/pubmed/26584677
http://dx.doi.org/10.1186/s12868-015-0220-0
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author Wakabayashi, Tokumitsu
Sakata, Kazumi
Togashi, Takuya
Itoi, Hiroaki
Shinohe, Sayaka
Watanabe, Miwa
Shingai, Ryuzo
author_facet Wakabayashi, Tokumitsu
Sakata, Kazumi
Togashi, Takuya
Itoi, Hiroaki
Shinohe, Sayaka
Watanabe, Miwa
Shingai, Ryuzo
author_sort Wakabayashi, Tokumitsu
collection PubMed
description BACKGROUND: Under experimental conditions, virtually all behaviors of Caenorhabditis elegans are achieved by combinations of simple locomotion, including forward, reversal movement, turning by deep body bending, and gradual shallow turning. To study how worms regulate these locomotion in response to sensory information, acidic pH avoidance behavior was analyzed by using worm tracking system. RESULTS: In the acidic pH avoidance, we characterized two types of behavioral maneuvers that have similar behavioral sequences in chemotaxis and thermotaxis. A stereotypic reversal-turn-forward sequence of reversal avoidance caused an abrupt random reorientation, and a shallow gradual turn in curve avoidance caused non-random reorientation in a less acidic direction to avoid the acidic pH. Our results suggest that these two maneuvers were each triggered by a distinct threshold pH. A simulation study using the two-distinct-threshold model reproduced the avoidance behavior of the real worm, supporting the presence of the threshold. Threshold pH for both reversal and curve avoidance was altered in mutants with reduced or enhanced glutamatergic signaling from acid-sensing neurons. CONCLUSIONS: C. elegans employ two behavioral maneuvers, reversal (klinokinesis) and curve (klinotaxis) to avoid acidic pH. Unlike the chemotaxis in C. elegans, reversal and curve avoidances were triggered by absolute pH rather than temporal derivative of stimulus concentration in this behavior. The pH threshold is different between reversal and curve avoidance. Mutant studies suggested that the difference results from a differential amount of glutamate released from ASH and ASK chemosensory neurons. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12868-015-0220-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-46539172015-11-21 Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans Wakabayashi, Tokumitsu Sakata, Kazumi Togashi, Takuya Itoi, Hiroaki Shinohe, Sayaka Watanabe, Miwa Shingai, Ryuzo BMC Neurosci Research Article BACKGROUND: Under experimental conditions, virtually all behaviors of Caenorhabditis elegans are achieved by combinations of simple locomotion, including forward, reversal movement, turning by deep body bending, and gradual shallow turning. To study how worms regulate these locomotion in response to sensory information, acidic pH avoidance behavior was analyzed by using worm tracking system. RESULTS: In the acidic pH avoidance, we characterized two types of behavioral maneuvers that have similar behavioral sequences in chemotaxis and thermotaxis. A stereotypic reversal-turn-forward sequence of reversal avoidance caused an abrupt random reorientation, and a shallow gradual turn in curve avoidance caused non-random reorientation in a less acidic direction to avoid the acidic pH. Our results suggest that these two maneuvers were each triggered by a distinct threshold pH. A simulation study using the two-distinct-threshold model reproduced the avoidance behavior of the real worm, supporting the presence of the threshold. Threshold pH for both reversal and curve avoidance was altered in mutants with reduced or enhanced glutamatergic signaling from acid-sensing neurons. CONCLUSIONS: C. elegans employ two behavioral maneuvers, reversal (klinokinesis) and curve (klinotaxis) to avoid acidic pH. Unlike the chemotaxis in C. elegans, reversal and curve avoidances were triggered by absolute pH rather than temporal derivative of stimulus concentration in this behavior. The pH threshold is different between reversal and curve avoidance. Mutant studies suggested that the difference results from a differential amount of glutamate released from ASH and ASK chemosensory neurons. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12868-015-0220-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-11-19 /pmc/articles/PMC4653917/ /pubmed/26584677 http://dx.doi.org/10.1186/s12868-015-0220-0 Text en © Wakabayashi et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Wakabayashi, Tokumitsu
Sakata, Kazumi
Togashi, Takuya
Itoi, Hiroaki
Shinohe, Sayaka
Watanabe, Miwa
Shingai, Ryuzo
Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans
title Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans
title_full Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans
title_fullStr Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans
title_full_unstemmed Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans
title_short Navigational choice between reversal and curve during acidic pH avoidance behavior in Caenorhabditis elegans
title_sort navigational choice between reversal and curve during acidic ph avoidance behavior in caenorhabditis elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4653917/
https://www.ncbi.nlm.nih.gov/pubmed/26584677
http://dx.doi.org/10.1186/s12868-015-0220-0
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