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Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function

INTRODUCTION: Planarians belong to an evolutionarily early group of organisms that possess a central nervous system including a well-organized brain with a simple architecture but many types of neurons. Planarians display a number of behaviors, such as phototaxis and thermotaxis, in response to exte...

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Autores principales: Inoue, Takeshi, Hoshino, Hajime, Yamashita, Taiga, Shimoyama, Seira, Agata, Kiyokazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657317/
https://www.ncbi.nlm.nih.gov/pubmed/26605052
http://dx.doi.org/10.1186/s40851-014-0010-z
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author Inoue, Takeshi
Hoshino, Hajime
Yamashita, Taiga
Shimoyama, Seira
Agata, Kiyokazu
author_facet Inoue, Takeshi
Hoshino, Hajime
Yamashita, Taiga
Shimoyama, Seira
Agata, Kiyokazu
author_sort Inoue, Takeshi
collection PubMed
description INTRODUCTION: Planarians belong to an evolutionarily early group of organisms that possess a central nervous system including a well-organized brain with a simple architecture but many types of neurons. Planarians display a number of behaviors, such as phototaxis and thermotaxis, in response to external stimuli, and it has been shown that various molecules and neural pathways in the brain are involved in controlling these behaviors. However, due to the lack of combinatorial assay methods, it remains obscure whether planarians possess higher brain functions, including integration in the brain, in which multiple signals coming from outside are coordinated and used in determining behavioral strategies. RESULTS: In the present study, we designed chemotaxis and thigmotaxis/kinesis tracking assays to measure several planarian behaviors in addition to those measured by phototaxis and thermotaxis assays previously established by our group, and used these tests to analyze planarian chemotactic and thigmotactic/kinetic behaviors. We found that headless planarian body fragments and planarians that had specifically lost neural activity following regeneration-dependent conditional gene knockdown (Readyknock) of synaptotagmin in the brain lost both chemotactic and thigmotactic behaviors, suggesting that neural activity in the brain is required for the planarian's chemotactic and thigmotactic behaviors. Furthermore, we compared the strength of phototaxis, chemotaxis, thigmotaxis/kinesis, and thermotaxis by presenting simultaneous binary stimuli to planarians. We found that planarians showed a clear order of predominance of these behaviors. For example, when planarians were simultaneously exposed to 400 lux of light and a chemoattractant, they showed chemoattractive behavior irrespective of the direction of the light source, although exposure to light of this intensity alone induces evasive behavior away from the light source. In contrast, when the light intensity was increased to 800 or 1600 lux and the same dose of chemoattractant was presented, planarian behaviors were gradually shifted to negative phototaxis rather than chemoattraction. These results suggest that planarians may be capable of selecting behavioral strategies via the integration of discrete brain functions when exposed to multiple stimuli. CONCLUSIONS: The planarian brain processes external signals received through the respective sensory neurons, thereby resulting in the production of appropriate behaviors. In addition, planarians can adjust behavioral features in response to stimulus conditions by integrating multiple external signals in the brain. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-014-0010-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-46573172015-11-24 Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function Inoue, Takeshi Hoshino, Hajime Yamashita, Taiga Shimoyama, Seira Agata, Kiyokazu Zoological Lett Research Article INTRODUCTION: Planarians belong to an evolutionarily early group of organisms that possess a central nervous system including a well-organized brain with a simple architecture but many types of neurons. Planarians display a number of behaviors, such as phototaxis and thermotaxis, in response to external stimuli, and it has been shown that various molecules and neural pathways in the brain are involved in controlling these behaviors. However, due to the lack of combinatorial assay methods, it remains obscure whether planarians possess higher brain functions, including integration in the brain, in which multiple signals coming from outside are coordinated and used in determining behavioral strategies. RESULTS: In the present study, we designed chemotaxis and thigmotaxis/kinesis tracking assays to measure several planarian behaviors in addition to those measured by phototaxis and thermotaxis assays previously established by our group, and used these tests to analyze planarian chemotactic and thigmotactic/kinetic behaviors. We found that headless planarian body fragments and planarians that had specifically lost neural activity following regeneration-dependent conditional gene knockdown (Readyknock) of synaptotagmin in the brain lost both chemotactic and thigmotactic behaviors, suggesting that neural activity in the brain is required for the planarian's chemotactic and thigmotactic behaviors. Furthermore, we compared the strength of phototaxis, chemotaxis, thigmotaxis/kinesis, and thermotaxis by presenting simultaneous binary stimuli to planarians. We found that planarians showed a clear order of predominance of these behaviors. For example, when planarians were simultaneously exposed to 400 lux of light and a chemoattractant, they showed chemoattractive behavior irrespective of the direction of the light source, although exposure to light of this intensity alone induces evasive behavior away from the light source. In contrast, when the light intensity was increased to 800 or 1600 lux and the same dose of chemoattractant was presented, planarian behaviors were gradually shifted to negative phototaxis rather than chemoattraction. These results suggest that planarians may be capable of selecting behavioral strategies via the integration of discrete brain functions when exposed to multiple stimuli. CONCLUSIONS: The planarian brain processes external signals received through the respective sensory neurons, thereby resulting in the production of appropriate behaviors. In addition, planarians can adjust behavioral features in response to stimulus conditions by integrating multiple external signals in the brain. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-014-0010-z) contains supplementary material, which is available to authorized users. BioMed Central 2015-02-01 /pmc/articles/PMC4657317/ /pubmed/26605052 http://dx.doi.org/10.1186/s40851-014-0010-z Text en © Inoue et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Inoue, Takeshi
Hoshino, Hajime
Yamashita, Taiga
Shimoyama, Seira
Agata, Kiyokazu
Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
title Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
title_full Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
title_fullStr Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
title_full_unstemmed Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
title_short Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
title_sort planarian shows decision-making behavior in response to multiple stimuli by integrative brain function
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4657317/
https://www.ncbi.nlm.nih.gov/pubmed/26605052
http://dx.doi.org/10.1186/s40851-014-0010-z
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