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Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans

BACKGROUND: Annotation of cell identity is an essential process in neuroscience that allows comparison of cells, including that of neural activities across different animals. In Caenorhabditis elegans, although unique identities have been assigned to all neurons, the number of annotatable neurons in...

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Autores principales: Toyoshima, Yu, Wu, Stephen, Kanamori, Manami, Sato, Hirofumi, Jang, Moon Sun, Oe, Suzu, Murakami, Yuko, Teramoto, Takayuki, Park, Chanhyun, Iwasaki, Yuishi, Ishihara, Takeshi, Yoshida, Ryo, Iino, Yuichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7081613/
https://www.ncbi.nlm.nih.gov/pubmed/32188430
http://dx.doi.org/10.1186/s12915-020-0745-2
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author Toyoshima, Yu
Wu, Stephen
Kanamori, Manami
Sato, Hirofumi
Jang, Moon Sun
Oe, Suzu
Murakami, Yuko
Teramoto, Takayuki
Park, Chanhyun
Iwasaki, Yuishi
Ishihara, Takeshi
Yoshida, Ryo
Iino, Yuichi
author_facet Toyoshima, Yu
Wu, Stephen
Kanamori, Manami
Sato, Hirofumi
Jang, Moon Sun
Oe, Suzu
Murakami, Yuko
Teramoto, Takayuki
Park, Chanhyun
Iwasaki, Yuishi
Ishihara, Takeshi
Yoshida, Ryo
Iino, Yuichi
author_sort Toyoshima, Yu
collection PubMed
description BACKGROUND: Annotation of cell identity is an essential process in neuroscience that allows comparison of cells, including that of neural activities across different animals. In Caenorhabditis elegans, although unique identities have been assigned to all neurons, the number of annotatable neurons in an intact animal has been limited due to the lack of quantitative information on the location and identity of neurons. RESULTS: Here, we present a dataset that facilitates the annotation of neuronal identities, and demonstrate its application in a comprehensive analysis of whole-brain imaging. We systematically identified neurons in the head region of 311 adult worms using 35 cell-specific promoters and created a dataset of the expression patterns and the positions of the neurons. We found large positional variations that illustrated the difficulty of the annotation task. We investigated multiple combinations of cell-specific promoters driving distinct fluorescence and generated optimal strains for the annotation of most head neurons in an animal. We also developed an automatic annotation method with human interaction functionality that facilitates annotations needed for whole-brain imaging. CONCLUSION: Our neuron ID dataset and optimal fluorescent strains enable the annotation of most neurons in the head region of adult C. elegans, both in full-automated fashion and a semi-automated version that includes human interaction functionalities. Our method can potentially be applied to model species used in research other than C. elegans, where the number of available cell-type-specific promoters and their variety will be an important consideration.
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spelling pubmed-70816132020-03-23 Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans Toyoshima, Yu Wu, Stephen Kanamori, Manami Sato, Hirofumi Jang, Moon Sun Oe, Suzu Murakami, Yuko Teramoto, Takayuki Park, Chanhyun Iwasaki, Yuishi Ishihara, Takeshi Yoshida, Ryo Iino, Yuichi BMC Biol Methodology Article BACKGROUND: Annotation of cell identity is an essential process in neuroscience that allows comparison of cells, including that of neural activities across different animals. In Caenorhabditis elegans, although unique identities have been assigned to all neurons, the number of annotatable neurons in an intact animal has been limited due to the lack of quantitative information on the location and identity of neurons. RESULTS: Here, we present a dataset that facilitates the annotation of neuronal identities, and demonstrate its application in a comprehensive analysis of whole-brain imaging. We systematically identified neurons in the head region of 311 adult worms using 35 cell-specific promoters and created a dataset of the expression patterns and the positions of the neurons. We found large positional variations that illustrated the difficulty of the annotation task. We investigated multiple combinations of cell-specific promoters driving distinct fluorescence and generated optimal strains for the annotation of most head neurons in an animal. We also developed an automatic annotation method with human interaction functionality that facilitates annotations needed for whole-brain imaging. CONCLUSION: Our neuron ID dataset and optimal fluorescent strains enable the annotation of most neurons in the head region of adult C. elegans, both in full-automated fashion and a semi-automated version that includes human interaction functionalities. Our method can potentially be applied to model species used in research other than C. elegans, where the number of available cell-type-specific promoters and their variety will be an important consideration. BioMed Central 2020-03-19 /pmc/articles/PMC7081613/ /pubmed/32188430 http://dx.doi.org/10.1186/s12915-020-0745-2 Text en © The Author(s). 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Methodology Article
Toyoshima, Yu
Wu, Stephen
Kanamori, Manami
Sato, Hirofumi
Jang, Moon Sun
Oe, Suzu
Murakami, Yuko
Teramoto, Takayuki
Park, Chanhyun
Iwasaki, Yuishi
Ishihara, Takeshi
Yoshida, Ryo
Iino, Yuichi
Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans
title Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans
title_full Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans
title_fullStr Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans
title_full_unstemmed Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans
title_short Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans
title_sort neuron id dataset facilitates neuronal annotation for whole-brain activity imaging of c. elegans
topic Methodology Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7081613/
https://www.ncbi.nlm.nih.gov/pubmed/32188430
http://dx.doi.org/10.1186/s12915-020-0745-2
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