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Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD

C. elegans neuronal system constitutes the ideal framework for studying simple, yet realistic, neuronal activity, since the whole nervous system is fully characterized with respect to the exact number of neurons and the neuronal connections. Most recent efforts are devoted to investigate and clarify...

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Autores principales: Nicoletti, Martina, Loppini, Alessandro, Chiodo, Letizia, Folli, Viola, Ruocco, Giancarlo, Filippi, Simonetta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6602206/
https://www.ncbi.nlm.nih.gov/pubmed/31260485
http://dx.doi.org/10.1371/journal.pone.0218738
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author Nicoletti, Martina
Loppini, Alessandro
Chiodo, Letizia
Folli, Viola
Ruocco, Giancarlo
Filippi, Simonetta
author_facet Nicoletti, Martina
Loppini, Alessandro
Chiodo, Letizia
Folli, Viola
Ruocco, Giancarlo
Filippi, Simonetta
author_sort Nicoletti, Martina
collection PubMed
description C. elegans neuronal system constitutes the ideal framework for studying simple, yet realistic, neuronal activity, since the whole nervous system is fully characterized with respect to the exact number of neurons and the neuronal connections. Most recent efforts are devoted to investigate and clarify the signal processing and functional connectivity, which are at the basis of sensing mechanisms, signal transmission, and motor control. In this framework, a refined modelof whole neuron dynamics constitutes a key ingredient to describe the electrophysiological processes, both at thecellular and at the network scale. In this work, we present Hodgkin-Huxley-based models of ion channels dynamics black, built on data available both from C. elegans and from other organisms, expressing homologous channels. We combine these channel models to simulate the electrical activity oftwo among the most studied neurons in C. elegans, which display prototypical dynamics of neuronal activation, the chemosensory AWC(ON) and the motor neuron RMD. Our model properly describes the regenerative responses of the two cells. We analyze in detail the role of ion currents, both in wild type and in in silico knockout neurons. Moreover, we specifically investigate the behavior of RMD, identifying a heterogeneous dynamical response which includes bistable regimes and sustained oscillations. We are able to assess the critical role of T-type calcium currents, carried by CCA-1 channels, and leakage currents in the regulation of RMD response. Overall, our results provide new insights in the activity of key C. elegans neurons. The developed mathematical framework constitute a basis for single-cell and neuronal networks analyses, opening new scenarios in the in silico modeling of C. elegans neuronal system.
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spelling pubmed-66022062019-07-12 Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD Nicoletti, Martina Loppini, Alessandro Chiodo, Letizia Folli, Viola Ruocco, Giancarlo Filippi, Simonetta PLoS One Research Article C. elegans neuronal system constitutes the ideal framework for studying simple, yet realistic, neuronal activity, since the whole nervous system is fully characterized with respect to the exact number of neurons and the neuronal connections. Most recent efforts are devoted to investigate and clarify the signal processing and functional connectivity, which are at the basis of sensing mechanisms, signal transmission, and motor control. In this framework, a refined modelof whole neuron dynamics constitutes a key ingredient to describe the electrophysiological processes, both at thecellular and at the network scale. In this work, we present Hodgkin-Huxley-based models of ion channels dynamics black, built on data available both from C. elegans and from other organisms, expressing homologous channels. We combine these channel models to simulate the electrical activity oftwo among the most studied neurons in C. elegans, which display prototypical dynamics of neuronal activation, the chemosensory AWC(ON) and the motor neuron RMD. Our model properly describes the regenerative responses of the two cells. We analyze in detail the role of ion currents, both in wild type and in in silico knockout neurons. Moreover, we specifically investigate the behavior of RMD, identifying a heterogeneous dynamical response which includes bistable regimes and sustained oscillations. We are able to assess the critical role of T-type calcium currents, carried by CCA-1 channels, and leakage currents in the regulation of RMD response. Overall, our results provide new insights in the activity of key C. elegans neurons. The developed mathematical framework constitute a basis for single-cell and neuronal networks analyses, opening new scenarios in the in silico modeling of C. elegans neuronal system. Public Library of Science 2019-07-01 /pmc/articles/PMC6602206/ /pubmed/31260485 http://dx.doi.org/10.1371/journal.pone.0218738 Text en © 2019 Nicoletti et al http://creativecommons.org/licenses/by/4.0/ 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 author and source are credited.
spellingShingle Research Article
Nicoletti, Martina
Loppini, Alessandro
Chiodo, Letizia
Folli, Viola
Ruocco, Giancarlo
Filippi, Simonetta
Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD
title Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD
title_full Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD
title_fullStr Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD
title_full_unstemmed Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD
title_short Biophysical modeling of C. elegans neurons: Single ion currents and whole-cell dynamics of AWC(on) and RMD
title_sort biophysical modeling of c. elegans neurons: single ion currents and whole-cell dynamics of awc(on) and rmd
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6602206/
https://www.ncbi.nlm.nih.gov/pubmed/31260485
http://dx.doi.org/10.1371/journal.pone.0218738
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