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Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans

C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body. Although central pattern generators (CPGs) are typically involved in animal locomotion, their presence in C. elegans has been questioned, mainly because there has been no evident circui...

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Autores principales: Olivares, Erick O., Izquierdo, Eduardo J., Beer, Randall D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6145852/
https://www.ncbi.nlm.nih.gov/pubmed/30294702
http://dx.doi.org/10.1162/netn_a_00036
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author Olivares, Erick O.
Izquierdo, Eduardo J.
Beer, Randall D.
author_facet Olivares, Erick O.
Izquierdo, Eduardo J.
Beer, Randall D.
author_sort Olivares, Erick O.
collection PubMed
description C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body. Although central pattern generators (CPGs) are typically involved in animal locomotion, their presence in C. elegans has been questioned, mainly because there has been no evident circuit that supports intrinsic network oscillations. With a fully reconstructed connectome, the question of whether it is possible to have a CPG in the ventral nerve cord (VNC) of C. elegans can be answered through computational models. We modeled a repeating neural unit based on segmentation analysis of the connectome. We then used an evolutionary algorithm to determine the unknown physiological parameters of each neuron so as to match the features of the neural traces of the worm during forward and backward locomotion. We performed 1,000 evolutionary runs and consistently found configurations of the neural circuit that produced oscillations matching the main characteristic observed in experimental recordings. In addition to providing an existence proof for the possibility of a CPG in the VNC, we suggest a series of testable hypotheses about its operation. More generally, we show the feasibility and fruitfulness of a methodology to study behavior based on a connectome, in the absence of complete neurophysiological details.
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spelling pubmed-61458522018-10-05 Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans Olivares, Erick O. Izquierdo, Eduardo J. Beer, Randall D. Netw Neurosci Research C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body. Although central pattern generators (CPGs) are typically involved in animal locomotion, their presence in C. elegans has been questioned, mainly because there has been no evident circuit that supports intrinsic network oscillations. With a fully reconstructed connectome, the question of whether it is possible to have a CPG in the ventral nerve cord (VNC) of C. elegans can be answered through computational models. We modeled a repeating neural unit based on segmentation analysis of the connectome. We then used an evolutionary algorithm to determine the unknown physiological parameters of each neuron so as to match the features of the neural traces of the worm during forward and backward locomotion. We performed 1,000 evolutionary runs and consistently found configurations of the neural circuit that produced oscillations matching the main characteristic observed in experimental recordings. In addition to providing an existence proof for the possibility of a CPG in the VNC, we suggest a series of testable hypotheses about its operation. More generally, we show the feasibility and fruitfulness of a methodology to study behavior based on a connectome, in the absence of complete neurophysiological details. MIT Press 2018-09-01 /pmc/articles/PMC6145852/ /pubmed/30294702 http://dx.doi.org/10.1162/netn_a_00036 Text en © 2017 Massachusetts Institute of Technology http://creativecommons.org/licenses/by/4.0 This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Olivares, Erick O.
Izquierdo, Eduardo J.
Beer, Randall D.
Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans
title Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans
title_full Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans
title_fullStr Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans
title_full_unstemmed Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans
title_short Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans
title_sort potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in caenorhabditis elegans
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6145852/
https://www.ncbi.nlm.nih.gov/pubmed/30294702
http://dx.doi.org/10.1162/netn_a_00036
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