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Modelling the mechanics of exploration in larval Drosophila

The Drosophila larva executes a stereotypical exploratory routine that appears to consist of stochastic alternation between straight peristaltic crawling and reorientation events through lateral bending. We present a model of larval mechanics for axial and transverse motion over a planar substrate,...

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Autores principales: Loveless, Jane, Lagogiannis, Konstantinos, Webb, Barbara
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6636753/
https://www.ncbi.nlm.nih.gov/pubmed/31276489
http://dx.doi.org/10.1371/journal.pcbi.1006635
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author Loveless, Jane
Lagogiannis, Konstantinos
Webb, Barbara
author_facet Loveless, Jane
Lagogiannis, Konstantinos
Webb, Barbara
author_sort Loveless, Jane
collection PubMed
description The Drosophila larva executes a stereotypical exploratory routine that appears to consist of stochastic alternation between straight peristaltic crawling and reorientation events through lateral bending. We present a model of larval mechanics for axial and transverse motion over a planar substrate, and use it to develop a simple, reflexive neuromuscular model from physical principles. The mechanical model represents the midline of the larva as a set of point masses which interact with each other via damped translational and torsional springs, and with the environment via sliding friction forces. The neuromuscular model consists of: 1. segmentally localised reflexes that amplify axial compression in order to counteract frictive energy losses, and 2. long-range mutual inhibition between reflexes in distant segments, enabling overall motion of the model larva relative to its substrate. In the absence of damping and driving, the mechanical model produces axial travelling waves, lateral oscillations, and unpredictable, chaotic deformations. The neuromuscular model counteracts friction to recover these motion patterns, giving rise to forward and backward peristalsis in addition to turning. Our model produces spontaneous exploration, even though the nervous system has no intrinsic pattern generating or decision making ability, and neither senses nor drives bending motions. Ultimately, our model suggests a novel view of larval exploration as a deterministic superdiffusion process which is mechanistically grounded in the chaotic mechanics of the body. We discuss how this may provide new interpretations for existing observations at the level of tissue-scale activity patterns and neural circuitry, and provide some experimental predictions that would test the extent to which the mechanisms we present translate to the real larva.
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spelling pubmed-66367532019-07-25 Modelling the mechanics of exploration in larval Drosophila Loveless, Jane Lagogiannis, Konstantinos Webb, Barbara PLoS Comput Biol Research Article The Drosophila larva executes a stereotypical exploratory routine that appears to consist of stochastic alternation between straight peristaltic crawling and reorientation events through lateral bending. We present a model of larval mechanics for axial and transverse motion over a planar substrate, and use it to develop a simple, reflexive neuromuscular model from physical principles. The mechanical model represents the midline of the larva as a set of point masses which interact with each other via damped translational and torsional springs, and with the environment via sliding friction forces. The neuromuscular model consists of: 1. segmentally localised reflexes that amplify axial compression in order to counteract frictive energy losses, and 2. long-range mutual inhibition between reflexes in distant segments, enabling overall motion of the model larva relative to its substrate. In the absence of damping and driving, the mechanical model produces axial travelling waves, lateral oscillations, and unpredictable, chaotic deformations. The neuromuscular model counteracts friction to recover these motion patterns, giving rise to forward and backward peristalsis in addition to turning. Our model produces spontaneous exploration, even though the nervous system has no intrinsic pattern generating or decision making ability, and neither senses nor drives bending motions. Ultimately, our model suggests a novel view of larval exploration as a deterministic superdiffusion process which is mechanistically grounded in the chaotic mechanics of the body. We discuss how this may provide new interpretations for existing observations at the level of tissue-scale activity patterns and neural circuitry, and provide some experimental predictions that would test the extent to which the mechanisms we present translate to the real larva. Public Library of Science 2019-07-05 /pmc/articles/PMC6636753/ /pubmed/31276489 http://dx.doi.org/10.1371/journal.pcbi.1006635 Text en © 2019 Loveless 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
Loveless, Jane
Lagogiannis, Konstantinos
Webb, Barbara
Modelling the mechanics of exploration in larval Drosophila
title Modelling the mechanics of exploration in larval Drosophila
title_full Modelling the mechanics of exploration in larval Drosophila
title_fullStr Modelling the mechanics of exploration in larval Drosophila
title_full_unstemmed Modelling the mechanics of exploration in larval Drosophila
title_short Modelling the mechanics of exploration in larval Drosophila
title_sort modelling the mechanics of exploration in larval drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6636753/
https://www.ncbi.nlm.nih.gov/pubmed/31276489
http://dx.doi.org/10.1371/journal.pcbi.1006635
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