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Humans use multi-objective control to regulate lateral foot placement when walking

A fundamental question in human motor neuroscience is to determine how the nervous system generates goal-directed movements despite inherent physiological noise and redundancy. Walking exhibits considerable variability and equifinality of task solutions. Existing models of bipedal walking do not yet...

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Detalles Bibliográficos
Autores principales: Dingwell, Jonathan B., Cusumano, Joseph P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6422313/
https://www.ncbi.nlm.nih.gov/pubmed/30840620
http://dx.doi.org/10.1371/journal.pcbi.1006850
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author Dingwell, Jonathan B.
Cusumano, Joseph P.
author_facet Dingwell, Jonathan B.
Cusumano, Joseph P.
author_sort Dingwell, Jonathan B.
collection PubMed
description A fundamental question in human motor neuroscience is to determine how the nervous system generates goal-directed movements despite inherent physiological noise and redundancy. Walking exhibits considerable variability and equifinality of task solutions. Existing models of bipedal walking do not yet achieve both continuous dynamic balance control and the equifinality of foot placement humans exhibit. Appropriate computational models are critical to disambiguate the numerous possibilities of how to regulate stepping movements to achieve different walking goals. Here, we extend a theoretical and computational Goal Equivalent Manifold (GEM) framework to generate predictive models, each posing a different experimentally testable hypothesis. These models regulate stepping movements to achieve any of three hypothesized goals, either alone or in combination: maintain lateral position, maintain lateral speed or “heading”, and/or maintain step width. We compared model predictions against human experimental data. Uni-objective control models demonstrated clear redundancy between stepping variables, but could not replicate human stepping dynamics. Most multi-objective control models that balanced maintaining two of the three hypothesized goals also failed to replicate human stepping dynamics. However, multi-objective models that strongly prioritized regulating step width over lateral position did successfully replicate all of the relevant step-to-step dynamics observed in humans. Independent analyses confirmed this control was consistent with linear error correction and replicated step-to-step dynamics of individual foot placements. Thus, the regulation of lateral stepping movements is inherently multi-objective and balances task-specific trade-offs between competing task goals. To determine how people walk in their environment requires understanding both walking biomechanics and how the nervous system regulates movements from step-to-step. Analogous to mechanical “templates” of locomotor biomechanics, our models serve as “control templates” for how humans regulate stepping movements from each step to the next. These control templates are symbiotic with well-established mechanical templates, providing complimentary insights into walking regulation.
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spelling pubmed-64223132019-04-01 Humans use multi-objective control to regulate lateral foot placement when walking Dingwell, Jonathan B. Cusumano, Joseph P. PLoS Comput Biol Research Article A fundamental question in human motor neuroscience is to determine how the nervous system generates goal-directed movements despite inherent physiological noise and redundancy. Walking exhibits considerable variability and equifinality of task solutions. Existing models of bipedal walking do not yet achieve both continuous dynamic balance control and the equifinality of foot placement humans exhibit. Appropriate computational models are critical to disambiguate the numerous possibilities of how to regulate stepping movements to achieve different walking goals. Here, we extend a theoretical and computational Goal Equivalent Manifold (GEM) framework to generate predictive models, each posing a different experimentally testable hypothesis. These models regulate stepping movements to achieve any of three hypothesized goals, either alone or in combination: maintain lateral position, maintain lateral speed or “heading”, and/or maintain step width. We compared model predictions against human experimental data. Uni-objective control models demonstrated clear redundancy between stepping variables, but could not replicate human stepping dynamics. Most multi-objective control models that balanced maintaining two of the three hypothesized goals also failed to replicate human stepping dynamics. However, multi-objective models that strongly prioritized regulating step width over lateral position did successfully replicate all of the relevant step-to-step dynamics observed in humans. Independent analyses confirmed this control was consistent with linear error correction and replicated step-to-step dynamics of individual foot placements. Thus, the regulation of lateral stepping movements is inherently multi-objective and balances task-specific trade-offs between competing task goals. To determine how people walk in their environment requires understanding both walking biomechanics and how the nervous system regulates movements from step-to-step. Analogous to mechanical “templates” of locomotor biomechanics, our models serve as “control templates” for how humans regulate stepping movements from each step to the next. These control templates are symbiotic with well-established mechanical templates, providing complimentary insights into walking regulation. Public Library of Science 2019-03-06 /pmc/articles/PMC6422313/ /pubmed/30840620 http://dx.doi.org/10.1371/journal.pcbi.1006850 Text en © 2019 Dingwell, Cusumano 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
Dingwell, Jonathan B.
Cusumano, Joseph P.
Humans use multi-objective control to regulate lateral foot placement when walking
title Humans use multi-objective control to regulate lateral foot placement when walking
title_full Humans use multi-objective control to regulate lateral foot placement when walking
title_fullStr Humans use multi-objective control to regulate lateral foot placement when walking
title_full_unstemmed Humans use multi-objective control to regulate lateral foot placement when walking
title_short Humans use multi-objective control to regulate lateral foot placement when walking
title_sort humans use multi-objective control to regulate lateral foot placement when walking
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6422313/
https://www.ncbi.nlm.nih.gov/pubmed/30840620
http://dx.doi.org/10.1371/journal.pcbi.1006850
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