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

ABSTRACT: 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.

SUBMITTER: Dingwell JB

PROVIDER: S-EPMC6422313 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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

Dingwell Jonathan B JB Cusumano Joseph P JP

PLoS computational biology 20190306 3

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 ...[more]

PMID: 30840620

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Project description:BackgroundPersons with lower limb amputation often experience decreased physical capacity, difficulty walking, and increased fall risk. To either prevent or recover from a loss of balance, one must effectively regulate their stepping movements. It is therefore critical to identify how well persons with amputation regulate stepping. Here, we used a multi-objective control framework based on Goal Equivalent Manifolds to identify how persons with transtibial amputation (TTA) regulate lateral stepping while walking without and with lateral perturbations.Research questionWhen walking in destabilizing environments, do otherwise healthy persons with TTA exhibit greater difficulty regulating lateral stepping due to impaired control? Or do they instead continue to use similar strategies to regulate lateral stepping despite their amputation?MethodsEight persons with unilateral TTA and thirteen able-bodied (AB) controls walked in a virtual environment under three conditions: no perturbations, laterally oscillating visual field, and laterally oscillating treadmill platform. We analyzed step-to-step time series of step widths and absolute lateral body positions. We computed means, standard deviations and Detrended Fluctuation Analysis scaling exponents for each time series and computed how much participants directly corrected step width and position deviations at each step. We compared our results to computational predictions to identify the underlying causes of our experimental findings.ResultsAll participants exhibited significantly increased variability, decreased scaling exponents, and tighter direct control when perturbed. Simulations from our stepping regulation models revealed that people responded to the increased variability produced by the imposed perturbations by tightening their control of both step width and lateral position. Participants with TTA exhibited only a few minor differences from AB in lateral stepping regulation, even when subjected to substantially destabilizing lateral perturbations.SignificanceSince control of stepping is intrinsically multi-objective, developing effective interventions to reduce fall risk in persons with amputation will likely require strategies that adopt multi-objective approaches.

Project description:It is widely accepted that humans and animals minimize energetic cost while walking. While such principles predict average behavior, they do not explain the variability observed in walking. For robust performance, walking movements must adapt at each step, not just on average. Here, we propose an analytical framework that reconciles issues of optimality, redundancy, and stochasticity. For human treadmill walking, we defined a goal function to formulate a precise mathematical definition of one possible control strategy: maintain constant speed at each stride. We recorded stride times and stride lengths from healthy subjects walking at five speeds. The specified goal function yielded a decomposition of stride-to-stride variations into new gait variables explicitly related to achieving the hypothesized strategy. Subjects exhibited greatly decreased variability for goal-relevant gait fluctuations directly related to achieving this strategy, but far greater variability for goal-irrelevant fluctuations. More importantly, humans immediately corrected goal-relevant deviations at each successive stride, while allowing goal-irrelevant deviations to persist across multiple strides. To demonstrate that this was not the only strategy people could have used to successfully accomplish the task, we created three surrogate data sets. Each tested a specific alternative hypothesis that subjects used a different strategy that made no reference to the hypothesized goal function. Humans did not adopt any of these viable alternative strategies. Finally, we developed a sequence of stochastic control models of stride-to-stride variability for walking, based on the Minimum Intervention Principle. We demonstrate that healthy humans are not precisely "optimal," but instead consistently slightly over-correct small deviations in walking speed at each stride. Our results reveal a new governing principle for regulating stride-to-stride fluctuations in human walking that acts independently of, but in parallel with, minimizing energetic cost. Thus, humans exploit task redundancies to achieve robust control while minimizing effort and allowing potentially beneficial motor variability.

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

Publications

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

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