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      Intrinsic ankle stiffness during standing increases with ankle torque and passive stretch of the Achilles tendon

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          Abstract

          Individuals may stand with a range of ankle angles. Furthermore, shoes or floor surfaces may elevate or depress their heels. Here we ask how these situations impact ankle stiffness and balance. We performed two studies (each with 10 participants) in which the triceps surae, Achilles tendon and aponeurosis were stretched either passively, by rotating the support surface, or actively by leaning forward. Participants stood freely on footplates which could rotate around the ankle joint axis. Brief, small stiffness-measuring perturbations (<0.7 deg; 140 ms) were applied at intervals of 4–5 s. In study 1, participants stood at selected angles of forward lean. In study 2, normal standing was compared with passive dorsiflexion induced by 15 deg toes-up tilt of the support surface. Smaller perturbations produced higher stiffness estimates, but for all perturbation sizes stiffness increased with active torque or passive stretch. Sway was minimally affected by stretch or lean, suggesting that this did not underlie the alterations in stiffness. In quiet stance, maximum ankle stiffness is limited by the tendon. As tendon strain increases, it becomes stiffer, causing an increase in overall ankle stiffness, which would explain the effects of leaning. However, stiffness also increased considerably with passive stretch, despite a modest torque increase. We discuss possible explanations for this increase.

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          Most cited references46

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          Adapting reflexes controlling the human posture.

          Doubt about the role of stretch reflexes in movement and posture control has remained in part because the questions of reflex "usefulness" and the postural "set" have not been adequately considered in the design of experimental paradigms. The intent of this study was to discover the stabilizing role of stretch reflexes acting upon the ankle musculature while human subjects performed stance tasks requiring several different postural "sets". Task specific differences of reflex function were investigated by experiments in which the role of stretch reflexes to stabilize sway doing stance could be altered to be useful, of no use, or inappropriate. Because the system has available a number of alternate inputs to posture (e.g., vestibular and visual), stretch reflex responses were in themselves not necessary to prevent a loss of balance. Nevertheless, 5 out of 12 subjects in this study used long-latency (120 msec) stretch reflexes to help reduce postural sway. Following an unexpected change in the usefulness of stretch reflexes, the 5 subjects progressively altered reflex gain during the succeeding 3-5 trials. Adaptive changes in gain were always in the sense to reduce sway, and therefore could be attenuating or facilitating the reflex response. Comparing subjects using the reflex with those not during so, stretch reflex control resulted in less swaying when the task conditions were unchanging. However, the 5 subjects using reflex controls oftentimes swayed more during the first 3-5 trials after a change, when inappropriate responses were elicited. Four patients with clinically diagnosed cerebellar deficits were studied briefly. Among the stance tasks, their performance was similar to normal in some and significantly poorer in others. Their most significant deficit appeared to be the inability to adapt long-latency reflex gain following changes in the stance task. The study concludes with a discussion of the role of stretch reflexes within a hierarchy of controls ranging from muscle stiffness up to centrally initiated responses.
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            Collagen self-assembly and the development of tendon mechanical properties.

            The development of the musculoskeleton and the ability to locomote requires controlled cell division as well as spatial control over deposition of extracellular matrix. Self-assembly of procollagen and its final processing into collagen fibrils occurs extracellularly. The formation of crosslinked collagen fibers results in the conversion of weak liquid-like embryonic tissues to tough elastic solids that can store energy and do work. Collagen fibers in the form of fascicles are the major structural units found in tendon. The purpose of this paper is to review the literature on collagen self-assembly and tendon development and to relate this information to the development of elastic energy storage in non-mineralizing and mineralizing tendons. Of particular interest is the mechanism by which energy is stored in tendons during locomotion. In vivo, collagen self-assembly occurs by the deposition of thin fibrils in recesses within the cell membrane. These thin fibrils later grow in length and width by lateral fusion of intermediates. In vitro, collagen self-assembly occurs by both linear and lateral growth steps with parallel events seen in vivo; however, in the absence of cellular control and enzymatic cleavage of the propeptides, the growth mechanism is altered, and the fibrils are irregular in cross section. Results of mechanical studies suggest that prior to locomotion the mechanical response of tendon to loading is dominated by the viscous sliding of collagen fibrils. In contrast, after birth when locomotion begins, the mechanical response is dominated by elastic stretching of crosslinked collagen molecules.
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              Can muscle stiffness alone stabilize upright standing?

              A stiffness control model for the stabilization of sway has been proposed recently. This paper discusses two inadequacies of the model: modeling and empiric consistency. First, we show that the in-phase relation between the trajectories of the center of pressure and the center of mass is determined by physics, not by control patterns. Second, we show that physiological values of stiffness of the ankle muscles are insufficient to stabilize the body "inverted pendulum." The evidence of active mechanisms of sway stabilization is reviewed, pointing out the potentially crucial role of foot skin and muscle receptors.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Methodology
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                20 March 2018
                2018
                : 13
                : 3
                : e0193850
                Affiliations
                [001]School of Sport, Exercise & Rehabilitation Sciences, University of Birmingham, Birmingham, West Midlands, United Kingodm
                University of L'Aquila, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-5031-3473
                Article
                PONE-D-17-21142
                10.1371/journal.pone.0193850
                5860743
                29558469
                ec6cdd26-3032-4a48-a051-540e987b8f47
                © 2018 Sakanaka et al

                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 author and source are credited.

                History
                : 2 June 2017
                : 19 February 2018
                Page count
                Figures: 7, Tables: 1, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/L02103X/1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000855, University of Birmingham;
                Award ID: PhD Scholarship for Research Excellence from Brazil
                Award Recipient :
                This work was funded by a grant from the Biotechnology and Biological Sciences Research Council (BB/LO2103X/1), and also a PhD scholarship for Research Excellence for Brazilian students from the University of Birmingham PhD Scholarship for Research Excellence from Brazil to Dr. Sakanaka. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Limbs (Anatomy)
                Legs
                Ankles
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Limbs (Anatomy)
                Legs
                Ankles
                Physical Sciences
                Physics
                Classical Mechanics
                Motion
                Torque
                Physical Sciences
                Materials Science
                Material Properties
                Mechanical Properties
                Stiffness
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Tendons
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Tendons
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Gastrocnemius Muscles
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Gastrocnemius Muscles
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Soleus Muscles
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Soleus Muscles
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Muscle Electrophysiology
                Electromyography
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Custom metadata
                All original data from this study have been uploaded to Figshare, and can be found using the following links: Study 1: https://doi.org/10.6084/m9.figshare.5692852; Study 2: https://doi.org/10.6084/m9.figshare.5692933.

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