Sway-dependent changes in standing ankle stiffness caused by muscle thixotropy.

Tania E. Sakanaka,Martin Lakie,Raymond F. Reynolds

doi:10.1113/jp271137

Abstract

Key points The passive stiffness of the calf muscles contributes to standing balance, although the properties of muscle tissue are highly labile.We investigated the effect of sway history upon intrinsic ankle stiffness and demonstrated reductions in stiffness of up to 43% during conditions of increased baseline sway.This sway dependence was most apparent when using low amplitude stiffness‐measuring perturbations, and the short‐range stiffness component was smaller during periods of high sway.These characteristics are consistent with the thixotropic properties of the calf muscles causing the observed changes in ankle stiffness.Periods of increased sway impair the passive stabilization of standing, demanding more active neural control of balance. Quiet standing is achieved through a combination of active and passive mechanisms, consisting of neural control and intrinsic mechanical stiffness of the ankle joint, respectively. The mechanical stiffness is partly determined by the calf muscles. However, the viscoelastic properties of muscle are highly labile, exhibiting a strong dependence on movement history. By measuring the effect of sway history upon ankle stiffness, the present study determines whether this lability has consequences for the passive stabilization of human standing. Ten subjects stood quietly on a rotating platform whose axis was collinear with the ankle joint. Ankle sway was increased by slowly tilting this platform in a random fashion, or decreased by fixing the body to a board. Ankle stiffness was measured by using the same platform to simultaneously apply small, brief perturbations (<0.6 deg; 140 ms) at the same time as the resulting torque response was recorded. The results show that increasing sway reduces ankle stiffness by up to 43% compared to the body‐fixed condition. Normal quiet stance was associated with intermediate values. The effect was most apparent when using smaller perturbation amplitudes to measure stiffness (0.1 vs. 0.6 deg). Furthermore, torque responses exhibited a biphasic pattern, consisting of an initial steep rise followed by a shallower increase. This transition occurred earlier during increased levels of ankle sway. These results are consistent with a movement‐dependent change in passive ankle stiffness caused by thixotropic properties of the calf muscle. The consequence is to place increased reliance upon active neural control during times when increased sway renders ankle stiffness low.

Highlights

In quiet standing, the body’s centre of mass is situated forward of the ankle joint, and so continuous ankle torque is required to prevent it from falling forwards (Schieppati et al 1994; Gatev et al 1999)
Ten healthy subjects were recruited for this non-invasive experiment (Table 1). All provided their written informed consent to the experimental procedures, which were approved by the local human ethics committee at the University of Birmingham and conformed to the principles of the Declaration of Helsinki
To identify changes in stiffness throughout the time course of each perturbation, we examined the relationship between ankle torque and position during the first 70 ms of each stimulus

Summary

Introduction

The body’s centre of mass is situated forward of the ankle joint, and so continuous ankle torque is required to prevent it from falling forwards (Schieppati et al 1994; Gatev et al 1999). Between-subject differences are indicated by the considerable variation in intrinsic ankle stiffness measured using rotary perturbations (Loram & Lakie, 2002; Casadio et al 2005). This has important implications for the neural control of balance because individuals who have inherently stiffer ankle joints (e.g. as a result of a stiffer Achilles tendon) can rely more upon the passive mechanism and less upon active modulation.

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Conclusion