Abstract

The human body is mechanically unstable during walking. Maintaining upright stability requires constant regulation of muscle force by the central nervous system to push against the ground and move the body mass in the desired way. Activation of muscles in the lower body in response to sensory or mechanical perturbations during walking is usually highly phase-dependent, because the effect any specific muscle force has on the body movement depends upon the body configuration. Yet the resulting movement patterns of the upper body after the same perturbations are largely phase-independent. This is puzzling, because any change of upper-body movement must be generated by parts of the lower body pushing against the ground. How do phase-dependent muscle activation patterns along the lower body generate phase-independent movement patterns of the upper body? We hypothesize that when a sensory system detects a deviation of the body in space from a desired state that indicates the onset of a fall, the nervous system generates a functional response by pushing against the ground in any way possible with the current body configuration. This predicts that the changes in the ground reaction force patterns following a balance perturbation should be phase-independent. Here we test this hypothesis by disturbing upright balance in the frontal plane using Galvanic vestibular stimulation at three different points in the gait cycle. We measure the resulting changes in whole-body center of mass movement and the location of the center of pressure of the ground reaction force. We find that the magnitude of the initial center of pressure shift in the direction of the perceived fall is larger for perturbations late in the gait cycle, while there is no statistically significant difference in onset time. These results contradict our hypothesis by showing that even the initial CoP shift in response to a balance perturbation depends upon the phase of the gait cycle. Contrary to expectation, we also find that the whole-body balance response is not phase-independent. Both the onset time and the magnitude of the whole-body center of mass shift depend on the phase of the perturbation. We conclude that the central nervous system recruits any available mechanism to generate a functional balance response by pushing against the ground as fast as possible in response to a perturbation, but that the different mechanisms available at different phases in the gait cycle are not equally strong, leading to phase-dependent differences in the overall response.

Highlights

  • The control of balance during walking for humans is an important problem because the failure to maintain balance leads to falls and often injury

  • We used Galvanic vestibular stimulation to perturb the sense of balance in walking humans at three different phases in the gait cycle

  • We analyzed the whole-body response to this sensory perturbation in the form of changes of the center of mass (CoM) movement, and the displacement of the center of pressure (CoP) relative to the CoM, which is one aspect of the ground reaction forces generating the whole-body movement changes

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Summary

Introduction

The control of balance during walking for humans is an important problem because the failure to maintain balance leads to falls and often injury. The upright human body is mechanically unstable, with a high center of mass and a relatively small base of support Balancing this body is already a challenge during standing, requiring continuous regulation of muscle activity by the central nervous system (Morasso and Schieppati, 1999). One well-studied mechanism is to shift the location of the foot placement when taking a step, which changes the pull of gravity on the body during the subsequent swing (Hof, 2008; Wang and Srinivasan, 2014; Bruijn and van Dieën, 2018; Reimann et al, 2018a) Another mechanism is to use ankle musculature to pull on the body during single stance (Hof et al, 2010; Hof and Duysens, 2018; Reimann et al, 2018b). A recent study by Vlutters et al (2019) shows that the (sagittal) ankle mechanisms is activated even when the ankle joint is blocked by an orthosis, indicating that it might be controlled by a dedicated reflex

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