Phase-Dependency of Medial-Lateral Balance Responses to Sensory Perturbations During Walking

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.

Interdependence of balance mechanisms during bipedal locomotion

“…The sequential onset of the balance mechanisms in the presence of the perceived fall (Fig 1) in combination with the large corrections being made for the variability of the use of earlier mechanisms (Fig 2) provides strong evidence that the CNS activates mechanisms separately based on continuous monitoring of the balance response. In this view, there would be a direct, reflex-like connection between the sensory information indicating a lateral fall and each balance mechanism, which is modulated depending on the phase of the gait cycle [39]. Since the ankle mechanism is relevant during single stance, it is possible that the effects of the ankle mechanism command could be observed via proprioception and the results fed back into the foot placement command with a negative sign.…”

Interactions Between Different Age-Related Factors Affecting Balance Control in Walking

“…The biomechanical effect of a muscle activation during walking is highly dependent on the point in the gait cycle (Reimann et al, 2019 ). The walking body is mechanically complex, with arms and legs moving largely independent from each other, though highly coordinated (Punt et al, 2015 ; Thompson et al, 2017 ).…”

“…Ankle roll, foot placement shift, and push-off modulation are three biomechanical mechanisms to change the ground reaction force and push the body to the left in response detecting a fall to the right. They become available at different times during the gait cycle and temporally coordinated by the neural control system, which shifts the response between mechanisms as they become available to generate a functional, whole-body balance response to a detected fall (Reimann et al, 2019 ). In section 3.5, we will review how these balance mechanisms interact with age-related factors affecting fall risk.…”

Flexible Recruitment of Balance Mechanisms to Environmental Constraints During Walking

“…et al, 2019), reflecting typical step-to-step variability. Furthermore, the relative use of the mechanisms is altered based on internal constraints, such as the phase of the gait cycle (Reimann et al, 2019), or the stepping cadence . This illustrates a highly flexible system that maintains balance during locomotion as it confronts changing task demands and environmental challenges.…”