Biarticular muscles are most responsive to upper-body pitch perturbations in human standing

Abstract

Balancing the upper body is pivotal for upright and efficient gait. While models have identified potentially useful characteristics of biarticular thigh muscles for postural control of the upper body, experimental evidence for their specific role is lacking. Based on theoretical findings, we hypothesised that biarticular muscle activity would increase strongly in response to upper-body perturbations. To test this hypothesis, we used a novel Angular Momentum Perturbator (AMP) that, in contrast to existing methods, perturbs the upper-body posture with only minimal effect on Centre of Mass (CoM) excursions. The impulse-like AMP torques applied to the trunk of subjects resulted in upper-body pitch deflections of up to 17° with only small CoM excursions below 2 cm. Biarticular thigh muscles (biceps femoris long head and rectus femoris) showed the strongest increase in muscular activity (mid- and long-latency reflexes, starting 100 ms after perturbation onset) of all eight measured leg muscles which highlights the importance of biarticular muscles for restoring upper-body balance. These insights could be used for improving technological aids like rehabilitation or assistive devices, and the effectiveness of physical training for fall prevention e.g. for elderly people.

Figure 1

Exemplary perturbation types: Schematic visualisation of Center of Mass (CoM), leg, and upper-body kinematics (transparent: before perturbation, solid: after perturbation). (a) Back and forth surface translations result in a whole-body balance perturbation by producing first an acceleration followed by a deceleration. (b) Force pushes or pulls can result in irregular body postures with small upper body perturbations. (c) Torque perturbation: the generated torque on the upper body (curved red arrow) is equivalent to a force pair (straight red arrows) with zero net horizontal force. This type of perturbation results mainly in rotational acceleration of the upper body. Minimal CoM excursions occur due to the muscular coupling of the upper body to the leg. (d) The Angular Momentum Perturbator (AMP) creates external torques by rotating a spinning flywheel (angular momentum H, purple arrow) around a perpendicular gimbal axis (here: longitudinal, angular velocity $\dot{\mathit{\gamma }}$, green arrow, initial gimbal position γ₀). The created torque τ_AMP is exerted in the direction perpendicular to both, the rotation of the spinning flywheel and the gimbal axis, and rotates together with the gimbal (red arrow).

Figure 2

AMP generated (a) positive and (b) negative torque perturbations resulting in forward and backward pitch of the upper body, respectively. Change in upper-body pitch angle of one subject (mean and standard deviation from the last 5 trials × 2 gimbal configurations) with respect to the initial upper-body posture (top left). The inset shows the desired (grey, 100 rise, hold and fall time) and actual pitch perturbation torque profile (orange/green: mean and SD). Change in sagittal CoM (grey: mean and SD) and CoP position (black: mean and SD) of the same subject with respect to the initial positions (top right). Exemplary EMG of the same subject (bottom panel): filtered and normalised signals of all trials (grey) and one individual response of mono- (yellow) and biarticular muscles (red).

Figure 3

Influence of AMP artefacts and prestimulation activity. Boxplots of muscular activity of the left leg in ‘Unloaded Standing’ (UL), ‘Loaded Standing’ (L) and the mean ‘Pre-Perturbation’ activation of the last 10 trials per block (‘Block 1’ and ‘Block 2’) for all 11 subjects. Reported EMGs (WEMG) are the mean intervals of the filtered EMG signals normalised by the muscle’s mean activity during walking (see Methods). Results are presented with significant (^*p < 0.05) comparisons of the paired t-test or two-sided Wilcoxon signed-rank test.

Figure 4

Reflex activity of mono- (yellow) and biarticular muscles (red) for (a) positive and (b) negative torque perturbations in different response intervals. Grand mean and SD of averaged relative reflex responses of the left leg (last 5 trials per condition × 2 gimbal configurations) for all 11 subjects. Relative reflex activity in each response interval is computed with respect to ‘Pre-Perturbation’ and normalised by the muscle’s mean activity during walking (see Methods).