Frequency-dependent force direction elucidates neural control of balance

Abstract

Background Maintaining upright posture is an unstable task that requires sophisticated neuro-muscular control. Humans use foot–ground interaction forces, characterized by point of application, magnitude, and direction to manage body accelerations. When analyzing the directions of the ground reaction forces of standing humans in the frequency domain, previous work found a consistent pattern in different frequency bands. To test whether this frequency-dependent behavior provided a distinctive signature of neural control or was a necessary consequence of biomechanics, this study simulated quiet standing and compared the results with human subject data. Methods Aiming to develop the simplest competent and neuromechanically justifiable dynamic model that could account for the pattern observed across multiple subjects, we first explored the minimum number of degrees of freedom required for the model. Then, we applied a well-established optimal control method that was parameterized to maximize physiologically-relevant insight to stabilize the balancing model. Results If a standing human was modeled as a single inverted pendulum, no controller could reproduce the experimentally observed pattern. The simplest competent model that approximated a standing human was a double inverted pendulum with torque-actuated ankle and hip joints. A range of controller parameters could stabilize this model and reproduce the general trend observed in experimental data; this result seems to indicate a biomechanical constraint and not a consequence of control. However, details of the frequency-dependent pattern varied substantially across tested control parameter values. The set of parameters that best reproduced the human experimental results suggests that the control strategy employed by human subjects to maintain quiet standing was best described by minimal control effort with an emphasis on ankle torque. Conclusions The findings suggest that the frequency-dependent pattern of ground reaction forces observed in quiet standing conveys quantitative information about human control strategies. This study’s method might be extended to investigate human neural control strategies in different contexts of balance, such as with an assistive device or in neurologically impaired subjects.

Vertical ground reaction force oscillation during standing on hard and compliant surfaces: The “postural rhythm”

“…While the twitch time course of a postural muscle can be of the order of several tenths of ms, the elicited movement of the body can be fast (but definitely not as fast as the twitch time-course) or extremely slow as when the postural conditions impose a quasi-isometric muscle contraction. If anything, our findings support the view that modeling body sway with an inverted pendulum hardly provides for a useful generalization of the balance strategies ( 5 , 22 , 99 ). Fluctuations in ankle, knee and hip joints participate in upright stance adjustments ( 100 ).…”

“…With EC, the RMS of the VGRF oscillations were greater than with EO [main effect, F (1, 22) = 37.16, p < 0.001, η 2 p = 0.63]. There was also an interaction between vision and support conditions [F (1,22) = 43.86, p < 0.001, η 2 p = 0.66], because the difference between EC and EO was significant with Foam (post-hoc, p < 0.001) but not with Solid support (p = 0.79). In Figure 2B, the VGRF RMS data of all the subjects are plotted Solid vs.…”

“…Figure 4A shows a summary of the Mean frequency values across subjects for each vision and support condition. There was a difference in Mean frequency between support conditions [main effect, Solid > Foam, F (1, 22) = 52.9, p < 0.001, η 2 p = 0.71], but not in Mean frequency between visual conditions [main effect, F (1,22) = 2.74, p = 0.11]. The interaction between visual and support conditions was significant [F (1,22) = 4.54, p < 0.05, η 2 p = 0.17], because there was a difference between EC and EO condition on Foam (post-hoc, p < 0.05) but not on Solid support (p = 0.78).…”

“…The mean SD was greater for Solid than Foam support [main effect, F (1, 22) = 110.4, p < 0.001, η 2 p = 0.83] under both EC and EO conditions. There was no significant difference between visual conditions [main effect, F (1, 22) = 0.76, p = 0.39] and no significant interaction between visual and base of support conditions [F (1,22) = 1.09, p = 0.31]. In Figure 4C, the individual values of the Mean frequency are plotted for Solid against Foam support condition, and the vision state is indicated by the colored dots (EC, pink; EO, gray).…”

“…This is opposed partly by the intrinsic ankle joint stiffness [ (7)(8)(9)(10)(11)(12), see (13,14)] and partly by corrective actions of the postural muscles (15-17). These act onto the upper and lower body masses and produce interacting torques about the hip, knee and ankle joints, thereby maintaining the body motion within a region much smaller than the boundary of the base of support (18)(19)(20)(21)(22)(23).…”