Adaptation of multijoint coordination during standing balance in healthy young and healthy old individuals

Abstract

Standing balance requires multijoint coordination between the ankles and hips. We investigated how humans adapt their multijoint coordination to adjust to various conditions and whether the adaptation differed between healthy young participants and healthy elderly. Balance was disturbed by push/pull rods, applying two continuous and independent force disturbances at the level of the hip and between the shoulder blades. In addition, external force fields were applied, represented by an external stiffness at the hip, either stabilizing or destabilizing the participants' balance. Multivariate closed-loop system-identification techniques were used to describe the neuromuscular control mechanisms by quantifying the corrective joint torques as a response to body sway, represented by frequency response functions (FRFs). Model fits on the FRFs resulted in an estimation of time delays, intrinsic stiffness, reflexive stiffness, and reflexive damping of both the ankle and hip joint. The elderly generated similar corrective joint torques but had reduced body sway compared with the young participants, corresponding to the increased FRF magnitude with age. When a stabilizing or destabilizing external force field was applied at the hip, both young and elderly participants adapted their multijoint coordination by lowering or respectively increasing their neuromuscular control actions around the ankles, expressed in a change of FRF magnitude. However, the elderly adapted less compared with the young participants. Model fits on the FRFs showed that elderly had higher intrinsic and reflexive stiffness of the ankle, together with higher time delays of the hip. Furthermore, the elderly adapted their reflexive stiffness around the ankle joint less compared with young participants. These results imply that elderly were stiffer and were less able to adapt to external force fields.

Keywords: adaptation; healthy elderly; multijoint coordination; standing balance control.

Fig. 1.

Double-inverted pendulum perturbator with a subject standing on a force plate (A) and attached to 2 manipulators at shoulder and hip level (B). Both manipulators are adjustable in height and driven by an electromotor, pushing and pulling the subject. Body kinematics are measured by potentiometers attached to the rod (C). A safety harness is attached to the pyramidal construction (D), and an emergency button is mounted on the frame (E).

Fig. 2.

Time series of the applied force disturbances at the pelvis and between the shoulder blades, with the corresponding power spectral density. The force disturbances are zippered multisine, as the excited frequencies (indicated with circles) are independent.

Fig. 3.

Schematics of the human balance control system. The human body was represented as a double-inverted pendulum, with disturbances acting at the hip and shoulder level. The model of the neuromuscular controller was used for parameter estimation. The inputs were the ankle and hip angle (θ_ank, θ_hip) and the outputs, the corrective joint torques (T_ank, T_hip). Intrinsic dynamics were modeled as a spring and were different for the ankle and hip joints. Reflexive control and time-delay dynamics were multiple-input, multiple-output transfer functions (shown as dotted boxes), in which interaction existed between the ankle and hip-joint signals. Hp, intrinsic feedback; Hr, reflexive feedback; Htd, feedback of time delay; θhat, segment angle of the head-arms-trunk segment; θleg, segment angle of the leg.

Fig. 4.

Joint angles and joint torques in response to the applied disturbances of a representative young (left) and elderly (right) participant in the baseline trial without force field (0%). The average over the 9 disturbance cycles is indicated with the black line; the gray area represents the SD.

Fig. 5.

Root mean square (RMS) values of the joint angles and torques for young and elderly participants per force-field level represented by means and SD. Significant differences with *age, **force field, or ***interaction between age and force field.

Fig. 6.

Covariance descriptor of the young and elderly participants per force-field level. λ₁ and λ₂, squared lengths of the major and minor ellipse axes, respectively; α, orientation of the ellipse.

Fig. 7.

Baseline differences in normalized frequency response function (FRF) between young (black lines) and elderly (gray lines) participants, where only the 2 disturbances were applied without additional force fields (0%), represented by means and SD. The FRF consists of 4 terms: 2 direct terms from ankle angle to ankle torque (θ_ank2T_ank) and from hip angle to hip torque (θ_hip2T_hip) and 2 indirect terms from hip angle to ankle torque (θ_hip2T_ank) and from ankle angle to hip torque (θ_ank2T_hip). *Frequency bins in which there is a significant difference with age.

Fig. 8.

Adaptation of normalized FRF magnitude in the young (top) and elderly (bottom) participants. For each force-field level, the mean is shown. For displaying reasons only, the SD was shown for the baseline trial. SDs of the other force-field levels were compared with the baseline trials. Frequency bins in which there are **significant differences with force field or the ***interaction between age and force field.

Fig. 9.

Normalized FRFs based on measured data (black dots) and model fits (gray lines) of a representative healthy young subject for the baseline trial (0%). The goodness of fit (GOF) values are shown for each term in the FRF.

Fig. 10.

Estimated parameters represented by means and SD (error bars) for young and old participants per force-field level. Stiffness and damping are normalized to the gravitational stiffness (mass × gravitation × center of mass height) for each subject. A: estimated time delays (τ_d); B: intrinsic properties (K_p); C: reflexive stiffness (K_ank2Tank, K_hip2Tank, K_ank2Thip, K_hip2Thip); D: reflexive damping (D_ank2Tank, D_hip2Tank, D_ank2Thip, D_hip2Thip). Significant differences with *age, **force field, or ***interaction between age and force field.