Changes in sensory reweighting of proprioceptive information during standing balance with age and disease

Abstract

With sensory reweighting, reliable sensory information is selected over unreliable information during balance by dynamically combining this information. We used system identification techniques to show the weight and the adaptive process of weight change of proprioceptive information during standing balance with age and specific diseases. Ten healthy young subjects (aged between 20 and 30 yr) and 44 elderly subjects (aged above 65 yr) encompassing 10 healthy elderly, 10 with cataract, 10 with polyneuropathy, and 14 with impaired balance, participated in the study. During stance, proprioceptive information of the ankles was disturbed by rotation of the support surface with specific frequency content where disturbance amplitude increased over trials. Body sway and reactive ankle torque were measured to determine sensitivity functions of these responses to the disturbance amplitude. Model fits resulted in a proprioceptive weight (changing over trials), time delay, force feedback, reflexive stiffness, and damping. The proprioceptive weight was higher in healthy elderly compared with young subjects and higher in elderly subjects with cataract and with impaired balance compared with healthy elderly subjects. Proprioceptive weight decreased with increasing disturbance amplitude; decrease was similar in all groups. In all groups, the time delay was higher and the reflexive stiffness was lower compared with young or healthy elderly subjects. In conclusion, proprioceptive information is weighted more with age and in patients with cataract and impaired balance. With age and specific diseases the time delay was higher and reflexive stiffness was lower. These results illustrate the opportunity to detect the underlying cause of impaired balance in the elderly with system identification.

Keywords: elderly; proprioception; sensory reweighting; standing balance; system identification techniques.

Fig. 1.

A: experimental setup with the bilateral ankle perturbator (BAP) with the motor (1), the lever arm (2), and the support surfaces (3) indicated. The participant wore a safety harness to prevent a fall and looked at a poster on the wall. B: schematic figure of the approach showing the support surface (SS) rotation around the ankle axis, the ankle torque (T), and the body sway (BS).

Fig. 2.

Time signal (top), presented with normalized amplitude, and the corresponding power spectrum (bottom) of the disturbance signal.

Fig. 3.

Model of the balance control system in which the body is represented by an inverted pendulum. This inverted pendulum is controlled by the neuromuscular controller, consisting of the weighting factors of the visual, vestibular, and proprioceptive information, a neural controller, force feedback, time delay, and muscle activation dynamics. The torque (T) generated by the neuromuscular controller affects the body sway (BS) angle. The control loop can be disturbed by support surface rotation (SS), resulting in a sensory disturbance of the proprioceptive information.

Fig. 4.

Root mean square (RMS) of leg and hip angle of each group and each trial. *Significantly different (P < 0.05) compared with young, ^xsignificantly different (P < 0.05) compared with healthy elderly, ⁺significantly different (P < 0.05) compared with elderly with cataract.

Fig. 5.

Mean sensitivity function of each group of the trial with disturbance amplitude of 0.02 rad. The (normalized) magnitude and phase of the sensitivities of the ankle torque (^SSS_T), the leg angle (^SSS_LA), the hip angle (^SSS_HA), and the body sway (^SSS_BS) to the rotation of the support surface are shown.

Fig. 6.

Proprioceptive weight (W_p) and reweighting (ΔW_p) per radian increase of disturbance amplitude of each group and each trial. *Significantly different (P < 0.05) compared with young, ^xsignificantly different (P < 0.05) compared with healthy elderly, ⁺significantly different (P < 0.05) compared with elderly with cataract.

Fig. 7.

Normalized reflexive stiffness and damping, time delay, and force feedback of each group and each trial. *Significantly different (P < 0.05) compared with young, ^xsignificantly different (P < 0.05) compared with healthy elderly, ⁺significantly different (P < 0.05) compared with elderly with cataract.