Influence of bilateral vestibular loss on spinal stabilization in humans

Abstract

The control of upper body (UB) orientation relative to the pelvis in the frontal plane was characterized in bilateral vestibular loss subjects (BVLs) and compared with healthy control subjects (Cs). UB responses to external perturbations were evoked using continuous pelvis tilts (eyes open and eyes closed) at various amplitudes. Lateral sway of the lower body was prevented on all tests. UB sway was summarized using root-mean-square measures and dynamic behavior was characterized using frequency response functions (FRFs) from 0.023 to 10.3 Hz. Both subject groups had similar FRF variations as a function of stimulus frequency and were relatively unaffected by visual availability, indicating that visual orientation cues contributed very little to UB control. BVLs had larger UB sway at frequencies below ∼1 Hz compared with Cs. A feedback model of UB orientation control was used to identify sensory contributions to spinal stability and differences between subject groups. The model-based interpretation of experimental results indicated that a phasic proprioceptive signal encoding the angular velocity of UB relative to lower body motion was a major contributor to overall system damping. Parametric system identification showed that BVLs used proprioceptive information that oriented the UB toward the pelvis to a greater extent compared with Cs. Both subject groups used sensory information that oriented the UB vertical in space to a greater extent as pelvis tilt amplitudes increased. In BVLs, proprioceptive information signaling the UB orientation relative to the fixed lower body provided the vertical reference, whereas in Cs, vestibular information also contributed to the vertical reference.

Fig. 1.

Upper body (UB) sway responses to pelvis tilt stimuli. A: surface rotations produced pelvis tilts that evoked UB sway while the lower body was prevented from moving laterally. B: Mean (±95% confidence intervals) UB sway from 1 bilateral vestibular loss (BVL) subject. C: root-mean-square (RMS) UB sway as a function of stimulus amplitude for individual BVLs and the mean (±1 SE) of control subjects (Cs).

Fig. 2.

Mean experimental frequency-response functions (FRFs) and coherence functions in BVLs and Cs for eyes closed (A) and eyes open (B) conditions. Error bars on FRFs in Cs for the 1° stimulus amplitude represent 95% confidence intervals on mean gain and phase.

Fig. 3.

Model of UB control includes feedback from 4 mechanisms. The model input is surface tilt-in-space (SS) and output is upper body-in-space (UBS) tilt angle. Actual kinematic variables are represented as thick solid lines and capital letters while internal estimates of kinematic variables are represented as dashed lines and lower case letters.

Fig. 4.

Model parameters for the 3 individual bilateral vestibular loss subjects (▴, *, or □) and mean of control subjects (○) with 95% confidence intervals (error bars or ▩). A: parameters that had fixed values across all test conditions. B: parameters that varied across test conditions. Units on K_P are N·m/rad, units on K_I are N·m/(rad·s), and units on K_D, B_V, and B_SL are N·m·s/rad. Sensory weight W_P1 is unitless. All parameters except W_P1 and time delays were normalized by UB mass, m, times UB center-of-mass height, h. The mean m·h was 9.0 kg·m in Cs and 13.2 kg·m in BVLs. Weight parameters W_P2 and W_V are not shown because they can be derived from W_P1. For BVLs in eyes closed conditions, W_V = 0 and W_P2 = 1 − W_P1. In eyes open conditions for BVLs and in all test conditions for Cs, W_P2 + W_V = 1 − W_P1.

Fig. 5.

Influence of W_P1 and K_I on FRFs shows that most of the FRF features that differ between Cs and BVLs can be accounted for with larger W_P1 values in BVLs across all test conditions (A) and larger K_I values in BVLs across EC conditions (B). The thick dotted line is the FRF predicted for the EC 2° stimulus amplitude condition using the mean Cs model parameters: K_IN = 73.5 N·m/rad, B_SL = 9.87 N·m·s/rad, τ_SL = 21.7 ms, τ_ML = 131 ms, τ_LL = 288 ms, W_P1 = 0.390, B_V = 35.7 N·m·s/rad, K_P = 149 N·m/rad, K_D = 6.60 N·m·s/rad, and K_I = 63.7 N·m/(rad·s).