Sensory reweighting dynamics in human postural control

Abstract

Healthy humans control balance during stance by using an active feedback mechanism that generates corrective torque based on a combination of movement and orientation cues from visual, vestibular, and proprioceptive systems. Previous studies found that the contribution of each of these sensory systems changes depending on perturbations applied during stance and on environmental conditions. The process of adjusting the sensory contributions to balance control is referred to as sensory reweighting. To investigate the dynamics of reweighting for the sensory modalities of vision and proprioception, 14 healthy young subjects were exposed to six different combinations of continuous visual scene and platform tilt stimuli while sway responses were recorded. Stimuli consisted of two components: 1) a pseudorandom component whose amplitude periodically switched between low and high amplitudes and 2) a low-amplitude sinusoidal component whose amplitude remained constant throughout a trial. These two stimuli were mathematically independent of one another and, thus, permitted separate analyses of sway responses to the two components. For all six stimulus combinations, the sway responses to the constant-amplitude sine were influenced by the changing amplitude of the pseudorandom component in a manner consistent with sensory reweighting. Results show clear evidence of intra- and intermodality reweighting. Reweighting dynamics were asymmetric, with slower reweighting dynamics following a high-to-low transition in the pseudorandom stimulus amplitude compared with low-to-high amplitude shifts, and were also slower for inter- compared with intramodality reweighting.

Keywords: balance; humans; posture control; reweighting; sensory integration.

Fig. 1.

A: sinusoidal and pseudorandom ternary sequence (prts) stimulus components (left) and combinations of sine and prts (right) that were applied to either the platform (PF) or the visual surround (VS) in the 6 experimental conditions. Note that the y-axis has different scales for the sine and prts components. B: description of the 6 experimental test conditions. Each test condition consisted of 2 separate trials, with the sine wave having opposite signs in the 2 trials. The 2 stimulus components (prts and sine) were either applied on PF and VS separately (Exps. 2 and 4) or combined, i.e., the sum of prts and sine on the PF (Exps. 1 and 3) or on the VS (Exps. 5 and 6). C: full-length PF tilt stimulus for 1 trial of Exp. 2 (the VS sine stimulus is not shown) and the evoked center of mass (COM) sway response of 1 subject. Two high-amplitude prts cycles (prts HI) were alternated with 2 low-amplitude cycles (prts LO). The first cycle following a change in prts amplitude was defined as a transition (trans) period, and the second cycle was defined as a steady-state period.

Fig. 2.

Analysis scheme for the separation of responses to the prts and sine stimulus components. Adding the COM responses of a pair of trials (and dividing by 2) yields the COM response to the prts, while the response to the sign-opposed sine stimulus components are canceled out. Subtracting the COM responses of a pair of trials (and dividing by 2) yields the sine response and cancels out the prts response.

Fig. 3.

Gain vs. stimulus frequency plots characterizing COM sway dynamics at the sine frequency (indicated by gray bar) and the prts frequencies. Gains were calculated from data during the steady-state cycles of prts LO conditions (open symbols) and prts HI conditions (filled symbols). Shown are mean gain values (±95% confidence limits) for PF prts (top; EC = eyes closed) and VS prts (bottom;, s.r. = sway referenced) experimental conditions. Circles indicate response gains to PF stimuli; triangles indicate response gains to VS stimuli. Note the y-axis scale difference in Exp. 6.

Fig. 4.

Analysis of COM responses to the 0.56-Hz sinusoidal stimulus component in the 6 experimental conditions. Vertical dashed lines demarcate the steady-state and transition periods of the prts HI amplitude and LO amplitude conditions. Top plot in each experimental condition shows the mean COM velocity responses to the sine component. Middle and bottom plots for each experimental condition show mean gain and phase values, respectively, calculated for each individual sine cycle. Gain is the ratio of COM response amplitude to stimulus amplitude, while phase represents the temporal dynamics. Mean values of gain and phase during steady-state periods are given in Table 1. Gray shaded areas in gain and phase plots indicate 95% confidence limits.

Fig. 5.

Results for all 6 experimental conditions of mathematical fits to the COM sway velocity responses evoked by the 0.56-Hz sine stimulus following LO-to-HI (top plot in each experimental condition) and HI-to-LO (bottom plot in each experimental condition) transitions in the prts stimulus amplitude. Shown for each experimental condition are the first 5.4 s (3 sine cycles) of the COM sway and fit results following a prts amplitude transition. Gray lines, experimentally measured across-subject mean COM velocity responses following prts amplitude transitions; black lines, mathematical fits to the mean COM velocity data (fit parameters in Table 2); dashed lines, virtual continuations of COM velocity responses to the sine component assuming there were no changes in sway characteristics from the end of the previous steady-state prts period.