Sensory reweighting dynamics following removal and addition of visual and proprioceptive cues

Abstract

Removing or adding sensory cues from one sensory system during standing balance causes a change in the contribution of the remaining sensory systems, a process referred to as sensory reweighting. While reweighting changes have been described in many studies under steady-state conditions, less is known about the temporal dynamics of reweighting following sudden transitions to different sensory conditions. The present study changed sensory conditions by periodically adding or removing visual (lights On/Off) or proprioceptive cues (surface sway referencing On/Off) in 12 young, healthy subjects. Evidence for changes in sensory contributions to balance was obtained by measuring the time course of medial-lateral sway responses to a constant-amplitude 0.56-Hz sinusoidal stimulus, applied as support surface tilt (proprioceptive contribution), as visual scene tilt (visual contribution), or as binaural galvanic vestibular stimulation (vestibular contribution), and by analyzing the time course of sway variability. Sine responses and variability of body sway velocity showed significant changes following transitions and were highly correlated under steady-state conditions. A dependence of steady-state responses on upcoming transitions was observed, suggesting that knowledge of impending changes can influence sensory weighting. Dynamic changes in sway in the period immediately following sensory transitions were very inhomogeneous across sway measures and in different experimental tests. In contrast to steady-state results, sway response and variability measures were not correlated with one another in the dynamic transition period. Several factors influence sway responses following addition or removal of sensory cues, partly instigated by but also obscuring the effects of reweighting dynamics.

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

Fig. 1.

A: table of experimental conditions and corresponding stimulus combinations. EC and EO refer to eyes-closed and eyes-open conditions. B: schema of the experimental setup. C: example of the applied stimulus sequence, showing the transient On and Off switching of sway referencing (Exps. 1–3) or lights (Exps. 4–6), the constant amplitude sinusoidal stimulus, and the measured COM sway of 1 representative subject.

Fig. 2.

COM sway velocity averaged across subjects and cycles (mean, top) and variability of COM sway velocity, calculated as the standard deviation across subjects and cycles (std, bottom) for each of the 6 experimental tests. The mean (sine response) resembles the component evoked by the constant-amplitude sinusoidal stimulus. The standard deviation (sway variability) across time resembles the component that is not evoked by the sinusoidal stimulus.

Fig. 3.

Steady-state values of sine response amplitude, sine response phase, and sway variability. A: Off (open bars) and On (gray bars) steady-state values, defined as the average values during the 10.8 s prior to a transition; error bars indicate 95% bootstrap confidence limits. Results of bootstrap significance tests for differences between On and Off values are represented by * (P < 0.05) or ** (P < 0.01). B: comparison of sway variability and sine response amplitude for each steady state. Diagonal line indicates identity of both parameters. C: selected parameters, with 95% confidence limits, for the comparison of pairs with identical steady-state conditions that were realized twice in different experimental tests. The only difference within each pair is that for one steady-state condition the upcoming transition is switching sway referencing On (P1) or Off (P4), while the other is switching lights On (P1) or Off (P4). Only parameters of pairs with significant differences are shown. Other combinations of identical steady-state conditions are indicated in Tables 1 and 2.

Fig. 4.

Time course of the identified exponential fit functions (black line) that best described the experimental COM sway velocity data (gray line). Shown are the Off-to-On and On-to-Off transitions of the sine responses (mean, top) and of the sway variability (std, bottom) for all experimental tests. Note that the scale of the y-axis changes across tests.

Fig. 5.

Transition times of all experimental tests. A: definition of transition times for the sine response amplitude (left) and sway variability (right). B and C: summary of transition times with sine response phase plotted over sine response amplitude (B) and sway variability plotted over sine response amplitude (C). Very large transition times are indicated with arrows and the corresponding values in parentheses.