Modulation of human vestibular reflexes with increased postural threat

Abstract

Anxiety and arousal have been shown to facilitate human vestibulo-ocular reflexes, presumably through direct neural connections between the vestibular nuclei and emotional processing areas of the brain. However, the effects of anxiety, fear and arousal on balance-relevant vestibular reflexes are currently unknown. The purpose of this study was to manipulate standing height to determine whether anxiety and fear can modulate the direct relationship between vestibular signals and balance reflexes during stance. Stochastic vestibular stimulation (SVS; 2-25 Hz) was used to evoke ground reaction forces (GRF) while subjects stood in both LOW and HIGH surface height conditions. Two separate experiments were conducted to investigate the SVS-GRF relationship, in terms of coupling (coherence and cumulant density) and gain, in the medio-lateral (ML) and antero-posterior (AP) directions. The short- and medium-latency cumulant density peaks were both significantly increased in the ML and AP directions when standing in HIGH, compared to LOW, conditions. Likewise, coherence was statistically greater between 4.3 Hz and 6.7 Hz in the ML, and between 5.5 and 17.7 Hz in the AP direction. When standing in the HIGH condition, the gain of the SVS-GRF relationship was increased 81% in the ML direction, and 231% in the AP direction. The significant increases in coupling and gain observed in both experiments demonstrate that vestibular-evoked balance responses are augmented in states of height-induced postural threat. These data support the possibility that fear or anxiety-mediated changes to balance control are affected by altered central processing of vestibular information.

Figure 1. Head orientation and height-induced threat

Participant head orientation with respect to the edge of the platform (A) and subject standing position at the edge in the HIGH threat condition in the head turned orientation (B).

Figure 2. Study 1 – Effects of height on SVS-GRF cumulant density

Mean LOW and HIGH cumulant density plots with peaks marked (arrows) for head forward (A) and head turned (C) experiments of Study 1. A positive deflection in the head forward cumulant density plot (A) means a positive current (anode right) is associated with a rightward GRF acting on the body or a negative current (anode left) causing a leftward GRF; a positive deflection in the head turned (C) trace indicates a positive current is associated with a forward GRF applied to the body. Mean SLP and MLP amplitudes in the head forward (B; n = 10) and head turned (D; n = 10) experiments; bars indicate SEM.

Figure 3. Study 1 – Effects of height on SVS-GRF coherence and gain

Pooled coherence plots for the LOW and HIGH conditions from the head forward (A) and head turned (D) experiments. Note: thin horizontal line above abscissa represents the threshold for significant within-conditions coherence for both LOW and HIGH conditions. Difference of coherence plotted (thick continuous line) for head forward (B) and head turned (E) experiments of Study 1. Thin horizontal lines represent the upper and lower 95% confidence limits for the test. Any points where the difference of coherence exceeds the 95% confidence limit are taken to be statistically different. Finally, LOW and HIGH gains (thick lines) of the pooled SVS–GRF data are plotted (on a log scale) for head forward (C) and head turned (F) experiments. Thin lines surrounding the gain traces represent point-wise 95% confidence limits; regions where the confidence limits do not overlap are taken to be statistically different.

Figure 4. Results of follow-up control experiments

Cumulant density, coherence, difference of coherence, and gain are plotted for LOW and HIGH conditions concatenated from a sample of 5 subjects with head right and visual fields controlled in Study 2 (A), and a single subject standing with head forward and receiving 0–25 Hz SVS stimulation (B). Conventions are the same as in Figs 2 and 3.