Feedforward versus feedback modulation of human vestibular-evoked balance responses by visual self-motion information

Abstract

Visual information modulates the balance response evoked by a pure vestibular perturbation (galvanic vestibular stimulation, GVS). Here we investigate two competing hypotheses underlying this visual-vestibular interaction. One hypothesis assumes vision acts in a feedforward manner by altering the weight of the vestibular channel of balance control. The other assumes vision acts in a feedback manner through shifts in the retinal image produced by the primary response. In the first experiment we demonstrate a phenomenon that is predicted by both hypotheses: the GVS-evoked balance response becomes progressively smaller as the amount of visual self-motion information is increased. In the second experiment we independently vary the pre-stimulus and post-stimulus visual environments. The rationale is that feedback effects would depend only upon the post-stimulus visual environment. Although the post-stimulus visual environment did affect later parts of the response (after approximately 400 ms), the pre-stimulus visual environment had a strong influence on the size of the early part of the response. We conclude that both feedforward and feedback mechanisms act in concert to modulate the GVS-evoked response. We suggest this dual interaction that we observe between visual and vestibular channels is likely to apply to all sensory channels that contribute to balance control.

Figure 1. Geometrical configuration of coloured LEDs used to generate the four visual environments

Subjects stood in a blacked-out room whilst viewing no LEDs (vis0), a single blue LED (vis1), a two-dimensional grid of alternating red and green LEDS (vis2), or a three-dimensional structure of red and green LEDs (vis3).

Figure 2. Effect of visual environment on group mean lateral responses

From top: lateral displacement of the neck marker at C7, lateral ground reaction force and GVS timing. Positive deflections are in the direction of the anodal ear. The visual environments were vis0 (black), vis1 (blue), vis2 (green) or vis3 (red). The same data are shown in A and B on different time scales.

Figure 3. Effect of visual environment on group mean summary responses

Histograms show mean (+s.e.m.) GVS-evoked response in the direction of the anodal ear as measured from: A, neck (C7) position at 2 s latency, and B, ground reaction force at 400 ms latency. C shows mean speed of spontaneous sway without GVS. Statistical contrasts shown by brackets (*P < 0.05; **P < 0.01).

Figure 4. Effect of switching the visual environment on group mean responses to GVS

Traces show mean C7 lateral displacement (top panels) and mean lateral ground reaction force (middle panels; note different time scale) to unswitched (vis0, continuous black lines; vis3, continuous red lines) and switched (vis0to3, dashed black lines; vis3to0, dashed red lines) environments. Positive deflections are in the direction of the anodal ear. GVS indicates time of stimulation. Scene indicates time of visual switch. Lower histograms show mean (+s.e.m.) force response magnitude at 400 ms latency for the four visual conditions. Statistical contrasts shown by brackets (**P < 0.01; ***P < 0.001). The scene switch occurred either 150 ms (A, C and E) or 0 ms (B, D and F) after GVS onset.