Dynamic transformation of vestibular signals for orientation

Callum J. Osler, Raymond F. Reynolds

The same pattern of vestibular afferent feedback may signify a loss of balance or a change in body orientation, depending upon the initial head posture. To resolve this ambiguity and generate an appropriate motor response, the CNS must transform vestibular information from a head-centred reference frame into relevant motor coordinates. But what if the reference frame is continuously moving? Here, we ask if this neural transformation process is continuously updated during a voluntary change in head posture. Galvanic vestibular stimulation (GVS) was used to induce a sensation of head roll motion in blindfolded subjects marching on the spot. When head orientation was fixed, this caused unconscious turning behaviour that was maximal during neck flexion, minimal with the head level and reversed direction with neck extension. Subjects were then asked to produce a continuous voluntary change in head pitch, while GVS was applied. As the neck moved from full flexion into extension, turn velocity was continuously modulated and even reversed direction, reflecting the pattern observed during the head-fixed condition. Hence, an identical vestibular input resulted in motor output which was dynamically modulated by changes in head pitch. However, response magnitude was significantly reduced, suggesting possible suppression of vestibular input during voluntary head movement. Nevertheless, these results show that the CNS continuously reinterprets vestibular exafference to account for ongoing voluntary changes in head posture. This may explain why the head can be moved freely without losing the sense of balance and orientation.