The internal representation of head orientation differs for conscious perception and balance control

We tested perceived head-on-feet orientation and the direction of vestibular-evoked balance responses in passively and actively held head-turned postures. The direction of vestibular-evoked balance responses was not aligned with perceived head-on-feet orientation while maintaining prolonged passively held head-turned postures. Furthermore, static visual cues of head-on-feet orientation did not update the estimate of head posture for the balance controller. A prolonged actively held head-turned posture did not elicit a rotation in the direction of the vestibular-evoked balance response despite a significant rotation in perceived angular head posture. It is proposed that conscious perception of head posture and the transformation of vestibular signals for standing balance relying on this head posture are not dependent on the same internal representation. Rather, the balance system may operate under its own sensorimotor principles, which are partly independent from perception.

Vestibular signals used for balance control must be integrated with other sensorimotor cues to allow transformation of descending signals according to an internal representation of body configuration. We explored two alternative models of sensorimotor integration that propose (1) a single internal representation of head-on-feet orientation is responsible for perceived postural orientation and standing balance or (2) conscious perception and balance control are driven by separate internal representations. During three experiments, participants stood quietly while passively or actively maintaining a prolonged head-turned posture (>10 min). Throughout the trials, participants intermittently reported their perceived head angular position, and subsequently electrical vestibular stimuli were delivered to elicit whole-body balance responses. Visual recalibration of head-on-feet posture was used to determine whether static visual cues are used to update the internal representation of body configuration for perceived orientation and standing balance. All three experiments involved situations in which the vestibular-evoked balance response was not orthogonal to perceived head-on-feet orientation, regardless of the visual information provided. For prolonged head-turned postures, balance responses consistent with actual head-on-feet posture occurred only during the active condition. Our results indicate that conscious perception of head-on-feet posture and vestibular control of balance do not rely on the same internal representation, but instead treat sensorimotor cues in parallel and may arrive at different conclusions regarding head-on-feet posture. The balance system appears to bypass static visual cues of postural orientation and mainly use other sensorimotor signals of head-on-feet position to transform vestibular signals of head motion, a mechanism appropriate for most daily activities.