Transformation of Vestibular Signals for the Control of Standing in Humans

Abstract

During standing balance, vestibular signals encode head movement and are transformed into coordinates that are relevant to maintaining upright posture of the whole body. This transformation must account for head-on-body orientation as well as the muscle actions generating the postural response. Here, we investigate whether this transformation is dependent upon a muscle's ability to stabilize the body along the direction of a vestibular disturbance. Subjects were braced on top of a robotic balance system that simulated the mechanics of standing while being exposed to an electrical vestibular stimulus that evoked a craniocentric vestibular error of head roll. The balance system was limited to move in a single plane while the vestibular error direction was manipulated by having subjects rotate their head in yaw. Vestibular-evoked muscle responses were greatest when the vestibular error was aligned with the balance direction and decreased to zero as the two directions became orthogonal. This demonstrates that muscles respond only to the component of the error that is aligned with the balance direction and thus relevant to the balance task, not to the cumulative afferent activity, as expected for vestibulospinal reflex loops. When we reversed the relationship between balancing motor commands and associated vestibular sensory feedback, the direction of vestibular-evoked ankle compensatory responses was also reversed. This implies that the nervous system quickly reassociates new relationships between vestibular sensory signals and motor commands related to maintaining balance. These results indicate that vestibular-evoked muscle activity is a highly flexible balance response organized to compensate for vestibular disturbances.

The effect of fear of falling on vestibular feedback control of balance

“…; Forbes et al. , ). Whether and how fear of falling influences these physiological control systems is currently debated (Horslen et al.…”

“…Forbes et al. () altered head yaw systematically and showed craniocentric modulation of muscle activities at short and medium latency. Mian and Day () altered stance width and head orientation and showed balance relevant modulation of response at short and medium latency.…”

“…For example, appendicular vestibular reflexes are task and posture dependent, whereas axial reflexes are less dependent on task and posture (Forbes et al. , , ).…”

The medium latency muscle response to a vestibular perturbation is increased after depression of the cerebellar vermis

“…Therefore, it is a strong possibility that there is sufficient time, and that the cerebellum does indeed affect the response, particularly since our data showed that there was a trend for an increase. Even if the SL response does not travel through the cerebellum, it is likely the cerebellar output is still able to modulate the excitability of the vestibular nuclei, which would result in a change in SL response amplitude (Forbes et al., 2016). We may not have been able to detect significant changes in the SL response due to certain parameters of the experimental protocol, including the intensity of the stimulus and the postural orientation.…”

“…There is literature to suggest that the SL response may not be consistent or reliable when the vestibular stimulus is below 2 mA (Ali, Rowen, & Iles, 2003; Fitzpatrick et al., 1994). Additionally, the quality of the reflexes may have been compromised with head orientation, as the reflexes are obtainable [as evidenced by the results of our study and other experiments (Dakin, Son, Inglis, & Blouin, 2007; Day et al., 1997; Forbes et al., 2016; Nashner & Wolfson, 1974)], yet not as prominent in the soleus muscle with the head facing forward (Fitzpatrick et al., 1994). Most studies examining vestibular reflexes have subjects stand with their head facing over the shoulder (Britton et al., 1993; Fitzpatrick et al., 1994; Lund & Broberg, 1983; Nashner & Wolfson, 1974; Welgampola & Colebatch, 2001), however, we opted to test the reflexes with head forward as we have shown in a previous experiment that depressing the cerebellar vermis with cTBS can result in a modulation in the postural sway direction, such that it is no longer intra‐aural with the head facing over the shoulder (Lam et al., 2016).…”