Prolonged asymmetric vestibular stimulation induces opposite, long‐term effects on self‐motion perception and ocular responses

Abstract

Key points• The semicircular canals of the labyrinths are a source of information for self-motion perception and reflex eye movements.• Prolonged vestibular asymmetric stimulation of standing humans about the earth-vertical axis, made of fast body rotation to one side and slow rotation to the other side, induced different adaptive mechanisms in the perception of body motion and in the vestibulo-ocular reflex (VOR).• Motion perception became progressively more asymmetric, increasing gradually in response to the fast body rotation and decreasing in response to the slow rotation. VOR became gradually more symmetric, decreasing for fast body movement and increasing for slow movement.• These oppositely directed adaptive effects in motion perception and VOR persisted for at least 30 min.• Long-lasting asymmetric stimulation discloses independent brain mechanisms for perception of body motion and eye movement control.• These adaptive mechanisms may enhance awareness toward the side where the body is moving faster, while improving eye stabilizing properties of the VOR.Abstract Self-motion perception and the vestibulo-ocular reflex (VOR) were investigated in healthy subjects during asymmetric whole body yaw plane oscillations while standing on a platform in the dark. Platform oscillation consisted of two half-sinusoidal cycles of the same amplitude (40 • ) but different duration, featuring a fast (FHC) and a slow half-cycle (SHC). Rotation consisted of four or 20 consecutive cycles to probe adaptation further with the longer duration protocol. Self-motion perception was estimated by subjects tracking with a pointer the remembered position of an earth-fixed visual target. VOR was measured by electro-oculography. The asymmetric stimulation pattern consistently induced a progressive increase of asymmetry in motion perception, whereby the gain of the tracking response gradually increased during FHCs and decreased during SHCs. The effect was observed already during the first few cycles and further increased during 20 cycles, leading to a totally distorted location of the initial straight-ahead. In contrast, after some initial interindividual variability, the gain of the slow phase VOR became symmetric, decreasing for FHCs and increasing for SHCs. These oppositely directed adaptive effects in motion perception and VOR persisted for nearly an hour. Control conditions using prolonged but symmetrical stimuli produced no adaptive effects on either motion perception or VOR. These findings show that prolonged asymmetric activation of the vestibular system leads to opposite patterns of adaptation of self-motion perception and VOR. The results provide strong evidence that semicircular canal inputs are processed centrally by independent mechanisms for perception of body motion and eye movement control. These divergent adaptation mechanisms enhance awareness of movement toward the faster body rotation, while improving the eye stabilizing properties of the VOR.

Vestibular Perception following Acute Unilateral Vestibular Lesions

“…Previous work has shown good correlation between VO-VP responses implying that vestibular perception of angular motion is driven by similar central processes as reflexive eye movements [10], [12], [46]. On the other hand, semicircular canal signals subserving perception appear to undergo differential central processing mechanisms [47]–[49] and here we present further evidence in support: a) the contrast between asymmetric VO and symmetric VP supra-threshold responses (Figures 4 and 5), b) the association between measures of peripheral vestibular function, such as caloric results and VOR gain, with supra-threshold VO but not VP responses and c) the absence of correlation between threshold and supra-threshold data in VP data despite a strong correlation between these variables for VO data (Figure 6). These findings therefore suggest additional neural processing for angular self-motion perception beyond the contribution of the brainstem velocity-storage mechanism of the VOR.…”

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

“… a , b ) and upright (Pettorossi et al . ) postures. We propose that the distinct internal representations of head‐on‐feet orientation for balance and perception may arise due to divergent multisensory and motor cue combinations, a process thought to be task‐ and context‐dependent (van Beers et al .…”

Stepping in Place While Voluntarily Turning Around Produces a Long-Lasting Posteffect Consisting in Inadvertent Turning While Stepping Eyes Closed

“…In the cases mentioned in Pettorossi et al [51, 52], the changes in the abnormal perception after a prolonged rotational vestibular stimulation and neck vibration are long-lasting. That duration is of the same order of magnitude as the duration of the PKARs, pointing to a central modulation of the deviated perception of the straight-ahead in both cases (see [24] for a review).…”