Asymmetric vestibular stimulation reveals persistent disruption of motion perception in unilateral vestibular lesions

Abstract

Self-motion perception was studied in patients with unilateral vestibular lesions (UVL) due to acute vestibular neuritis at 1 wk and 4, 8, and 12 mo after the acute episode. We assessed vestibularly mediated self-motion perception by measuring the error in reproducing the position of a remembered visual target at the end of four cycles of asymmetric whole-body rotation. The oscillatory stimulus consists of a slow (0.09 Hz) and a fast (0.38 Hz) half cycle. A large error was present in UVL patients when the slow half cycle was delivered toward the lesion side, but minimal toward the healthy side. This asymmetry diminished over time, but it remained abnormally large at 12 mo. In contrast, vestibulo-ocular reflex responses showed a large direction-dependent error only initially, then they normalized. Normalization also occurred for conventional reflex vestibular measures (caloric tests, subjective visual vertical, and head shaking nystagmus) and for perceptual function during symmetric rotation. Vestibular-related handicap, measured with the Dizziness Handicap Inventory (DHI) at 12 mo correlated with self-motion perception asymmetry but not with abnormalities in vestibulo-ocular function. We conclude that 1) a persistent self-motion perceptual bias is revealed by asymmetric rotation in UVLs despite vestibulo-ocular function becoming symmetric over time, 2) this dissociation is caused by differential perceptual-reflex adaptation to high- and low-frequency rotations when these are combined as with our asymmetric stimulus, 3) the findings imply differential central compensation for vestibuloperceptual and vestibulo-ocular reflex functions, and 4) self-motion perception disruption may mediate long-term vestibular-related handicap in UVL patients.NEW & NOTEWORTHY A novel vestibular stimulus, combining asymmetric slow and fast sinusoidal half cycles, revealed persistent vestibuloperceptual dysfunction in unilateral vestibular lesion (UVL) patients. The compensation of motion perception after UVL was slower than that of vestibulo-ocular reflex. Perceptual but not vestibulo-ocular reflex deficits correlated with dizziness-related handicap.

Different time course of compensation of subjective visual vertical and ocular torsion after acute unilateral vestibular lesion

“…Dissociation of the recovery time course between reflex and perceptual vestibular responses has already been observed for the self-motion perception and VOR in the horizontal plane after vestibular neuritis. Indeed, the lesion induces an asymmetry of both horizontal VOR and motion perception, but VOR recovers earlier than the motion perception [ 29 ].…”

An fMRI study of visuo-vestibular interactions following vestibular neuritis

“…Whether the development of such chronic symptoms following VN is predominantly mediated by peripheral or central mechanisms remains unclear. Recent data suggests that central mechanisms are more important as supported by, (i) a lack of association between the degree of functional inner-ear loss and symptom load ( Best et al, 2006 ; Cousins et al, 2017 ; Palla et al, 2008 ; Patel et al, 2016 ) and, (ii) the degree of visual reliance during central integration of sensory cues (“visual dependence”) ( Cousins et al, 2017 ), and selective vestibulo-perceptual deficits ( Panichi et al, 2017 ) closely predicting clinical outcome following VN.…”

Derealization and motion-perception related to repeated exposure to 3T Magnetic Resonance Image scanner in healthy adults

“…The short duration of the motion-perception related to the exposure, when the oculomotor (nystagmic) response is known to continue as long as the stimulus [10,25], is an example of the dissociation between perceptual and reflex vestibular responses. To start with, vestibulo-perceptual thresholds are higher than vestibulo-ocular reflex thresholds but, more importantly, vestibulo-perceptual adaption can be quicker and more profound than vestibulo-ocular reflex adaptation in healthy subjects [36], in trained subjects such as dancers [37], and in vestibular patients [38]. The finding that subjects who reported motion perception in and out of the bore showed the lowest vestibular gain to rotation implies that central vestibular processing and adaptation modulated subjects' individual susceptibility for motion perception and derealization symptoms.…”