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

Author:

Panichi R.1,Faralli M.2,Bruni R.1,Kiriakarely A.1,Occhigrossi C.1,Ferraresi A.1,Bronstein A. M.3,Pettorossi V. E.1ORCID

Affiliation:

1. Dipartimento di Medicina Sperimentale, Sezione di Fisiologia Umana, Università di Perugia, Perugia, Italy

2. Dipartimento di Specialità Medico-Chirurgiche e Sanità Pubblica, Sezione di Otorinolaringoiatria, Università di Perugia, Perugia, Italy

3. Academic Neuro-Otology, Centre for Neuroscience, Charing Cross Hospital, Imperial College London, London, United Kingdom

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.

Funder

Ministero della Salute (Ministry of Health, Italy)

Fondazione Cassa di Risparmio di Perugia

UK MRC and BRC NIHR

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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