Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.

The normal vestibulo-ocular reflex (VOR) generates almost perfectly compensatory smooth eye movements during a 'head-impulse' rotation. An imperfect VOR gain provokes additional compensatory saccades to re-acquire an earth-fixed target. In the present study, we investigated vestibular and...

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Main Authors: Jacob M Pogson, Rachael L Taylor, Leigh A McGarvie, Andrew P Bradshaw, Mario D'Souza, Sean Flanagan, Jonathan Kong, G Michael Halmagyi, Miriam S Welgampola
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0227406
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author Jacob M Pogson
Rachael L Taylor
Leigh A McGarvie
Andrew P Bradshaw
Mario D'Souza
Sean Flanagan
Jonathan Kong
G Michael Halmagyi
Miriam S Welgampola
author_facet Jacob M Pogson
Rachael L Taylor
Leigh A McGarvie
Andrew P Bradshaw
Mario D'Souza
Sean Flanagan
Jonathan Kong
G Michael Halmagyi
Miriam S Welgampola
author_sort Jacob M Pogson
collection DOAJ
description The normal vestibulo-ocular reflex (VOR) generates almost perfectly compensatory smooth eye movements during a 'head-impulse' rotation. An imperfect VOR gain provokes additional compensatory saccades to re-acquire an earth-fixed target. In the present study, we investigated vestibular and visual contributions on saccade production. Eye position and velocity during horizontal and vertical canal-plane head-impulses were recorded in the light and dark from 16 controls, 22 subjects after complete surgical unilateral vestibular deafferentation (UVD), eight subjects with idiopathic bilateral vestibular loss (BVL), and one subject after complete bilateral vestibular deafferentation (BVD). When impulses were delivered in the horizontal-canal plane, in complete darkness compared with light, first saccade frequency mean(SEM) reduced from 96.6(1.3)-62.3(8.9) % in BVL but only 98.3(0.6)-92.0(2.3) % in UVD; saccade amplitudes reduced from 7.0(0.5)-3.6(0.4) ° in BVL but were unchanged 6.2(0.3)-5.5(0.6) ° in UVD. In the dark, saccade latencies were prolonged in lesioned ears, from 168(8.4)-240(24.5) ms in BVL and 177(5.2)-196(5.7) ms in UVD; saccades became less clustered. In BVD, saccades were not completely abolished in the dark, but their amplitudes decreased from 7.3-3.0 ° and latencies became more variable. For unlesioned ears (controls and unlesioned ears of UVD), saccade frequency also reduced in the dark, but their small amplitudes slightly increased, while latency and clustering remained unchanged. First and second saccade frequencies were 75.3(4.5) % and 20.3(4.1) %; without visual fixation they dropped to 32.2(5.0) % and 3.8(1.2) %. The VOR gain was affected by vision only in unlesioned ears of UVD; gains for the horizontal-plane rose slightly, and the vertical-planes reduced slightly. All head-impulse compensatory saccades have a visual contribution, the magnitude of which depends on the symmetry of vestibular-function and saccade latency: BVL is more profoundly affected by vision than UVD, and second saccades more than first saccades. Saccades after UVD are probably triggered by contralateral vestibular function.
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spelling doaj.art-cddeed44b26e4de3bbaa4b116e7af4bf2022-12-21T19:28:52ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01151e022740610.1371/journal.pone.0227406Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.Jacob M PogsonRachael L TaylorLeigh A McGarvieAndrew P BradshawMario D'SouzaSean FlanaganJonathan KongG Michael HalmagyiMiriam S WelgampolaThe normal vestibulo-ocular reflex (VOR) generates almost perfectly compensatory smooth eye movements during a 'head-impulse' rotation. An imperfect VOR gain provokes additional compensatory saccades to re-acquire an earth-fixed target. In the present study, we investigated vestibular and visual contributions on saccade production. Eye position and velocity during horizontal and vertical canal-plane head-impulses were recorded in the light and dark from 16 controls, 22 subjects after complete surgical unilateral vestibular deafferentation (UVD), eight subjects with idiopathic bilateral vestibular loss (BVL), and one subject after complete bilateral vestibular deafferentation (BVD). When impulses were delivered in the horizontal-canal plane, in complete darkness compared with light, first saccade frequency mean(SEM) reduced from 96.6(1.3)-62.3(8.9) % in BVL but only 98.3(0.6)-92.0(2.3) % in UVD; saccade amplitudes reduced from 7.0(0.5)-3.6(0.4) ° in BVL but were unchanged 6.2(0.3)-5.5(0.6) ° in UVD. In the dark, saccade latencies were prolonged in lesioned ears, from 168(8.4)-240(24.5) ms in BVL and 177(5.2)-196(5.7) ms in UVD; saccades became less clustered. In BVD, saccades were not completely abolished in the dark, but their amplitudes decreased from 7.3-3.0 ° and latencies became more variable. For unlesioned ears (controls and unlesioned ears of UVD), saccade frequency also reduced in the dark, but their small amplitudes slightly increased, while latency and clustering remained unchanged. First and second saccade frequencies were 75.3(4.5) % and 20.3(4.1) %; without visual fixation they dropped to 32.2(5.0) % and 3.8(1.2) %. The VOR gain was affected by vision only in unlesioned ears of UVD; gains for the horizontal-plane rose slightly, and the vertical-planes reduced slightly. All head-impulse compensatory saccades have a visual contribution, the magnitude of which depends on the symmetry of vestibular-function and saccade latency: BVL is more profoundly affected by vision than UVD, and second saccades more than first saccades. Saccades after UVD are probably triggered by contralateral vestibular function.https://doi.org/10.1371/journal.pone.0227406
spellingShingle Jacob M Pogson
Rachael L Taylor
Leigh A McGarvie
Andrew P Bradshaw
Mario D'Souza
Sean Flanagan
Jonathan Kong
G Michael Halmagyi
Miriam S Welgampola
Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.
PLoS ONE
title Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.
title_full Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.
title_fullStr Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.
title_full_unstemmed Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.
title_short Head impulse compensatory saccades: Visual dependence is most evident in bilateral vestibular loss.
title_sort head impulse compensatory saccades visual dependence is most evident in bilateral vestibular loss
url https://doi.org/10.1371/journal.pone.0227406
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