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      Postural Control in Bilateral Vestibular Failure: Its Relation to Visual, Proprioceptive, Vestibular, and Cognitive Input

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          Abstract

          Patients with bilateral vestibular failure (BVF) suffer from postural and gait unsteadiness with an increased risk of falls. The aim of this study was to elucidate the differential role of otolith, semicircular canal (SSC), visual, proprioceptive, and cognitive influences on the postural stability of BVF patients. Center-of-pressure displacements were recorded by posturography under six conditions: target visibility; tonic head positions in the pitch plane; horizontal head shaking; sensory deprivation; dual task; and tandem stance. Between-group analysis revealed larger postural sway in BVF patients on eye closure; but with the eyes open, BVF did not differ from healthy controls (HCs). Head tilts and horizontal head shaking increased sway but did not differ between groups. In the dual task condition, BVF patients maintained posture indistinguishable from controls. On foam and tandem stance, postural sway was larger in BVF, even with the eyes open. The best predictor for the severity of bilateral vestibulopathy was standing on foam with eyes closed. Postural control of our BVF was indistinguishable from HCs once visual and proprioceptive feedback is provided. This distinguishes them from patients with vestibulo-cerebellar disorders or functional dizziness. It confirms previous reports and explains that postural unsteadiness of BVF patients can be missed easily if not examined by conditions of visual and/or proprioceptive deprivation. In fact, the best predictor for vestibular hypofunction (VOR gain) was examining patients standing on foam with the eyes closed. Postural sway in that condition increased with the severity of vestibular impairment but not with disease duration. In the absence of visual control, impaired otolith input destabilizes BVF with head retroflexion. Stimulating deficient SSC does not distinguish patients from controls possibly reflecting a shift of intersensory weighing toward proprioceptive-guided postural control. Accordingly, proprioceptive deprivation heavily destabilizes BVF, even when visual control is provided.

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          Most cited references68

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          Vestibular evoked myogenic potentials: past, present and future.

          Since the first description of sound-evoked short-latency myogenic reflexes recorded from neck muscles, vestibular evoked myogenic potentials (VEMPs) have become an important part of the neuro-otological test battery. VEMPs provide a means of assessing otolith function: stimulation of the vestibular system with air-conducted sound activates predominantly saccular afferents, while bone-conducted vibration activates a combination of saccular and utricular afferents. The conventional method for recording the VEMP involves measuring electromyographic (EMG) activity from surface electrodes placed over the tonically-activated sternocleidomastoid (SCM) muscles. The "cervical VEMP" (cVEMP) is thus a manifestation of the vestibulo-collic reflex. However, recent research has shown that VEMPs can also be recorded from the extraocular muscles using surface electrodes placed near the eyes. These "ocular VEMPs" (oVEMPs) are a manifestation of the vestibulo-ocular reflex. Here we describe the historical development and neurophysiological properties of the cVEMP and oVEMP and provide recommendations for recording both reflexes. While the cVEMP has documented diagnostic utility in many disorders affecting vestibular function, relatively little is known as yet about the clinical value of the oVEMP. We therefore outline the known cVEMP and oVEMP characteristics in common central and peripheral disorders encountered in neuro-otology clinics. Copyright 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
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            Regularity of center-of-pressure trajectories depends on the amount of attention invested in postural control

            The influence of attention on the dynamical structure of postural sway was examined in 30 healthy young adults by manipulating the focus of attention. In line with the proposed direct relation between the amount of attention invested in postural control and regularity of center-of-pressure (COP) time series, we hypothesized that: (1) increasing cognitive involvement in postural control (i.e., creating an internal focus by increasing task difficulty through visual deprivation) increases COP regularity, and (2) withdrawing attention from postural control (i.e., creating an external focus by performing a cognitive dual task) decreases COP regularity. We quantified COP dynamics in terms of sample entropy (regularity), standard deviation (variability), sway-path length of the normalized posturogram (curviness), largest Lyapunov exponent (local stability), correlation dimension (dimensionality) and scaling exponent (scaling behavior). Consistent with hypothesis 1, standing with eyes closed significantly increased COP regularity. Furthermore, variability increased and local stability decreased, implying ineffective postural control. Conversely, and in line with hypothesis 2, performing a cognitive dual task while standing with eyes closed led to greater irregularity and smaller variability, suggesting an increase in the “efficiency, or “automaticity” of postural control”. In conclusion, these findings not only indicate that regularity of COP trajectories is positively related to the amount of attention invested in postural control, but also substantiate that in certain situations an increased internal focus may in fact be detrimental to postural control.
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              Adaptation to altered support and visual conditions during stance: patients with vestibular deficits.

              Patients whose deficits were limited to clinically well qualified vestibular disorders have been exposed to a number of altered support surface and visual environments while standing unsupported. A six-degrees-of-freedom platform employing movable support surfaces for each foot and a movable visual surround deprived patients of normal inputs derived from a fixed level support surface and from an immobile surround. Various tests employing EMG, force, and body movement recording identified quantitative changes in the patients' strategy for the relative weighting of proprioceptive, vestibular, and visual inputs. The most dramatic performance deficit of patients was their inability to suppress the influence of visual and proprioceptive inputs appropriately whenever motions of external surface disturbed the orientation information provided by these inputs. Thus, the more mildly afflicted patients experienced instability not so much because of the loss of vestibular inputs directly to posture but because of their inappropriate responses to proprioceptive inputs and vision. Discussion is centered on the role of vestibular input as an internal reference system for orientation about which adaptive changes in proprioceptive and visual inputs are made.
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                Author and article information

                Contributors
                URI : http://frontiersin.org/people/u/94479
                URI : http://frontiersin.org/people/u/468221
                URI : http://frontiersin.org/people/u/19440
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                01 September 2017
                2017
                : 8
                : 444
                Affiliations
                [1] 1Department of Neurology, University of Lübeck , Lubeck, Germany
                [2] 2Institute of Psychology II, University of Lübeck , Lubeck, Germany
                Author notes

                Edited by: Herman Kingma, Maastricht University, Netherlands

                Reviewed by: Pierre-Paul Vidal, Université Paris Descartes, France; Andrés Soto-Varela, Complejo Hospitalario Universitario de Santiago, Spain

                *Correspondence: Andreas Sprenger, andreas.sprenger@ 123456neuro.uni-luebeck.de

                Specialty section: This article was submitted to Neuro-Otology, a section of the journal Frontiers in Neurology

                Article
                10.3389/fneur.2017.00444
                5585141
                28919878
                506393a1-b206-4fab-870c-fc577ef4e4b4
                Copyright © 2017 Sprenger, Wojak, Jandl and Helmchen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 18 May 2017
                : 14 August 2017
                Page count
                Figures: 5, Tables: 0, Equations: 1, References: 75, Pages: 10, Words: 7500
                Categories
                Neuroscience
                Original Research

                Neurology
                bilateral vestibular failure,postural control,posturography,proprioception,multisensory integration

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