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      Plasticity during Vestibular Compensation: The Role of Saccades

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          Abstract

          This paper is focused on one major aspect of compensation: the recent measures of saccadic responses to high acceleration head turns during human vestibular compensation and their possible implications for recovery after unilateral vestibular loss (UVL). New measurement techniques have provided additional insights into how patients recover after UVL and have given clues for vestibular rehabilitation. Prior to this it has not been possible to quantify the level of function of all the peripheral vestibular sense organs. Now it is. By using vestibular-evoked myogenic potentials to measure utricular and saccular function and by new video head impulse testing to measure semicircular canal function to natural values of head accelerations. With these new video procedures it is now possible to measure both slow phase eye velocity and also saccades during head movements with natural values of angular acceleration. The present evidence is that after UVL there is little or no restoration/compensation of slow phase eye velocity responses to natural head accelerations. It is doubtful as to whether the modest changes in slow phase eye velocity to small angular accelerations are functionally effective during compensation. On the other hand it is now clear that saccades can play a very important role in helping patients compensate and return to a normal lifestyle. Preliminary evidence suggests that different patterns of saccadic response may predict how well patients recover. Furthermore it may be possible to train patients to produce more effective saccadic patterns in the first days after their unilateral loss and possibly improve their compensation process. Some patients do learn new strategies, new behaviors, to conceal their inadequate vestibulo-ocular response but when those strategies are prevented from operating by using passive, unpredictable, high acceleration natural head movements, as in the head impulse test, the vestibular loss can be demonstrated. It is those very strategies which the tests exclude, which may be the cause of their successful compensation.

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          Most cited references26

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          A clinical sign of canal paresis.

          Unilateral loss of horizontal semicircular canal function, termed canal paresis, is an important finding in dizzy patients. To our knowledge, apart from head-shaking nystagmus, no clinical sign of canal paresis has yet been described and the term derives from the characteristic finding on caloric tests: little or no nystagmus evoked by either hot or cold irrigation of the affected ear. We describe a simple and reliable clinical sign of total unilateral loss of horizontal semicircular canal function: one large or several small oppositely directed, compensatory, refixation saccades elicited by rapid horizontal head rotation toward the lesioned side. Using magnetic search coils to measure head and eye movement, we have validated this sign in 12 patients who had undergone unilateral vestibular neurectomy.
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            The video head impulse test: diagnostic accuracy in peripheral vestibulopathy.

            The head impulse test (HIT) is a useful bedside test to identify peripheral vestibular deficits. However, such a deficit of the vestibulo-ocular reflex (VOR) may not be diagnosed because corrective saccades cannot always be detected by simple observation. The scleral search coil technique is the gold standard for HIT measurements, but it is not practical for routine testing or for acute patients, because they are required to wear an uncomfortable contact lens. To develop an easy-to-use video HIT system (vHIT) as a clinical tool for identifying peripheral vestibular deficits. To validate the diagnostic accuracy of vHIT by simultaneous measures with video and search coil recordings across healthy subjects and patients with a wide range of previously identified peripheral vestibular deficits. Horizontal HIT was recorded simultaneously with vHIT (250 Hz) and search coils (1,000 Hz) in 8 normal subjects, 6 patients with vestibular neuritis, 1 patient after unilateral intratympanic gentamicin, and 1 patient with bilateral gentamicin vestibulotoxicity. Simultaneous video and search coil recordings of eye movements were closely comparable (average concordance correlation coefficient r(c) = 0.930). Mean VOR gains measured with search coils and video were not significantly different in normal (p = 0.107) and patients (p = 0.073). With these groups, the sensitivity and specificity of both the reference and index test were 1.0 (95% confidence interval 0.69-1.0). vHIT measures detected both overt and covert saccades as accurately as coils. The video head impulse test is equivalent to search coils in identifying peripheral vestibular deficits but easier to use in clinics, even in patients with acute vestibular neuritis.
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              Myogenic potentials generated by a click-evoked vestibulocollic reflex.

              Electromyograms (EMGs) were recorded from surface electrodes over the sternomastoid muscles and averaged in response to brief (0.1 ms) clicks played through headphones. In normal subjects, clicks 85 to 100 dB above our reference (45 dB SPL: close to perceptual threshold for normal subjects for such clicks) evoked reproducible changes in the averaged EMG beginning at a mean latency of 8.2 ms. The earliest potential change, a biphasic positive-negativity (p13-n23), occurred in all subjects and the response recorded from over the muscle on each side was predominantly generated by afferents originating from the ipsilateral ear. Later potentials (n34, p44), present in most but not all subjects, were generated bilaterally after unilateral ear stimulation. The amplitude of the averaged responses increased in direct proportion to the mean level of tonic muscle activation during the recording period. The p13-n23 response was abolished in patients who had undergone selective section of the vestibular nerve but was preserved in subjects with severe sensorineural hearing loss. It is proposed that the p13-n23 response is generated by activation of vestibular afferents, possibly those arising from the saccule, and transmitted via a rapidly conducting oligosynaptic pathway to anterior neck muscles. Conversely, the n34 and p44 potentials do not depend on the integrity of the vestibular nerve and probably originate from cochlear afferents.
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                Author and article information

                Journal
                Front Neurol
                Front Neurol
                Front. Neur.
                Frontiers in Neurology
                Frontiers Research Foundation
                1664-2295
                30 November 2011
                28 February 2012
                2012
                : 3
                : 21
                Affiliations
                [1] 1simpleVestibular Research Laboratory, School of Psychology, The University of Sydney Sydney, NSW, Australia
                Author notes

                Edited by: Pierre-Paul Vidal, Universite Rene Descartes/CNRS, France

                Reviewed by: Ted Raphan, Brooklyn College of CUNY, USA; Seong-Hae Jeong, Chungnam National University Hospital, South Korea

                *Correspondence: Ian S. Curthoys, Vestibular Research Laboratory, School of Psychology, The University of Sydney, A18, Sydney, NSW, Australia. e-mail: ianc@ 123456psych.usyd.edu.au

                This article was submitted to Frontiers in Neuro-otology, a specialty of Frontiers in Neurology.

                Article
                10.3389/fneur.2012.00021
                3289127
                22403569
                72e160f0-f00b-4354-9651-272136d5be51
                Copyright © 2012 MacDougall and Curthoys.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                : 07 November 2011
                : 03 February 2012
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 26, Pages: 9, Words: 7592
                Categories
                Neuroscience
                Review Article

                Neurology
                otolith,saccular,labyrinth,semicircular canal,utricular,ovemp,bone conduction
                Neurology
                otolith, saccular, labyrinth, semicircular canal, utricular, ovemp, bone conduction

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