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      The vestibular implant: frequency-dependency of the electrically evoked vestibulo-ocular reflex in humans

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          Abstract

          The vestibulo-ocular reflex (VOR) shows frequency-dependent behavior. This study investigated whether the characteristics of the electrically evoked VOR (eVOR) elicited by a vestibular implant, showed the same frequency-dependency. Twelve vestibular electrodes implanted in seven patients with bilateral vestibular hypofunction (BVH) were tested. Stimuli consisted of amplitude-modulated electrical stimulation with a sinusoidal profile at frequencies of 0.5, 1, and 2 Hz. The main characteristics of the eVOR were evaluated and compared to the “natural” VOR characteristics measured in a group of age-matched healthy volunteers who were subjected to horizontal whole body rotations with equivalent sinusoidal velocity profiles at the same frequencies. A strong and significant effect of frequency was observed in the total peak eye velocity of the eVOR. This effect was similar to that observed in the “natural” VOR. Other characteristics of the (e)VOR (angle, habituation-index, and asymmetry) showed no significant frequency-dependent effect. In conclusion, this study demonstrates that, at least at the specific (limited) frequency range tested, responses elicited by a vestibular implant closely mimic the frequency-dependency of the “normal” vestibular system.

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          Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey.

          Most vestibular nerve afferents can be classified as regularly or irregularly discharging. Two factors are theoretically identified as being potentially responsible for differences in discharge regularity. The first, ascribable to synaptic noise, is the variance (sigma v2) characterizing the transmembrane voltage fluctuations of the axon's spike trigger site, i.e., the place where impulses normally arise. The second factor is the slope (dmuv/dt) of the trigger site's postspike recovery function. Were (dmuv/dt) a major determinant of discharge regularity, the theory predicts that the more irregular the discharge of a unit, the greater should be its sensitivity to externally applied galvanic currents and the faster should be the postspike recovery of its electrical excitability. The predictions would not hold if differences in the discharge regularity between units largely reflected variations in sigma v. To test these predictions, the responses of vestibular nerve afferents to externally applied galvanic currents were studied in the barbiturate-anesthetized squirrel monkey. Current steps of 5-s duration and short (50 microsecond) shocks were delivered by way of the perilymphatic space of the vestibule. Results were similar regardless of which end organ an afferent innervated. The regularity of discharge of each unit was expressed by a normalized coefficient of variation (CV*). The galvanic sensitivity (beta p) of a unit, measured from its response to current steps, was linearly related to discharge regularity (CV*), there being approximately 20-fold variations in both variables across the afferent population. Various geometric factors--including fiber diameter, position of individual axons within the various nerve branches, and the configuration of unmyelinated processes within the sensory epithelium--are unlikely to have made a major contribution to the positive relation between beta P and CV*. The postspike recovery of electrical excitability was measured as response thresholds to shocks, synchronized to follow naturally occurring impulses at several different delays. Recovery in irregular units was more rapid than in regular units. Evidence is presented that externally applied currents acted at the spike trigger site rather than elsewhere in the sensory transduction process. We argue that the irregular discharge of some vestibular afferents offers no functional advantage in the encoding and transmission of sensory information. Rather, the irregularity of discharge is better viewed as a consequence of the enhanced sensitivity of these units to depolarizing influences, including afferent and efferent synaptic inputs.
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            Prevalence and impact of bilateral vestibular hypofunction: results from the 2008 US National Health Interview Survey.

            Profound bilateral vestibular hypofunction (BVH) causes disabling oscillopsia, chronic disequilibrium, and postural instability, but little is known about its epidemiology and impact. To assess prevalence and functional impact of BVH in the US adult population. National cross-sectional survey using a national database and corollary validation study. Adult respondents to the 2008 Balance and Dizziness Supplement to the US National Health Interview Survey (N = 21 782). Prevalence of BVH, socioeconomic and quality-of-life impact of BVH, and fall risk. Criteria for the survey-based diagnosis of BVH included all of the following: presence of visual blurring with head movement; unsteadiness; difficulty walking in darkness or unsteady surfaces and in a straight path; and symptoms being at least "a big problem" and present for at least 1 year, in the absence of other neurologic conditions or eye pathologic conditions affecting vision. Adjusted national estimates from this survey indicate the prevalence of BVH in 2008 was 28 per 100 000 US adults (64 046 Americans). Of the participants with BVH, 44% reported changing their driving habits because of their symptoms, 56% reported reduced participation in social activities, and 58% reported difficulties with activities of daily living. Respondents with BVH had a 31-fold increase in the odds of falling in multivariate analyses compared with all respondents, with 25% reporting a recent fall-related injury. As estimated by the presence of specific symptoms in a nationally representative survey, BVH has considerable socioeconomic and quality-of-life impacts and significantly increases fall risk. These data support the need for new therapeutic strategies for BVH, including vestibular rehabilitation and implantable vestibular prostheses.
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              Quality of life of patients with bilateral vestibulopathy.

              Currently, there is no evidence of an effective treatment for patients with bilateral vestibulopathy (BV). Their main complaints are oscillopsia and imbalance. Opinions about the impact of BV on their quality of life are controversial, and their handicap is not always recognized, even among otoneurologists. The aim of this study was to objectively assess the health status of BV patients in order to evaluate the need for pursuing efforts toward the development of new treatments. The short-form health survey (SF-36), the dizziness handicap inventory (DHI), the short falls efficacy scale-international (short FES-I), and an oscillopsia severity questionnaire were submitted to 39 BV patients. The SF-36 scores were compared to the scores of a general Dutch population. The DHI scores were correlated to the oscillopsia severity scores. The short FES-I scores were compared to scores in an elderly population. Residual otolithic function was correlated to all scores, and hearing to SF-36 scores. Compared to the general Dutch population, the BV patients scored significantly worse on the "physical functioning", "role physical", "general health", "vitality", and "social functioning" SF-36 variables (p < 0.05). The DHI scores were strongly correlated with the oscillopsia severity scores (r = 0.75; p < 0.000001). The short FES-I scores indicated a slight to moderate increase in the patients' fear of falling. No significant score differences were found between BV patients with residual otolithic function and patients with complete BV. There was no correlation between hearing status and SF-36 scores. The results correlate with our clinical impression that BV has a strong negative impact on physical and social functioning, leading to a quality-of-life deterioration. There is a clear need for a therapeutic solution. Efforts toward the development of a vestibular implant are justified.
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                Author and article information

                Contributors
                Journal
                Front Syst Neurosci
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Media S.A.
                1662-5137
                20 January 2015
                2014
                : 8
                : 255
                Affiliations
                [1] 1Division of Balance Disorders, Department of Otorhinolaryngology and Head and Neck Surgery, Faculty of Health Medicine and Life Sciences, School for Mental Health and Neuroscience, Maastricht University Medical Center Maastricht, Netherlands
                [2] 2Faculty of Physics, Tomsk State University Tomsk, Russia
                [3] 3Service of Otorhinolaryngology and Head and Neck Surgery, Department of Clinical Neurosciences, Geneva University Hospitals Geneva, Switzerland
                [4] 4Translational Neural Engineering Lab, Center for Neuroprosthetics, Interfaculty Institute of Bioengineering, École Polytechnique Fédérale de Lausanne Lausanne, Switzerland
                Author notes

                Edited by: Mikhail Lebedev, Duke University, USA

                Reviewed by: Bernard Cohen, Mount Sinai School of Medicine, USA; Hans VanDerSteen, Erasmus Medical Center, Netherlands; Stefano Ramat, Università degli Studi di Pavia, Italy; Maria Cervera De La Rosa, Universidad Carlos III de Madrid, Spain

                *Correspondence: Raymond van de Berg, Department of Otorhinolaryngology and Head and Neck Surgery, Maastricht University Medical Center, Postbus 5800, 6202 AZ Maastricht, Netherlands e-mail: raymond.vande.berg@ 123456mumc.nl

                This article was submitted to the journal Frontiers in Systems Neuroscience.

                Article
                10.3389/fnsys.2014.00255
                4299437
                25653601
                68f16e0f-fdf6-4d66-bfc3-47d903a7c056
                Copyright © 2015 van de Berg, Guinand, Nguyen, Ranieri, Cavuscens, Guyot, Stokroos, Kingma and Perez-Fornos.

                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
                : 29 October 2014
                : 29 December 2014
                Page count
                Figures: 7, Tables: 2, Equations: 0, References: 54, Pages: 12, Words: 7185
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                vestibular implant,vestibular prosthesis,neural prosthesis,bilateral vestibular areflexia,bilateral vestibulopathy,vestibulo-ocular reflex

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