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      Artificial Balance: Restoration of the Vestibulo-Ocular Reflex in Humans with a Prototype Vestibular Neuroprosthesis


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          The vestibular system plays a crucial role in the multisensory control of balance. When vestibular function is lost, essential tasks such as postural control, gaze stabilization, and spatial orientation are limited and the quality of life of patients is significantly impaired. Currently, there is no effective treatment for bilateral vestibular deficits. Research efforts both in animals and humans during the last decade set a solid background to the concept of using electrical stimulation to restore vestibular function. Still, the potential clinical benefit of a vestibular neuroprosthesis has to be demonstrated to pave the way for a translation into clinical trials. An important parameter for the assessment of vestibular function is the vestibulo-ocular reflex (VOR), the primary mechanism responsible for maintaining the perception of a stable visual environment while moving. Here we show that the VOR can be artificially restored in humans using motion-controlled, amplitude modulated electrical stimulation of the ampullary branches of the vestibular nerve. Three patients received a vestibular neuroprosthesis prototype, consisting of a modified cochlear implant providing vestibular electrodes. Significantly higher VOR responses were observed when the prototype was turned ON. Furthermore, VOR responses increased significantly as the intensity of the stimulation increased, reaching on average 79% of those measured in healthy volunteers in the same experimental conditions. These results constitute a fundamental milestone and allow us to envision for the first time clinically useful rehabilitation of patients with bilateral vestibular loss.

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          Causative factors and epidemiology of bilateral vestibulopathy in 255 patients.

          To determine the causative factors and epidemiology of bilateral vestibulopathy (BV). This is a retrospective review of 255 patients (mean age, 62 +/- 16 years) with BV diagnosed in our dizziness unit between 1988 and 2005. All patients had undergone a standardized neurophthalmological and neurootological examination, electronystagmography with caloric irrigation, cranial magnetic resonance imaging or computed tomography (n = 214), and laboratory tests. Sixty-two percent of the study population were male subjects. Previous vertigo attacks had occurred in 36%, indicating a sequential manifestation. The definite cause of BV was determined in 24% and the probable cause in 25%: The most common causes were ototoxic aminoglycosides (13%), Menière's disease (7%), and meningitis (5%). Strikingly, 25% exhibited cerebellar signs. Cerebellar dysfunction was associated with peripheral polyneuropathy in 32% compared with 18% in BV patients without cerebellar signs. Hypoacusis occurred bilaterally in 25% and unilaterally in 6% of all patients. It appeared most often in patients with BV caused by Cogan's syndrome, meningitis, or Menière's disease. The cause of BV remains unclear in about half of all patients despite intensive examinations. A large subgroup of these patients have associated cerebellar dysfunction and peripheral polyneuropathy. This suggests a new syndrome that may be caused by neurodegenerative or autoimmune processes.
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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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              Head impulse testing using video-oculography.

              Head impulses are a routine clinical test of semicircular canal function. At the bedside, they are used to detect malfunctioning of the horizontal semicircular canals. So far, 3-D-search-coil recording is required to reliably test anterior and posterior canal function and to determine the gain of the vestibulo-ocular reflex (VOR). Search-coil recording cannot be done at the bedside. Here we tested whether video-oculography (VOG) is suitable to assess VOR gain for individual canals at the bedside. We recorded head impulses in healthy subjects using a mobile high-frame-rate, head-mounted VOG-device and compared the results with those obtained with standard search-coil recording. Our preliminary results indicate that high-frame-rate VOG is a promising tool to measure and quantify individual semicircular canal function not only at the bedside.

                Author and article information

                URI : http://frontiersin.org/people/u/24607
                URI : http://frontiersin.org/people/u/20261
                URI : http://frontiersin.org/people/u/30372
                URI : http://frontiersin.org/people/u/33777
                URI : http://frontiersin.org/people/u/75884
                URI : http://frontiersin.org/people/u/15431
                URI : http://frontiersin.org/people/u/17513
                URI : http://frontiersin.org/people/u/33824
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                29 April 2014
                : 5
                : 66
                [1] 1Service of Otorhinolaryngology and Head and Neck Surgery, Department of Clinical Neurosciences, Geneva University Hospitals , Geneva, Switzerland
                [2] 2Division 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
                [3] 3Translational Neural Engineering Laboratory, Center for Neuroprosthetics, Institute of Bioengineering, École Polytechnique Fédérale de Lausanne , Lausanne, Switzerland
                [4] 4The BioRobotics Institute, Scuola Superiore Sant’Anna , Pisa, Italy
                Author notes

                Edited by: Michael Strupp, Ludwig-Maximilians-Universität München, Germany

                Reviewed by: Michael Strupp, Ludwig-Maximilians-Universität München, Germany; Alexandre Bisdorff, Centre Hospitalier Emile Mayrisch, Luxembourg; Klaus Jahn, University of Munich, Germany

                *Correspondence: Angelica Perez Fornos, Service of Otorhinolaryngology and Head and Neck Surgery, Department of Clinical Neurosciences, Cochlear Implant Center for French Speaking Switzerland, Geneva University Hospitals, Rue Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland e-mail: angelica.perez-fornos@ 123456hcuge.ch

                Angelica Perez Fornos and Nils Guinand are shared first authors.

                This article was submitted to Neuro-otology, a section of the journal Frontiers in Neurology.

                Copyright © 2014 Perez Fornos, Guinand, van de Berg, Stokroos, Micera, Kingma, Pelizzone and Guyot.

                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.

                : 23 February 2014
                : 16 April 2014
                Page count
                Figures: 7, Tables: 2, Equations: 1, References: 41, Pages: 11, Words: 6997
                Original Research

                vestibular implant,balance,sensory neuroprostheses,rehabilitation,vestibulo-ocular reflex


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