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      Errors of Upright Perception in Patients With Vestibular Migraine

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          Abstract

          Patients with vestibular migraine (VM) often report dizziness with changes in the head or body position. Such symptoms raise the possibility of dysfunction in neural mechanisms underlying spatial orientation in these patients. Here we addressed this issue by investigating the effect of static head tilts on errors of upright perception in a group of 27 VM patients in comparison with a group of 27 healthy controls. Perception of upright was measured in a dark room using a subjective visual vertical (SVV) paradigm at three head tilt positions (upright, ±20°). VM patients were also surveyed about the quality of their dizziness and spatial symptoms during daily activities. In the upright head position, SVV errors were within the normal range for VM patients and healthy controls (within 2° from true vertical). During the static head tilts of 20° to the right, VM patients showed larger SVV errors consistent with overestimation of the tilt magnitude (i.e., as if they felt further tilted toward the right side) (VM: −3.21° ± 0.93 vs. Control: 0.52° ± 0.70; p = 0.002). During the head tilt to the left, SVV errors in VM patients did not differ significantly from controls (VM: 0.77° ± 1.05 vs. Control: −0.04° ± 0.68; p = 0.52). There was no significant difference in SVV precision between the VM patients and healthy controls at any head tilt position. Consistent with the direction of the SVV errors in VM patients, they largely reported spatial symptoms toward the right side. These findings suggest an abnormal sensory integration for spatial orientation in vestibular migraine, related to daily dizziness in these patients.

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          Most cited references33

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          Vestibular migraine: diagnostic criteria.

          This paper presents diagnostic criteria for vestibular migraine, jointly formulated by the Committee for Classification of Vestibular Disorders of the Bárány Society and the Migraine Classification Subcommittee of the International Headache Society (IHS). The classification includes vestibular migraine and probable vestibular migraine. Vestibular migraine will appear in an appendix of the third edition of the International Classification of Headache Disorders (ICHD) as a first step for new entities, in accordance with the usual IHS procedures. Probable vestibular migraine may be included in a later version of the ICHD, when further evidence has been accumulated. The diagnosis of vestibular migraine is based on recurrent vestibular symptoms, a history of migraine, a temporal association between vestibular symptoms and migraine symptoms and exclusion of other causes of vestibular symptoms. Symptoms that qualify for a diagnosis of vestibular migraine include various types of vertigo as well as head motion-induced dizziness with nausea. Symptoms must be of moderate or severe intensity. Duration of acute episodes is limited to a window of between 5 minutes and 72 hours.
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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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              Humans use internal models to construct and update a sense of verticality.

              Internal models serve sensory processing, sensorimotor integration and motor control. They could be a way to construct and update a sense of verticality, by combining vestibular and somatosensory graviception. We tested this hypothesis by investigating self-orientation relative to gravity in 39 normal subjects and in subjects with various somatosensory losses showing either a complete deafferentation of trunk and lower limbs (14 paraplegic patients after complete traumatic spinal cord injury) or a gradient in the degree of a hemibody sensory loss (23 hemiplegic patients after stroke). We asked subjects to estimate, in the dark, the direction of the Earth vertical in two postural conditions-upright and at lateral whole body tilt. For upright conditions, verticality estimates were not different from the direction of the Earth vertical in normal (0.24° ± 1; P = 0.42) and paraplegic subjects (0.87° ± 0.9; P = 0.14). The within-subject variability was much greater in hemiplegic than in normal subjects (2.05° ± 1.15 versus 1.06° ± 0.4; P < 0.01) and greater in paraplegic than in normal subjects (1.13° ± 0.4 versus 0.72° ± 0.4; P < 0.01). These findings indicate that, even if vestibular graviception is intact, somaesthetic graviception contributes to the sense of verticality, leading to a more robust judgement about the direction of verticality when vestibular and somaesthetic graviception yield congruent information. As expected, when normal subjects were tilted, their verticality estimates were biased in the direction of the body tilt (5.55° ± 3.9). This normal modulation of verticality perception (Aubert effect), was preserved in hemiplegics on the side of the normoaesthetic hemibody (ipsilesional) (6.09° ± 6.3), and abolished both in paraplegics (1.06° ± 2.5) and in hemiplegics (0.04° ± 6.7) on the side of hypoaesthetic hemibody (contralesional). This incongruence did not exist in deafferented paraplegics who exclusively used vestibular graviception with a similar efficacy no matter what the lateral body position. The Aubert effect was not an on-off phenomenon since the degree of hemiplegics' somatosensory loss correlated with the modulation of verticality perception when they were tilted to the side of hypoaesthetic hemibody (r = -0.55; P < 0.01). The analysis of anatomical correlates showed that the Aubert effect required the integrity of the posterolateral thalamus. This study reveals the existence of a synthesis of vestibular and somaesthetic graviception for which the posterolateral thalamus plays a major role. This corresponds to a primary property of internal models and yields the neural bases of the Aubert effect. We conclude that humans construct and update internal models of verticality in which somatosensory information plays an important role.
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                Author and article information

                Contributors
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                30 October 2018
                2018
                : 9
                : 892
                Affiliations
                [1] 1Department of Neurology, The Johns Hopkins University School of Medicine , Baltimore, MD, United States
                [2] 2Department of Neurology, Neuro-medical Scientific Center, Taichung Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation , Taichung, Taiwan
                [3] 3Department of Medicine, Tzu Chi University, Buddhist Tzu Chi Medical Foundation , Hualien, Taiwan
                [4] 4Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins University School of Medicine , Baltimore, MD, United States
                Author notes

                Edited by: Christophe Lopez, Centre National de la Recherche Scientifique (CNRS), France

                Reviewed by: Bernard Cohen, Icahn School of Medicine at Mount Sinai, United States; Hong Ju Park, Asan Medical Center, South Korea

                *Correspondence: Amir Kheradmand akherad@ 123456jhu.edu

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

                †These authors have contributed equally to this work

                Article
                10.3389/fneur.2018.00892
                6218433
                30425678
                7c0523c9-c0d3-4efd-9137-7c3338e89d52
                Copyright © 2018 Winnick, Sadeghpour, Otero-Millan, Chang and Kheradmand.

                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) and the copyright owner(s) 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
                : 04 July 2018
                : 01 October 2018
                Page count
                Figures: 3, Tables: 3, Equations: 0, References: 38, Pages: 8, Words: 5469
                Funding
                Funded by: National Institute on Deafness and Other Communication Disorders 10.13039/100000055
                Award ID: K23DC013552
                Categories
                Neurology
                Original Research

                Neurology
                vestibular migraine,head tilt,subjective visual vertical,perception of upright,dizziness
                Neurology
                vestibular migraine, head tilt, subjective visual vertical, perception of upright, dizziness

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