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      Anchoring the Self to the Body in Bilateral Vestibular Failure

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          Abstract

          Recent findings suggest that vestibular information plays a significant role in anchoring the self to the body. Out-of-body experiences of neurological origin are frequently associated with vestibular sensations, and galvanic vestibular stimulation in healthy participants anchors the self to the body. Here, we provide the first objective measures of anchoring the self to the body in chronic bilateral vestibular failure (BVF). We compared 23 patients with idiopathic BVF to 23 healthy participants in a series of experiments addressing several aspects of visuo-spatial perspective taking and embodiment. In Experiment 1, participants were involved in a virtual “dot-counting task” from their own perspective or the perspective of a distant avatar, to measure implicit and explicit perspective taking, respectively. In both groups, response times increased similarly when the avatar’s and participant’s viewpoint differed, for both implicit and explicit perspective taking. In Experiment 2, participants named ambiguous letters (such as “b” or “q”) traced on their forehead that could be perceived from an internal or external perspective. The frequency of perceiving ambiguous letters from an internal perspective was similar in both groups. In Experiment 3, participants completed a questionnaire measuring the experienced self/body and self/environment “closeness”. Both groups reported a similar embodied experience. Altogether, our data show that idiopathic BVF does not change implicit and explicit perspective taking nor subjective anchoring of the self to the body. Our negative findings offer insight into the multisensory mechanisms of embodiment. Only acute peripheral vestibular disorders and neurological disorders in vestibular brain areas (characterized by strong multisensory conflicts) may evoke disembodied experiences.

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          Most cited references54

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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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            The thalamocortical vestibular system in animals and humans.

            The vestibular system provides the brain with sensory signals about three-dimensional head rotations and translations. These signals are important for postural and oculomotor control, as well as for spatial and bodily perception and cognition, and they are subtended by pathways running from the vestibular nuclei to the thalamus, cerebellum and the "vestibular cortex." The present review summarizes current knowledge on the anatomy of the thalamocortical vestibular system and discusses data from electrophysiology and neuroanatomy in animals by comparing them with data from neuroimagery and neurology in humans. Multiple thalamic nuclei are involved in vestibular processing, including the ventroposterior complex, the ventroanterior-ventrolateral complex, the intralaminar nuclei and the posterior nuclear group (medial and lateral geniculate nuclei, pulvinar). These nuclei contain multisensory neurons that process and relay vestibular, proprioceptive and visual signals to the vestibular cortex. In non-human primates, the parieto-insular vestibular cortex (PIVC) has been proposed as the core vestibular region. Yet, vestibular responses have also been recorded in the somatosensory cortex (area 2v, 3av), intraparietal sulcus, posterior parietal cortex (area 7), area MST, frontal cortex, cingulum and hippocampus. We analyze the location of the corresponding regions in humans, and especially the human PIVC, by reviewing neuroimaging and clinical work. The widespread vestibular projections to the multimodal human PIVC, somatosensory cortex, area MST, intraparietal sulcus and hippocampus explain the large influence of vestibular signals on self-motion perception, spatial navigation, internal models of gravity, one's body perception and bodily self-consciousness. Copyright © 2011 Elsevier B.V. All rights reserved.
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              Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective.

              Self-consciousness has mostly been approached by philosophical enquiry and not by empirical neuroscientific study, leading to an overabundance of diverging theories and an absence of data-driven theories. Using robotic technology, we achieved specific bodily conflicts and induced predictable changes in a fundamental aspect of self-consciousness by altering where healthy subjects experienced themselves to be (self-location). Functional magnetic resonance imaging revealed that temporo-parietal junction (TPJ) activity reflected experimental changes in self-location that also depended on the first-person perspective due to visuo-tactile and visuo-vestibular conflicts. Moreover, in a large lesion analysis study of neurological patients with a well-defined state of abnormal self-location, brain damage was also localized at TPJ, providing causal evidence that TPJ encodes self-location. Our findings reveal that multisensory integration at the TPJ reflects one of the most fundamental subjective feelings of humans: the feeling of being an entity localized at a position in space and perceiving the world from this position and perspective. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                20 January 2017
                2017
                : 12
                : 1
                : e0170488
                Affiliations
                [1 ]Aix Marseille Univ, CNRS, LNIA, FR3C, Marseille, France
                [2 ]IRON, Institut de Recherche en Oto-Neurologie, Paris, France
                [3 ]Centre d’Explorations Fonctionnelles Oto-Neurologiques, Paris, France
                [4 ]Unité Troubles de l’Equilibre et Vertiges, CHU Brugmann, Bruxelles, Belgique
                [5 ]Unité de Neuro-Ophtalmologie, CHU Erasme, Bruxelles, Belgique
                [6 ]Clinique des Vertiges, Bruxelles, Belgique
                [7 ]Service ORL, Hôpital Lariboisière, Paris, France
                Universite de Bretagne Occidentale, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: DD CL UD CH CV MT.

                • Data curation: DD.

                • Formal analysis: DD CL.

                • Funding acquisition: CL.

                • Investigation: DD CL UD CH CV MT.

                • Methodology: DD CL UD CH CV MT.

                • Project administration: MT CL.

                • Resources: MT CL.

                • Software: DD CL.

                • Supervision: CL MT.

                • Validation: DD CL UD CH CV MT.

                • Visualization: DD CL UD CH CV MT.

                • Writing – original draft: CL DD MT CV.

                • Writing – review & editing: DD CL UD CH CV MT.

                Author information
                http://orcid.org/0000-0001-5710-9419
                Article
                PONE-D-16-32174
                10.1371/journal.pone.0170488
                5249123
                28107424
                16fd1e74-54bf-46d5-b847-12d9cc1248b6
                © 2017 Deroualle et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 12 August 2016
                : 5 January 2017
                Page count
                Figures: 6, Tables: 0, Pages: 21
                Funding
                CL’s research is supported by a grant from the VolkswagenStiftung (Grant no. 89434: “Finding Perspective: Determining the embodiment of perspectival experience”). The sponsor was not involved in the study design, collection, analysis, and interpretation of data, writing the report and in the decision to submit the manuscript for publication.
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