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      Balancing body ownership: Visual capture of proprioception and affectivity during vestibular stimulation

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          Abstract

          The experience of our body as our own (i.e. body ownership) involves integrating different sensory signals according to their contextual relevance (i.e. multisensory integration). Until recently, most studies of multisensory integration and body ownership concerned only vision, touch and proprioception; the role of other modalities, such as the vestibular system and interoception, has been neglected and remains poorly understood. In particular, no study to date has directly explored the combined effect of vestibular and interoceptive signals on body ownership. Here, we investigated for the first time how Galvanic Vestibular Stimulation (left, right, sham), tactile affectivity (a reclassified interoceptive modality manipulated by applying touch at C-tactile optimal versus non-optimal velocities), and their combination, influence proprioceptive and subjective measures of body ownership during a rubber hand illusion paradigm with healthy participants (N = 26). Our results show that vestibular stimulation (left GVS) significantly increased proprioceptive drift towards the rubber hand during mere visual exposure to the rubber hand. Moreover, it also enhanced participants’ proprioceptive drift towards the rubber hand during manipulations of synchronicity and affective touch. These findings suggest that the vestibular system influences multisensory integration, possibly by re-weighting both the two-way relationship between proprioception and vision, as well as the three-way relationship between proprioception, vision and affective touch. We discuss these findings in relation to current predictive coding models of multisensory integration and body ownership.

          Highlights

          • We studied vestibular and affective contributions to body ownership.

          • We stimulated the vestibular system in a Rubber Hand paradigm with affective touch.

          • Right-hemisphere stimulation increased proprioceptive drift during vision of a RH.

          • Applying affective touch further increased proprioceptive drift.

          • Affective and vestibular signals may favour vision in multisensory integration.

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          Most cited references51

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          Interoception: the sense of the physiological condition of the body.

          Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.
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            Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas.

            In the "rubber-hand illusion," the sight of brushing of a rubber hand at the same time as brushing of the person's own hidden hand is sufficient to produce a feeling of ownership of the fake hand. We shown previously that this illusion is associated with activity in the multisensory areas, most notably the ventral premotor cortex (Ehrsson et al., 2004). However, it remains to be demonstrated that this illusion does not simply reflect the dominant role of vision and that the premotor activity does not reflect a visual representation of an object near the hand. To address these issues, we introduce a somatic rubber-hand illusion. The experimenter moved the blindfolded participant's left index finger so that it touched the fake hand, and simultaneously, he touched the participant's real right hand, synchronizing the touches as perfectly as possible. After approximately 9.7 s, this stimulation elicited an illusion that one was touching one's own hand. We scanned brain activity during this illusion and two control conditions, using functional magnetic resonance imaging. Activity in the ventral premotor cortices, intraparietal cortices, and the cerebellum was associated with the illusion of touching one's own hand. Furthermore, the rated strength of the illusion correlated with the degree of premotor and cerebellar activity. This finding suggests that the activity in these areas reflects the detection of congruent multisensory signals from one's own body, rather than of visual representations. We propose that this could be the mechanism for the feeling of body ownership.
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              Neural signatures of body ownership: a sensory network for bodily self-consciousness.

              Body ownership refers to the special perceptual status of one's own body, which makes bodily sensations seem unique to oneself. We studied the neural correlates of body ownership by controlling whether an external object was accepted as part of the body or not. In the rubber hand illusion (RHI), correlated visuotactile stimulation causes a fake hand to be perceived as part of one's own body. In the present study, we distinguished between the causes (i.e., multisensory stimulation) and the effect (i.e., the feeling of ownership) of the RHI. Participants watched a right or a left rubber hand being touched either synchronously or asynchronously with respect to their own unseen right hand. A quantifiable correlate of the RHI is a shift in the perceived position of the subject's hand toward the rubber hand. We used positron emission tomography to identify brain areas whose activity correlated with this proprioceptive measure of body ownership. Body ownership was related to activity in the right posterior insula and the right frontal operculum. Conversely, when the rubber hand was not attributed to the self, activity was observed in the contralateral parietal cortex, particularly the somatosensory cortex. These structures form a network that plays a fundamental role in linking current sensory stimuli to one's own body and thus also in self-consciousness.
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                Author and article information

                Contributors
                Journal
                Neuropsychologia
                Neuropsychologia
                Neuropsychologia
                Pergamon Press
                0028-3932
                1873-3514
                1 August 2018
                August 2018
                : 117
                : 311-321
                Affiliations
                [a ]School of Life and Medical Sciences, University of Hertfordshire, UK
                [b ]Clinical, Educational & Health Psychology Research Department, Division of Psychology & Language Sciences, University College London, UK
                Author notes
                [* ]Correspondence to: Department of Psychology and Sport Science, School of Life and Medical Sciences, University of Hertfordshire, College Lane, Hatfield AL10 9AB, UK. s.ponzo@ 123456herts.ac.uk
                [1]

                These authors have shared the senior authorship.

                Article
                S0028-3932(18)30292-6
                10.1016/j.neuropsychologia.2018.06.020
                6092558
                29940194
                7787ed39-0c06-4a52-8197-423a9e1ce609
                © 2018 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 6 March 2018
                : 1 June 2018
                : 21 June 2018
                Categories
                Article

                Neurology
                affective touch,body ownership,multisensory integration,vestibular stimulation,bodily self

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