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      Are Movements Necessary for the Sense of Body Ownership? Evidence from the Rubber Hand Illusion in Pure Hemiplegic Patients

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          Abstract

          A question still debated within cognitive neuroscience is whether signals present during actions significantly contribute to the emergence of human’s body ownership. In the present study, we aimed at answer this question by means of a neuropsychological approach. We administered the classical rubber hand illusion paradigm to a group of healthy participants and to a group of neurological patients affected by a complete left upper limb hemiplegia, but without any propriceptive/tactile deficits. The illusion strength was measured both subjectively (i.e., by a self-report questionnaire) and behaviorally (i.e., the location of one’s own hand is shifted towards the rubber hand). We aimed at examining whether, and to which extent, an enduring absence of movements related signals affects body ownership. Our results showed that patients displayed, respect to healthy participants, stronger illusory effects when the left (affected) hand was stimulated and no effects when the right (unaffected) hand was stimulated. In other words, hemiplegics had a weaker/more flexible sense of body ownership for the affected hand, but an enhanced/more rigid one for the healthy hand. Possible interpretations of such asymmetrical distribution of body ownership, as well as limits of our results, are discussed. Broadly speaking, our findings suggest that the alteration of the normal flow of signals present during movements impacts on human’s body ownership. This in turn, means that movements have a role per se in developing and maintaining a coherent body ownership.

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          Most cited references25

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          An internal model for sensorimotor integration.

          On the basis of computational studies it has been proposed that the central nervous system internally simulates the dynamic behavior of the motor system in planning, control, and learning; the existence and use of such an internal model is still under debate. A sensorimotor integration task was investigated in which participants estimated the location of one of their hands at the end of movements made in the dark and under externally imposed forces. The temporal propagation of errors in this task was analyzed within the theoretical framework of optimal state estimation. These results provide direct support for the existence of an internal model.
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            The rubber hand illusion: sensitivity and reference frame for body ownership.

            When subjects view stimulation of a rubber hand while feeling congruent stimulation of their own hand, they may come to feel that the rubber hand is part of their own body. This illusion of body ownership is termed 'Rubber Hand Illusion' (RHI). We investigated sensitivity of RHI to spatial mismatches between visual and somatic experience. We compared the effects of spatial mismatch between the stimulation of the two hands, and equivalent mismatches between the postures of the two hands. We created the mismatch either by adjusting stimulation or posture of the subject's hand, or, in a separate group of subjects, by adjusting stimulation or posture of the rubber hand. The matching processes underlying body ownership were asymmetrical. The illusion survived small changes in the subject's hand posture, but disappeared when the same posture transformations were applied to the rubber hand. Mismatch between the stimulation delivered to the subject's hand and the rubber hand abolished the illusion. The combination of these two situations is of particular interest. When the subject's hand posture was slightly different from the rubber hand posture, the RHI remained as long as stimulation of the two hands was congruent in a hand-centred spatial reference frame, even though the altered posture of the subject's hand meant that stimulation was incongruent in external space. Conversely, the RHI was reduced when the stimulation was incongruent in hand-centred space but congruent in external space. We conclude that the visual-tactile correlation that causes the RHI is computed within a hand-centred frame of reference, which is updated with changes in body posture. Current sensory evidence about what is 'me' is interpreted with respect to a prior mental body representation.
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              The moving rubber hand illusion revisited: comparing movements and visuotactile stimulation to induce illusory ownership.

              The rubber hand illusion is a perceptual illusion in which a model hand is experienced as part of one's own body. In the present study we directly compared the classical illusion, based on visuotactile stimulation, with a rubber hand illusion based on active and passive movements. We examined the question of which combinations of sensory and motor cues are the most potent in inducing the illusion by subjective ratings and an objective measure (proprioceptive drift). In particular, we were interested in whether the combination of afferent and efferent signals in active movements results in the same illusion as in the purely passive modes. Our results show that the illusion is equally strong in all three cases. This demonstrates that different combinations of sensory input can lead to a very similar phenomenological experience and indicates that the illusion can be induced by any combination of multisensory information. Copyright © 2014 The Authors. Published by Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 March 2015
                2015
                : 10
                : 3
                : e0117155
                Affiliations
                [1 ]SAMBA (SpAtial, Motor & Bodily Awareness) Research Group, Psychology Department, University of Turin, Turin, Italy
                [2 ]NIT Neuroscience Institute of Turin, Turin, Italy
                [3 ]San Camillo Hospital, Turin, Italy
                Duke University, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: AF LP. Performed the experiments: DB AL FG CF. Analyzed the data: DB AF LP AL. Wrote the paper: DB AF LP AL CF FG. Managed the main patients' selection and administered the baseline neuropsychological assessment: PG.

                Article
                PONE-D-14-33734
                10.1371/journal.pone.0117155
                4361688
                25775041
                06480199-cf59-444a-baed-331c19551194
                Copyright @ 2015

                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
                : 30 July 2014
                : 19 December 2014
                Page count
                Figures: 4, Tables: 1, Pages: 12
                Funding
                This work was supported by MASTER DEI TALENTI 2013 Scholarship to DB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper.

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