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      Sensorimotor and Posterior Brain Activations During the Observation of Illusory Embodied Fake Hand Movement

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          Abstract

          In the rubber hand illusion (RHI), the subject recognizes a fake hand as his or her own. We recently found that the observation of embodied fake hand movement elicited mu-rhythm (8–13 Hz) desynchronization on electroencephalography (EEG), suggesting brain activation in the sensorimotor regions. However, it is known that mu-rhythm desynchronization during action observation is confounded with occipital alpha-rhythm desynchronization, which is modulated by attention. This study examined the independence of brain activities in the sensorimotor and occipital regions relating to the movement observation under the RHI. The invisible participant’s left and fake right hands were stroked simultaneously, which was interrupted by unexpected fake hand movements. A mirror-reversed image of the fake hand was shown on a monitor in front of the participant with a delay of 80, 280, or 480 ms. Illusion strength decreased as a function of the delay. EEG independent component analysis (ICA) and ICA clustering revealed six clusters with observation-induced desynchronization of 8–13 Hz frequency band. In the right sensorimotor cluster, mu-rhythm desynchronization was the greatest under the 80-ms delay, while alpha-rhythm desynchronization of the occipital clusters did not show delay-dependence. These results suggest that brain activation in the sensorimotor areas (i.e., mu-rhythm desynchronization) induced by embodied fake hand movement is independent of that in the occipital areas (alpha-rhythm desynchronization).

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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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            Moving a Rubber Hand that Feels Like Your Own: A Dissociation of Ownership and Agency

            During voluntary hand movement, we sense that we generate the movement and that the hand is a part of our body. These feelings of control over bodily actions, or the sense of agency, and the ownership of body parts are two fundamental aspects of the way we consciously experience our bodies. However, little is known about how these processes are functionally linked. Here, we introduce a version of the rubber hand illusion in which participants control the movements of the index finger of a model hand, which is in full view, by moving their own right index finger. We demonstrated that voluntary finger movements elicit a robust illusion of owning the rubber hand and that the senses of ownership and agency over the model hand can be dissociated. We systematically varied the relative timing of the finger movements (synchronous versus asynchronous), the mode of movement (active versus passive), and the position of the model hand (anatomically congruent versus incongruent positions). Importantly, asynchrony eliminated both ownership and agency, passive movements abolished the sense of agency but left ownership intact, and incongruent positioning of the model hand diminished ownership but did not eliminate agency. These findings provide evidence for a double dissociation of ownership and agency, suggesting that they represent distinct cognitive processes. Interestingly, we also noted that the sense of agency was stronger when the hand was perceived to be a part of the body, and only in this condition did we observe a significant correlation between the subjects’ ratings of agency and ownership. We discuss this in the context of possible differences between agency over owned body parts and agency over actions that involve interactions with external objects. In summary, the results obtained in this study using a simple moving rubber hand illusion paradigm extend previous findings on the experience of ownership and agency and shed new light on their relationship.
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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
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                15 October 2019
                2019
                : 13
                : 367
                Affiliations
                [1] 1Department of Integrative Physiology, School of Medicine, Kyorin University , Tokyo, Japan
                [2] 2Department of Sport Education, School of Lifelong Sport, Hokusho University , Ebetsu, Japan
                [3] 3Department of Electronics and Bioinformatics, School of Science and Technology, Meiji University , Kawasaki, Japan
                Author notes

                Edited by: Juliana Yordanova, Institute of Neurobiology (BAS), Bulgaria

                Reviewed by: Antonio Ivano Triggiani, University of Foggia, Italy; Hisato Sugata, Oita University, Japan

                *Correspondence: Satoshi Shibuya, shibuyas@ 123456ks.kyorin-u.ac.jp

                This article was submitted to Sensory Neuroscience, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2019.00367
                6803621
                31680917
                a283801d-7b66-451a-b719-743080930068
                Copyright © 2019 Shibuya, Unenaka, Zama, Shimada and Ohki.

                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
                : 28 June 2019
                : 30 September 2019
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 46, Pages: 12, Words: 0
                Categories
                Neuroscience
                Original Research

                Neurosciences
                body ownership,delayed visual feedback,independent component analysis,electroencephalography,mu-rhythm desynchronization,alpha-rhythm desynchronization,rubber hand illusion

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