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      Losing One's Hand: Visual-Proprioceptive Conflict Affects Touch Perception

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          Abstract

          Background

          While the sense of bodily ownership has now been widely investigated through the rubber hand illusion (RHI), very little is known about the sense of disownership. It has been hypothesized that the RHI also affects the ownership feelings towards the participant's own hand, as if the rubber hand replaced the participant's actual hand. Somatosensory changes observed in the participants' hand while experiencing the RHI have been taken as evidence for disownership of their real hand. Here we propose a theoretical framework to disambiguate whether such somatosensory changes are to be ascribed to the disownership of the real hand or rather to the anomalous visuo-proprioceptive conflict experienced by the participant during the RHI.

          Methodology/Principal Findings

          In experiment 1, reaction times (RTs) to tactile stimuli delivered to the participants' hand slowed down following the establishment of the RHI. In experiment 2, the misalignment of visual and proprioceptive inputs was obtained via prismatic displacement, a situation in which ownership of the seen hand was doubtless. This condition slowed down the participants' tactile RTs. Thus, similar effects on touch perception emerged following RHI and prismatic displacement. Both manipulations also induced a proprioceptive drift, toward the fake hand in the first experiment and toward the visual position of the participants' hand in the second experiment.

          Conclusions/Significance

          These findings reveal that somatosensory alterations in the experimental hand resulting from the RHI result from cross-modal mismatch between the seen and felt position of the hand. As such, they are not necessarily a signature of disownership.

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          Most cited references16

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          On the other hand: dummy hands and peripersonal space.

          Where are my hands? The brain can answer this question using sensory information arising from vision, proprioception, or touch. Other sources of information about the position of our hands can be derived from multisensory interactions (or potential interactions) with our close environment, such as when we grasp or avoid objects. The pioneering study of multisensory representations of peripersonal space was published in Behavioural Brain Research almost 30 years ago [Rizzolatti G, Scandolara C, Matelli M, Gentilucci M. Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 1981;2:147-63]. More recently, neurophysiological, neuroimaging, neuropsychological, and behavioural studies have contributed a wealth of evidence concerning hand-centred representations of objects in peripersonal space. This evidence is examined here in detail. In particular, we focus on the use of artificial dummy hands as powerful instruments to manipulate the brain's representation of hand position, peripersonal space, and of hand ownership. We also review recent studies of the 'rubber hand illusion' and related phenomena, such as the visual capture of touch, and the recalibration of hand position sense, and discuss their findings in the light of research on peripersonal space. Finally, we propose a simple model that situates the 'rubber hand illusion' in the neurophysiological framework of multisensory hand-centred representations of space.
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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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              Somatoparaphrenia: a body delusion. A review of the neuropsychological literature.

              A review of published brain-damaged patients showing delusional beliefs concerning the contralesional side of the body (somatoparaphrenia) is presented. Somatoparaphrenia has been reported, with a few exceptions, in right-brain-damaged patients, with motor and somatosensory deficits, and the syndrome of unilateral spatial neglect. Somatoparaphrenia, most often characterized by a delusion of disownership of left-sided body parts, may however occur without associated anosognosia for motor deficits, and personal neglect. Also somatosensory deficits may not be a core pathological mechanism of somatoparaphrenia, and visual field disorders may be absent. Deficits of proprioception, however, may play a relevant role. Somatoparaphrenia is often brought about by extensive right-sided lesions, but patients with posterior (parietal-temporal), and insular damage are on record, as well as a few patients with subcortical lesions. Possible pathological factors include a deranged representation of the body concerned with ownership, mainly right-hemisphere-based, and deficits of multisensory integration. Finally, the rubber hand illusion, that brings about a bodily misattribution in neurologically unimpaired participants, as somatoparaphrenia does in brain-damaged patients, is briefly discussed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2009
                7 September 2009
                : 4
                : 9
                : e6920
                Affiliations
                [1 ]UMR-S 864 “Espace et Action,” INSERM, Bron, France
                [2 ]Department of Psychology, University of Turin, Turin, Italy
                [3 ]Hospices Civils de Lyon, Hôpital Neurologique, Mouvement et Handicap, Lyon, France
                [4 ]Institut Jean Nicod, EHESS-ENS-CNRS, Paris, France
                [5 ]Transitions, NYU-CNRS, New York, New York, United States of America
                [6 ]Department of Cognitive Sciences and Education, University of Trento, Trento, Italy
                [7 ]Center for Mind/Brain Sciences (CIMeC), University of Trento, Trento, Italy
                [8 ]Université Claude Bernard Lyon I, Lyon, France
                University of Sydney, Australia
                Author notes

                Conceived and designed the experiments: AF FdV FP YR AF. Performed the experiments: AF. Analyzed the data: AF AF. Contributed reagents/materials/analysis tools: AF. Wrote the paper: AF FdV FP AF.

                Article
                09-PONE-RA-10147R1
                10.1371/journal.pone.0006920
                2732904
                19738900
                18e80c9a-e71c-4d6c-83e5-56f30b322bd1
                Folegatti 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
                : 5 May 2009
                : 27 July 2009
                Page count
                Pages: 9
                Categories
                Research Article
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Cognitive Neuroscience
                Neuroscience/Neural Homeostasis
                Neuroscience/Sensory Systems
                Neuroscience/Psychology
                Neuroscience/Experimental Psychology

                Uncategorized
                Uncategorized

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