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      An Investigation of Lower Limb Representations Underlying Vision, Touch, and Proprioception in Body Integrity Identity Disorder

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          Abstract

          Individuals with Body Integrity Identity Disorder (BIID) have a (non-psychotic) longstanding desire to amputate or paralyze one or more fully-functioning limbs, often the legs. This desire presumably arises from experiencing a mismatch between one’s perceived mental image of the body and the physical structural and/or functional boundaries of the body itself. While neuroimaging studies suggest a disturbed body representation network in individuals with BIID, few behavioral studies have looked at the manifestation of this disrupted lower limb representations in this population. Specifically, people with BIID feel like they are overcomplete in their current body. Perhaps sensory input, processed normally on and about the limb, cannot communicate with a higher-order model of the leg in the brain (which might be underdeveloped). We asked individuals who desire paralysis or amputation of the lower legs (and a group of age- and sex-matched controls) to make explicit and implicit judgments about the size and shape of their legs while relying on vision, touch, and proprioception. We hypothesized that BIID participants would mis-estimate the size of their affected leg(s) more than the same leg of controls. Using a multiple single-case analysis, we found no global differences in lower limb representations between BIID participants and controls. Thus, while people with BIID feel that part of the body is foreign, they can still make normal sensory-guided implicit and explicit judgments about the limb. Moreover, these results suggest that BIID is not a body image disorder, per se, and that an examination of leg representation does not uncover the disturbed bodily experience that individuals with BIID have.

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          Separate visual pathways for perception and action.

          Accumulating neuropsychological, electrophysiological and behavioural evidence suggests that the neural substrates of visual perception may be quite distinct from those underlying the visual control of actions. In other words, the set of object descriptions that permit identification and recognition may be computed independently of the set of descriptions that allow an observer to shape the hand appropriately to pick up an object. We propose that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting from the striate cortex to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects.
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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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              A neurological dissociation between perceiving objects and grasping them.

              Studies of the visual capacity of neurological patients have provided evidence for a dissociation between the perceptual report of a visual stimulus and the ability to direct spatially accurate movements toward that stimulus. Some patients with damage to the parietal lobe, for example, are unable to reach accurately towards visual targets that they unequivocally report seeing. Conversely, some patients with extensive damage to primary visual cortex can make accurate pointing movements or saccades toward a stimulus presented in their 'blind' scotoma. But in investigations of visuomotor control in patients with visual disorders, little consideration has been given to complex acts such as manual prehension. Grasping a three-dimensional object requires knowledge not only of the object's spatial location, but also of its form, orientation and size. We have examined a patient with a profound disorder in the perception of such object qualities. Our quantitative analyses demonstrate strikingly accurate guidance of hand and finger movements directed at the very objects whose qualities she fails to perceive. These data suggest that the neural substrates for the visual perception of object qualities such as shape, orientation and size are distinct from those underlying the use of those qualities in the control of manual skills.
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                Author and article information

                Contributors
                Journal
                Front Psychiatry
                Front Psychiatry
                Front. Psychiatry
                Frontiers in Psychiatry
                Frontiers Media S.A.
                1664-0640
                25 February 2020
                2020
                : 11
                : 15
                Affiliations
                [1] 1 Department of Experimental Psychology, Helmholtz Institute, Utrecht University , Utrecht, Netherlands
                [2] 2 Department of Psychiatry, Amsterdam UMC, Vrije Universiteit Amsterdam , Amsterdam, Netherlands
                Author notes

                Edited by: Stephan Zipfel, University of Tübingen, Germany

                Reviewed by: Anna Sedda, Heriot-Watt University, United Kingdom; Michael First, Columbia University, United States

                *Correspondence: Kayla D. Stone, k.d.stone@ 123456uu.nl

                This article was submitted to Psychosomatic Medicine, a section of the journal Frontiers in Psychiatry

                Article
                10.3389/fpsyt.2020.00015
                7052367
                32161554
                96ddf405-8c15-4226-80f7-bf333506f5bd
                Copyright © 2020 Stone, Kornblad, Engel, Dijkerman, Blom and Keizer

                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
                : 29 March 2019
                : 08 January 2020
                Page count
                Figures: 5, Tables: 2, Equations: 2, References: 103, Pages: 18, Words: 11914
                Funding
                Funded by: Nederlandse Organisatie voor Wetenschappelijk Onderzoek 10.13039/501100003246
                Award ID: 406.15.282
                Funded by: Natural Sciences and Engineering Research Council of Canada 10.13039/501100000038
                Categories
                Psychiatry
                Original Research

                Clinical Psychology & Psychiatry
                xenomelia,body integrity dysphoria,lower limbs,body perception,multisensory,body ownership

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