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

PLOS ONE, Dec 2019

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.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0117155&type=printable

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

March Are Movements Necessary for the Sense of Body Ownership? Evidence from the Rubber Hand Illusion in Pure Hemiplegic Patients Dalila Burin 0 1 Alessandro Livelli 0 1 Francesca Garbarini 0 1 Carlotta Fossataro 0 1 Alessia Folegatti 0 1 Patrizia Gindri 0 1 Lorenzo Pia 0 1 0 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 1 Academic Editor: Mikhail A. Lebedev, Duke University , UNITED STATES 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. - Competing Interests: The authors have declared that no competing interests exist. Body ownership is the conscious experience of the body as ones own [1]. Indeed, it is an ubiquitous perceptual experience that stands at the root of human nature since we all sense what its like having a body and we experience the boundaries between our own body and the external world [2]. Recent theoretical and methodological advances have leaded to the development of new approaches to examine in depth the neurocognitive processes underpinning the conscious experience of ones own body. Perhaps, one of the most compelling demonstration of the mechanisms subserving body ownership has been obtained in healthy participants by means of an experimental manipulation in which the physical constraints subserving body ownership are altered. Such paradigm is known as the rubber hand illusion [3]. Basically, it is shown that synchronous, but not asynchronous, touches onto a static visible rubber hand and onto the static hidden participants hand produce the compelling change in the believes of ownership of that hand (e.g., [37]). The attribution is typically measured both objectively (i.e., the perceived location of ones own hand toward the rubber hand) and subjectively (the experience of owning the rubber hand). It is worth noticing that incongruent rubber hand postures, incongruent identity (e.g., neutral objects) does not seem to induce the illusion (e.g., [8]). The rubber hand illusion effects are explained with the fact that when the rubber hand is congruent with the participants hand in terms of posture and identity, the conflict between somatosensory representations of the own hand and vision of the fake hand disappears in favor of a strong multisensory integration (i.e., touch, proprioception and vision). This, in turns, induces a unitary multisensory perception of the fake hand as ones own hand receiving the tactile stimuli [9,10]. Interestingly, other recent approaches have extended this paradigm to the whole body by employing virtual reality [11,12]. The classical version of the rubber hand illusion paradigm [9,10] reveals that when visual and tactile stimuli delivered to ones own body part match in terms of space, time and identity, a feeling of ownership arises. However, human body receives stimulations also during actions and, in fact, the feeling that one's body belongs to oneself is present also when we move: I know that this moving hand is mine. In these situations, further signals add to vision and touch: skin/joint receptors, muscles spindles give us kinesthetic information (see [13] for a review). Additionally, during willed actions the brain process also centrally generated motor commands (efferent signals) and the sensory predictions they produce (efference copy; see, for instance [14]). Consistently with these observations, (...truncated)


This is a preview of a remote PDF: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0117155&type=printable

Dalila Burin, Alessandro Livelli, Francesca Garbarini, Carlotta Fossataro, Alessia Folegatti, Patrizia Gindri, Lorenzo Pia. Are Movements Necessary for the Sense of Body Ownership? Evidence from the Rubber Hand Illusion in Pure Hemiplegic Patients, PLOS ONE, 2015, Volume 10, Issue 3, DOI: 10.1371/journal.pone.0117155