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      Motor and sensory disturbances induced by sensorimotor conflicts during passive and active movements in healthy participants

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          Abstract

          Sensorimotor conflict induces both sensory and motor disturbances, but the specific factors playing a role in conflict-induced disturbances are still misunderstood. For example, we still do not know the role played by motor intention (vs. a purely visuo-proprioceptive conflict) or the influence of specific types of incongruent visual feedback. The objective of this study was threefold: 1- to compare the effect of passive and active movement during sensorimotor conflict on sensory disturbances measured with a questionnaire; 2- to compare the effect of three incongruent visual feedback conditions on sensory and motor (mediolateral drift and movement amplitude) disturbances; 3- to test whether conflict-induced sensory and motor disturbances were stable over time. 20 healthy participants realized active or passive cyclic upper limb movements while viewing either congruent or incongruent visual feedback about their movement using a robotized exoskeleton combined with 2D virtual reality interface. First, results showed that in condition of conflict, participants reported higher sensory disturbances during active movements compared to passive movements (p = 0.034), suggesting that the efference copy reinforces the conflict between vision and proprioception. Second, the three conditions of incongruence in the active condition induced similar sensory (all p>0.45) and motor disturbances (medio-lateral drift: all p>0.59 and amplitude: all p>0.25), suggesting that conflict induced motor disturbances could be related more to the observation of another movement rather than to a detection of conflict between motor intention and sensory feedback. Finally, both sensory and motor disturbances were stable over time (all ICCs between 0.76 and 0.87), demonstrating low variability within participants. Overall, our results suggest that the efference copy is more involved in sensory disturbances than in motor disturbances, suggesting that they might rely on independent processes.

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          Most cited references33

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          Why can't you tickle yourself?

          It is well known that you cannot tickle yourself. Here, we discuss the proposal that such attenuation of self-produced tactile stimulation is due to the sensory predictions made by an internal forward model of the motor system. A forward model predicts the sensory consequences of a movement based on the motor command. When a movement is self-produced, its sensory consequences can be accurately predicted, and this prediction can be used to attenuate the sensory effects of the movement. Studies are reviewed that demonstrate that as the discrepancy between predicted and actual sensory feedback increases during self-produced tactile stimulation there is a concomitant decrease in the level of sensory attenuation and an increase in tickliness. Functional neuroimaging studies have demonstrated that this sensory attenuation might be mediated by somatosensory cortex and anterior cingulate cortex: these areas are activated less by a self-produced tactile stimulus than by the same stimulus when it is externally produced. Furthermore, evidence suggests that the cerebellum might be involved in generating the prediction of the sensory consequences of movement. Finally, recent evidence suggests that this predictive mechanism is abnormal in patients with auditory hallucinations and/or passivity experiences.
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            An interference effect of observed biological movement on action.

            It has been proposed that actions are intrinsically linked to perception and that imagining, observing, preparing, or in any way representing an action excites the motor programs used to execute that same action. There is neurophysiological evidence that certain brain regions involved in executing actions are activated by the mere observation of action (the so-called "mirror system;" ). However, it is unknown whether this mirror system causes interference between observed and simultaneously executed movements. In this study we test the hypothesis that, because of the overlap between action observation and execution, observed actions should interfere with incongruous executed actions. Subjects made arm movements while observing either a robot or another human making the same or qualitatively different arm movements. Variance in the executed movement was measured as an index of interference to the movement. The results demonstrate that observing another human making incongruent movements has a significant interference effect on executed movements. However, we found no evidence that this interference effect occurred when subjects observed a robotic arm making incongruent movements. These results suggest that the simultaneous activation of the overlapping neural networks that process movement observation and execution infers a measurable cost to motor control.
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              Cortical origin of pathological pain.

              A Harris (1999)
              Pain without accompanying tissue pathology poses a classic puzzle, presented in extreme form by phantom pain in a non-existent amputated limb. A clue to the origin of such pain is given by the recent discovery of a region of cortex active in response to incongruence between motor intention, awareness of movement, and visual feedback. Phantom-limb sensation, and repetitive strain injuries or focal hand dystonias in writers, musicians, or keyboard operators, are accompanied by plastic changes in sensorimotor cortex and by pathological pain. Disorganised or inappropriate cortical representation of proprioception may falsely signal incongruence between motor intention and movement, which results in pathological pain in the same way that incongruence between vestibular and visual sensation results in motion sickness.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: SoftwareRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 August 2018
                2018
                : 13
                : 8
                : e0203206
                Affiliations
                [1 ] Center for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS), Québec, QC, Canada
                [2 ] Department of Rehabilitation, Laval University, Québec, QC, Canada
                [3 ] Royal United Hospitals NHS Foundation Trust, Bath, United Kingdom
                [4 ] University of the West of England, Bristol, United Kingdom
                [5 ] The Florence Nightingale Foundation, London, United Kingdom
                University of Ottawa, CANADA
                Author notes

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

                Author information
                http://orcid.org/0000-0002-2037-6916
                Article
                PONE-D-18-10959
                10.1371/journal.pone.0203206
                6114925
                30157264
                e862f9dd-d5d7-43eb-9939-cc54f6a90474
                © 2018 Brun 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
                : 11 April 2018
                : 16 August 2018
                Page count
                Figures: 4, Tables: 1, Pages: 15
                Funding
                We thank Nicolas Robitaille, eng. Ph.D. for his help in the development of the task and technical support. This study was supported by a Discovery grant from Natural Sciences and Engineering Research Council of Canada (NSERC, RGPIN 355896-2012, www.nserc-crsng.gc.ca). C. Brun was supported by fellowships from Centre interdisciplinaire de recherche en réadaptation et en intégration sociale (CIRRIS, www.cirris.ulaval.ca), from Centre thématique de recherche en neurosciences (CTRN, www.neuro.ulaval.ca), from the Faculté de médecine de l’Université Laval ( www.fmed.ulaval.ca) and from the Fonds de Recherche Québec – Nature et Technologies (FRQNT, www.frqnt.gouv.qc.ca). C. Mercier is supported by a salary award from Fonds de recherche Québec-Santé (FRQS, no. 29251, www.frqs.gouv.qc.ca).
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Social Sciences
                Psychology
                Sensory Perception
                Biology and Life Sciences
                Physiology
                Sensory Physiology
                Somatosensory System
                Pain Sensation
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Somatosensory System
                Pain Sensation
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
                Somatosensory System
                Pain Sensation
                Engineering and Technology
                Mechanical Engineering
                Robotics
                Robots
                Biology and Life Sciences
                Zoology
                Animal Physiology
                Exoskeleton
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Proprioception
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Proprioception
                Social Sciences
                Psychology
                Sensory Perception
                Proprioception
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Limbs (Anatomy)
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Limbs (Anatomy)
                Custom metadata
                Raw data tables for all relevant data are available from the Harvard Dataverse, V1 ( https://doi.org/10.7910/DVN/O2ZCVO).

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