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      Body ownership determines the attenuation of self-generated tactile sensations

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          Significance

          When we touch one hand with the other, the touch feels less intense than identical touches generated by another person or robot. This is because our brain predicts the contact between our hands and attenuates the expected sensation. Here, we describe how the attenuation of self-touch depends on the experienced ownership of the touching hand. We found that illusory self-touch with a rubber hand that feels like one’s own is attenuated. We also found the reverse: The attenuation of real self-touch is reduced when the rubber hand that feels like one’s own is far from the receiving hand. These findings are important because they demonstrate that sensory predictions and sensory attenuation depend on the sense of ownership of the body.

          Abstract

          Self-perception depends on the brain’s abilities to differentiate our body from the environment and to distinguish between the sensations generated as a consequence of voluntary movement and those arising from events in the external world. The first process refers to the sense of ownership of our body and relies on the dynamic integration of multisensory (afferent) signals. The second process depends on internal forward models that use (efferent) information from our motor commands to predict and attenuate the sensory consequences of our movements. However, the relationship between body ownership and sensory attenuation driven by the forward models remains unknown. To address this issue, we combined the rubber hand illusion, which allows experimental manipulation of body ownership, and the force-matching paradigm, which allows psychophysical quantification of somatosensory attenuation. We found that a rubber right hand pressing on the left index finger produced somatosensory attenuation but only when the model hand felt like one’s own (illusory self-touch); reversely, the attenuation that was expected to occur during actual self-touch with the real hands was reduced when the participants simultaneously experienced ownership of a rubber right hand that was placed at a distance from their left hand. These results demonstrate that the sense of body ownership determines somatosensory attenuation. From a theoretical perspective, our results are important because they suggest that body ownership updates the internal representation of body state that provides the input to the forward model generating sensory predictions during voluntary action.

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          Most cited references33

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          Control of mental activities by internal models in the cerebellum.

          Masao ITO (2008)
          The intricate neuronal circuitry of the cerebellum is thought to encode internal models that reproduce the dynamic properties of body parts. These models are essential for controlling the movement of these body parts: they allow the brain to precisely control the movement without the need for sensory feedback. It is thought that the cerebellum might also encode internal models that reproduce the essential properties of mental representations in the cerebral cortex. This hypothesis suggests a possible mechanism by which intuition and implicit thought might function and explains some of the symptoms that are exhibited by psychiatric patients. This article examines the conceptual bases and experimental evidence for this hypothesis.
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            Principles of sensorimotor learning.

            The exploits of Martina Navratilova and Roger Federer represent the pinnacle of motor learning. However, when considering the range and complexity of the processes that are involved in motor learning, even the mere mortals among us exhibit abilities that are impressive. We exercise these abilities when taking up new activities - whether it is snowboarding or ballroom dancing - but also engage in substantial motor learning on a daily basis as we adapt to changes in our environment, manipulate new objects and refine existing skills. Here we review recent research in human motor learning with an emphasis on the computational mechanisms that are involved.
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              A computational neuroanatomy for motor control.

              The study of patients to infer normal brain function has a long tradition in neurology and psychology. More recently, the motor system has been subject to quantitative and computational characterization. The purpose of this review is to argue that the lesion approach and theoretical motor control can mutually inform each other. Specifically, one may identify distinct motor control processes from computational models and map them onto specific deficits in patients. Here we review some of the impairments in motor control, motor learning and higher-order motor control in patients with lesions of the corticospinal tract, the cerebellum, parietal cortex, the basal ganglia, and the medial temporal lobe. We attempt to explain some of these impairments in terms of computational ideas such as state estimation, optimization, prediction, cost, and reward. We suggest that a function of the cerebellum is system identification: to build internal models that predict sensory outcome of motor commands and correct motor commands through internal feedback. A function of the parietal cortex is state estimation: to integrate the predicted proprioceptive and visual outcomes with sensory feedback to form a belief about how the commands affected the states of the body and the environment. A function of basal ganglia is related to optimal control: learning costs and rewards associated with sensory states and estimating the "cost-to-go" during execution of a motor task. Finally, functions of the primary and the premotor cortices are related to implementing the optimal control policy by transforming beliefs about proprioceptive and visual states, respectively, into motor commands.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                1 August 2017
                17 July 2017
                17 July 2017
                : 114
                : 31
                : 8426-8431
                Affiliations
                [1] aDepartment of Neuroscience, Karolinska Institutet , 17177 Stockholm, Sweden
                Author notes
                1To whom correspondence should be addressed. Email: konstantina.kilteni@ 123456ki.se .

                Edited by Peter L. Strick, University of Pittsburgh, Pittsburgh, PA, and approved June 16, 2017 (received for review February 27, 2017)

                Author contributions: K.K. and H.H.E. designed research; K.K. performed research; K.K. analyzed data; and K.K. and H.H.E. wrote the paper.

                Author information
                http://orcid.org/0000-0002-6887-6434
                Article
                PMC5547616 PMC5547616 5547616 201703347
                10.1073/pnas.1703347114
                5547616
                28716932
                b8056a62-8bcf-4161-8100-9a8fe39c68e9

                Freely available online through the PNAS open access option.

                History
                Page count
                Pages: 6
                Categories
                Biological Sciences
                Psychological and Cognitive Sciences

                sensory attenuation,predictive motor control,state estimation,forward models,body ownership

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