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      Somato-Motor Haptic Processing in Posterior Inner Perisylvian Region (SII/pIC) of the Macaque Monkey

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          Abstract

          The posterior inner perisylvian region including the secondary somatosensory cortex (area SII) and the adjacent region of posterior insular cortex (pIC) has been implicated in haptic processing by integrating somato-motor information during hand-manipulation, both in humans and in non-human primates. However, motor-related properties during hand-manipulation are still largely unknown. To investigate a motor-related activity in the hand region of SII/pIC, two macaque monkeys were trained to perform a hand-manipulation task, requiring 3 different grip types (precision grip, finger exploration, side grip) both in light and in dark conditions. Our results showed that 70% ( n = 33/48) of task related neurons within SII/pIC were only activated during monkeys’ active hand-manipulation. Of those 33 neurons, 15 (45%) began to discharge before hand-target contact, while the remaining neurons were tonically active after contact. Thirty-percent ( n = 15/48) of studied neurons responded to both passive somatosensory stimulation and to the motor task. A consistent percentage of task-related neurons in SII/pIC was selectively activated during finger exploration (FE) and precision grasping (PG) execution, suggesting they play a pivotal role in control skilled finger movements. Furthermore, hand-manipulation-related neurons also responded when visual feedback was absent in the dark. Altogether, our results suggest that somato-motor neurons in SII/pIC likely contribute to haptic processing from the initial to the final phase of grasping and object manipulation. Such motor-related activity could also provide the somato-motor binding principle enabling the translation of diachronic somatosensory inputs into a coherent image of the explored object.

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          Coding and use of tactile signals from the fingertips in object manipulation tasks.

          During object manipulation tasks, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output to the physical properties of the objects involved. Analysis of signals in tactile afferent neurons and central processes in humans reveals how contact events are encoded and used to monitor and update task performance.
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            An internal model for sensorimotor integration.

            On the basis of computational studies it has been proposed that the central nervous system internally simulates the dynamic behavior of the motor system in planning, control, and learning; the existence and use of such an internal model is still under debate. A sensorimotor integration task was investigated in which participants estimated the location of one of their hands at the end of movements made in the dark and under externally imposed forces. The temporal propagation of errors in this task was analyzed within the theoretical framework of optimal state estimation. These results provide direct support for the existence of an internal model.
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              Central cancellation of self-produced tickle sensation.

              A self-produced tactile stimulus is perceived as less ticklish than the same stimulus generated externally. We used fMRI to examine neural responses when subjects experienced a tactile stimulus that was either self-produced or externally produced. More activity was found in somatosensory cortex when the stimulus was externally produced. In the cerebellum, less activity was associated with a movement that generated a tactile stimulus than with a movement that did not. This difference suggests that the cerebellum is involved in predicting the specific sensory consequences of movements, providing the signal that is used to cancel the sensory response to self-generated stimulation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                30 July 2013
                : 8
                : 7
                : e69931
                Affiliations
                [1 ]Italian Institute of Technology (IIT), Brain Center for Motor and Social Cognition (BCSMC), Parma, Italy
                [2 ]Department of Neuroscience, Unit of Physiology, Parma University Parma, Italy
                University of Ottawa, Canada
                Author notes

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

                Conceived and designed the experiments: HI VG. Performed the experiments: HI LF LCG. Analyzed the data: HI LCG LF MAU. Wrote the paper: HI VG.

                Article
                PONE-D-13-09301
                10.1371/journal.pone.0069931
                3728371
                23936121
                24aeb71e-cd4d-46b1-9498-e609cd5448c9
                Copyright @ 2013

                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
                : 28 February 2013
                : 12 June 2013
                Page count
                Pages: 14
                Funding
                This work was supported by Rete Tecnologica Mulidisciplinare, Italian Institute of Technology, and by European Grant “Cogsystem”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Model Organisms
                Animal Models
                Macaque
                Molecular Cell Biology
                Cellular Types
                Neurons
                Neuroscience
                Cognitive Neuroscience
                Motor Reactions
                Neurophysiology
                Motor Systems
                Motor Systems
                Sensory Systems

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                Uncategorized

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