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      The Right Supramarginal Gyrus Is Important for Proprioception in Healthy and Stroke-Affected Participants: A Functional MRI Study

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          Abstract

          Human proprioception is essential for motor control, yet its central processing is still debated. Previous studies of passive movements and illusory vibration have reported inconsistent activation patterns related to proprioception, particularly in high-order sensorimotor cortices. We investigated brain activation specific to proprioception, its laterality, and changes following stroke. Twelve healthy and three stroke-affected individuals with proprioceptive deficits participated. Proprioception was assessed clinically with the Wrist Position Sense Test, and participants underwent functional magnetic resonance imaging scanning. An event-related study design was used, where each proprioceptive stimulus of passive wrist movement was followed by a motor response of mirror ­copying with the other wrist. Left (LWP) and right (RWP) wrist proprioception were tested separately. Laterality indices (LIs) were calculated for the main cortical regions activated during proprioception. We found proprioception-related brain activation in high-order sensorimotor cortices in healthy participants especially in the supramarginal gyrus (SMG LWP z = 4.51, RWP z = 4.24) and the dorsal premotor cortex (PMd LWP z = 4.10, RWP z = 3.93). Right hemispheric dominance was observed in the SMG (LI LWP mean 0.41, SD 0.22; RWP 0.29, SD 0.20), and to a lesser degree in the PMd (LI LWP 0.34, SD 0.17; RWP 0.13, SD 0.25). In stroke-affected participants, the main difference in proprioception-related brain activation was reduced laterality in the right SMG. Our findings indicate that the SMG and PMd play a key role in proprioception probably due to their role in spatial processing and motor control, respectively. The findings from stroke-­affected individuals suggest that decreased right SMG function may be associated with decreased proprioception. We recommend that clinicians pay particular attention to the assessment and rehabilitation of proprioception following right hemispheric lesions.

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          Most cited references71

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          Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space.

          Experiments were made on the posterior parietal association cortical areas 5 and in 17 hemispheres of 11 monkeys, 6 M. mulatta and 5 M. arctoides. The electrical signs of the activity of single cortical cells were recorded with microelectrodes in waking animals as they carried out certain behavioral acts in response to a series of sensory cues. The behavioral paradigms were one for detection alone, and a second for detection plus projection of the arm to contact a stationary or moving target placed at arm's length. Of the 125 microelectrode penetrations made, 1,451 neurons were identified in terms of the correlation of their activity with the behavioral acts and their sensitivity or lack of it to sensory stimuli delivered passively; 180 were studied quantitatively. The locations of cortical neurons were identified in serial sections; 94 penetrations and 1,058 neurons were located with certainty. About two-thirds of the neurons of area 5 were activated by passive rotation of the limbs at their joints; of these, 82% were related to single, contralateral joints, 10% to two or more contralateral joints, 6% to ipsilateral, and 2% to joints on both sides of the body. A few of the latter were active during complex bodily postures. A large proportion of area 5 neurons were relatively insensitive to passive joint rotations, as compared with similar neurons of the postcentral gyrus, but were driven to high rates of discharge when the same joint was rotated during an active movement of the animal...
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            Premotor and parietal cortex: corticocortical connectivity and combinatorial computations.

            The dorsal premotor cortex is a functionally distinct cortical field or group of fields in the primate frontal cortex. Anatomical studies have confirmed that most parietal input to the dorsal premotor cortex originates from the superior parietal lobule. However, these projections arise not only from the dorsal aspect of area 5, as has long been known, but also from newly defined areas of posterior parietal cortex, which are directly connected with the extrastriate visual cortex. Thus, the dorsal premotor cortex receives much more direct visual input than previously accepted. It appears that this fronto-parietal network functions as a visuomotor controller-one that makes computations based on proprioceptive, visual, gaze, attentional, and other information to produce an output that reflects the selection, preparation, and execution of movements.
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              The mirror neuron system.

              Mirror neurons are a class of neurons, originally discovered in the premotor cortex of monkeys, that discharge both when individuals perform a given motor act and when they observe others perform that same motor act. Ample evidence demonstrates the existence of a cortical network with the properties of mirror neurons (mirror system) in humans. The human mirror system is involved in understanding others' actions and their intentions behind them, and it underlies mechanisms of observational learning. Herein, we will discuss the clinical implications of the mirror system.
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                Author and article information

                Contributors
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                03 December 2015
                2015
                : 6
                : 248
                Affiliations
                [1] 1Neurorehabilitation and Recovery, Stroke, Florey Institute of Neuroscience and Mental Health , Melbourne, VIC, Australia
                [2] 2Occupational Therapy, School of Allied Health, College of Science, Health and Engineering, La Trobe University , Melbourne, VIC, Australia
                Author notes

                Edited by: Roland Wiest, University of Bern, Switzerland

                Reviewed by: Maarten G. Lansberg, Stanford University, USA; Nobutaka Kawahara, Yokohama City University, Japan

                *Correspondence: Ettie Ben-Shabat, ebenshabat@ 123456gmail.com

                Amy Brodtmann and Leeanne M. Carey have contributed equally to this work.

                Specialty section: This article was submitted to Stroke, a section of the journal Frontiers in Neurology

                Article
                10.3389/fneur.2015.00248
                4668288
                26696951
                340c2593-4fb6-4d39-a52c-36e33111e822
                Copyright © 2015 Ben-Shabat, Matyas, Pell, Brodtmann and Carey.

                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) or licensor 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 August 2015
                : 12 November 2015
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 85, Pages: 14, Words: 10530
                Funding
                Funded by: National Health and Medical Research Council 10.13039/501100000925
                Award ID: 307905, 307902, 1022694, CCRE 219280
                Funded by: Australian Research Council 10.13039/501100000923
                Award ID: Future Fellowship FT0992299
                Funded by: La Trobe University 10.13039/501100001215
                Award ID: Post-graduate Research award
                Funded by: State Government of Victoria 10.13039/501100004752
                Award ID: Operational Infrastructure Support Program
                Funded by: Centre for Clinical Research Excellence (Neuroscience)
                Funded by: National Stroke Research Institute
                Categories
                Neuroscience
                Original Research

                Neurology
                proprioception,kinesthesis,upper extremity,functional laterality,stroke,magnetic resonance imaging,cerebral cortex

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