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      Transcranial Direct Current Stimulation Improves Ipsilateral Selective Muscle Activation in a Frequency Dependent Manner

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          Abstract

          Failure to suppress antagonist muscles can lead to movement dysfunction, such as the abnormal muscle synergies often seen in the upper limb after stroke. A neurophysiological surrogate of upper limb synergies, the selectivity ratio (SR), can be determined from the ratio of biceps brachii (BB) motor evoked potentials to transcranial magnetic stimulation prior to forearm pronation versus elbow flexion. Surprisingly, cathodal transcranial direct current stimulation (c-TDCS) over ipsilateral primary motor cortex (M1) reduces (i.e. improves) the SR in healthy adults, and chronic stroke patients. The ability to suppress antagonist muscles may be exacerbated at high movement rates. The aim of the present study was to investigate whether the selective muscle activation of the biceps brachii (BB) is dependent on altering frequency demands, and whether the c-tDCS improvement of SR is dependent on task frequency. Seventeen healthy participants performed repetitive isometric elbow flexion and forearm pronation at three rates, before and after c-tDCS or sham delivered to ipsilateral left M1. Ipsilateral c-tDCS improved the SR in a frequency dependent manner by selectively suppressing BB antagonist excitability. Our findings confirm that c-tDCS is an effective tool for improving selective muscle activation, and provide novel evidence for its efficacy at rates of movement where it is most likely to benefit task performance.

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          Most cited references32

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          Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation.

          In this paper we demonstrate in the intact human the possibility of a non-invasive modulation of motor cortex excitability by the application of weak direct current through the scalp. Excitability changes of up to 40 %, revealed by transcranial magnetic stimulation, were accomplished and lasted for several minutes after the end of current stimulation. Excitation could be achieved selectively by anodal stimulation, and inhibition by cathodal stimulation. By varying the current intensity and duration, the strength and duration of the after-effects could be controlled. The effects were probably induced by modification of membrane polarisation. Functional alterations related to post-tetanic potentiation, short-term potentiation and processes similar to postexcitatory central inhibition are the likely candidates for the excitability changes after the end of stimulation. Transcranial electrical stimulation using weak current may thus be a promising tool to modulate cerebral excitability in a non-invasive, painless, reversible, selective and focal way.
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            Level of action of cathodal DC polarisation induced inhibition of the human motor cortex.

            To induce prolonged motor cortical excitability reductions by transcranial direct current stimulation in the human. Cathodal direct current stimulation was applied transcranially to the hand area of the human primary motor cortex from 5 to 9 min in separate sessions in twelve healthy subjects. Cortico-spinal excitability was tested by single pulse transcranial magnetic stimulation. Transcranial electrical stimulation and H-reflexes were used to learn about the origin of the excitability changes. Neurone specific enolase was measured before and after the stimulation to prove the safety of the stimulation protocol. Five and 7 min direct current stimulation resulted in motor cortical excitability reductions, which lasted for minutes after the end of stimulation, 9 min stimulation induced after-effects for up to an hour after the end of stimulation, as revealed by transcranial magnetic stimulation. Muscle evoked potentials elicited by transcranial electric stimulation and H-reflexes did not change. Neurone specific enolase concentrations remained stable throughout the experiments. Cathodal transcranial direct current stimulation is capable of inducing prolonged excitability reductions in the human motor cortex non-invasively. These changes are most probably localised intracortically.
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              Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity.

              Functional imaging studies have revealed recruitment of ipsilateral motor areas during the production of sequential unimanual finger movements. This phenomenon is more prominent in the left hemisphere during left-hand movements than in the right hemisphere during right-hand movements. Here we investigate whether this lateralization pattern is related specifically to the sequential structure of the unimanual action or generalizes to other complex movements. Using event-related fMRI, we measured activation changes in the motor cortex during three types of unimanual movements: repetitions of a sequence of movements with multiple fingers, repetitive "chords" composed of three simultaneous key presses, and simple repetitive tapping movements with a single finger. During sequence and chord movements, strong ipsilateral activation was observed and was especially pronounced in the left hemisphere during left-hand movements. This pattern was evident for both right-handed and, to a lesser degree, left-handed individuals. Ipsilateral activation was less pronounced in the tapping condition. The site of ipsilateral activation was shifted laterally, ventrally, and anteriorly with respect to that observed during contralateral movements and the time course of activation implied a role in the execution rather than planning of the movement. A control experiment revealed that strong ipsilateral activity in left motor cortex is specific to complex movements and does not depend on the number of required muscles. These findings indicate a prominent role of left hemisphere in the execution of complex movements independent of the sequential nature of the task.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 March 2015
                2015
                : 10
                : 3
                : e0122434
                Affiliations
                [1 ]Movement Neuroscience Laboratory, Department of Sport & Exercise Science, The University of Auckland, Auckland, New Zealand
                [2 ]Centre for Brain Research, The University of Auckland, Auckland, New Zealand
                [3 ]Human Motor Control Laboratory, Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, Higashi-Hiroshima, Hiroshima, Japan
                The University of Western Ontario, CANADA
                Author notes

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

                Conceived and designed the experiments: KU JPC WDB. Performed the experiments: KU JPC. Analyzed the data: KU JPC. Wrote the paper: JPC WDB KU.

                [¤a]

                Current address: Department of Advanced Neuroimaging, Integrative Brain Imaging Center, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan

                [¤b]

                Current address: School of Psychological Sciences, Faculty of Biomedical and Psychological Sciences, Faculty of Medicine, Nursing and Health Sciences, Monash University, Victoria, Australia

                Article
                PONE-D-14-53226
                10.1371/journal.pone.0122434
                4376864
                25816204
                28105d09-0065-430f-8f3c-71ac2cd9d377
                Copyright @ 2015

                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
                : 26 November 2014
                : 13 February 2015
                Page count
                Figures: 5, Tables: 3, Pages: 14
                Funding
                KU is supported by a postdoctoral fellow from Japan Society for the Promotion of Science (24-393). JPC is supported by a postdoctoral fellowship from the Aotearoa Foundation of New Zealand (9133-3627269). This study was financially supported by a Faculty Research Development Fund (FRDF) grant awarded to WDB (3704166). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article
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