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      Quantitative evaluation of muscle synergy models: a single-trial task decoding approach

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          Abstract

          Muscle synergies, i.e., invariant coordinated activations of groups of muscles, have been proposed as building blocks that the central nervous system (CNS) uses to construct the patterns of muscle activity utilized for executing movements. Several efficient dimensionality reduction algorithms that extract putative synergies from electromyographic (EMG) signals have been developed. Typically, the quality of synergy decompositions is assessed by computing the Variance Accounted For (VAF). Yet, little is known about the extent to which the combination of those synergies encodes task-discriminating variations of muscle activity in individual trials. To address this question, here we conceive and develop a novel computational framework to evaluate muscle synergy decompositions in task space. Unlike previous methods considering the total variance of muscle patterns (VAF based metrics), our approach focuses on variance discriminating execution of different tasks. The procedure is based on single-trial task decoding from muscle synergy activation features. The task decoding based metric evaluates quantitatively the mapping between synergy recruitment and task identification and automatically determines the minimal number of synergies that captures all the task-discriminating variability in the synergy activations. In this paper, we first validate the method on plausibly simulated EMG datasets. We then show that it can be applied to different types of muscle synergy decomposition and illustrate its applicability to real data by using it for the analysis of EMG recordings during an arm pointing task. We find that time-varying and synchronous synergies with similar number of parameters are equally efficient in task decoding, suggesting that in this experimental paradigm they are equally valid representations of muscle synergies. Overall, these findings stress the effectiveness of the decoding metric in systematically assessing muscle synergy decompositions in task space.

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          Most cited references40

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          Extracting information from neuronal populations: information theory and decoding approaches.

          To a large extent, progress in neuroscience has been driven by the study of single-cell responses averaged over several repetitions of stimuli or behaviours. However,the brain typically makes decisions based on single events by evaluating the activity of large neuronal populations. Therefore, to further understand how the brain processes information, it is important to shift from a single-neuron, multiple-trial framework to multiple-neuron, single-trial methodologies. Two related approaches--decoding and information theory--can be used to extract single-trial information from the activity of neuronal populations. Such population analysis can give us more information about how neurons encode stimulus features than traditional single-cell studies.
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            Shared and specific muscle synergies in natural motor behaviors.

            Selecting the appropriate muscle pattern to achieve a given goal is an extremely complex task because of the dimensionality of the search space and because of the nonlinear and dynamical nature of the transformation between muscle activity and movement. To investigate whether the central nervous system uses a modular architecture to achieve motor coordination we characterized the motor output over a large set of movements. We recorded electromyographic activity from 13 muscles of the hind limb of intact and freely moving frogs during jumping, swimming, and walking in naturalistic conditions. We used multidimensional factorization techniques to extract invariant amplitude and timing relationships among the muscle activations. A decomposition of the instantaneous muscle activations as combinations of nonnegative vectors, synchronous muscle synergies, revealed a spatial organization in the muscle patterns. A decomposition of the same activations as a combination of temporal sequences of nonnegative vectors, time-varying muscle synergies, further uncovered specific characteristics in the muscle activation waveforms. A mixture of synergies shared across behaviors and synergies for specific behaviors captured the invariances across the entire dataset. These results support the hypothesis that the motor controller has a modular organization.
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              The case for and against muscle synergies.

              A long standing goal in motor control is to determine the fundamental output controlled by the CNS: does the CNS control the activation of individual motor units, individual muscles, groups of muscles, kinematic or dynamic features of movement, or does it simply care about accomplishing a task? Of course, the output controlled by the CNS might not be exclusive but instead multiple outputs might be controlled in parallel or hierarchically. In this review we examine one particular hypothesized level of control: that the CNS produces movement through the flexible combination of groups of muscles, or muscle synergies. Several recent studies have examined this hypothesis, providing evidence both in support and in opposition to it. We discuss these results and the current state of the muscle synergy hypothesis. Copyright 2009 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Front Comput Neurosci
                Front Comput Neurosci
                Front. Comput. Neurosci.
                Frontiers in Computational Neuroscience
                Frontiers Media S.A.
                1662-5188
                26 February 2013
                2013
                : 7
                : 8
                Affiliations
                [1] 1Robotics, Brain and Cognitive Sciences Department, Istituto Italiano di Tecnologia Genoa, Italy
                [2] 2Communication, Computer and System Sciences Department, Doctoral School on Life and Humanoid Technologies, University of Genoa Genoa, Italy
                [3] 3UR CIAMS, EA 4532 – Motor Control and Perception Team, Université Paris-Sud 11 Orsay, France
                [4] 4Institut Universitaire de France, Université de Bourgogne, Campus Universitaire UFR STAPS Dijon, France
                [5] 5INSERM, U1093, Action Cognition et Plasticité Sensorimotrice Dijon, France
                [6] 6Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia Rovereto, Italy
                [7] 7Institute of Neuroscience and Psychology, University of Glasgow Glasgow, UK
                Author notes

                Edited by: Andrea D'Avella, IRCCS Fondazione Santa Lucia, Italy

                Reviewed by: Simon Giszter, Drexel Med School, USA; Dominik M. Endres, HIH, CIN, BCCN and University of Tübingen, Germany

                *Correspondence: Ioannis Delis, Robotics, Brain and Cognitive Sciences Department, Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genoa, Italy. e-mail: ioannis.delis@ 123456iit.it
                Stefano Panzeri, Institute of Neuroscience and Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK. e-mail: stefano.panzeri@ 123456glasgow.ac.uk
                Article
                10.3389/fncom.2013.00008
                3590454
                23471195
                0f52a7fb-fcab-47b6-839a-41359c6f47d7
                Copyright © 2013 Delis, Berret, Pozzo and Panzeri.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 06 November 2012
                : 07 February 2013
                Page count
                Figures: 9, Tables: 0, Equations: 6, References: 60, Pages: 21, Words: 16409
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                muscle synergies,reaching,arm movement,task decoding,single-trial analysis
                Neurosciences
                muscle synergies, reaching, arm movement, task decoding, single-trial analysis

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