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      Granger Causality Mapping during Joint Actions Reveals Evidence for Forward Models That Could Overcome Sensory-Motor Delays

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      PLoS ONE

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          Abstract

          Studies investigating joint actions have suggested a central role for the putative mirror neuron system (pMNS) because of the close link between perception and action provided by these brain regions [1], [2], [3]. In contrast, our previous functional magnetic resonance imaging (fMRI) experiment demonstrated that the BOLD response of the pMNS does not suggest that it directly integrates observed and executed actions during joint actions [4]. To test whether the pMNS might contribute indirectly to the integration process by sending information to brain areas responsible for this integration (integration network), here we used Granger causality mapping (GCM) [5]. We explored the directional information flow between the anterior sites of the pMNS and previously identified integrative brain regions. We found that the left BA44 sent more information than it received to both the integration network (left thalamus, right middle occipital gyrus and cerebellum) and more posterior nodes of the pMNS (BA2). Thus, during joint actions, two anatomically separate networks therefore seem effectively connected and the information flow is predominantly from anterior to posterior areas of the brain. These findings suggest that the pMNS is involved indirectly in joint actions by transforming observed and executed actions into a common code and is part of a generative model that could predict the future somatosensory and visual consequences of observed and executed actions in order to overcome otherwise inevitable neural delays.

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          Most cited references 32

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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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            ALE meta-analysis of action observation and imitation in the human brain.

            Over the last decade, many neuroimaging studies have assessed the human brain networks underlying action observation and imitation using a variety of tasks and paradigms. Nevertheless, questions concerning which areas consistently contribute to these networks irrespective of the particular experimental design and how such processing may be lateralized remain unresolved. The current study aimed at identifying cortical areas consistently involved in action observation and imitation by combining activation likelihood estimation (ALE) meta-analysis with probabilistic cytoarchitectonic maps. Meta-analysis of 139 functional magnetic resonance and positron emission tomography experiments revealed a bilateral network for both action observation and imitation. Additional subanalyses for different effectors within each network revealed highly comparable activation patterns to the overall analyses on observation and imitation, respectively, indicating an independence of these findings from potential confounds. Conjunction analysis of action observation and imitation meta-analyses revealed a bilateral network within frontal premotor, parietal, and temporo-occipital cortex. The most consistently rostral inferior parietal area was PFt, providing evidence for a possible homology of this region to macaque area PF. The observation and imitation networks differed particularly with respect to the involvement of Broca's area: whereas both networks involved a caudo-dorsal part of BA 44, activation during observation was most consistent in a more rostro-dorsal location, i.e., dorsal BA 45, while activation during imitation was most consistent in a more ventro-caudal aspect, i.e., caudal BA 44. The present meta-analysis thus summarizes and amends previous descriptions of the human brain networks related to action observation and imitation. Copyright 2009 Elsevier Inc. All rights reserved.
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              Predictive coding: an account of the mirror neuron system.

              Is it possible to understand the intentions of other people by simply observing their actions? Many believe that this ability is made possible by the brain's mirror neuron system through its direct link between action and observation. However, precisely how intentions can be inferred through action observation has provoked much debate. Here we suggest that the function of the mirror system can be understood within a predictive coding framework that appeals to the statistical approach known as empirical Bayes. Within this scheme the most likely cause of an observed action can be inferred by minimizing the prediction error at all levels of the cortical hierarchy that are engaged during action observation. This account identifies a precise role for the mirror system in our ability to infer intentions from actions and provides the outline of the underlying computational mechanisms.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                21 October 2010
                : 5
                : 10
                Affiliations
                [1 ]Department of Neuroscience, BCN Neuroimaging Centre, University Medical Center Groningen, Groningen, The Netherlands
                [2 ]The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences (KNAW), Amsterdam, The Netherlands
                The University of Western Ontario, Canada
                Author notes

                Conceived and designed the experiments: IK CK. Performed the experiments: IK. Analyzed the data: IK CK. Wrote the paper: IK CK.

                Article
                10-PONE-RA-18894R2
                10.1371/journal.pone.0013507
                2958830
                20975836
                52765e79-7bd6-4acd-849c-697496dcce0f
                Kokal, Keysers. 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.
                Page count
                Pages: 10
                Categories
                Research Article
                Neuroscience
                Neuroscience/Motor Systems
                Neuroscience/Sensory Systems

                Uncategorized

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