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      Visual detection is locked to the internal dynamics of cortico-motor control

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          Abstract

          Movements overtly sample sensory information, making sensory analysis an active-sensing process. In this study, we show that visual information sampling is not just locked to the (overt) movement dynamics but to the internal (covert) dynamics of cortico-motor control. We asked human participants to perform continuous isometric contraction while detecting unrelated and unpredictable near-threshold visual stimuli. The motor output (force) shows zero-lag coherence with brain activity (recorded via electroencephalography) in the beta-band, as previously reported. In contrast, cortical rhythms in the alpha-band systematically forerun the motor output by 200 milliseconds. Importantly, visual detection is facilitated when cortico-motor alpha (not beta) synchronization is enhanced immediately before stimulus onset, namely, at the optimal phase relationship for sensorimotor communication. These findings demonstrate an ongoing coupling between visual sampling and motor control, suggesting the operation of an internal and alpha-cycling visuomotor loop.

          Abstract

          The motor rhythm of perception. Movements overtly sample sensory information, making sensory analysis an active-sensing process. This study shows that visual information sampling is not just synchronized to the (overt) movement dynamics, but to the internal (covert) dynamics of cortico-motor control.

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          Most cited references 84

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          Dynamic predictions: oscillations and synchrony in top-down processing.

          Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.
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            FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data

            This paper describes FieldTrip, an open source software package that we developed for the analysis of MEG, EEG, and other electrophysiological data. The software is implemented as a MATLAB toolbox and includes a complete set of consistent and user-friendly high-level functions that allow experimental neuroscientists to analyze experimental data. It includes algorithms for simple and advanced analysis, such as time-frequency analysis using multitapers, source reconstruction using dipoles, distributed sources and beamformers, connectivity analysis, and nonparametric statistical permutation tests at the channel and source level. The implementation as toolbox allows the user to perform elaborate and structured analyses of large data sets using the MATLAB command line and batch scripting. Furthermore, users and developers can easily extend the functionality and implement new algorithms. The modular design facilitates the reuse in other software packages.
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              Nonparametric statistical testing of EEG- and MEG-data.

              In this paper, we show how ElectroEncephaloGraphic (EEG) and MagnetoEncephaloGraphic (MEG) data can be analyzed statistically using nonparametric techniques. Nonparametric statistical tests offer complete freedom to the user with respect to the test statistic by means of which the experimental conditions are compared. This freedom provides a straightforward way to solve the multiple comparisons problem (MCP) and it allows to incorporate biophysically motivated constraints in the test statistic, which may drastically increase the sensitivity of the statistical test. The paper is written for two audiences: (1) empirical neuroscientists looking for the most appropriate data analysis method, and (2) methodologists interested in the theoretical concepts behind nonparametric statistical tests. For the empirical neuroscientist, a large part of the paper is written in a tutorial-like fashion, enabling neuroscientists to construct their own statistical test, maximizing the sensitivity to the expected effect. And for the methodologist, it is explained why the nonparametric test is formally correct. This means that we formulate a null hypothesis (identical probability distribution in the different experimental conditions) and show that the nonparametric test controls the false alarm rate under this null hypothesis.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                20 October 2020
                October 2020
                20 October 2020
                : 18
                : 10
                Affiliations
                [1 ] Istituto Italiano di Tecnologia, Center for Translational Neurophysiology of Speech and Communication (CTNSC), Ferrara, Italy
                [2 ] Radboud University, Donders Institute for Brain, Cognition and Behavior, Centre for Cognition (DCC), Nijmegen, The Netherlands
                [3 ] Università di Ferrara, Dipartimento di Scienze Biomediche e Chirurgico Specialistiche, Ferrara, Italy
                German Primate Center, GERMANY
                Author notes

                The authors have declared that no competing interests exists.

                Article
                PBIOLOGY-D-20-01860
                10.1371/journal.pbio.3000898
                7598921
                33079930
                © 2020 Tomassini et al

                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
                Figures: 7, Tables: 0, Pages: 25
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003196, Ministero della Salute;
                Award ID: GR-2016-02361008
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003196, Ministero della Salute;
                Award ID: GR-2018-12366027
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100007601, Horizon 2020;
                Award ID: FETPROACT-824160
                Award Recipient :
                This work has been supported by Ministero della Salute, Ricerca Finalizzata 2016 - Giovani Ricercatori (GR-2016-02361008) and Ministero della Salute, Ricerca Finalizzata 2018 - Giovani Ricercatori (GR-2018-12366027) to AD and by the European Union H2020 - EnTimeMent (FETPROACT-824160) to LF. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                2020-10-30
                All data files are available from the Open Science Framework Data Repository ( osf.io): DOI 10.17605/OSF.IO/VSZCB

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