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      MVPA Analysis of Intertrial Phase Coherence of Neuromagnetic Responses to Words Reliably Classifies Multiple Levels of Language Processing in the Brain

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          Abstract

          Neural processing of language is still among the most poorly understood functions of the human brain, whereas a need to objectively assess the neurocognitive status of the language function in a participant-friendly and noninvasive fashion arises in various situations. Here, we propose a solution for this based on a short task-free recording of MEG responses to a set of spoken linguistic contrasts. We used spoken stimuli that diverged lexically (words/pseudowords), semantically (action-related/abstract), or morphosyntactically (grammatically correct/ungrammatical). Based on beamformer source reconstruction we investigated intertrial phase coherence (ITPC) in five canonical bands (α, β, and low, medium, and high γ) using multivariate pattern analysis (MVPA). Using this approach, we could successfully classify brain responses to meaningful words from meaningless pseudowords, correct from incorrect syntax, as well as semantic differences. The best classification results indicated distributed patterns of activity dominated by core temporofrontal language circuits and complemented by other areas. They varied between the different neurolinguistic properties across frequency bands, with lexical processes classified predominantly by broad γ, semantic distinctions by α and β, and syntax by low γ feature patterns. Crucially, all types of processing commenced in a near-parallel fashion from ∼100 ms after the auditory information allowed for disambiguating the spoken input. This shows that individual neurolinguistic processes take place simultaneously and involve overlapping yet distinct neuronal networks that operate at different frequency bands. This brings further hope that brain imaging can be used to assess neurolinguistic processes objectively and noninvasively in a range of populations.

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          Most cited references61

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          The mismatch negativity (MMN) in basic research of central auditory processing: a review.

          In the present article, the basic research using the mismatch negativity (MMN) and analogous results obtained by using the magnetoencephalography (MEG) and other brain-imaging technologies is reviewed. This response is elicited by any discriminable change in auditory stimulation but recent studies extended the notion of the MMN even to higher-order cognitive processes such as those involving grammar and semantic meaning. Moreover, MMN data also show the presence of automatic intelligent processes such as stimulus anticipation at the level of auditory cortex. In addition, the MMN enables one to establish the brain processes underlying the initiation of attention switch to, conscious perception of, sound change in an unattended stimulus stream.
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            On the interpretation of weight vectors of linear models in multivariate neuroimaging.

            The increase in spatiotemporal resolution of neuroimaging devices is accompanied by a trend towards more powerful multivariate analysis methods. Often it is desired to interpret the outcome of these methods with respect to the cognitive processes under study. Here we discuss which methods allow for such interpretations, and provide guidelines for choosing an appropriate analysis for a given experimental goal: For a surgeon who needs to decide where to remove brain tissue it is most important to determine the origin of cognitive functions and associated neural processes. In contrast, when communicating with paralyzed or comatose patients via brain-computer interfaces, it is most important to accurately extract the neural processes specific to a certain mental state. These equally important but complementary objectives require different analysis methods. Determining the origin of neural processes in time or space from the parameters of a data-driven model requires what we call a forward model of the data; such a model explains how the measured data was generated from the neural sources. Examples are general linear models (GLMs). Methods for the extraction of neural information from data can be considered as backward models, as they attempt to reverse the data generating process. Examples are multivariate classifiers. Here we demonstrate that the parameters of forward models are neurophysiologically interpretable in the sense that significant nonzero weights are only observed at channels the activity of which is related to the brain process under study. In contrast, the interpretation of backward model parameters can lead to wrong conclusions regarding the spatial or temporal origin of the neural signals of interest, since significant nonzero weights may also be observed at channels the activity of which is statistically independent of the brain process under study. As a remedy for the linear case, we propose a procedure for transforming backward models into forward models. This procedure enables the neurophysiological interpretation of the parameters of linear backward models. We hope that this work raises awareness for an often encountered problem and provides a theoretical basis for conducting better interpretable multivariate neuroimaging analyses. Copyright © 2013 The Authors. Published by Elsevier Inc. All rights reserved.
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              Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization.

              Cortical activity and perception are not driven by the external stimulus alone; rather sensory information has to be integrated with various other internal constraints such as expectations, recent memories, planned actions, etc. The question is how large scale integration over many remote and size-varying processes might be performed by the brain. We have conducted a series of EEG recordings during processes thought to involve neuronal assemblies of varying complexity. While local synchronization during visual processing evolved in the gamma frequency range, synchronization between neighboring temporal and parietal cortex during multimodal semantic processing evolved in a lower, the beta1 (12-18 Hz) frequency range, and long range fronto-parietal interactions during working memory retention and mental imagery evolved in the theta and alpha (4-8 Hz, 8-12 Hz) frequency range. Thus, a relationship seems to exist between the extent of functional integration and the synchronization-frequency. In particular, long-range interactions in the alpha and theta ranges seem specifically involved in processing of internal mental context, i.e. for top-down processing. We propose that large scale integration is performed by synchronization among neurons and neuronal assemblies evolving in different frequency ranges.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                5 August 2019
                14 August 2019
                Jul-Aug 2019
                : 6
                : 4
                : ENEURO.0444-18.2019
                Affiliations
                [1 ]Center of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University , 8000 Aarhus, Denmark
                [2 ]Laboratory of Behavioural Neurodynamics, St. Petersburg State University , St. Petersburg, 199034, Russia
                Author notes

                The authors declare no competing financial interests.

                Author contributions: M.J. and Y.S. contributed unpublished reagents/analytic tools; M.J. analyzed data; M.J. and Y.S. wrote the paper; R.H. and Y.S. designed research; R.H. performed research.

                This work was supported by the Danish Council for Independent Research (DFF, grant 6110-00486), Lundbeck Foundation (grants R164-2013-15801, R140-2013-12951), Central Jutland Regional Government (MINDLab infrastructure grant), RF Government (grant contract No 14.W03.31.0010), and Aarhus University.

                Correspondence should be addressed to Mads Jensen at mads@ 123456cfin.au.dk .
                Author information
                https://orcid.org/0000-0003-3777-1514
                Article
                eN-NWR-0444-18
                10.1523/ENEURO.0444-18.2019
                6709219
                31383728
                6d9ecb87-e43e-4aa9-b8c5-21b87b2eaaed
                Copyright © 2019 Jensen et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 7 November 2018
                : 30 May 2019
                : 28 June 2019
                Page count
                Figures: 8, Tables: 4, Equations: 2, References: 85, Pages: 16, Words: 11006
                Funding
                Funded by: http://doi.org/10.13039/501100004836Det Frie Forskningsråd (DFF)
                Award ID: 6110-00486
                Funded by: http://doi.org/10.13039/100008628Institut for Klinisk Medicin, Aarhus Universitet (Department of Clinical Medicine, Aarhus University)
                Award ID: 14.W03.31.0010
                Funded by: http://doi.org/10.13039/501100003554Lundbeckfonden (Lundbeck Foundation)
                Award ID: R164-2013-15801
                Award ID: R140-2013-12951
                Categories
                8
                8.1
                New Research
                Sensory and Motor Systems
                Custom metadata
                July/August 2019

                language,magnetoencephalography (meg),multivariate pattern analysis (mvpa),oscillations,lexical access,semantics,morphosyntax

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