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      Targeting the sensory feedback within the swallowing network—Reversing artificially induced pharyngolaryngeal hypesthesia by central and peripheral stimulation strategies

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          Abstract

          Pharyngolaryngeal hypesthesia is a major reason for dysphagia in various neurological diseases. Emerging neuromodulation devices have shown potential to foster dysphagia rehabilitation, but the optimal treatment strategy is unknown. Because functional imaging studies are difficult to conduct in severely ill patients, we induced a virtual sensory lesion in healthy volunteers and evaluated the effects of central and peripheral neurostimulation techniques. In a sham‐controlled intervention study with crossover design on 10 participants, we tested the potential of (peripheral) pharyngeal electrical stimulation (PES) and (central) transcranial direct current stimulation (tDCS) to revert the effects of lidocaine‐induced pharyngolaryngeal hypesthesia on central sensorimotor processing. Changes were observed during pharyngeal air‐pulse stimulation and voluntary swallowing applying magnetoencephalography before and after the interventions. PES induced a significant ( p < .05) increase of activation during swallowing in the bihemispheric sensorimotor network in alpha and low gamma frequency ranges, peaking in the right premotor and left primary sensory area, respectively. With pneumatic stimulation, significant activation increase was found after PES in high gamma peaking in the left premotor area. Significant changes of brain activation after tDCS could neither be detected for pneumatic stimulation nor for swallowing. Due to the peripheral cause of dysphagia in this model, PES was able to revert the detrimental effects of reduced sensory input on central processing, whereas tDCS was not. Results may have implications for therapeutic decisions in the clinical context.

          Abstract

          Pharyngolaryngeal hypesthesia is a major reason for dysphagia in various neurological diseases. Here, we investigated whether pharyngeal electrical stimulation (PES) or transcranial direct current stimulation can revert the effects of experimentally induced pharyngeal hypesthesia on cortical activation in healthy adults in a crossover sham‐controlled design by means of magnetoencephalography. PES was able to revert the detrimental effects of reduced sensory input on central processing, whereas transcranial direct current stimulation was not.

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          Most cited references71

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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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              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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                Author and article information

                Contributors
                muhlep@uni-muenster.de , paul.muhle@ukmuenster.de
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                17 October 2020
                1 February 2021
                : 42
                : 2 ( doiID: 10.1002/hbm.v42.2 )
                : 427-438
                Affiliations
                [ 1 ] Department of Neurology with Institute of Translational Neurology University Hospital Muenster Muenster Germany
                [ 2 ] Institute for Biomagnetism and Biosignalanalysis University Hospital Muenster Muenster Germany
                Author notes
                [*] [* ] Correspondence

                Paul Muhle, Department of Neurology with Institute of Translational Neurology, University Hospital Muenster, Albert‐Schweitzer Campus 1 A, Muenster 48149, Germany.

                Email: muhlep@ 123456uni-muenster.de , paul.muhle@ 123456ukmuenster.de

                Author information
                https://orcid.org/0000-0003-0865-0297
                Article
                HBM25233
                10.1002/hbm.25233
                7776007
                33068056
                a49c902d-ae78-4c23-ac40-d244ec4bc54a
                © 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 May 2020
                : 21 August 2020
                : 29 September 2020
                Page count
                Figures: 2, Tables: 2, Pages: 12, Words: 10704
                Funding
                Funded by: Deutsche Forschungsgemeinschaft , open-funder-registry 10.13039/501100001659;
                Award ID: SU 922/1–1
                Award ID: WO1425/6–1
                Award ID: DZ 78/1–1
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                February 1, 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.6 mode:remove_FC converted:02.01.2021

                Neurology
                dysphagia,neuromodulation,pharyngeal electrical stimulation,pharyngeal pneumatic stimulation,swallowing,transcranial direct current stimulation

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