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      On the Role of Bilateral Brain Hypofunction and Abnormal Lateralization of Cortical Information Flow as Neural Underpinnings of Conventional Metaphor Processing Impairment in Schizophrenia: An fMRI and EEG Study

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          Abstract

          Figurative language processing (e.g. metaphors) is commonly impaired in schizophrenia. In the present study, we investigated the neural activity and propagation of information within neural circuits related to the figurative speech, as a neural substrate of impaired conventional metaphor processing in schizophrenia. The study included 30 schizophrenia outpatients and 30 healthy controls, all of whom were assessed with a functional Magnetic Resonance Imaging (fMRI) and electroencephalography (EEG) punchline-based metaphor comprehension task including literal (neutral), figurative (metaphorical) and nonsense (absurd) endings. The blood oxygenation level-dependent signal was recorded with 3T MRI scanner and direction and strength of cortical information flow in the time course of task processing was estimated with a 64-channel EEG input for directed transfer function. The presented results revealed that the behavioral manifestation of impaired figurative language in schizophrenia is related to the hypofunction in the bilateral fronto-temporo-parietal brain regions (fMRI) and various differences in effective connectivity in the fronto-temporo-parietal circuit (EEG). Schizophrenia outpatients showed an abnormal pattern of connectivity during metaphor processing which was related to bilateral (but more pronounced at the left hemisphere) hypoactivation of the brain. Moreover, we found reversed lateralization patterns, i.e. a rightward-shifted pattern during metaphor processing in schizophrenia compared to the control group. In conclusion, the presented findings revealed that the impairment of the conventional metaphor processing in schizophrenia is related to the bilateral brain hypofunction, which supports the evidence on reversed lateralization of the language neural network and the existence of compensatory recruitment of alternative neural circuits in schizophrenia.

          Supplementary Information

          The online version contains supplementary material available at 10.1007/s10548-021-00849-x.

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          World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects.

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            The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment.

            To develop a 10-minute cognitive screening tool (Montreal Cognitive Assessment, MoCA) to assist first-line physicians in detection of mild cognitive impairment (MCI), a clinical state that often progresses to dementia. Validation study. A community clinic and an academic center. Ninety-four patients meeting MCI clinical criteria supported by psychometric measures, 93 patients with mild Alzheimer's disease (AD) (Mini-Mental State Examination (MMSE) score > or =17), and 90 healthy elderly controls (NC). The MoCA and MMSE were administered to all participants, and sensitivity and specificity of both measures were assessed for detection of MCI and mild AD. Using a cutoff score 26, the MMSE had a sensitivity of 18% to detect MCI, whereas the MoCA detected 90% of MCI subjects. In the mild AD group, the MMSE had a sensitivity of 78%, whereas the MoCA detected 100%. Specificity was excellent for both MMSE and MoCA (100% and 87%, respectively). MCI as an entity is evolving and somewhat controversial. The MoCA is a brief cognitive screening tool with high sensitivity and specificity for detecting MCI as currently conceptualized in patients performing in the normal range on the MMSE.
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              EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis

              We have developed a toolbox and graphic user interface, EEGLAB, running under the crossplatform MATLAB environment (The Mathworks, Inc.) for processing collections of single-trial and/or averaged EEG data of any number of channels. Available functions include EEG data, channel and event information importing, data visualization (scrolling, scalp map and dipole model plotting, plus multi-trial ERP-image plots), preprocessing (including artifact rejection, filtering, epoch selection, and averaging), independent component analysis (ICA) and time/frequency decompositions including channel and component cross-coherence supported by bootstrap statistical methods based on data resampling. EEGLAB functions are organized into three layers. Top-layer functions allow users to interact with the data through the graphic interface without needing to use MATLAB syntax. Menu options allow users to tune the behavior of EEGLAB to available memory. Middle-layer functions allow users to customize data processing using command history and interactive 'pop' functions. Experienced MATLAB users can use EEGLAB data structures and stand-alone signal processing functions to write custom and/or batch analysis scripts. Extensive function help and tutorial information are included. A 'plug-in' facility allows easy incorporation of new EEG modules into the main menu. EEGLAB is freely available (http://www.sccn.ucsd.edu/eeglab/) under the GNU public license for noncommercial use and open source development, together with sample data, user tutorial and extensive documentation.
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                Author and article information

                Contributors
                przemyslaw.adamczyk@uj.edu.pl , przemyslaw.adamczyk@mailplus.pl
                Journal
                Brain Topogr
                Brain Topogr
                Brain Topography
                Springer US (New York )
                0896-0267
                1573-6792
                10 May 2021
                10 May 2021
                2021
                : 34
                : 4
                : 537-554
                Affiliations
                [1 ]GRID grid.5522.0, ISNI 0000 0001 2162 9631, Institute of Psychology, , Jagiellonian University, ; Ingardena 6, 30-060 Kraków, Poland
                [2 ]GRID grid.412554.3, ISNI 0000 0004 0609 2751, Department of Psychiatry, Faculty of Medicine, , Masaryk University and University Hospital Brno, ; Brno, Czech Republic
                [3 ]GRID grid.5522.0, ISNI 0000 0001 2162 9631, Community Psychiatry and Psychosis Research Center, Chair of Psychiatry, Medical College, , Jagiellonian University, ; Kraków, Poland
                Author notes

                Handling Editor: Christoph M Michel

                Author information
                http://orcid.org/0000-0003-0100-986X
                http://orcid.org/0000-0002-1613-1895
                http://orcid.org/0000-0002-2420-7204
                http://orcid.org/0000-0002-0117-5844
                http://orcid.org/0000-0002-3330-2705
                http://orcid.org/0000-0003-1091-5485
                Article
                849
                10.1007/s10548-021-00849-x
                8195899
                33973137
                004e07dc-441b-451c-94c1-800f2c1958a4
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 30 October 2020
                : 5 May 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: 2016/23/B/HS6/00286
                Award Recipient :
                Categories
                Original Paper
                Custom metadata
                © Springer Science+Business Media, LLC, part of Springer Nature 2021

                Neurology
                metaphor,schizophrenia,effective connectivity,lateralization,electroencephalography,directed transfer function,functional magnetic resonance imaging

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