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      Alterations in the default mode network in rolandic epilepsy with mild spike-wave index in non-rapid eye movement sleep

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          Abstract

          Purpose

          Rolandic epilepsy (RE) is one of the most common epilepsy syndromes during childhood. The aim of this study was to investigate the alterations in the default mode network (DMN) of RE patients whose spike-wave index (SWI) was within the 50–85% range during non-rapid eye movement (NREM) during sleep, as well as to detect early neuroimaging markers.

          Methods

          Resting-state data was recorded for each subject using magnetoencephalography (MEG). DMN-related brain regions were chosen as regions of interest. The spectral power and functional connectivity (FC) of the DMN were estimated through the use of minimum norm estimation (MNE) combined with Welch technique and corrected amplitude envelope correlation (AEC-c).

          Results

          The patient group included 20 patients with NREM phase 50% ≤ SWI < 85% (mild SWI group), and 18 typical RE patients (SWI < 50% group). At the regional level, the mild SWI group exhibited enhanced spectral power in the delta band of the bilateral posterial cingulate cortex and attenuated the spectral power in the alpha band of the bilateral posterial cingulate cortex. Enhanced spectral power in the bilateral precuneus (PCu) in the delta band and attenuated spectral power in the right lateral temporal cortex (LTC) in the alpha band were common across all RE patients. At the FC level, patients in the mild SWI group indicated increased AEC-c values between the bilateral posterial cingulate cortex in the delta band and between the left medial frontal cortex (MFC) and bilateral posterial cingulate cortex in the alpha band. Increased AEC-c values between the right PCu and left MFC in the delta band, and between the left PCu and right MFC in the theta band, were common across all RE patients. Moreover, the spectral power in the bilateral posterial cingulate cortex in the alpha band and the AEC-c value between the bilateral posterial cingulate cortex in the delta band demonstrated good discrimination ability.

          Conclusion

          The spectral power of the bilateral posterior cingulate cortex (PCC) in the alpha band and the AEC-c value between the bilateral PCC in the delta band may be promising indicators of early differentiation between mild SWI and typical RE.

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          Most cited references61

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          Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

          An anatomical parcellation of the spatially normalized single-subject high-resolution T1 volume provided by the Montreal Neurological Institute (MNI) (D. L. Collins et al., 1998, Trans. Med. Imag. 17, 463-468) was performed. The MNI single-subject main sulci were first delineated and further used as landmarks for the 3D definition of 45 anatomical volumes of interest (AVOI) in each hemisphere. This procedure was performed using a dedicated software which allowed a 3D following of the sulci course on the edited brain. Regions of interest were then drawn manually with the same software every 2 mm on the axial slices of the high-resolution MNI single subject. The 90 AVOI were reconstructed and assigned a label. Using this parcellation method, three procedures to perform the automated anatomical labeling of functional studies are proposed: (1) labeling of an extremum defined by a set of coordinates, (2) percentage of voxels belonging to each of the AVOI intersected by a sphere centered by a set of coordinates, and (3) percentage of voxels belonging to each of the AVOI intersected by an activated cluster. An interface with the Statistical Parametric Mapping package (SPM, J. Ashburner and K. J. Friston, 1999, Hum. Brain Mapp. 7, 254-266) is provided as a freeware to researchers of the neuroimaging community. We believe that this tool is an improvement for the macroscopical labeling of activated area compared to labeling assessed using the Talairach atlas brain in which deformations are well known. However, this tool does not alleviate the need for more sophisticated labeling strategies based on anatomical or cytoarchitectonic probabilistic maps.
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            The brain's default network: anatomy, function, and relevance to disease.

            Thirty years of brain imaging research has converged to define the brain's default network-a novel and only recently appreciated brain system that participates in internal modes of cognition. Here we synthesize past observations to provide strong evidence that the default network is a specific, anatomically defined brain system preferentially active when individuals are not focused on the external environment. Analysis of connectional anatomy in the monkey supports the presence of an interconnected brain system. Providing insight into function, the default network is active when individuals are engaged in internally focused tasks including autobiographical memory retrieval, envisioning the future, and conceiving the perspectives of others. Probing the functional anatomy of the network in detail reveals that it is best understood as multiple interacting subsystems. The medial temporal lobe subsystem provides information from prior experiences in the form of memories and associations that are the building blocks of mental simulation. The medial prefrontal subsystem facilitates the flexible use of this information during the construction of self-relevant mental simulations. These two subsystems converge on important nodes of integration including the posterior cingulate cortex. The implications of these functional and anatomical observations are discussed in relation to possible adaptive roles of the default network for using past experiences to plan for the future, navigate social interactions, and maximize the utility of moments when we are not otherwise engaged by the external world. We conclude by discussing the relevance of the default network for understanding mental disorders including autism, schizophrenia, and Alzheimer's disease.
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              Functional connectivity in the resting brain: a network analysis of the default mode hypothesis.

              Functional imaging studies have shown that certain brain regions, including posterior cingulate cortex (PCC) and ventral anterior cingulate cortex (vACC), consistently show greater activity during resting states than during cognitive tasks. This finding led to the hypothesis that these regions constitute a network supporting a default mode of brain function. In this study, we investigate three questions pertaining to this hypothesis: Does such a resting-state network exist in the human brain? Is it modulated during simple sensory processing? How is it modulated during cognitive processing? To address these questions, we defined PCC and vACC regions that showed decreased activity during a cognitive (working memory) task, then examined their functional connectivity during rest. PCC was strongly coupled with vACC and several other brain regions implicated in the default mode network. Next, we examined the functional connectivity of PCC and vACC during a visual processing task and show that the resultant connectivity maps are virtually identical to those obtained during rest. Last, we defined three lateral prefrontal regions showing increased activity during the cognitive task and examined their resting-state connectivity. We report significant inverse correlations among all three lateral prefrontal regions and PCC, suggesting a mechanism for attenuation of default mode network activity during cognitive processing. This study constitutes, to our knowledge, the first resting-state connectivity analysis of the default mode and provides the most compelling evidence to date for the existence of a cohesive default mode network. Our findings also provide insight into how this network is modulated by task demands and what functions it might subserve.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                09 August 2022
                2022
                : 16
                : 944391
                Affiliations
                [1] 1Department of Neurology, The Affiliated Brain Hospital of Nanjing Medical University , Nanjing, China
                [2] 2MEG Center, Nanjing Brain Hospital , Nanjing, China
                Author notes

                Edited by: Radek Marecek, Central European Institute of Technology (CEITEC), Czechia

                Reviewed by: Ana Paula Millán Vidal, Amsterdam University Medical Center, Netherlands; Sara Spadone, University of Studies G. d’Annunzio Chieti and Pescara, Italy

                *Correspondence: Xiaoshan Wang, lidou2005@ 123456126.com

                These authors have contributed equally to this work

                This article was submitted to Brain Imaging Methods, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2022.944391
                9395966
                36017188
                693f3e0f-2046-4bf7-bc13-59608bfd2c89
                Copyright © 2022 Li, Wang, Jiang, Sun, Chen and Wang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 15 May 2022
                : 25 July 2022
                Page count
                Figures: 3, Tables: 3, Equations: 2, References: 61, Pages: 13, Words: 10020
                Funding
                Funded by: National Natural Science Foundation of China, doi 10.13039/501100001809;
                Award ID: Grant No. 81471324
                Funded by: Natural Science Foundation of Jiangsu Province, doi 10.13039/501100004608;
                Award ID: Grant No. BK20191127
                Funded by: Jiangsu Commission of Health, doi 10.13039/100017962;
                Award ID: Grant No. H2018062
                Funded by: Nanjing Science and Technology Commission, doi 10.13039/501100011990;
                Award ID: Grant No. 201911044
                Categories
                Neuroscience
                Original Research

                Neurosciences
                rolandic epilepsy,default mode network,magnetoencephalography,spectral power,functional connectivity

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