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      Increased resting‐state activity in the cerebellum with mothers having less adaptive sensory processing and trait anxiety

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          Abstract

          Child‐rearing mothers with high levels of trait anxiety have a tendency for less adaptive sensory processing, which causes parenting stress. However, the neural mechanisms underlying this sensory processing and trait anxiety remain unclear. We aimed to determine the whole‐brain spontaneous neural activity and sensory processing characteristics in mothers with varying parenting stress levels. Using resting‐state functional magnetic resonance imaging, we assessed mothers caring for more than one preschool aged (2–5 years) child and presenting with varying levels of sensory processing, trait anxiety, and parenting stress. Spontaneous neural activities in select brain regions were evaluated by whole‐brain correlation analyses based on the fractional amplitude of low‐frequency fluctuations (fALFF). We found significant positive correlations between levels of sensory processing with trait anxiety and parenting stress. Mothers having less adaptive sensory processing had significantly increased resting‐state network activities in the left lobule VI of the cerebellum. Increased fALFF values in the left lobule VI confirmed the mediation effect on the relationship between trait anxiety and sensory processing. A tendency for less adaptive sensory processing involving increased brain activity in lobule VI could be an indicator of maternal trait anxiety and the risk of parenting stress.

          Abstract

          Mothers having less adaptive sensory processing had significantly increased resting‐state network activities in the left lobule VI of the cerebellum. Increased the fractional amplitude of low‐frequency fluctuations (fALFF) values in the left lobule VI confirmed the mediation effect on the relationship between trait anxiety and sensory processing. A tendency for less adaptive sensory processing involving increased brain activity in lobule VI could be an indicator of maternal trait anxiety and the risk of parenting stress.

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          Most cited references77

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          Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion.

          Here, we demonstrate that subject motion produces substantial changes in the timecourses of resting state functional connectivity MRI (rs-fcMRI) data despite compensatory spatial registration and regression of motion estimates from the data. These changes cause systematic but spurious correlation structures throughout the brain. Specifically, many long-distance correlations are decreased by subject motion, whereas many short-distance correlations are increased. These changes in rs-fcMRI correlations do not arise from, nor are they adequately countered by, some common functional connectivity processing steps. Two indices of data quality are proposed, and a simple method to reduce motion-related effects in rs-fcMRI analyses is demonstrated that should be flexibly implementable across a variety of software platforms. We demonstrate how application of this technique impacts our own data, modifying previous conclusions about brain development. These results suggest the need for greater care in dealing with subject motion, and the need to critically revisit previous rs-fcMRI work that may not have adequately controlled for effects of transient subject movements. Copyright © 2011 Elsevier Inc. All rights reserved.
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            A fast diffeomorphic image registration algorithm.

            This paper describes DARTEL, which is an algorithm for diffeomorphic image registration. It is implemented for both 2D and 3D image registration and has been formulated to include an option for estimating inverse consistent deformations. Nonlinear registration is considered as a local optimisation problem, which is solved using a Levenberg-Marquardt strategy. The necessary matrix solutions are obtained in reasonable time using a multigrid method. A constant Eulerian velocity framework is used, which allows a rapid scaling and squaring method to be used in the computations. DARTEL has been applied to intersubject registration of 471 whole brain images, and the resulting deformations were evaluated in terms of how well they encode the shape information necessary to separate male and female subjects and to predict the ages of the subjects.
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              Saliency, switching, attention and control: a network model of insula function.

              The insula is a brain structure implicated in disparate cognitive, affective, and regulatory functions, including interoceptive awareness, emotional responses, and empathic processes. While classically considered a limbic region, recent evidence from network analysis suggests a critical role for the insula, particularly the anterior division, in high-level cognitive control and attentional processes. The crucial insight and view we present here is of the anterior insula as an integral hub in mediating dynamic interactions between other large-scale brain networks involved in externally oriented attention and internally oriented or self-related cognition. The model we present postulates that the insula is sensitive to salient events, and that its core function is to mark such events for additional processing and initiate appropriate control signals. The anterior insula and the anterior cingulate cortex form a "salience network" that functions to segregate the most relevant among internal and extrapersonal stimuli in order to guide behavior. Within the framework of our network model, the disparate functions ascribed to the insula can be conceptualized by a few basic mechanisms: (1) bottom-up detection of salient events, (2) switching between other large-scale networks to facilitate access to attention and working memory resources when a salient event is detected, (3) interaction of the anterior and posterior insula to modulate autonomic reactivity to salient stimuli, and (4) strong functional coupling with the anterior cingulate cortex that facilitates rapid access to the motor system. In this manner, with the insula as its integral hub, the salience network assists target brain regions in the generation of appropriate behavioral responses to salient stimuli. We suggest that this framework provides a parsimonious account of insula function in neurotypical adults, and may provide novel insights into the neural basis of disorders of affective and social cognition.
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                Author and article information

                Contributors
                atomoda@u-fukui.ac.jp
                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
                16 July 2021
                15 October 2021
                : 42
                : 15 ( doiID: 10.1002/hbm.v42.15 )
                : 4985-4995
                Affiliations
                [ 1 ] Research Center for Child Mental Development University of Fukui Fukui Japan
                [ 2 ] Division of Developmental Higher Brain Functions United Graduate School of Child Development, University of Fukui Fukui Japan
                [ 3 ] Japan Society for the Promotion of Science Tokyo Japan
                [ 4 ] Department of Rehabilitation, Faculty of Health Science Fukui Health Science University Fukui Japan
                [ 5 ] Japan Biomedical Imaging Research Center University of Fukui Fukui Japan
                [ 6 ] Department of Child and Adolescent Psychological Medicine University of Fukui Hospital Fukui Japan
                Author notes
                [*] [* ] Correspondence

                Akemi Tomoda, Research Center for Child Mental Development, University of Fukui, 23‐3 Matsuoka‐Shimoaizuki, Eiheiji‐cho, Fukui 910‐1193, Japan.

                Email: atomoda@ 123456u-fukui.ac.jp

                Author information
                https://orcid.org/0000-0002-7699-9485
                https://orcid.org/0000-0003-2776-5129
                https://orcid.org/0000-0003-2507-1385
                https://orcid.org/0000-0002-3720-0394
                https://orcid.org/0000-0002-6558-5017
                Article
                HBM25594
                10.1002/hbm.25594
                8449103
                34270152
                3cbcee3f-9cd6-43b7-bab7-a5e86b63c531
                © 2021 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-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 04 July 2021
                : 01 February 2021
                : 06 July 2021
                Page count
                Figures: 4, Tables: 2, Pages: 11, Words: 9839
                Funding
                Funded by: Japan Agency for Medical Research and Development (AMED) , doi 10.13039/100009619;
                Award ID: JP20gk0110052
                Funded by: Japan‐United States Brain Research Cooperation Program and Grant‐in‐Aid for Translational Research from the Life Science Innovation Center, University of Fukui to Akemi Tomoda
                Funded by: Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan
                Award ID: 19H00617
                Award ID: 17K19898
                Award ID: 15H03106
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                October 15, 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.7 mode:remove_FC converted:18.09.2021

                Neurology
                amplitude of low‐frequency fluctuations,cerebellum,less adaptive sensory processing,parenting stress,resting‐state fmri,trait anxiety

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