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      Neonatal amygdala resting-state functional connectivity and socio-emotional development in very preterm children

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          Abstract

          Very preterm children are more likely to exhibit difficulties in socio-emotional processing than their term-born peers. Emerging socio-emotional problems may be partly due to alterations in limbic system development associated with infants’ early transition to extrauterine life. The amygdala is a key structure in this system and plays a critical role in various aspects of socio-emotional development, including emotion regulation. The current study tested the hypothesis that amygdala resting-state functional connectivity at term-equivalent age would be associated with socio-emotional outcomes in childhood. Participants were 129 very preterm infants (<33 weeks' gestation) who underwent resting-state functional MRI at term and received a neurodevelopmental assessment at 4–7 years (median = 4.64). Using the left and right amygdalae as seed regions, we investigated associations between whole-brain seed-based functional connectivity and three socio-emotional outcome factors which were derived using exploratory factor analysis ( Emotion Moderation, Social Function and Empathy), controlling for sex, neonatal sickness, post-menstrual age at scan and social risk. Childhood Emotion Moderation scores were significantly associated with neonatal resting-state functional connectivity of the right amygdala with right parahippocampal gyrus and right middle occipital gyrus, as well as with functional connectivity of the left amygdala with the right thalamus. No significant associations were found between amygdalar resting-state functional connectivity and either Social Function or Empathy scores. The current findings show that amygdalar functional connectivity assessed at term is associated with later socio-emotional outcomes in very preterm children.

          Abstract

          This study shows that both stronger and weaker resting-state functional connectivity between the amygdala and cortical and limbic areas in the neonatal period is associated with socio-emotional outcomes in children who were born very preterm.

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          Development and validation of brief measures of positive and negative affect: The PANAS scales.

          In recent studies of the structure of affect, positive and negative affect have consistently emerged as two dominant and relatively independent dimensions. A number of mood scales have been created to measure these factors; however, many existing measures are inadequate, showing low reliability or poor convergent or discriminant validity. To fill the need for reliable and valid Positive Affect and Negative Affect scales that are also brief and easy to administer, we developed two 10-item mood scales that comprise the Positive and Negative Affect Schedule (PANAS). The scales are shown to be highly internally consistent, largely uncorrelated, and stable at appropriate levels over a 2-month time period. Normative data and factorial and external evidence of convergent and discriminant validity for the scales are also presented.
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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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              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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                Author and article information

                Contributors
                Journal
                Brain Commun
                Brain Commun
                braincomms
                Brain Communications
                Oxford University Press
                2632-1297
                2022
                27 January 2022
                27 January 2022
                : 4
                : 1
                : fcac009
                Affiliations
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King’s College London , London, UK
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King’s College London , London, UK
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Developmental Imaging, Murdoch Children’s Research Institute , Melbourne, Australia
                Department of Paediatrics, University of Melbourne , Melbourne, Australia
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King’s College London , London, UK
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Neonatal Unit, Evelina London Children’s Hospital , London SE1 7EH, UK
                MRC Centre for Neurodevelopmental Disorders, King’s College London , UK
                Centre for the Developing Brain, School of Imaging Sciences & Biomedical Engineering & Imaging Sciences, King’s College London , London, UK
                Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King’s College London , London, UK
                Author notes
                Correspondence to: Chiara Nosarti Centre for the Developing Brain School of Bioengineering and Imaging Sciences King’s College London and Evelina Children’s Hospital London SE1 7EH, UK E-mail: chiara.nosarti@ 123456kcl.ac.uk
                [*]

                Joint senior authors.

                Author information
                https://orcid.org/0000-0002-0111-1760
                https://orcid.org/0000-0002-6486-1462
                https://orcid.org/0000-0003-3509-1435
                https://orcid.org/0000-0001-6305-9710
                Article
                fcac009
                10.1093/braincomms/fcac009
                8846580
                35178519
                0ea6caf8-fc59-43fc-8954-faa9ef444a36
                © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 August 2021
                : 04 November 2021
                : 24 January 2022
                Page count
                Pages: 14
                Funding
                Funded by: Medical Research Council, doi 10.13039/501100000265;
                Award ID: MR/K006355/1
                Award ID: MR/L011530/1
                Award ID: MR/S026460/1
                Funded by: Wellcome/EPSRC Centre for Medical Engineering;
                Award ID: 203148/Z/16/Z
                Funded by: Biotechnology and Biological Sciences Research Council, doi 10.13039/501100000268;
                Award ID: BB/J014567/1
                Funded by: Action Medical Research and Dangoor Education;
                Award ID: GN2606
                Funded by: NIHR, doi 10.13039/501100000272;
                Award ID: RP-PG-0707-10154
                Categories
                Original Article
                AcademicSubjects/MED00310
                AcademicSubjects/SCI01870

                resting-state fmri,socio-emotional outcomes,very preterm,child development

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