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      Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: mega-analytic findings from a large multi-site cohort

      research-article
      1 , 2 , 1 , 3 , 4 , 3 , 5 , 1 , 6 , 7 , 6 , 6 , 8 , 4 , 9 , 4 , 4 , 10 , 11 , 11 , 12 , 13 , 3 , 14 , 15 , 16 , 17 , 18 , 18 , 18 , 19 , 20 , 21 , 22 , 23 , 23 , 23 , 23 , 23 , 18 , 23 , 24 , 18 , 18 , 25 , 26 , 27 , 28 , 29 , 28 , 3 , 30 , 31 , 30 , 32 , 30 , 33 , 30 , 32 , 34 , 4 , 35 , 1 , 34 , 36 , 37 , 38 , 39 , 35 , 18 , 40 , 41 , 42 , 43 , 44 , 45 , 39 , 35 , 45 , 46 , 47 , 1 , 6 , 48
      Psychological medicine
      Childhood maltreatment, cortical thickness, ENIGMA, major depressive disorder

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          Abstract

          Background.

          Childhood maltreatment (CM) plays an important role in the development of major depressive disorder (MDD). The aim of this study was to examine whether CM severity and type are associated with MDD-related brain alterations, and how they interact with sex and age.

          Methods.

          Within the ENIGMA-MDD network, severity and subtypes of CM using the Childhood Trauma Questionnaire were assessed and structural magnetic resonance imaging data from patients with MDD and healthy controls were analyzed in a mega-analysis comprising a total of 3872 participants aged between 13 and 89 years. Cortical thickness and surface area were extracted at each site using FreeSurfer.

          Results.

          CM severity was associated with reduced cortical thickness in the banks of the superior temporal sulcus and supramarginal gyrus as well as with reduced surface area of the middle temporal lobe. Participants reporting both childhood neglect and abuse had a lower cortical thickness in the inferior parietal lobe, middle temporal lobe, and precuneus compared to participants not exposed to CM. In males only, regardless of diagnosis, CM severity was associated with higher cortical thickness of the rostral anterior cingulate cortex. Finally, a significant interaction between CM and age in predicting thickness was seen across several prefrontal, temporal, and temporo-parietal regions.

          Conclusions.

          Severity and type of CM may impact cortical thickness and surface area. Importantly, CM may influence age-dependent brain maturation, particularly in regions related to the default mode network, perception, and theory of mind.

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          Most cited references49

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          An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.

          In this study, we have assessed the validity and reliability of an automated labeling system that we have developed for subdividing the human cerebral cortex on magnetic resonance images into gyral based regions of interest (ROIs). Using a dataset of 40 MRI scans we manually identified 34 cortical ROIs in each of the individual hemispheres. This information was then encoded in the form of an atlas that was utilized to automatically label ROIs. To examine the validity, as well as the intra- and inter-rater reliability of the automated system, we used both intraclass correlation coefficients (ICC), and a new method known as mean distance maps, to assess the degree of mismatch between the manual and the automated sets of ROIs. When compared with the manual ROIs, the automated ROIs were highly accurate, with an average ICC of 0.835 across all of the ROIs, and a mean distance error of less than 1 mm. Intra- and inter-rater comparisons yielded little to no difference between the sets of ROIs. These findings suggest that the automated method we have developed for subdividing the human cerebral cortex into standard gyral-based neuroanatomical regions is both anatomically valid and reliable. This method may be useful for both morphometric and functional studies of the cerebral cortex as well as for clinical investigations aimed at tracking the evolution of disease-induced changes over time, including clinical trials in which MRI-based measures are used to examine response to treatment.
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            Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain.

            We present a technique for automatically assigning a neuroanatomical label to each voxel in an MRI volume based on probabilistic information automatically estimated from a manually labeled training set. In contrast to existing segmentation procedures that only label a small number of tissue classes, the current method assigns one of 37 labels to each voxel, including left and right caudate, putamen, pallidum, thalamus, lateral ventricles, hippocampus, and amygdala. The classification technique employs a registration procedure that is robust to anatomical variability, including the ventricular enlargement typically associated with neurological diseases and aging. The technique is shown to be comparable in accuracy to manual labeling, and of sufficient sensitivity to robustly detect changes in the volume of noncortical structures that presage the onset of probable Alzheimer's disease.
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              • Article: not found

              Emotional processing in anterior cingulate and medial prefrontal cortex.

              Negative emotional stimuli activate a broad network of brain regions, including the medial prefrontal (mPFC) and anterior cingulate (ACC) cortices. An early influential view dichotomized these regions into dorsal-caudal cognitive and ventral-rostral affective subdivisions. In this review, we examine a wealth of recent research on negative emotions in animals and humans, using the example of fear or anxiety, and conclude that, contrary to the traditional dichotomy, both subdivisions make key contributions to emotional processing. Specifically, dorsal-caudal regions of the ACC and mPFC are involved in appraisal and expression of negative emotion, whereas ventral-rostral portions of the ACC and mPFC have a regulatory role with respect to limbic regions involved in generating emotional responses. Moreover, this new framework is broadly consistent with emerging data on other negative and positive emotions. Published by Elsevier Ltd.
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                Author and article information

                Journal
                1254142
                6777
                Psychol Med
                Psychol Med
                Psychological medicine
                0033-2917
                1469-8978
                17 June 2022
                April 2020
                14 May 2019
                05 July 2022
                : 50
                : 6
                : 1020-1031
                Affiliations
                [1 ]Department of Psychiatry and Psychotherapy, Otto von Guericke University, Magdeburg, Germany
                [2 ]Department of Psychiatry and Behavioral Sciences, Stanford University, California, USA
                [3 ]Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany
                [4 ]SAMRC Unit on Risk & Resilience in Mental Disorders, UCT Department of Psychiatry and Mental Health, Cape Town, South Africa
                [5 ]German Center for Neurodegenerative Diseases (DZNE), Site Rostock/Greifswald, Germany
                [6 ]Brain and Mind Centre, University of Sydney, Camperdown, Australia
                [7 ]Sunshine Coast Mind and Neuroscience – Thompson Institute, Queensland, Australia
                [8 ]Trinity College Institute of Neuroscience, Trinity College Dublin, Ireland
                [9 ]School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK
                [10 ]Department of Psychiatry, University of Vermont, Burlington, VT, USA
                [11 ]Division of Mind and Brain Research, Department of Psychiatry and Psychotherapy CCM, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
                [12 ]Institute for Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Germany
                [13 ]Institute for Community Medicine, University Medicine Greifswald, and Center of Cardiovascular Research (DZHK), Germany, partner site Greifswald
                [14 ]Department of General Psychiatry, University Hospital Heidelberg, Germany
                [15 ]Department of Psychiatry and Psychotherapy, University Medical Center Göttingen, Göttingen, Germany
                [16 ]Department of Psychiatry and Psychotherapy, Asklepios Fachklinikum Göttingen, Göttingen, Germany
                [17 ]Department of Psychiatry and Psychotherapy, University of Bonn, Germany, and Department of Psychiatry and Psychotherapy, Vitos Weil-Lahn, Hesse, Germany
                [18 ]Department of Psychiatry and Psychotherapy, University of Münster, Germany
                [19 ]Institute of Clinical Radiology, University of Münster, Germany
                [20 ]Department of Psychiatry and Psychotherapy, Medical Center, University of Freiburg, Germany
                [21 ]Psychiatric University Clinic, Basel, Switzerland
                [22 ]Department of Psychiatry and Psychotherapy, Agaplesion Diakoniklinikum, Rotenburg, Germany
                [23 ]Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Germany
                [24 ]Core Facility Brain Imaging, Faculty of Medicine, Philipps-University of Marburg, Germany
                [25 ]Center for Integrative Psychiatry, University of Lübeck, Lübeck, Germany
                [26 ]School of Psychology, College of Applied Health and Communities, University of East London, London, UK
                [27 ]Centre for Affective Disorders, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK
                [28 ]Department of Psychology, School of Arts and Social Sciences, City, University of London, London, UK
                [29 ]Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK
                [30 ]Department of Psychiatry & Langley Porter Psychiatric Institute, UCSF Weill Institute for Neurosciences, University of California, San Francisco, USA
                [31 ]Department of Biomedical Sciences, Florida State University Tallahassee, FL, USA
                [32 ]Department of Psychiatry, Division of Child and Adolescent Psychiatry, University of California, San Francisco (UCSF), USA
                [33 ]Department of Psychology and Department of Psychiatry & Behavioral Sciences, Stanford University, Stanford, CA, USA
                [34 ]Leibniz Institute for Neurobiology, Magdeburg, Germany
                [35 ]Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of University of California, Marina del Rey, CA, USA
                [36 ]Department of Psychiatry and Psychotherapy, University of Tuebingen, Germany
                [37 ]VA San Diego Healthcare, San Francisco, CA, USA
                [38 ]School of Medicine, Department of Psychiatry and Human Behavior, University of California, Irvine, CA, USA
                [39 ]Clinical Translational Neuroscience Laboratory, Department of Psychiatry and Human Behavior, University of California, Irvine, CA, USA
                [40 ]Discipline of Psychiatry, School of Medicine, University of Adelaide, SA 5005 Adelaide, Australia
                [41 ]Department of Psychiatry, Melbourne Medical School, The University of Melbourne, VIC 3010 Melbourne, Australia
                [42 ]The Florey Institute of Neuroscience and Mental Health, The University of Melbourne, Melbourne, Australia
                [43 ]Department of Psychiatry, Leiden Institute for Brain and Cognition, Leiden University Medical Center, Leiden, The Netherlands
                [44 ]Department of Biomedical Sciences of Cells and Systems, Cognitive Neuroscience Center, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
                [45 ]Department of Psychiatry and Neuroscience Campus Amsterdam, VU University Medical Center, Amsterdam, The Netherlands
                [46 ]Orygen, The National Centre of Excellence in Youth Mental Health, Melbourne, Australia
                [47 ]Centre for Youth Mental Health, The University of Melbourne, Melbourne, Australia
                [48 ]German Center of Neurodegenerative Diseases (DZNE), Site Magdeburg, Germany
                Author notes
                Author for correspondence: Thomas Frodl, Thomas.Frodl@ 123456med.ovgu.de
                [*]

                Contributed equally.

                Article
                NIHMS1814604
                10.1017/S003329171900093X
                9254722
                31084657
                45fa6ee3-c142-4902-8524-9fd404f24bca

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

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                Clinical Psychology & Psychiatry
                childhood maltreatment,cortical thickness,enigma,major depressive disorder

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