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      Childhood trauma is associated with reduced frontal gray matter volume: a large transdiagnostic structural MRI study

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          Abstract

          Background

          Childhood trauma increases risk for psychopathology and cognitive impairment. Prior research mainly focused on the hippocampus and amygdala in single diagnostic categories. However, other brain regions may be impacted by trauma as well, and effects may be independent of diagnosis. This cross-sectional study investigated cortical and subcortical gray matter volume in relation to childhood trauma severity.

          Methods

          We included 554 participants: 250 bipolar-I patients, 84 schizophrenia-spectrum patients and 220 healthy individuals without a psychiatric history. Participants filled in the Childhood Trauma Questionnaire. Anatomical T1 MRI scans were acquired at 3T, regional brain morphology was assessed using Freesurfer.

          Results

          In the total sample, trauma-related gray matter reductions were found in the frontal lobe ( β = −0.049, p = 0.008; q = 0.048), this effect was driven by the right medial orbitofrontal, paracentral, superior frontal regions and the left precentral region. No trauma-related volume reductions were observed in any other (sub)cortical lobes nor the hippocampus or amygdala, trauma-by-group (i.e. both patient groups and healthy subjects) interaction effects were absent. A categorical approach confirmed a pattern of more pronounced frontal gray matter reductions in individuals reporting multiple forms of trauma and across quartiles of cumulative trauma scores. Similar dose−response patterns were revealed within the bipolar and healthy subgroups, but did not reach significance in schizophrenia-spectrum patients.

          Conclusions

          Findings show that childhood trauma is linked to frontal gray matter reductions, independent of psychiatric morbidity. Our results indicate that childhood trauma importantly contributes to the neurobiological changes commonly observed across psychiatric disorders. Frontal volume alterations may underpin affective and cognitive disturbances observed in trauma-exposed individuals.

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          Most cited references86

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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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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              Effects of stress throughout the lifespan on the brain, behaviour and cognition.

              Chronic exposure to stress hormones, whether it occurs during the prenatal period, infancy, childhood, adolescence, adulthood or aging, has an impact on brain structures involved in cognition and mental health. However, the specific effects on the brain, behaviour and cognition emerge as a function of the timing and the duration of the exposure, and some also depend on the interaction between gene effects and previous exposure to environmental adversity. Advances in animal and human studies have made it possible to synthesize these findings, and in this Review a model is developed to explain why different disorders emerge in individuals exposed to stress at different times in their lives.
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                Author and article information

                Journal
                Psychol Med
                Psychol Med
                PSM
                Psychological Medicine
                Cambridge University Press (Cambridge, UK )
                0033-2917
                1469-8978
                February 2023
                03 June 2021
                : 53
                : 3
                : 741-749
                Affiliations
                [1 ]Department of Biomedical Sciences of Cells & Systems, Section Cognitive Neurosciences, University Medical Center Groningen, University of Groningen , Groningen, the Netherlands
                [2 ]Department of Psychiatry, UMCU Brain Center, Utrecht University , Utrecht, the Netherlands
                [3 ]Department of Child and Adolescent Psychiatry/Psychology, Erasmus University Medical Center-Sophia Children's Hospital , Rotterdam, the Netherlands
                [4 ]Department of Psychiatry, Amsterdam UMC (location VUmc) , Amsterdam, the Netherlands
                [5 ]Department of Anatomy and Neurosciences, Amsterdam UMC (location VUmc) , Amsterdam, the Netherlands
                Author notes
                Author for correspondence: Marieke J. H. Begemann, E-mail: m.j.h.begemann@ 123456umcg.nl
                Author information
                https://orcid.org/0000-0001-6448-2799
                Article
                S0033291721002087
                10.1017/S0033291721002087
                9975993
                34078485
                62229257-2925-4913-9b07-f406b8be4db8
                © The Author(s) 2021

                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, provided the original article is properly cited.

                History
                : 01 December 2020
                : 27 April 2021
                : 04 May 2021
                Page count
                Figures: 3, Tables: 2, References: 78, Pages: 9
                Categories
                Original Article

                Clinical Psychology & Psychiatry
                bipolar disorder,childhood trauma,frontal lobe,gray matter volume,psychosis

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