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      Longitudinal structural brain development and externalizing behavior in adolescence

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          Abstract

          Background

          Cross‐sectional studies report relations between externalizing behavior and structural abnormalities in cortical thickness of prefrontal regions and volume reductions in subcortical regions. To understand how these associations emerge and develop, longitudinal designs are pivotal.

          Method

          In the current longitudinal study, a community sample of children, adolescents and young adults ( =  271) underwent magnetic resonance imaging ( MRI) in three biennial waves (680 scans). At each wave, aspects of externalizing behavior were assessed with parent‐reported aggression and rule‐breaking scores (Child Behavior Checklist), and self‐reported aggression scores (Buss‐Perry Aggression Questionnaire). Regions of interest ( ROIs) were selected based on prior research: dorsolateral prefrontal (dl PFC), orbitofrontal ( OFC), anterior cingulate cortex ( ACC), insula, and parahippocampal cortex, as well as subcortical regions. Linear mixed models were used to assess the longitudinal relation between externalizing behavior and structural brain development. Structural covariance analyses were employed to identify whether longitudinal relations between ROIs (maturational coupling) were associated with externalizing behavior.

          Results

          Linear mixed model analyses showed a negative relation between parent‐reported aggression and right hippocampal volume. Moreover, this longitudinal relation was driven by change in hippocampal volume and not initial volume of hippocampus at time point 1. Exploratory analyses showed that stronger maturational coupling between prefrontal regions, the limbic system, and striatum was associated with both low and high externalizing behavior.

          Conclusions

          Together, these findings reinforce the hypothesis that altered structural brain development coincides with development of more externalizing behavior. These findings may guide future research on normative and deviant development of externalizing behavior.

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          Most cited references23

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          Structural brain development between childhood and adulthood: Convergence across four longitudinal samples

          Longitudinal studies including brain measures acquired through magnetic resonance imaging (MRI) have enabled population models of human brain development, crucial for our understanding of typical development as well as neurodevelopmental disorders. Brain development in the first two decades generally involves early cortical grey matter volume (CGMV) increases followed by decreases, and monotonic increases in cerebral white matter volume (CWMV). However, inconsistencies regarding the precise developmental trajectories call into question the comparability of samples. This issue can be addressed by conducting a comprehensive study across multiple datasets from diverse populations. Here, we present replicable models for gross structural brain development between childhood and adulthood (ages 8–30 years) by repeating analyses in four separate longitudinal samples (391 participants; 852 scans). In addition, we address how accounting for global measures of cranial/brain size affect these developmental trajectories. First, we found evidence for continued development of both intracranial volume (ICV) and whole brain volume (WBV) through adolescence, albeit following distinct trajectories. Second, our results indicate that CGMV is at its highest in childhood, decreasing steadily through the second decade with deceleration in the third decade, while CWMV increases until mid-to-late adolescence before decelerating. Importantly, we show that accounting for cranial/brain size affects models of regional brain development, particularly with respect to sex differences. Our results increase confidence in our knowledge of the pattern of brain changes during adolescence, reduce concerns about discrepancies across samples, and suggest some best practices for statistical control of cranial volume and brain size in future studies.
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            Male antisocial behaviour in adolescence and beyond

            Male antisocial behavior is concentrated in the adolescent period of the life course, as documented by the curve of crime over age. This article reviews recent evidence regarding the hypothesis that the age-crime curve conceals two groups with different causes. Life-course persistent males show extreme, pervasive, persistent antisocial behavior from early childhood to adulthood. They are hypothesized to be rare, with pathological risk factors and poor life outcomes. In contrast, adolescence-limited males show similar levels of antisocial behavior but primarily during the adolescent stage of development. They are hypothesized to be common and normative, whereas abstainers from offending are rare. This article recaps the taxonomy’s 25-year history, concluding that it is standing the test of time in research, and making an impact on policy in early-years prevention and juvenile justice. Research is needed into how the taxonomy relates to neuroscience, health, genetics, and changes in modern crime, including digital crime.
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              Brain development during adolescence: A mixed-longitudinal investigation of cortical thickness, surface area, and volume.

              What we know about cortical development during adolescence largely stems from analyses of cross-sectional or cohort-sequential samples, with few studies investigating brain development using a longitudinal design. Further, cortical volume is a product of two evolutionarily and genetically distinct features of the cortex - thickness and surface area, and few studies have investigated development of these three characteristics within the same sample. The current study examined maturation of cortical thickness, surface area and volume during adolescence, as well as sex differences in development, using a mixed longitudinal design. 192 MRI scans were obtained from 90 healthy (i.e., free from lifetime psychopathology) adolescents (11-20 years) at three time points (with different MRI scanners used at time 1 compared to 2 and 3). Developmental trajectories were estimated using linear mixed models. Non-linear increases were present across most of the cortex for surface area. In comparison, thickness and volume were both characterised by a combination of non-linear decreasing and increasing trajectories. While sex differences in volume and surface area were observed across time, no differences in thickness were identified. Furthermore, few regions exhibited sex differences in the cortical development. Our findings clearly illustrate that volume is a product of surface area and thickness, with each exhibiting differential patterns of development during adolescence, particularly in regions known to contribute to the development of social-cognition and behavioral regulation. These findings suggest that thickness and surface area may be driven by different underlying mechanisms, with each measure potentially providing independent information about brain development. Hum Brain Mapp 37:2027-2038, 2016. © 2016 Wiley Periodicals, Inc.
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                Author and article information

                Contributors
                m.g.n.bos@fsw.leidenuniv.nl
                Journal
                J Child Psychol Psychiatry
                J Child Psychol Psychiatry
                10.1111/(ISSN)1469-7610
                JCPP
                Journal of Child Psychology and Psychiatry, and Allied Disciplines
                John Wiley and Sons Inc. (Hoboken )
                0021-9630
                1469-7610
                25 September 2018
                October 2018
                : 59
                : 10 , Risk pathways and developmental phenotypes of ADHD and externalizing problems ( doiID: 10.1111/jcpp.2018.59.issue-10 )
                : 1061-1072
                Affiliations
                [ 1 ] Institute of Psychology Leiden University Leiden The Netherlands
                [ 2 ] Leiden Institute for Brain and Cognition Leiden The Netherlands
                [ 3 ] Institute of Education and Child Studies Leiden University Leiden The Netherlands
                [ 4 ] Department of Child and Adolescent Psychiatry VU University Medical Center Amsterdam The Netherlands
                [ 5 ] Department of Developmental Psychology Tilburg University Tilburg The Netherlands
                [ 6 ] Department of Psychology University of Oslo Oslo Norway
                [ 7 ] Department of Psychiatry Diakonhjemmet Hospital Oslo Norway
                Author notes
                [*] [* ] Correspondence

                Marieke Bos, Faculty of Social Sciences, Leiden University; Leiden University; Wassenaarseweg 52, 2333 AK Leiden, The Netherlands; Email: m.g.n.bos@ 123456fsw.leidenuniv.nl

                Article
                JCPP12972
                10.1111/jcpp.12972
                6175471
                30255501
                4fb51379-c0f2-489e-83f4-bfbf479baad8
                © 2018 The Authors. Journal of Child Psychology and Psychiatry published by John Wiley & Sons Ltd on behalf of Association for Child and Adolescent Mental Health.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 31 July 2018
                Page count
                Figures: 5, Tables: 1, Pages: 12, Words: 7058
                Funding
                Funded by: European Research Council (ERC)
                Award ID: ERC‐2010‐StG‐263234
                Funded by: Research Council of Norway
                Award ID: FRIMEDBIO 230345
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                jcpp12972
                October 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.0 mode:remove_FC converted:08.10.2018

                Clinical Psychology & Psychiatry
                externalizing behavior,aggression,adolescence,structural mri,longitudinal design

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