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Age-related brain deviations and aggression

Published online by Cambridge University Press:  22 April 2022

Nathalie E. Holz*
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands
Dorothea L. Floris
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands Methods of Plasticity Research, Department of Psychology, University of Zurich, Zurich, Switzerland
Alberto Llera
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands
Pascal M. Aggensteiner
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Seyed Mostafa Kia
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands
Thomas Wolfers
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
Sarah Baumeister
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Boris Böttinger
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Jeffrey C. Glennon
Affiliation:
Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands
Pieter J. Hoekstra
Affiliation:
Department of Child and Adolescent Psychiatry, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands
Andrea Dietrich
Affiliation:
Department of Child and Adolescent Psychiatry, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands
Melanie C. Saam
Affiliation:
Department of Child and Adolescent Psychiatry/Psychotherapy, University Hospital, University of Ulm, Ulm, Germany
Ulrike M. E. Schulze
Affiliation:
Department of Child and Adolescent Psychiatry/Psychotherapy, University Hospital, University of Ulm, Ulm, Germany
David J. Lythgoe
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Steve C. R. Williams
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Paramala Santosh
Affiliation:
Department of Child Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK Centre for Interventional Paediatric Psychopharmacology and Rare Diseases (CIPPRD), South London and Maudsley NHS Trust, London, UK
Mireia Rosa-Justicia
Affiliation:
Clinic Image Diagnostic Center (CDIC), Hospital Clinic of Barcelona; Magnetic Resonance Image Core Facility, IDIBAPS, Barcelona, Spain Child and Adolescent Psychiatry and Psychology Department, Institute Clinic of Neurosciences, Hospital Clinic of Barcelona, IDIBAPS, Barcelona, Spain
Nuria Bargallo
Affiliation:
Clinic Image Diagnostic Center (CDIC), Hospital Clinic of Barcelona; Magnetic Resonance Image Core Facility, IDIBAPS, Barcelona, Spain
Josefina Castro-Fornieles
Affiliation:
Child and Adolescent Psychiatry and Psychology Department, Department of Medicine, 2017SGR881, Institute Clinic of Neurosciences, Hospital Clinic of Barcelona, CIBERSAM, IDIBAPS, University of Barcelona, Barcelona, Spain
Celso Arango
Affiliation:
Child and Adolescent Psychiatry Department, Institute of Psychiatry and Mental health, Hospital General Universitario Gregorio Marañón School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain
Maria J. Penzol
Affiliation:
Child and Adolescent Psychiatry Department, Institute of Psychiatry and Mental health, Hospital General Universitario Gregorio Marañón School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain
Susanne Walitza
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland
Andreas Meyer-Lindenberg
Affiliation:
Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Marcel Zwiers
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands
Barbara Franke
Affiliation:
Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Medical Center, Nijmegen, The Netherlands
Jan Buitelaar
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands Karakter Child and Adolescent Psychiatry University Center, Nijmegen, The Netherlands
Jilly Naaijen
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands
Daniel Brandeis
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany Child and Adolescent Psychiatry and Psychology Department, Institute Clinic of Neurosciences, Hospital Clinic of Barcelona, IDIBAPS, Barcelona, Spain Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland Neuroscience Center Zurich, University of Zurich and ETH Zurich, Zurich, Switzerland
Christian Beckmann
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands Centre for Functional MRI of the Brain, University of Oxford, Oxford, UK
Tobias Banaschewski
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Andre F. Marquand*
Affiliation:
Donders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, The Netherlands Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
*
Authors for correspondence: Nathalie E. Holz, E-mail: nathalie.holz@zi-mannheim.de; Andre F. Marquand, E-mail: a.marquand@donders.ru.nl
Authors for correspondence: Nathalie E. Holz, E-mail: nathalie.holz@zi-mannheim.de; Andre F. Marquand, E-mail: a.marquand@donders.ru.nl

Abstract

Background

Disruptive behavior disorders (DBD) are heterogeneous at the clinical and the biological level. Therefore, the aims were to dissect the heterogeneous neurodevelopmental deviations of the affective brain circuitry and provide an integration of these differences across modalities.

Methods

We combined two novel approaches. First, normative modeling to map deviations from the typical age-related pattern at the level of the individual of (i) activity during emotion matching and (ii) of anatomical images derived from DBD cases (n = 77) and controls (n = 52) aged 8–18 years from the EU-funded Aggressotype and MATRICS consortia. Second, linked independent component analysis to integrate subject-specific deviations from both modalities.

Results

While cases exhibited on average a higher activity than would be expected for their age during face processing in regions such as the amygdala when compared to controls these positive deviations were widespread at the individual level. A multimodal integration of all functional and anatomical deviations explained 23% of the variance in the clinical DBD phenotype. Most notably, the top marker, encompassing the default mode network (DMN) and subcortical regions such as the amygdala and the striatum, was related to aggression across the whole sample.

Conclusions

Overall increased age-related deviations in the amygdala in DBD suggest a maturational delay, which has to be further validated in future studies. Further, the integration of individual deviation patterns from multiple imaging modalities allowed to dissect some of the heterogeneity of DBD and identified the DMN, the striatum and the amygdala as neural signatures that were associated with aggression.

Type
Original Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

Shared first authorship.

Shared last authorship.

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