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The effects of callous-unemotional traits and aggression subtypes on amygdala activity in response to negative faces

Published online by Cambridge University Press:  06 July 2020

Pascal-M Aggensteiner Open the ORCID record for Pascal-M Aggensteiner [Opens in a new window] ,
Nathalie E. Holz ,
Boris W. Böttinger ,
Sarah Baumeister ,
Sarah Hohmann ,
Julia E. Werhahn ,
Jilly Naaijen ,
Shahrzad Ilbegi ,
Jeffrey C. Glennon  and
Pieter J. Hoekstra
...Show all authors
Pascal-M Aggensteiner*
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Nathalie E. Holz
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Boris W. Böttinger
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Sarah Baumeister
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Sarah Hohmann
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Julia E. Werhahn
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland Neuroscience Center Zurich, University and ETH Zurich, Zurich, Switzerland
Jilly Naaijen
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behavior, Nijmegen, The Netherlands Radboud University, Donders Institute for Brain, Cognition and Behavior, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands
Shahrzad Ilbegi
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behavior, Nijmegen, The Netherlands
Jeffrey C. Glennon
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behavior, 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
Renee Kleine Deters
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, Germany
Ulrike M. E. Schulze
Affiliation:
Department of Child and Adolescent Psychiatry/Psychotherapy, University Hospital, University of Ulm, Germany
David J. Lythgoe
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Arjun Sethi
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Michael C. Craig
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Mathilde Mastroianni
Affiliation:
Department of Child Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Ilyas Sagar-Ouriaghli
Affiliation:
Department of Child Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Paramala J. Santosh
Affiliation:
Department of Child Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Mireia Rosa
Affiliation:
Clinic Image Diagnostic Center (CDIC), Hospital Clinic of Barcelona; Magnetic Resonance Image Core Facility, 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, 2017SGR881, Institute Clinic of Neurosciences, Hospital Clinic of Barcelona, CIBERSAM, IDIBAPS, Department of Medicine, University of Barcelona, Barcelona, Spain
Celso Arango
Affiliation:
Child and Adolescent Psychiatry Department, Hospital General Universitario Gregorio Marañón School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain
Maria J. Penzol
Affiliation:
Child and Adolescent Psychiatry Department, Hospital General Universitario Gregorio Marañón School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain
Jorge Vidal
Affiliation:
Child and Adolescent Psychiatry Department, Hospital General Universitario Gregorio Marañón School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain
Barbara Franke
Affiliation:
Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behavior, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behavior, Nijmegen, The Netherlands
Marcel P. Zwiers
Affiliation:
Radboud University, Donders Institute for Brain, Cognition and Behavior, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands
Jan K. Buitelaar
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behavior, Nijmegen, The Netherlands Karakter Child and Adolescent Psychiatry University Center, Nijmegen, The Netherlands
Susanne Walitza
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland Neuroscience Center Zurich, University and ETH Zurich, Zurich, Switzerland
Tobias Banaschewski
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Daniel Brandeis
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland Neuroscience Center Zurich, University and ETH Zurich, Zurich, Switzerland
*
Author for correspondence: Pascal-M Aggensteiner, E-mail: [email protected]
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Abstract

Background

Brain imaging studies have shown altered amygdala activity during emotion processing in children and adolescents with oppositional defiant disorder (ODD) and conduct disorder (CD) compared to typically developing children and adolescents (TD). Here we aimed to assess whether aggression-related subtypes (reactive and proactive aggression) and callous-unemotional (CU) traits predicted variation in amygdala activity and skin conductance (SC) response during emotion processing.

Methods

We included 177 participants (n = 108 cases with disruptive behaviour and/or ODD/CD and n = 69 TD), aged 8–18 years, across nine sites in Europe, as part of the EU Aggressotype and MATRICS projects. All participants performed an emotional face-matching functional magnetic resonance imaging task.

Results

Differences between cases and TD in affective processing, as well as specificity of activation patterns for aggression subtypes and CU traits, were assessed. Simultaneous SC recordings were acquired in a subsample (n = 63). Cases compared to TDs showed higher amygdala activity in response to negative faces (fearful and angry) v. shapes. Subtyping cases according to aggression-related subtypes did not significantly influence on amygdala activity; while stratification based on CU traits was more sensitive and revealed decreased amygdala activity in the high CU group. SC responses were significantly lower in cases and negatively correlated with CU traits, reactive and proactive aggression.

Conclusions

Our results showed differences in amygdala activity and SC responses to emotional faces between cases with ODD/CD and TD, while CU traits moderate both central (amygdala) and peripheral (SC) responses. Our insights regarding subtypes and trait-specific aggression could be used for improved diagnostics and personalized treatment.

Keywords

Aggressionconduct disorderCU traitsneuroimagingoppositional defiant disordersubtypes
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 3 , February 2022 , pp. 476 - 484
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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