Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior

Julia E. Werhahn; Susanna Mohl; David Willinger; Lukasz Smigielski; Alexander Roth; Christoph Hofstetter; Philipp Stämpfli; Jilly Naaijen; Leandra M. Mulder; Jeffrey C. Glennon; Pieter J. Hoekstra; Andrea Dietrich; Renee Kleine Deters; Pascal M. Aggensteiner; Nathalie E. Holz; Sarah Baumeister; Tobias Banaschewski; Melanie C. Saam; Ulrike M.E. Schulze; David J. Lythgoe; Arjun Sethi; Michael C. Craig; Mathilde Mastroianni; Ilyas Sagar-Ouriaghli; Paramala J. Santosh; Mireia Rosa; Nuria Bargallo; Josefina Castro-Fornieles; Celso Arango; Maria J. Penzol; Marcel P. Zwiers; Barbara Franke; Jan K. Buitelaar; Susanne Walitza; Daniel Brandeis

doi:10.1007/s00787-020-01601-9

Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior

Julia E. Werhahn^*, Susanna Mohl, David Willinger, Lukasz Smigielski, Alexander Roth, Christoph Hofstetter, Philipp Stämpfli, Jilly Naaijen, Leandra M. Mulder, Jeffrey C. Glennon, Pieter J. Hoekstra, Andrea Dietrich, Renee Kleine Deters, Pascal M. Aggensteiner, Nathalie E. Holz, Sarah Baumeister, Tobias Banaschewski, Melanie C. Saam, Ulrike M.E. Schulze, David J. LythgoeArjun Sethi, Michael C. Craig, Mathilde Mastroianni, Ilyas Sagar-Ouriaghli, Paramala J. Santosh, Mireia Rosa, Nuria Bargallo, Josefina Castro-Fornieles, Celso Arango, Maria J. Penzol, Marcel P. Zwiers, Barbara Franke, Jan K. Buitelaar, Susanne Walitza, Daniel Brandeis

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

22 Citations (Scopus)

Abstract

There is increasing evidence for altered brain resting state functional connectivity in adolescents with disruptive behavior. While a considerable body of behavioral research points to differences between reactive and proactive aggression, it remains unknown whether these two subtypes have dissociable effects on connectivity. Additionally, callous-unemotional traits are important specifiers in subtyping aggressive behavior along the affective dimension. Accordingly, we examined associations between two aggression subtypes along with callous-unemotional traits using a seed-to-voxel approach. Six functionally relevant seeds were selected to probe the salience and the default mode network, based on their presumed role in aggression. The resting state sequence was acquired from 207 children and adolescents of both sexes [mean age (standard deviation) = 13.30 (2.60); range = 8.02–18.35] as part of a Europe-based multi-center study. One hundred eighteen individuals exhibiting disruptive behavior (conduct disorder/oppositional defiant disorder) with varying comorbid attention-deficit/hyperactivity disorder (ADHD) symptoms were studied, together with 89 healthy controls. Proactive aggression was associated with increased left amygdala–precuneus coupling, while reactive aggression related to hyper-connectivities of the posterior cingulate cortex (PCC) to the parahippocampus, the left amygdala to the precuneus and to hypo-connectivity between the right anterior insula and the nucleus caudate. Callous-unemotional traits were linked to distinct hyper-connectivities to frontal, parietal, and cingulate areas. Additionally, compared to controls, cases demonstrated reduced connectivity of the PCC and left anterior insula to left frontal areas, the latter only when controlling for ADHD scores. Taken together, this study revealed aggression-subtype-specific patterns involving areas associated with emotion, empathy, morality, and cognitive control.

Original language	English
Journal	European Child and Adolescent Psychiatry
DOIs	https://doi.org/10.1007/s00787-020-01601-9
Publication status	Accepted/In press - 1 Jan 2020

Keywords

Amygdala
Callous-unemotional traits
Default mode network
Functional connectivity
Proactive aggression
Reactive aggression

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1007/s00787-020-01601-9

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Werhahn, J. E., Mohl, S., Willinger, D., Smigielski, L., Roth, A., Hofstetter, C., Stämpfli, P., Naaijen, J., Mulder, L. M., Glennon, J. C., Hoekstra, P. J., Dietrich, A., Kleine Deters, R., Aggensteiner, P. M., Holz, N. E., Baumeister, S., Banaschewski, T., Saam, M. C., Schulze, U. M. E., ... Brandeis, D. (Accepted/In press). Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior. European Child and Adolescent Psychiatry. https://doi.org/10.1007/s00787-020-01601-9

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title = "Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior",

abstract = "There is increasing evidence for altered brain resting state functional connectivity in adolescents with disruptive behavior. While a considerable body of behavioral research points to differences between reactive and proactive aggression, it remains unknown whether these two subtypes have dissociable effects on connectivity. Additionally, callous-unemotional traits are important specifiers in subtyping aggressive behavior along the affective dimension. Accordingly, we examined associations between two aggression subtypes along with callous-unemotional traits using a seed-to-voxel approach. Six functionally relevant seeds were selected to probe the salience and the default mode network, based on their presumed role in aggression. The resting state sequence was acquired from 207 children and adolescents of both sexes [mean age (standard deviation) = 13.30 (2.60); range = 8.02–18.35] as part of a Europe-based multi-center study. One hundred eighteen individuals exhibiting disruptive behavior (conduct disorder/oppositional defiant disorder) with varying comorbid attention-deficit/hyperactivity disorder (ADHD) symptoms were studied, together with 89 healthy controls. Proactive aggression was associated with increased left amygdala–precuneus coupling, while reactive aggression related to hyper-connectivities of the posterior cingulate cortex (PCC) to the parahippocampus, the left amygdala to the precuneus and to hypo-connectivity between the right anterior insula and the nucleus caudate. Callous-unemotional traits were linked to distinct hyper-connectivities to frontal, parietal, and cingulate areas. Additionally, compared to controls, cases demonstrated reduced connectivity of the PCC and left anterior insula to left frontal areas, the latter only when controlling for ADHD scores. Taken together, this study revealed aggression-subtype-specific patterns involving areas associated with emotion, empathy, morality, and cognitive control.",

keywords = "Amygdala, Callous-unemotional traits, Default mode network, Functional connectivity, Proactive aggression, Reactive aggression",

author = "Werhahn, {Julia E.} and Susanna Mohl and David Willinger and Lukasz Smigielski and Alexander Roth and Christoph Hofstetter and Philipp St{\"a}mpfli and Jilly Naaijen and Mulder, {Leandra M.} and Glennon, {Jeffrey C.} and Hoekstra, {Pieter J.} and Andrea Dietrich and {Kleine Deters}, Renee and Aggensteiner, {Pascal M.} and Holz, {Nathalie E.} and Sarah Baumeister and Tobias Banaschewski and Saam, {Melanie C.} and Schulze, {Ulrike M.E.} and Lythgoe, {David J.} and Arjun Sethi and Craig, {Michael C.} and Mathilde Mastroianni and Ilyas Sagar-Ouriaghli and Santosh, {Paramala J.} and Mireia Rosa and Nuria Bargallo and Josefina Castro-Fornieles and Celso Arango and Penzol, {Maria J.} and Zwiers, {Marcel P.} and Barbara Franke and Buitelaar, {Jan K.} and Susanne Walitza and Daniel Brandeis",

year = "2020",

month = jan,

day = "1",

doi = "10.1007/s00787-020-01601-9",

language = "English",

journal = "European Child and Adolescent Psychiatry",

issn = "1018-8827",

publisher = "Dr. Dietrich Steinkopff Verlag GmbH and Co. KG",

}

Werhahn, JE, Mohl, S, Willinger, D, Smigielski, L, Roth, A, Hofstetter, C, Stämpfli, P, Naaijen, J, Mulder, LM, Glennon, JC, Hoekstra, PJ, Dietrich, A, Kleine Deters, R, Aggensteiner, PM, Holz, NE, Baumeister, S, Banaschewski, T, Saam, MC, Schulze, UME, Lythgoe, DJ , Sethi, A, Craig, MC, Mastroianni, M, Sagar-Ouriaghli, I, Santosh, PJ, Rosa, M, Bargallo, N, Castro-Fornieles, J, Arango, C, Penzol, MJ, Zwiers, MP, Franke, B, Buitelaar, JK, Walitza, S & Brandeis, D 2020, 'Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior', European Child and Adolescent Psychiatry. https://doi.org/10.1007/s00787-020-01601-9

TY - JOUR

T1 - Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior

AU - Werhahn, Julia E.

AU - Mohl, Susanna

AU - Willinger, David

AU - Smigielski, Lukasz

AU - Roth, Alexander

AU - Hofstetter, Christoph

AU - Stämpfli, Philipp

AU - Naaijen, Jilly

AU - Mulder, Leandra M.

AU - Glennon, Jeffrey C.

AU - Hoekstra, Pieter J.

AU - Dietrich, Andrea

AU - Kleine Deters, Renee

AU - Aggensteiner, Pascal M.

AU - Holz, Nathalie E.

AU - Baumeister, Sarah

AU - Banaschewski, Tobias

AU - Saam, Melanie C.

AU - Schulze, Ulrike M.E.

AU - Lythgoe, David J.

AU - Sethi, Arjun

AU - Craig, Michael C.

AU - Mastroianni, Mathilde

AU - Sagar-Ouriaghli, Ilyas

AU - Santosh, Paramala J.

AU - Rosa, Mireia

AU - Bargallo, Nuria

AU - Castro-Fornieles, Josefina

AU - Arango, Celso

AU - Penzol, Maria J.

AU - Zwiers, Marcel P.

AU - Franke, Barbara

AU - Buitelaar, Jan K.

AU - Walitza, Susanne

AU - Brandeis, Daniel

PY - 2020/1/1

Y1 - 2020/1/1

N2 - There is increasing evidence for altered brain resting state functional connectivity in adolescents with disruptive behavior. While a considerable body of behavioral research points to differences between reactive and proactive aggression, it remains unknown whether these two subtypes have dissociable effects on connectivity. Additionally, callous-unemotional traits are important specifiers in subtyping aggressive behavior along the affective dimension. Accordingly, we examined associations between two aggression subtypes along with callous-unemotional traits using a seed-to-voxel approach. Six functionally relevant seeds were selected to probe the salience and the default mode network, based on their presumed role in aggression. The resting state sequence was acquired from 207 children and adolescents of both sexes [mean age (standard deviation) = 13.30 (2.60); range = 8.02–18.35] as part of a Europe-based multi-center study. One hundred eighteen individuals exhibiting disruptive behavior (conduct disorder/oppositional defiant disorder) with varying comorbid attention-deficit/hyperactivity disorder (ADHD) symptoms were studied, together with 89 healthy controls. Proactive aggression was associated with increased left amygdala–precuneus coupling, while reactive aggression related to hyper-connectivities of the posterior cingulate cortex (PCC) to the parahippocampus, the left amygdala to the precuneus and to hypo-connectivity between the right anterior insula and the nucleus caudate. Callous-unemotional traits were linked to distinct hyper-connectivities to frontal, parietal, and cingulate areas. Additionally, compared to controls, cases demonstrated reduced connectivity of the PCC and left anterior insula to left frontal areas, the latter only when controlling for ADHD scores. Taken together, this study revealed aggression-subtype-specific patterns involving areas associated with emotion, empathy, morality, and cognitive control.

AB - There is increasing evidence for altered brain resting state functional connectivity in adolescents with disruptive behavior. While a considerable body of behavioral research points to differences between reactive and proactive aggression, it remains unknown whether these two subtypes have dissociable effects on connectivity. Additionally, callous-unemotional traits are important specifiers in subtyping aggressive behavior along the affective dimension. Accordingly, we examined associations between two aggression subtypes along with callous-unemotional traits using a seed-to-voxel approach. Six functionally relevant seeds were selected to probe the salience and the default mode network, based on their presumed role in aggression. The resting state sequence was acquired from 207 children and adolescents of both sexes [mean age (standard deviation) = 13.30 (2.60); range = 8.02–18.35] as part of a Europe-based multi-center study. One hundred eighteen individuals exhibiting disruptive behavior (conduct disorder/oppositional defiant disorder) with varying comorbid attention-deficit/hyperactivity disorder (ADHD) symptoms were studied, together with 89 healthy controls. Proactive aggression was associated with increased left amygdala–precuneus coupling, while reactive aggression related to hyper-connectivities of the posterior cingulate cortex (PCC) to the parahippocampus, the left amygdala to the precuneus and to hypo-connectivity between the right anterior insula and the nucleus caudate. Callous-unemotional traits were linked to distinct hyper-connectivities to frontal, parietal, and cingulate areas. Additionally, compared to controls, cases demonstrated reduced connectivity of the PCC and left anterior insula to left frontal areas, the latter only when controlling for ADHD scores. Taken together, this study revealed aggression-subtype-specific patterns involving areas associated with emotion, empathy, morality, and cognitive control.

KW - Amygdala

KW - Callous-unemotional traits

KW - Default mode network

KW - Functional connectivity

KW - Proactive aggression

KW - Reactive aggression

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U2 - 10.1007/s00787-020-01601-9

DO - 10.1007/s00787-020-01601-9

M3 - Article

AN - SCOPUS:85089363019

SN - 1018-8827

JO - European Child and Adolescent Psychiatry

JF - European Child and Adolescent Psychiatry

ER -

Aggression subtypes relate to distinct resting state functional connectivity in children and adolescents with disruptive behavior

Abstract

Keywords

UN SDGs

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