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

Pascal-M Aggensteiner; Nathalie E Holz; Boris W Böttinger; Sarah Baumeister; Sarah Hohmann; Julia E Werhahn; Jilly Naaijen; Shahrzad Ilbegi; Jeffrey C Glennon; Pieter J Hoekstra; Andrea Dietrich; Renee Kleine Deters; 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; Jorge Vidal; Barbara Franke; Marcel P Zwiers; Jan K Buitelaar; Susanne Walitza; Tobias Banaschewski; Daniel Brandeis

doi:10.1017/S0033291720002111

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

Pascal-M Aggensteiner, Nathalie E Holz, Boris W Böttinger, Sarah Baumeister, Sarah Hohmann, Julia E Werhahn, Jilly Naaijen, Shahrzad Ilbegi, Jeffrey C Glennon, Pieter J Hoekstra, Andrea Dietrich, Renee Kleine Deters, Melanie C Saam, Ulrike M E Schulze, David J Lythgoe, Arjun Sethi, Michael C Craig, Mathilde Mastroianni, Ilyas Sagar-Ouriaghli, Paramala J SantoshMireia Rosa, Nuria Bargallo, Josefina Castro-Fornieles, Celso Arango, Maria J Penzol, Jorge Vidal, Barbara Franke, Marcel P Zwiers, Jan K Buitelaar, Susanne Walitza, Tobias Banaschewski, Daniel Brandeis

School of Psychology

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

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.

Original language	English
Pages (from-to)	1-9
Number of pages	9
Journal	Psychological Medicine
Early online date	6 Jul 2020
DOIs	https://doi.org/10.1017/S0033291720002111
Publication status	E-pub ahead of print - 6 Jul 2020

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10.1017/S0033291720002111

Cite this

Aggensteiner, P.-M., Holz, N. E., Böttinger, B. W., Baumeister, S., Hohmann, S., Werhahn, J. E., Naaijen, J., Ilbegi, S., Glennon, J. C., Hoekstra, P. J., Dietrich, A., Deters, R. K., Saam, M. C., Schulze, U. M. E., Lythgoe, D. J., Sethi, A., Craig, M. C., Mastroianni, M., Sagar-Ouriaghli, I., ... Brandeis, D. (2020). The effects of callous-unemotional traits and aggression subtypes on amygdala activity in response to negative faces. Psychological Medicine, 1-9. Advance online publication. https://doi.org/10.1017/S0033291720002111

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

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.",

author = "Pascal-M Aggensteiner and Holz, {Nathalie E} and B{\"o}ttinger, {Boris W} and Sarah Baumeister and Sarah Hohmann and Werhahn, {Julia E} and Jilly Naaijen and Shahrzad Ilbegi and Glennon, {Jeffrey C} and Hoekstra, {Pieter J} and Andrea Dietrich and Deters, {Renee Kleine} 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 Jorge Vidal and Barbara Franke and Zwiers, {Marcel P} and Buitelaar, {Jan K} and Susanne Walitza and Tobias Banaschewski and Daniel Brandeis",

year = "2020",

month = jul,

day = "6",

doi = "10.1017/S0033291720002111",

language = "English",

pages = "1--9",

journal = "Psychological Medicine",

issn = "0033-2917",

publisher = "Cambridge University Press",

}

Aggensteiner, P-M, Holz, NE, Böttinger, BW, Baumeister, S, Hohmann, S, Werhahn, JE, Naaijen, J, Ilbegi, S, Glennon, JC, Hoekstra, PJ, Dietrich, A, Deters, RK, 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, Vidal, J, Franke, B, Zwiers, MP, Buitelaar, JK, Walitza, S, Banaschewski, T & Brandeis, D 2020, 'The effects of callous-unemotional traits and aggression subtypes on amygdala activity in response to negative faces', Psychological Medicine, pp. 1-9. https://doi.org/10.1017/S0033291720002111

TY - JOUR

T1 - The effects of callous-unemotional traits and aggression subtypes on amygdala activity in response to negative faces

AU - Aggensteiner, Pascal-M

AU - Holz, Nathalie E

AU - Böttinger, Boris W

AU - Baumeister, Sarah

AU - Hohmann, Sarah

AU - Werhahn, Julia E

AU - Naaijen, Jilly

AU - Ilbegi, Shahrzad

AU - Glennon, Jeffrey C

AU - Hoekstra, Pieter J

AU - Dietrich, Andrea

AU - Deters, Renee Kleine

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 - Vidal, Jorge

AU - Franke, Barbara

AU - Zwiers, Marcel P

AU - Buitelaar, Jan K

AU - Walitza, Susanne

AU - Banaschewski, Tobias

AU - Brandeis, Daniel

PY - 2020/7/6

Y1 - 2020/7/6

N2 - 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.

AB - 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.

U2 - 10.1017/S0033291720002111

DO - 10.1017/S0033291720002111

M3 - Article

C2 - 32624021

SN - 0033-2917

SP - 1

EP - 9

JO - Psychological Medicine

JF - Psychological Medicine

ER -