Sex differences in neural correlates of common psychopathological symptoms in early adolescence

Francesca Biondo; Charlotte Nymberg Thunell; Bing Xu; Congying Chu; Tianye Jia; Alex Ing; Erin Burke Quinlan; Nicole Tay; Tobias Banaschewski; Arun L.W. Bokde; Christian Büchel; Sylvane Desrivières; Herta Flor; Vincent Frouin; Hugh Garavan; Penny Gowland; Andreas Heinz; Bernd Ittermann; Jean Luc Martinot; Hervé Lemaitre; Frauke Nees; Dimitri Papadopoulos Orfanos; Luise Poustka; Sabina Millenet; Juliane H. Fröhner; Michael N. Smolka; Henrik Walter; Robert Whelan; Edward D. Barker; Gunter Schumann

doi:10.1017/S0033291720005140

Sex differences in neural correlates of common psychopathological symptoms in early adolescence

Francesca Biondo^*, Charlotte Nymberg Thunell, Bing Xu, Congying Chu, Tianye Jia, Alex Ing, Erin Burke Quinlan, Nicole Tay, Tobias Banaschewski, Arun L.W. Bokde, Christian Büchel, Sylvane Desrivières, Herta Flor, Vincent Frouin, Hugh Garavan, Penny Gowland, Andreas Heinz, Bernd Ittermann, Jean Luc Martinot, Hervé LemaitreFrauke Nees, Dimitri Papadopoulos Orfanos, Luise Poustka, Sabina Millenet, Juliane H. Fröhner, Michael N. Smolka, Henrik Walter, Robert Whelan, Edward D. Barker, Gunter Schumann

^*Corresponding author for this work

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

3 Citations (Scopus)

Abstract

Background Sex-related differences in psychopathology are known phenomena, with externalizing and internalizing symptoms typically more common in boys and girls, respectively. However, the neural correlates of these sex-by-psychopathology interactions are underinvestigated, particularly in adolescence. Methods Participants were 14 years of age and part of the IMAGEN study, a large (N = 1526) community-based sample. To test for sex-by-psychopathology interactions in structural grey matter volume (GMV), we used whole-brain, voxel-wise neuroimaging analyses based on robust non-parametric methods. Psychopathological symptom data were derived from the Strengths and Difficulties Questionnaire (SDQ). Results We found a sex-by-hyperactivity/inattention interaction in four brain clusters: right temporoparietal-opercular region (p < 0.01, Cohen's d = -0.24), bilateral anterior and mid-cingulum (p < 0.05, Cohen's d = -0.18), right cerebellum and fusiform (p < 0.05, Cohen's d = -0.20) and left frontal superior and middle gyri (p < 0.05, Cohen's d = -0.26). Higher symptoms of hyperactivity/inattention were associated with lower GMV in all four brain clusters in boys, and with higher GMV in the temporoparietal-opercular and cerebellar-fusiform clusters in girls. Conclusions Using a large, sex-balanced and community-based sample, our study lends support to the idea that externalizing symptoms of hyperactivity/inattention may be associated with different neural structures in male and female adolescents. The brain regions we report have been associated with a myriad of important cognitive functions, in particular, attention, cognitive and motor control, and timing, that are potentially relevant to understand the behavioural manifestations of hyperactive and inattentive symptoms. This study highlights the importance of considering sex in our efforts to uncover mechanisms underlying psychopathology during adolescence.

Original language	English
Pages (from-to)	1-11
Number of pages	11
Journal	Psychological Medicine
DOIs	https://doi.org/10.1017/S0033291720005140
Publication status	Accepted/In press - 2021

Keywords

Adolescence
attention-deficit hyperactivity disorder
externalizing symptoms
grey matter
IMAGEN
internalizing symptoms
psychopathology
sex differences
voxel-wise morphometry

UN SDGs

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

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10.1017/S0033291720005140

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Biondo, F., Thunell, C. N., Xu, B., Chu, C., Jia, T., Ing, A., Quinlan, E. B., Tay, N., Banaschewski, T., Bokde, A. L. W., Büchel, C., Desrivières, S., Flor, H., Frouin, V., Garavan, H., Gowland, P., Heinz, A., Ittermann, B., Martinot, J. L., ... Schumann, G. (Accepted/In press). Sex differences in neural correlates of common psychopathological symptoms in early adolescence. Psychological Medicine, 1-11. https://doi.org/10.1017/S0033291720005140

@article{e91b502c520b43cca4bbf2949a7c9ecd,

title = "Sex differences in neural correlates of common psychopathological symptoms in early adolescence",

abstract = "Background Sex-related differences in psychopathology are known phenomena, with externalizing and internalizing symptoms typically more common in boys and girls, respectively. However, the neural correlates of these sex-by-psychopathology interactions are underinvestigated, particularly in adolescence. Methods Participants were 14 years of age and part of the IMAGEN study, a large (N = 1526) community-based sample. To test for sex-by-psychopathology interactions in structural grey matter volume (GMV), we used whole-brain, voxel-wise neuroimaging analyses based on robust non-parametric methods. Psychopathological symptom data were derived from the Strengths and Difficulties Questionnaire (SDQ). Results We found a sex-by-hyperactivity/inattention interaction in four brain clusters: right temporoparietal-opercular region (p < 0.01, Cohen's d = -0.24), bilateral anterior and mid-cingulum (p < 0.05, Cohen's d = -0.18), right cerebellum and fusiform (p < 0.05, Cohen's d = -0.20) and left frontal superior and middle gyri (p < 0.05, Cohen's d = -0.26). Higher symptoms of hyperactivity/inattention were associated with lower GMV in all four brain clusters in boys, and with higher GMV in the temporoparietal-opercular and cerebellar-fusiform clusters in girls. Conclusions Using a large, sex-balanced and community-based sample, our study lends support to the idea that externalizing symptoms of hyperactivity/inattention may be associated with different neural structures in male and female adolescents. The brain regions we report have been associated with a myriad of important cognitive functions, in particular, attention, cognitive and motor control, and timing, that are potentially relevant to understand the behavioural manifestations of hyperactive and inattentive symptoms. This study highlights the importance of considering sex in our efforts to uncover mechanisms underlying psychopathology during adolescence.",

keywords = "Adolescence, attention-deficit hyperactivity disorder, externalizing symptoms, grey matter, IMAGEN, internalizing symptoms, psychopathology, sex differences, voxel-wise morphometry",

author = "Francesca Biondo and Thunell, {Charlotte Nymberg} and Bing Xu and Congying Chu and Tianye Jia and Alex Ing and Quinlan, {Erin Burke} and Nicole Tay and Tobias Banaschewski and Bokde, {Arun L.W.} and Christian B{\"u}chel and Sylvane Desrivi{\`e}res and Herta Flor and Vincent Frouin and Hugh Garavan and Penny Gowland and Andreas Heinz and Bernd Ittermann and Martinot, {Jean Luc} and Herv{\'e} Lemaitre and Frauke Nees and Orfanos, {Dimitri Papadopoulos} and Luise Poustka and Sabina Millenet and Fr{\"o}hner, {Juliane H.} and Smolka, {Michael N.} and Henrik Walter and Robert Whelan and Barker, {Edward D.} and Gunter Schumann",

year = "2021",

doi = "10.1017/S0033291720005140",

language = "English",

pages = "1--11",

journal = "Psychological Medicine",

issn = "0033-2917",

publisher = "Cambridge University Press",

}

Biondo, F, Thunell, CN, Xu, B , Chu, C , Jia, T , Ing, A , Quinlan, EB , Tay, N, Banaschewski, T, Bokde, ALW, Büchel, C, Desrivières, S, Flor, H, Frouin, V, Garavan, H, Gowland, P, Heinz, A, Ittermann, B, Martinot, JL, Lemaitre, H, Nees, F, Orfanos, DP, Poustka, L, Millenet, S, Fröhner, JH, Smolka, MN, Walter, H, Whelan, R, Barker, ED & Schumann, G 2021, 'Sex differences in neural correlates of common psychopathological symptoms in early adolescence', Psychological Medicine, pp. 1-11. https://doi.org/10.1017/S0033291720005140

TY - JOUR

T1 - Sex differences in neural correlates of common psychopathological symptoms in early adolescence

AU - Biondo, Francesca

AU - Thunell, Charlotte Nymberg

AU - Xu, Bing

AU - Chu, Congying

AU - Jia, Tianye

AU - Ing, Alex

AU - Quinlan, Erin Burke

AU - Tay, Nicole

AU - Banaschewski, Tobias

AU - Bokde, Arun L.W.

AU - Büchel, Christian

AU - Desrivières, Sylvane

AU - Flor, Herta

AU - Frouin, Vincent

AU - Garavan, Hugh

AU - Gowland, Penny

AU - Heinz, Andreas

AU - Ittermann, Bernd

AU - Martinot, Jean Luc

AU - Lemaitre, Hervé

AU - Nees, Frauke

AU - Orfanos, Dimitri Papadopoulos

AU - Poustka, Luise

AU - Millenet, Sabina

AU - Fröhner, Juliane H.

AU - Smolka, Michael N.

AU - Walter, Henrik

AU - Whelan, Robert

AU - Barker, Edward D.

AU - Schumann, Gunter

PY - 2021

Y1 - 2021

N2 - Background Sex-related differences in psychopathology are known phenomena, with externalizing and internalizing symptoms typically more common in boys and girls, respectively. However, the neural correlates of these sex-by-psychopathology interactions are underinvestigated, particularly in adolescence. Methods Participants were 14 years of age and part of the IMAGEN study, a large (N = 1526) community-based sample. To test for sex-by-psychopathology interactions in structural grey matter volume (GMV), we used whole-brain, voxel-wise neuroimaging analyses based on robust non-parametric methods. Psychopathological symptom data were derived from the Strengths and Difficulties Questionnaire (SDQ). Results We found a sex-by-hyperactivity/inattention interaction in four brain clusters: right temporoparietal-opercular region (p < 0.01, Cohen's d = -0.24), bilateral anterior and mid-cingulum (p < 0.05, Cohen's d = -0.18), right cerebellum and fusiform (p < 0.05, Cohen's d = -0.20) and left frontal superior and middle gyri (p < 0.05, Cohen's d = -0.26). Higher symptoms of hyperactivity/inattention were associated with lower GMV in all four brain clusters in boys, and with higher GMV in the temporoparietal-opercular and cerebellar-fusiform clusters in girls. Conclusions Using a large, sex-balanced and community-based sample, our study lends support to the idea that externalizing symptoms of hyperactivity/inattention may be associated with different neural structures in male and female adolescents. The brain regions we report have been associated with a myriad of important cognitive functions, in particular, attention, cognitive and motor control, and timing, that are potentially relevant to understand the behavioural manifestations of hyperactive and inattentive symptoms. This study highlights the importance of considering sex in our efforts to uncover mechanisms underlying psychopathology during adolescence.

AB - Background Sex-related differences in psychopathology are known phenomena, with externalizing and internalizing symptoms typically more common in boys and girls, respectively. However, the neural correlates of these sex-by-psychopathology interactions are underinvestigated, particularly in adolescence. Methods Participants were 14 years of age and part of the IMAGEN study, a large (N = 1526) community-based sample. To test for sex-by-psychopathology interactions in structural grey matter volume (GMV), we used whole-brain, voxel-wise neuroimaging analyses based on robust non-parametric methods. Psychopathological symptom data were derived from the Strengths and Difficulties Questionnaire (SDQ). Results We found a sex-by-hyperactivity/inattention interaction in four brain clusters: right temporoparietal-opercular region (p < 0.01, Cohen's d = -0.24), bilateral anterior and mid-cingulum (p < 0.05, Cohen's d = -0.18), right cerebellum and fusiform (p < 0.05, Cohen's d = -0.20) and left frontal superior and middle gyri (p < 0.05, Cohen's d = -0.26). Higher symptoms of hyperactivity/inattention were associated with lower GMV in all four brain clusters in boys, and with higher GMV in the temporoparietal-opercular and cerebellar-fusiform clusters in girls. Conclusions Using a large, sex-balanced and community-based sample, our study lends support to the idea that externalizing symptoms of hyperactivity/inattention may be associated with different neural structures in male and female adolescents. The brain regions we report have been associated with a myriad of important cognitive functions, in particular, attention, cognitive and motor control, and timing, that are potentially relevant to understand the behavioural manifestations of hyperactive and inattentive symptoms. This study highlights the importance of considering sex in our efforts to uncover mechanisms underlying psychopathology during adolescence.

KW - Adolescence

KW - attention-deficit hyperactivity disorder

KW - externalizing symptoms

KW - grey matter

KW - IMAGEN

KW - internalizing symptoms

KW - psychopathology

KW - sex differences

KW - voxel-wise morphometry

UR - http://www.scopus.com/inward/record.url?scp=85103355349&partnerID=8YFLogxK

U2 - 10.1017/S0033291720005140

DO - 10.1017/S0033291720005140

M3 - Article

AN - SCOPUS:85103355349

SN - 0033-2917

SP - 1

EP - 11

JO - Psychological Medicine

JF - Psychological Medicine

ER -

Sex differences in neural correlates of common psychopathological symptoms in early adolescence

Abstract

Keywords

UN SDGs

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