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Oxytocin Receptor Genotype Modulates Ventral Striatal Activity to Social Cues and Response to Stressful Life Events

Loth, Eva; Poline, Jean-Baptiste; Thyreau, Benjamin; Jia, Tianye; Tao, Chenyang; Lourdusamy, Anbarasu; Stacey, David; Cattrell, Anna; Desrivières, Sylvane; Ruggeri, Barbara; Fritsch, Virgile; Banaschewski, Tobias; Barker, Gareth J.; Bokde, Arun L.W.; Büchel, Christian; Carvalho, Fabiana M.; Conrod, Patricia J.; Fauth-Buehler, Mira; Flor, Herta; Gallinat, Jürgen; Garavan, Hugh; Heinz, Andreas; Bruehl, Ruediger; Lawrence, Claire; Mann, Karl; Martinot, Jean-Luc; Nees, Frauke; Paus, Tomáš; Pausova, Zdenka; Poustka, Luise; Rietschel, Marcella; Smolka, Michael; Struve, Maren; Feng, Jianfeng; Schumann, Gunter

Authors

Eva Loth

Jean-Baptiste Poline

Benjamin Thyreau

Tianye Jia

Chenyang Tao

David Stacey

Anna Cattrell

Sylvane Desrivières

Barbara Ruggeri

Virgile Fritsch

Tobias Banaschewski

Gareth J. Barker

Arun L.W. Bokde

Christian Büchel

Fabiana M. Carvalho

Patricia J. Conrod

Mira Fauth-Buehler

Herta Flor

Jürgen Gallinat

Hugh Garavan

Andreas Heinz

Ruediger Bruehl

Claire Lawrence

Karl Mann

Jean-Luc Martinot

Frauke Nees

Tomáš Paus

Zdenka Pausova

Luise Poustka

Marcella Rietschel

Michael Smolka

Maren Struve

Jianfeng Feng

Gunter Schumann



Contributors

IMAGEN Consortium
Research Group

Abstract

Background Common variants in the oxytocin receptor gene (OXTR) have been shown to influence social and affective behavior and to moderate the effect of adverse experiences on risk for social-affective problems. However, the intermediate neurobiological mechanisms are not fully understood. Although human functional neuroimaging studies have reported that oxytocin effects on social behavior and emotional states are mediated by amygdala function, animal models indicate that oxytocin receptors in the ventral striatum (VS) modulate sensitivity to social reinforcers. This study aimed to comprehensively investigate OXTR-dependent brain mechanisms associated with social-affective problems. Methods In a sample of 1445 adolescents we tested the effect of 23-tagging single nucleotide polymorphisms across the OXTR region and stressful life events (SLEs) on functional magnetic resonance imaging blood oxygen level-dependent activity in the VS and amygdala to animated angry faces. Single nucleotide polymorphisms for which gene-wide significant effects on brain function were found were then carried forward to examine associations with social-affective problems. Results A gene-wide significant effect of rs237915 showed that adolescents with minor CC-genotype had significantly lower VS activity than CT/TT-carriers. Significant or nominally significant gene × environment effects on emotional problems (in girls) and peer problems (in boys) revealed a strong increase in clinical symptoms as a function of SLEs in CT/TT-carriers but not CC-homozygotes. However, in low-SLE environments, CC-homozygotes had more emotional problems (girls) and peer problems (boys). Moreover, among CC-homozygotes, reduced VS activity was related to more peer problems. Conclusions These findings suggest that a common OXTR-variant affects brain responsiveness to negative social cues and that in "risk- carriers" reduced sensitivity is simultaneously associated with more social-affective problems in "favorable environments" and greater resilience against stressful experiences. © 2014 Society of Biological Psychiatry.

Citation

Loth, E., Poline, J., Thyreau, B., Jia, T., Tao, C., Lourdusamy, A., …Schumann, G. (2014). Oxytocin Receptor Genotype Modulates Ventral Striatal Activity to Social Cues and Response to Stressful Life Events. Biological Psychiatry, 76(5), 367-376. https://doi.org/10.1016/j.biopsych.2013.07.043

Journal Article Type Article
Acceptance Date Jul 2, 2013
Online Publication Date Oct 8, 2013
Publication Date Sep 1, 2014
Deposit Date Jul 4, 2019
Publicly Available Date Jul 4, 2019
Journal Biological Psychiatry
Print ISSN 0006-3223
Electronic ISSN 1873-2402
Publisher Elsevier
Peer Reviewed Peer Reviewed
Volume 76
Issue 5
Pages 367-376
DOI https://doi.org/10.1016/j.biopsych.2013.07.043
Public URL https://nottingham-repository.worktribe.com/output/2266664
Publisher URL https://www.sciencedirect.com/science/article/pii/S000632231300810X

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