Oxytocin receptor genotype modulates ventral striatal activity to social cues and response to stressful life events
Open accessAbstract
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.
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Early life stress in humans can interact with OXTR variation to influence adult social behavior and emotional regulation.
“Early life stress in humans can interact with OXTR variation to influence adult social behavior and emotional regulation (28–31).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [28]
Girls who experienced stressful life events and were CT- and TT-carriers had increased numbers of emotional problems.
“Girls who experienced stressful life events and were CT- and TT-carriers had increased numbers of emotional problems”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Loth et al., 2014
There are sex-specific interactions between the rs237915 SNP, early life adversity, and emotional and peer problems in adolescents.
“There were also sex-specific interactions between the rs237915 SNP, early life adversity, and emotional and peer problems in adolescents.”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Loth et al., 2014
Boys who experienced stressful events and were TT-homozygotes had an increase in peer problems.
“boys who experienced stressful events and were TT-homozygotes had an increase in peer problems (Loth et al., 2014).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Loth et al., 2014
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- Authors
- Loth, E., Poline, J.-B., Thyreau, B., Jia, T., Tao, C., Lourdusamy, A., Stacey, D., Cattrell, A., Desrivières, S., Ruggeri, B., Fritsch, V., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Büchel, C., Carvalho, F. M., Conrod, P. J., Fauth-Buehler, M., Flor, H., Gallinat, J., Garavan, H., Heinz, A., Bruehl, R., Lawrence, C., Mann, K., Martinot, J.-L., Nees, F., Paus, T., Pausova, Z., Poustka, L., Rietschel, M., Smolka, M., Struve, M., Feng, J., & Schumann, G.
- Affiliations
- King's College London (GB)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Fudan University (CN)
- University of Mannheim (DE)
- Trinity College Dublin (IE)
- University Medical Center Hamburg-Eppendorf (DE)
- Charité – Universitätsmedizin Berlin (DE)
- University of Vermont (US)
- University of Nottingham (GB)
- Heidelberg University (DE)
- Inserm (FR)
- Montreal Neurological Institute and Hospital (CA)
- Neuroimaging Center (DE)
- University of Warwick (GB)
- Corresponding author
- Loth, Eva
- ORCID
- Loth, Eva
- Poline, Jean-Baptiste
- Thyreau, Benjamin
- Jia, Tianye
- Tao, Chenyang
- Lourdusamy, Anbarasu
- Stacey, David
- Desrivières, Sylvane
- Ruggeri, Barbara
- Banaschewski, Tobias
- Barker, Gareth J.
- Bokde, Arun L.W.
- Büchel, Christian
- Carvalho, Fabiana M.
- Conrod, Patricia J.
- Flor, Herta
- Gallinat, Jürgen
- Garavan, Hugh
- Heinz, Andreas
- Lawrence, Claire
- Mann, Karl
- Martinot, Jean-Luc
- Nees, Frauke
- Paus, Tomáš
- Poustka, Luise
- Rietschel, Marcella
- Smolka, Michael
- Struve, Maren
- Feng, Jianfeng
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2014-09
- Volume
- 76
- Issue
- 5
- Pages
- 367-376
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2098110443
- Cited by
- 65
- References
- 53
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 3 · 2023: 4 · 2022: 5 · 2021: 2 · 2020: 3 · 2019: 5 · 2018: 3 · 2017: 7 · 2016: 6 · 2015: 15 · 2014: 6 · 2013: 1
- FWCI
- 14.01
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc-nd)
- HAL (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- GRO (submittedVersion)
- Funders
- Bundesministerium für Bildung und Forschung (01EV0711)
- Vetenskapsrådet
- Seventh Framework Programme
- Svenska Forskningsrådet Formas
- Medical Research Council (G93558)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- oxytocin receptor gene, oxytocin receptor, ventral striatum, amygdala, life events, gene-environment interaction, single nucleotide polymorphisms, peer problems, emotional problems, adolescents, angry faces, resilience
- MeSH terms
- Adolescent, Amygdala, Child, Corpus Striatum, Cues, Female, Genotype, Humans, Life Change Events, Magnetic Resonance Imaging, Male, Oxygen, Signal Processing, Computer-Assisted, Social Behavior, Receptors, Oxytocin, Polymorphism, Single Nucleotide, White People, Genotyping Techniques
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