A common allele in the oxytocin receptor gene ( OXTR ) impacts prosocial temperament and human hypothalamic-limbic structure and function
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The evolutionarily highly conserved neuropeptide oxytocin is a key mediator of social and emotional behavior in mammals, including humans. A common variant (rs53576) in the oxytocin receptor gene ( OXTR ) has been implicated in social-behavioral phenotypes, such as maternal sensitivity and empathy, and with neuropsychiatric disorders associated with social impairment, but the intermediate neural mechanisms are unknown. Here, we used multimodal neuroimaging in a large sample of healthy human subjects to identify structural and functional alterations in OXTR risk allele carriers and their link to temperament. Activation and interregional coupling of the amygdala during the processing of emotionally salient social cues was significantly affected by genotype. In addition, evidence for structural alterations in key oxytocinergic regions emerged, particularly in the hypothalamus. These neural characteristics predicted lower levels of reward dependence, specifically in male risk allele carriers. Our findings identify sex-dependent mechanisms impacting the structure and function of hypothalamic-limbic circuits that are of potential clinical and translational significance.
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Homozygous carriers of the minor allele (A) of rs53576 have been shown to exhibit lower interpersonal sensitivity.
“Homozygous carriers of the minor allele (A; hitherto referred to as ‘risk allele’) of rs53576 have been shown to exhibit lower interpersonal sensitivity59–62.”
From Voluntary upregulation of heart rate variability through biofeedback is improved by mental contemplative training (2019) · cites this paper as [61]
AA-carriers exhibit lower interpersonal sensitivity.
“Previous studies have shown that AA-carriers exhibit lower interpersonal sensitivity59–62.”
From Voluntary upregulation of heart rate variability through biofeedback is improved by mental contemplative training (2019) · cites this paper as [61]
OXTR polymorphisms are linked to other measures of social behavior, such as empathy, prosocial temperament, and pair-bonding behavior, in non-ASD populations.
“Results from studies in non-ASD populations have also linked OXTR polymorphisms to other measures of social behavior, such as empathy13, prosocial temperament14, and pair-bonding behavior15.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [14]
During pair bond formation in prairie voles, OXTR signaling boosts functional connectivity across a network of regions.
“In addition to region-specific effects, OXTR signaling enhances functional connectivity within a network of regions during prairie vole pair bond formation (79).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [79]
Reduced positive affect and reward dependence were found in men only among carriers of the A allele in rs53576.
“whereas reduced positive affect (Lucht et al., 2009) and reward dependence (Tost et al., 2010) were found in men only.”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Tost et al., 2010
Naturally-occurring polymorphisms in human OXTR are associated with correlated fluctuations in BOLD responses between hypothalamic, limbic, and/or cortical brain areas during social tasks.
“Two studies have shown that naturally-occurring polymorphisms in human OXTR (the gene encoding OTR) are associated with correlated fluctuations in BOLD responses between hypothalamic, limbic, and/or cortical brain areas during social tasks (Tost et al., 2010; Tost et al., 2011), and one has shown that methylation of OXTR in peripheral blood cells is associated with decreased correlated fluct”
From Oxytocin receptors modulate a social salience neural network in male prairie voles (2017) · cites this paper as Tost et al., 2010
In humans, alterations in amygdala responses to positive and negative emotions have been reported in neuropsychiatric conditions such as autism and schizophrenia, in association with OXTR genetic variants or following intranasal OXT.
“In humans, alterations in amygdala responses to positive and negative emotions have been reported in neuropsychiatric conditions, such as autism and schizophrenia [72,73], in association with OXTR genetic variants [41,102] or following intranasal OXT [33,36,38,103].”
From Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice (2019) · cites this paper as [41]
A allele carriers have reduced amygdala activation during the processing of faces compared to non-carriers.
“Specifically, it has been shown that A allele carriers have reduced amygdala activation during the processing of faces compared to non-carriers42.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [42]
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“…SNP, rs53576, show reduced empathy (Rodrigues et al., 2009; Uzefovsky et al., 2015), and have lower levels of optimism, mastery, and self-esteem (Saphire-Bernstein et al., 2011), whereas reduced positive affect (Lucht et al., 2009) and reward dependence (Tost et al., 2010) were found in men only.”
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“…amygdala activations during the perception of emotional facial expressions and OXTR and vasopressin (Avpr1a) receptorgene polymorphisms, which even correlated with individual measures of emotional reactivity and prosocial temperament in one study (Meyer-Lindenberg et al., 2009; Tost et al., 2010).”
BackgroundProsocial effects of oxytocin and clinical evidence for its therapeutic potential
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“Research in humans found that intronic OXTR variants predicted individual differences in functional connectivity between brain regions during the processing of social information (79,80).”
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“This SNP is also associated with structural differences in oxytonergic brain regions including amygdala and hypothalamus, as well as functional differences during emotional face processing (Tost et al., 2010).”
BackgroundReduced plasma oxytocin levels in female patients with borderline personality disorder
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A precision medicine approach to oxytocin trials
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The sociability spectrum: evidence from reciprocal genetic copy number variations
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- Authors
- Tost, H., Kolachana, B., Hakimi, S., Lemaitre, H., Verchinski, B. A., Mattay, V. S., Weinberger, D. R., & Meyer–Lindenberg, A.
- Affiliations
- National Institutes of Health (US)
- Clinical Brain Disorders Branch, Genes, Cognition, and Psychosis Program, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD 20892; and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-07-20
- Volume
- 107
- Issue
- 31
- Pages
- 13936-13941
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2922278
- OpenAlex
- W2074783654
- Cited by
- 564
- References
- 97
- Citations by year
- 2026: 11 · 2025: 7 · 2024: 14 · 2023: 16 · 2022: 17 · 2021: 25 · 2020: 41 · 2019: 39 · 2018: 62 · 2017: 53 · 2016: 59 · 2015: 51 · 2014: 48 · 2013: 48 · 2012: 44
- FWCI
- 51.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- National Institutes of Health
- National Institute of Mental Health
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- oxytocin receptor gene, oxytocin receptor, rs53576, oxytocin, reward dependence, amygdala activation, hypothalamus, sex differences, social behavior, genotype-phenotype correlation, neural coupling
- MeSH terms
- Adult, Alleles, Brain Mapping, Emotions, Female, Humans, Hypothalamus, Male, Sex Characteristics, Social Behavior, Temperament, Receptors, Oxytocin
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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