Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Open accessAbstract
Trust and betrayal of trust are ubiquitous in human societies. Recent behavioral evidence shows that the neuropeptide oxytocin increases trust among humans, thus offering a unique chance of gaining a deeper understanding of the neural mechanisms underlying trust and the adaptation to breach of trust. We examined the neural circuitry of trusting behavior by combining the intranasal, double-blind, administration of oxytocin with fMRI. We find that subjects in the oxytocin group show no change in their trusting behavior after they learned that their trust had been breached several times while subjects receiving placebo decrease their trust. This difference in trust adaptation is associated with a specific reduction in activation in the amygdala, the midbrain regions, and the dorsal striatum in subjects receiving oxytocin, suggesting that neural systems mediating fear processing (amygdala and midbrain regions) and behavioral adaptations to feedback information (dorsal striatum) modulate oxytocin's effect on trust. These findings may help to develop deeper insights into mental disorders such as social phobia and autism, which are characterized by persistent fear or avoidance of social interactions.
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Kosfeld's seminal finding on oxytocin and trust has not always been replicated; Baumgartner et al. found no significant effect of oxytocin on the pre-betrayal trust game, and two independent studies also failed to replicate Kosfeld's findings.
“We noticed that Kosfeld’s [1] seminal finding was not always replicated either. Indeed, Baumgartner et al. [7] found no significant effect of OT on the pre-betrayal trust game. More recently, two independent studies also failed to replicate Kosfeld’s findings [20] [21].”
From Failed Replication of Oxytocin Effects on Trust: The Envelope Task Case (2015) · cites this paper as [7]
Previous studies indicate that oxytocin may induce sex-dependent changes in amygdala activation to emotional stimuli, but in opposite directions to the present findings.
“Previous studies on amygdala responses to fearful faces and fearful/threatening scenes (14 -17, 30) and social risk (31) have also indicated that OXT may induce sex-dependent changes in amygdala activation to emotional stimuli.”
From Oxytocin, the peptide that bonds the sexes also divides them (2016) · cites this paper as [31]
Participants in a trust game tend to discount feedback information regarding their partner's unreciprocal behavior more so when they are given intranasal oxytocin compared with a placebo.
“An earlier study by Baumgartner et al. (2008) reported that participants in a trust game tend to discount feedback information regarding their partner's unreciprocal behavior more so when they are given intranasal OT compared with a placebo.”
From The effect of oxytocin on cooperation in a prisoner's dilemma depends on the social context and a person's social value orientation (2014) · cites this paper as Baumgartner et al. (2008)
Oxytocin reduces social anxiety by attenuating the amygdala response to fearful social signals.
“On the other hand, there are several reports that OT reduces social anxiety by attenuating the amygdala response to fearful social signals (Kirsch et al., 2005;Baumgartner et al., 2008).”
From The effect of oxytocin on cooperation in a prisoner's dilemma depends on the social context and a person's social value orientation (2014) · cites this paper as Baumgartner et al., 2008
Intranasal application of oxytocin increases trusting behavior in humans.
“Intriguingly, intranasal application of OT has been shown to increase trusting behavior in humans [20], [21], identification of others' affective states [22] and amygdala responses to emotional faces [23].”
From The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task (2009) · cites this paper as [20]
In healthy volunteers, intranasal OXT administration dampens amygdala reactivity to threatening facial expressions and naturalistic social interactions.
“Consistent with this evidence, functional magnetic imaging (fMRI) studies with healthy volunteers have shown that intranasal OXT administration dampens amygdala reactivity to threatening facial expressions (Domes et al, 2007;Kirsch et al, 2005), and naturalistic social interactions (Baumgartner et al, 2008).”
From Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder (2015) · cites this paper as Baumgartner et al, 2008
Neuroimaging studies demonstrate that intranasal administration of oxytocin attenuates amygdala activation following stressful and fearful stimuli.
“In agreement, neuroimaging studies demonstrate that intranasal administration of oxytocin attenuates amygdala activation following stressful and fearful stimuli (Baumgartner et al., 2008; Domes et al., 2007; Kirsch et al., 2005; Labuschagne et al., 2010).”
From Effect of oxytocin on craving and stress response in marijuana-dependent individuals: A pilot study (2013) · cites this paper as Baumgartner et al., 2008
Intranasal OXT administration in healthy humans attenuates activation of the amygdala to social stimuli.
“attenuating activation of amygdala to social stimuli (Baumgartner et al, 2008;Domes et al, 2007a;Gamer et al, 2010;Kirsch et al, 2005)”
From Chronic and acute intranasal oxytocin produce divergent social effects in mice (2014) · cites this paper as Baumgartner et al, 2008
Human studies have prevalently used acute administration of OXT in healthy subjects, whereas prolonged OXT treatments have been adopted only in pathological states presenting social deficits.
“human studies have prevalently used acute administration of OXT in healthy subjects”
From Chronic and acute intranasal oxytocin produce divergent social effects in mice (2014) · cites this paper as Baumgartner et al, 2008
IN-OT increases trust by reducing BOLD activity of amygdala and midbrain regions, neural systems that mediate fear processing.
“IN-OT increases trust by reducing the BOLD activity of amygdala and midbrain regions, neural systems that mediate fear processing (Baumgartner et al. 2008).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Baumgartner et al. 2008
Of the six studies in Nave et al.'s meta-analysis, four had fictional partners, one was completely devoid of human contact with other participants, and the sixth had participants' previous experience in a dictator game likely to confound the decision to trust.
“Of the six studies that entered the meta-analysis in Nave et al.21 -in addition to the Kosfeld 8 et al. study -four studies had fictional partners [25][26][27][28] , one was completely devoid of human contact with other participants 29 , and participants' previous experience in a dictator game was likely to confound the decision to trust in the sixth study 30 .”
From A registered replication study on oxytocin and trust (2020) · cites this paper as [29]
Inhaling OT reduces BOLD activation in the amygdala when viewing or associating aversive social stimuli, during trust formation, in response to pain, and in response to infant crying.
“Human functional neuroimaging studies have shown that inhaling OT reduces BOLD (blood-oxygen-level dependent) activation in the amygdala when viewing or associating aversive social stimuli (Kirsch, 2005; Petrovic et al., 2008), during trust formation (Baumgartner et al., 2008), in response to pain (Singer et al., 2008), and in response to infant crying (Riem et al., 2011).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Baumgartner et al., 2008
Previous studies showed that OT reduced recognition of and affective responses to negative signals, and failed to change behavior after the receipt of negative information.
“Consistently, previous studies showed that OT reduced recognition of and affective responses to negative signals, and failed to change behavior after the receipt of negative information (i.e., social betrayal; ref. 17).”
From Distinct oxytocin effects on belief updating in response to desirable and undesirable feedback (2016) · cites this paper as [17]
Oxytocin promotes prosocial approach, such as trust and cooperative behaviors.
“Oxytocin, the hypothalamic neuropeptide important for social cognition and behavior, has been shown to promote prosocial approach, such as trust and cooperative behaviors (16, 21, 22, but also see ref. 23)”
From Placebo treatment facilitates social trust and approach behavior (2018) · cites this paper as [22]
Oxytocin is an important neuropeptide for social cognition and behavior.
“Oxytocin, the hypothalamic neuropeptide important for social cognition and behavior, has been shown to promote prosocial approach, such as trust and cooperative behaviors (16, 21, 22, but also see ref. 23)”
From Placebo treatment facilitates social trust and approach behavior (2018) · cites this paper as [22]
The effects of exogenously administered oxytocin on trust and trust adaptation are associated with reductions in neural activity of brain regions implicated in fear processing (amygdala and midbrain regions).
“subsequent neuroimaging work provided indications that the effects of exogenously administered OT on trust and trust adaptation were associated with reductions in neural activity of brain regions that are implicated in fear processing (amygdala and midbrain regions) (Baumgartner et al., 2008).”
From Long-term oxytocin administration enhances the experience of attachment (2017) · cites this paper as Baumgartner et al., 2008
Prior reputation of a partner alters striatum responses to reciprocated or non-reciprocated cooperation.
“Further research utilizing cooperative economic games has shown that the prior reputation of a partner alters striatum responses to reciprocated or non-reciprocated cooperation and influences decisions to cooperate or not 75–79.”
From The social brain and reward: Social information processing in the human striatum (2014) · cites this paper as [79]
Prior reputation of a partner influences decisions to cooperate or not.
“Further research utilizing cooperative economic games has shown that the prior reputation of a partner alters striatum responses to reciprocated or non-reciprocated cooperation and influences decisions to cooperate or not 75–79.”
From The social brain and reward: Social information processing in the human striatum (2014) · cites this paper as [79]
Decisions to cooperate with another person are influenced by information learned about the person thus far.
“Decisions to cooperate with another person are colored by the information we have learnt about the person thus far.”
From The social brain and reward: Social information processing in the human striatum (2014) · cites this paper as [79]
The observed inhibitory effects of OT on striatum and AI activity conflict with previous findings that OT-induced alterations on human social behavior are associated with increased activity in the striatum and AI.
“and some previous findings that OT-induced alterations on human social behavior are associated with increased activity in the striatum and AI (Baumgartner et al., 2008; Strathearn et al., 2009; Striepens et al., 2011; Yao et al., 2018).”
From Oxytocin facilitates approach behavior to positive social stimuli via decreasing anterior insula activity (2018) · cites this paper as Baumgartner et al., 2008
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Self-citationDifferent amygdala subregions mediate valence-related and attentional effects of oxytocin in humans
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“It has been shown to do so in other experimental contexts (Baumgartner et al., 2008; De Dreu, 2012a,b; Israel et al., 2012; Kosfeld et al., 2005).”
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Oxytocin makes people trusting, not gullible
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“…increases trust behavior (e.g., Kosfeld et al., 2005; Mikolajczak et al., 2010a,b) as well as shapes the neural circuitry of trust and trust adaptation (Baumgartner et al., 2008), recently confirmed by a meta-analysis on exogenous OXT trust studies (Van Ijzendoorn and Bakermans-Kranenburg, 2011).”
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Self-citationIntranasal oxytocin blocks alcohol withdrawal in human subjects
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- Authors
- Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E.
- Affiliations
- University of Zurich (CH)
- Corresponding author
- Fehr, Ernst
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2008-05
- Volume
- 58
- Issue
- 4
- Pages
- 639-650
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2102027817
- Cited by
- 1,258
- References
- 78
- Citations by year
- 2026: 16 · 2025: 32 · 2024: 42 · 2023: 28 · 2022: 38 · 2021: 51 · 2020: 105 · 2019: 64 · 2018: 51 · 2017: 73 · 2016: 96 · 2015: 86 · 2014: 92 · 2013: 118 · 2012: 111
- FWCI
- 112.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1939 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Research Bank (Australian Catholic University) (submittedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion)
- FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Universität Zürich (PP001-114788)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin, trust, betrayal of trust, amygdala, midbrain, dorsal striatum, fear processing, social cognition, social anxiety disorder, autism spectrum disorder
- MeSH terms
- Adaptation, Psychological, Adult, Analysis of Variance, Brain, Brain Mapping, Double-Blind Method, Games, Experimental, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Nerve Net, Oxygen, Oxytocin, Psychometrics, Surveys and Questionnaires, Reaction Time, Risk-Taking, Trust
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