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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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In the citing paper
“Functioning as both a neurotransmitter and a hormone, oxytocin's targets are widespread and include the hippocampus and the amygdala (10–12).”
From Oxytocin promotes human ethnocentrism (2011) · cites this paper as [10]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“adapted version of the well‐established trust game.[ 21 ]”
From Loneliness and the Social Brain: How Perceived Social Isolation Impairs Human Interactions (2021) · cites this paper as [21]
The cited source says what the claim attributes to it.
In the citing paper
“There is no doubt that oxytocin is implicated in the development of trust (10, 18), empathy, and prosociality (11), but these tendencies appear limited to individuals belonging to one's in-group (16, 17).”
From Oxytocin promotes human ethnocentrism (2011) · cites this paper as [10]
In the citing paper
“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]
In the citing paper
“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)
In the citing paper
“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
In the citing paper
“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 the citing paper
“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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 the citing paper
“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
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“To conform with prior research showing that effects of oxytocin peak after ∼30–40 min (10, 16, 18), after 38–42 min, the computer switched to the experimental task (lasting 15–20 min).”
From Oxytocin promotes human ethnocentrism (2011) · cites this paper as [10]
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“Moreover, in conjunction with its effect on social threat, the ability of oxytocin to specifically modulate the interplay between positive and negative social evaluative processes (increase in vector angle) may promote social approach behaviors associated with an increased willingness to trust (Baumgartner et al., 200…”
BackgroundWu, H., Zhou, Y., Wang, Y., Tong, L., Wang, F., Song, S., Xu, L., Liu, B., Yan, H., & Sun, Z. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.717192 · Cited by 90
Antiaggressive activity of central oxytocin in male rats
Calcagnoli, F., de Boer, S. F., Althaus, M., den Boer, J. A., & Koolhaas, J. M. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3124-7 · Cited by 90
Alvares, G. A., Quintana, D. S., & Whitehouse, A. J. O. (2017) · Autism Research · doi:10.1002/aur.1692 · Cited by 91
Long-term oxytocin administration enhances the experience of attachment
Bernaerts, S., Prinsen, J., Berra, E., Bosmans, G., Steyaert, J., & Alaerts, K. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.01.010 · Cited by 90
Oxytocin, but not vasopressin, increases both parochial and universal altruism
Israel, S., Weisel, O., Ebstein, R. P., & Bornstein, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.02.001 · Cited by 88
Links between the neurobiology of oxytocin and human musicality
Harvey, A. R. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.00350 · Cited by 85
Marsh, A. A., Yu, H. H., Pine, D. S., Gorodetsky, E. K., Goldman, D., & Blair, R. J. R. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2775-0 · Cited by 87
Bahji, A., Forsyth, A., Groll, D., & Hawken, E. R. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109735 · Cited by 88
Rocchetti, M., Radua, J., Paloyelis, Y., Xenaki, L., Frascarelli, M., Caverzasi, E., Politi, P., & Fusar‐Poli, P. (2014) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12185 · Cited by 83
Oxytocin’s effect on resting-state functional connectivity varies by age and sex
Ebner, N. C., Chen, H., Porges, E., Lin, T., Fischer, H., Feifel, D., & Cohen, R. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.03.013 · Cited by 84
Prehn, K., Kazzer, P., Lischke, A., Heinrichs, M., Herpertz, S. C., & Domes, G. (2013) · Psychophysiology · doi:10.1111/psyp.12042 · Cited by 81
Self-citationPohl, T. T., Young, L. J., & Bosch, O. J. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.12.011 · Cited by 83
van IJzendoorn, M. H., Huffmeijer, R., Alink, L. R. A., Bakermans-Kranenburg, M. J., & Tops, M. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2011.00258 · Cited by 83
“In particular its positive role in parenting (Feldman et al., 2007; Naber et al., 2010) and interpersonal trust (Baumgartner et al., 2008; Theodoridou et al., 2009; De Dreu et al., 2010; Declerck et al., 2010) has been documented.”
BackgroundEllenbogen, M. A., Linnen, A., Grumet, R., Cardoso, C., & Joober, R. (2012) · Psychophysiology · doi:10.1111/j.1469-8986.2011.01278.x · Cited by 82
Chen, X., Hackett, P. D., DeMarco, A. C., Feng, C., Stair, S., Haroon, E., Ditzen, B., Pagnoni, G., & Rilling, J. K. (2016) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9411-7 · Cited by 81
Naismith, I., Zarate Guerrero, S., & Feigenbaum, J. (2019) · Clinical Psychology & Psychotherapy · doi:10.1002/cpp.2357 · Cited by 80
Oxytocin and socioemotional aging: current knowledge and future trends
Ebner, N. C., Maura, G. M., MacDonald, K., Westberg, L., & Fischer, H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00487 · Cited by 78
Calcagnoli, F., Stubbendorff, C., Meyer, N., de Boer, S. F., Althaus, M., & Koolhaas, J. M. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.012 · Cited by 77
Oxytocin, sexually dimorphic features of the social brain, and autism
Yamasue, H., Kuwabara, H., Kawakubo, Y., & Kasai, K. (2009) · Psychiatry and Clinical Neurosciences · doi:10.1111/j.1440-1819.2009.01944.x · Cited by 78
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Pupil-mimicry conditions trust in partners: moderation by oxytocin and group membership
Kret, M. E., & De Dreu, C. K. W. (2017) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2016.2554 · Cited by 75
The other side of the coin: oxytocin decreases the adherence to fairness norms
Radke, S., & de Bruijn, E. R. A. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00193 · Cited by 73
Oxytocin makes females, but not males, less forgiving following betrayal of trust
Yao, S., Zhao, W., Cheng, R., Geng, Y., Luo, L., & Kendrick, K. M. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114571400090x · Cited by 74
Chang, S. W. C., & Platt, M. L. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.006 · Cited by 71
Oxytocin selectively moderates negative cognitive appraisals in high trait anxious males
Alvares, G. A., Chen, N. T. M., Balleine, B. W., Hickie, I. B., & Guastella, A. J. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.04.018 · Cited by 71
Restoring effects of oxytocin on the attentional preference for faces in autism
Kanat, M., Spenthof, I., Riedel, A., van Elst, L. T., Heinrichs, M., & Domes, G. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.67 · Cited by 70
Self-citationOxytocin and vasopressin: signalling, behavioural modulation and potential therapeutic effects
Rae, M., Lemos Duarte, M., Gomes, I., Camarini, R., & Devi, L. A. (2022) · British Journal of Pharmacology · doi:10.1111/bph.15481 · Cited by 72
Striepens, N., Matusch, A., Kendrick, K. M., Mihov, Y., Elmenhorst, D., Becker, B., Lang, M., Coenen, H. H., Maier, W., Hurlemann, R., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.026 · Cited by 71
Oxytocin promotes intuitive rather than deliberated cooperation with the in-group
Ten Velden, F. S., Daughters, K., & De Dreu, C. K. W. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.06.005 · Cited by 66
When Two Become One: The Role of Oxytocin in Interpersonal Coordination and Cooperation
Arueti, M., Perach-Barzilay, N., Tsoory, M. M., Berger, B., Getter, N., & Shamay-Tsoory, S. G. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00400 · Cited by 67
Oxytocin modulates fMRI responses to facial expression in macaques
Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. B., & Ungerleider, L. G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508097112 · Cited by 65
Oxytocin: Parallel Processing in the Social Brain?
Dölen, G. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12284 · Cited by 65
Oxytocin's Fingerprint in Personality Traits and Regional Brain Volume
Andari, E., Schneider, F. C., Mottolese, R., Vindras, P., & Sirigu, A. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhs328 · Cited by 63
Oxytocin and the salience of social cues
Averbeck, B. B. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004892107 · Cited by 64
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Failed Replication of Oxytocin Effects on Trust: The Envelope Task Case
Lane, A., Mikolajczak, M., Treinen, E., Samson, D., Corneille, O., de Timary, P., & Luminet, O. (2015) · PLOS ONE · doi:10.1371/journal.pone.0137000 · Cited by 60
“Using a “non-monetary” trust assessment paradigm, that we shall call the “Envelope Task” (see below), they showed that OT did increase trust toward strangers, thereby confirming Kostfeld [1] and Baumgartner’s [7] hypothesis that OT increases trust.”
Background
Metadata
- 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
- 77
- 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
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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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