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Cited by 99Neuroendocrine regulation and behaviorFace Recognition and PerceptionNeural and Behavioral Psychology Studies

Oxytocin decreases aversion to angry faces in an associative learning task

Open access
Evans, Simon, Shergill, Sukhwinder S, Averbeck, Bruno B·2010·Neuropsychopharmacology
DOI 10.1038/npp.2010.110PMC PMC2978766
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Abstract

Social and financial considerations are often integrated when real life decisions are made, and recent studies have provided evidence that similar brain networks are engaged when either social or financial information is integrated. Other studies, however, have suggested that the neuropeptide oxytocin can specifically affect social behaviors, which would suggest separable mechanisms at the pharmacological level. Thus, we examined the hypothesis that oxytocin would specifically affect social and not financial information in a decision making task, in which participants learned which of the two faces, one smiling and the other angry or sad, was most often being rewarded. We found that oxytocin specifically decreased aversion to angry faces, without affecting integration of positive or negative financial feedback or choices related to happy vs sad faces.

AI snapshot

Written from the paper’s full text.

TL;DR

In a double-blind placebo-controlled crossover study, intranasal oxytocin reduced aversion to angry faces in an associative learning task, increasing choices of angry faces when financial evidence supported them. Oxytocin did not affect overall learning, integration of positive or negative financial feedback, or choices involving happy vs. sad faces.

Key findings

  • Overall learning did not differ between drug and placebo: happy vs. angry placebo mean 0.69 vs. drug 0.68 (t17 = 0.7, p = 0.473); happy vs. sad placebo 0.67 vs. drug 0.64 (t17 = 1.5, p > 0.149).
  • Participants preferred happy faces over angry faces under placebo (mean difference = 0.159, t17 = 2.9, p = 0.009), but this preference was not significant under oxytocin (mean difference = 0.069, t17 = 1.2, p = 0.261).
  • In the happy vs. angry task, the placebo−drug difference curve had a significant intercept (mean a0 = 0.17, t17 = 2.80, p = 0.012); when evidence strongly supported the angry face, placebo participants chose it just over 60% of the time, whereas oxytocin participants chose it over 80% of the time.
  • Oxytocin did not alter learning from positive vs. negative financial feedback: happy vs. angry valence effect F1,17 = 31.51, p < 0.001, with no drug main effect (F1,17 = 0.03, p = 0.854) or interaction (F1,17 = 1.08, p = 0.306); happy vs. sad valence effect F1,17 = 56.47, p < 0.001, with no drug main effect (F1,17 = 2.89, p = 0.108) or interaction (F1,17 = 0.02, p = 0.890).

Methods

  • 18 male participants (average age 26.5) completed a double-blind, placebo-controlled crossover study of intranasal oxytocin (24 IU Syntocinon, Novartis) vs. saline placebo, with sessions separated by at least one week and testing beginning 50 minutes after administration.
  • Participants performed four blocks of 26 trials in both a happy vs. angry task and a happy vs. sad task; within each block one face was rewarded 60% of the time and the other 40%, and choices were referenced to an ideal observer model using a Bernoulli distribution.
  • An extended model fit free parameters for weighting positive and negative feedback, and evidence-vs.-choice probability curves were compared between drug conditions using regression coefficients on individual difference curves.

Limitations

  • Stated: the study did not include an explicit loss condition in which subjects actually lost money; it used highly polar emotions without a neutral condition; it included only male subjects; and the effect is conceptualized as reduced aversion to angry faces, though it could also reflect happy faces becoming less appetitive.
  • Stated: the lack of an oxytocin effect in the happy vs. sad task may relate to oxytocin specifically affecting approach/withdrawal behaviors, since sad faces may not elicit withdrawal responses as angry faces do.
  • Evident from the text: the sample was small (18 male participants), limiting generalizability, and the study did not include imaging or other direct measures of the proposed neural or pharmacological mechanisms.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1038/npp.2010.110

Cites

51 of 51 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 15 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    There was no overall effect of drug on learning to respond to the most rewarded target.

    “Thus, there was no overall effect of drug on learning to respond to the most rewarded target.”
    Quote in the paperNot a substantial claim
  • Findingown data

    In the happy vs. sad task, there was no main effect of drug on the amount that positive and negative feedback drove future decisions.

    “but again, no main effects of drug (F1,17 = 2.89, p = 0.108)”
    Quote in the paperNot a substantial claim
  • Findingown data

    In the happy vs. angry task, there was no valence by drug interaction on face preference.

    “and no valence by drug interaction (F1,17 = 1.84, p = 0.192)”
    Quote in the paperNot a substantial claim
  • Findingown data

    Oxytocin did not affect integration of positive or negative financial feedback.

    “We found that oxytocin specifically decreased aversion to angry faces, without affecting integration of positive or negative financial feedback or choices related to happy vs. sad faces.”
    • Also stated in: § Results · plain
      “Thus, subjects learned more from positive feedback than negative feedback across tasks, but oxytocin did not modify this learning.”
    Quote in the paperSubstantial claim
  • Findingown data

    In the happy vs. angry task, there was no main effect of drug on the amount that positive and negative feedback drove future decisions.

    “but no main effects of drug (F1,17 = 0.03, p = 0.854)”
    Quote in the paperNot a substantial claim
  • May combine two claims. 15
  • Classified as probably not a substantial claim. 22
  • The quote only partly states this claim. 2

  • May combine two claims.

    Findingown data

    In the happy vs. sad task, when the evidence strongly supported the happy face, participants picked it about 80% of the time, but when the evidence strongly supported the sad face, participants picked it about 70% of the time.

    “However, when the evidence strongly supported the happy face, participants picked it about 80% of the time, but when the evidence strongly supported the sad face participants picked it about 70% of the time.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Participants were more likely to pick the happy face when the evidence strongly supported it than the sad face.

    “Thus, participants were more likely to pick the happy face when the evidence strongly supported it than the sad face.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The difference between placebo and drug conditions did not reach significance in either the happy vs. angry or the happy vs. sad tasks.

    “The difference between placebo and drug conditions, however, did not reach significance in either the happy vs. angry (t17 = 0.7, p = 0.473) or the happy vs. sad (t17=1.5, p > 0.149) tasks (Fig. 2A and D).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    When the evidence strongly supported the angry face, participants in the placebo condition picked it just over 60% of the time, whereas participants in the drug condition picked it over 80% of the time.

    “However, when the evidence strongly supported the angry face, participants in the placebo condition picked it just over 60% of the time, whereas participants in the drug condition picked it over 80% of the time.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    Participants were above chance for the happy vs. sad task in the placebo (0.67) and drug (mean 0.64) conditions.

    “Similarly, they were above chance for the happy vs. sad task in the placebo (0.67, p < 0.001, t17 = 6.5) and drug (mean 0.64, p < 0.001, t17 = 6.3) conditions.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    When the evidence was 0.5 for the happy face in the happy vs. angry task, participants picked the happy face about 60% of the time and the angry face about 40% of the time, under both placebo and drug conditions.

    “What we found instead, was that participants picked the happy face about 60% of the time, and correspondingly the angry face about 40% of the time (Fig 2C), consistent with the significant preference effects reported above. This was true under both placebo and drug conditions.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    In the happy vs. sad task, there was a significant preference for happy over sad in both the placebo and drug conditions.

    “Planned comparisons showed that there was a significant preference in both the placebo (mean difference = 0.089, t17 = 2.27, p = 0.037) and drug conditions (mean difference = 0.126, t17 = 2.20, p = 0.042).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Participants were above chance for the happy vs. angry task in the placebo (mean 0.69) and drug (mean 0.68) conditions.

    “Participants were above chance for the happy vs. angry task in the placebo (mean 0.69, p < 0.001, t17 = 7.1) and drug (mean 0.68, p < 0.001, t17 = 8.2) conditions.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The valence effect (preference for happy over angry) was significant under placebo but not under oxytocin.

    “We also carried out planned comparisons on the valence effect separately in the drug and placebo conditions and found that the valence effect was significant under placebo (mean difference = 0.159, t17 = 2.9, p = 0.009) but not under drug (mean difference = 0.069, t17 = 1.2, p = 0.261).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    There was a main effect of before/after on mood, with subjects' mood decreasing slightly after drug administration.

    “but there was a main effect of before/after (F1,17 = 5.27, p = 0.035), with subject’s mood decreasing slightly after drug administration.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    On drug, subjects chose the angry face when the evidence strongly supported it about as often (~80%) as they chose the happy face when the evidence strongly supported it (~80%), on placebo.

    “In fact, on drug, subjects chose the angry face when the evidence strongly supported it about as often (~80%) as they chose the happy face when the evidence strongly supported it (~80%), on placebo.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    There were few differences between drug and placebo conditions for the happy vs. sad task.

    “Qualitatively, however, there were few differences between drug and placebo conditions for the happy vs. sad task.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Participants displayed choice preference in the happy vs. sad task.

    “although participants did display choice preference in this task as well.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Oxytocin had no effect on choice in the happy vs. sad task, with no systematic difference between placebo and drug.

    “Therefore there was no systematic difference between placebo and drug in how the participants chose the happy vs. the sad face, as a function of the evidence (Fig. 2H).”
    • Also stated in: § Discussion · plain
      “Interestingly, there was no effect of oxytocin in the happy vs. sad task, although participants did display choice preference in this task as well.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Recent studies have provided evidence that similar brain networks are engaged when either social or financial information is integrated.

    “Both social and financial considerations are often integrated when real life decisions are made, and recent studies have provided evidence that similar brain networks are engaged when either social or financial information is integrated.”
    • Also stated in: § Introduction · hedged
      “This presents an interesting contrast, as several recent papers have suggested that social and financial reward stimuli are processed by similar brain networks (Izuma et al., 2008, Zink et al., 2008).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Izuma et al., 2008 source

      Not checked in the free run.

    • cites Zink et al., 2008 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    The study used a double-blind placebo-controlled crossover design.

    “18 male participants (average age 26.5) were recruited for this double-blind placebo controlled crossover study of intranasal oxytocin.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Intranasally delivered oxytocin can improve inference of emotions from images of the eyes.

    “improve inference of emotions from images of the eyes (Domes et al., 2007b)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Domes et al., 2007b

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The order of high reward vs. low reward associated with the happy and angry/sad face was randomized across participants.

    “The order of high reward vs. low reward associated with the happy and angry/sad face was randomized across participants”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    The analysis modeled participants' belief trial-by-trial, so it does not rely on whether participants know which face should be correct in each block.

    “This point is not directly relevant to our analysis, however, because we modeled the participants’ belief trial-by-trial, and therefore we do not rely on whether or not the participants know which face “should” be correct in each block.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The order in which participants received oxytocin and placebo was randomized.

    “Each participant received both oxytocin and placebo and the order in which they received them was randomized.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Oxytocin can specifically affect social behaviors, suggesting separable mechanisms at the pharmacological level.

    “Other studies, however, have suggested that the neuropeptide oxytocin can specifically affect social behaviors, which would suggest separable mechanisms at the pharmacological level.”
    • Also stated in: § Introduction · hedged
      “Interestingly, despite the fact that oxytocin receptors are found throughout brain areas involved in motivation and reward, including the amygdala and ventral striatum (Schorscher-Petcu et al., 2009, Skuse and Gallagher, 2009), the effects of oxytocin seem to be specific to social stimuli (Ferguson et al., 2001) and may not extend to financial or other rewards.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ferguson et al., 2001 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims. The quote only partly states this claim.

    Study design and conductown data

    The parameters a and b were fit by maximizing the likelihood of the sequence of decisions of each participant, starting from multiple initial values to minimize the chance of falling into a local minima.

    “We started from multiple initial values to minimize the chance of falling into a local minima.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Intranasally delivered oxytocin can increase fixations to the eye region in human faces.

    “increase fixations to the eye region in human faces (Guastella et al., 2008a)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Guastella et al., 2008a

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    The identities alternated across blocks, and whether identity A or B was shown in the first block was counterbalanced.

    “The identities alternated across blocks, and we counterbalanced whether identity A or B was shown in the first block.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The order of the tasks (happy vs. angry and happy vs. sad) was randomized across participants.

    “The order of the tasks was randomized across participants.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductcitation

    Exploration should be minimized to perform optimally in this task because stationary distributions were used and it is a 2-armed bandit task.

    “Although it could be argued that participants should explore in this task and therefore that referencing choices to an ideal observer is not optimal, exploration should be minimized to perform optimally, as we used stationary distributions and therefore this is a 2-armed bandit task (Tsitsiklis, 1994).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Tsitsiklis, 1994 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    An ideal observer is able to identify the most highly rewarded face correctly in 85% of blocks of 26 trials with the probability values used.

    “We chose 26 trials because an ideal observer is able to identify the most highly rewarded face correctly in 85% of blocks of this length with the probability values we used (Averbeck and Duchaine, 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Averbeck and Duchaine, 2009 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Referencing all decisions to an ideal observer model controlled for the fact that feedback could be more positive for the face with a lower probability of being rewarded in the block.

    “Referencing to an ideal observer, which based its decisions on exactly the same information that the participant received on a trial-by-trial basis, controlled for the fact that the feedback could be more positive for the face which had a lower probability of being rewarded in the block.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Intranasally delivered oxytocin can increase trust or generosity in economic games.

    “These studies have shown that intranasally delivered oxytocin can increase trust or generosity in economic games (Kosfeld et al., 2005, Zak et al., 2007)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Kosfeld et al., 2005 source

      Not checked in the free run.

    • cites Zak et al., 2007 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Our task shows this effect more specifically, and also shows within the same paradigm that learning from financial feedback is not affected by oxytocin.

    “Our task shows this effect more specifically, and also shows within the same paradigm that learning from financial feedback is not affected by oxytocin.”
    Quote in the paperSubstantial claim

  • The quote only partly states this claim.

    Interpretationcitation

    Oxytocin exerts its effects by decreasing the aversive aspect of social stimuli.

    “Results from non-human animal studies also support the hypothesis that oxytocin exerts its effects by decreasing the aversive aspect of social stimuli.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Our study used only male subjects.

    “Third, our study used only male subjects, and there is evidence that male and female subjects respond differently to oxytocin (Domes et al., 2010).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    There is evidence that male and female subjects respond differently to oxytocin.

    “Third, our study used only male subjects, and there is evidence that male and female subjects respond differently to oxytocin (Domes et al., 2010).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Domes et al., 2010 source

      Not checked in the free run.

33 of 33

  • The paper relies on this without support.

    Participants believed their performance related to the amount they would be paid during the experiment.

    “Thus, during the experiment they believed their performance related to the amount they would be paid.”

  • The paper relies on this without support.

    It is unclear whether oxytocin's pro-social effects arise from increasing appetitive effects of positive stimuli, decreasing aversive effects of negative stimuli, or both.

    “Although oxytocin is often considered pro-social, whether it achieves these effects by increasing the appetitive effects of positively valenced stimuli, or decreasing the aversive effects of negatively valenced stimuli, or both has not been clear.”

  • The paper relies on this without support.

    It is unclear whether oxytocin affects only social stimuli or a broader class of stimuli with positive and negative emotional valence.

    “Additionally, whether it affects only social stimuli or a broader class of stimuli with positive and negative emotional valence has not been clear.”

  • The paper relies on this without support.

    Negative feedback generates a withdrawal response in our participants.

    “Our results are further specific in that negative feedback, which also generates a withdrawal response in our participants, is not affected by oxytocin.”
4 of 4

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Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Figure 2D is assigned to two different results

    Minor

    Figure 2D is cited for the comparison of overall task performance between drug and placebo, but later for the evidence-dependent difference in choices between those conditions. These are described as separate analyses, so at least one figure reference appears incorrect.

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Authors
Evans, S., Shergill, S. S., & Averbeck, B. B.
Affiliations
  • UCL Queen Square Institute of Neurology (GB)
  • King's College London (GB)
Corresponding author
Averbeck, Bruno B
ORCID
Venue
Neuropsychopharmacology
Publisher
Springer Science and Business Media LLC
Published
2010-09-15
Volume
35
Issue
13
Pages
2502-2509
ISSN
  • 0893-133X (ISSN-L)
  • 1740-634X
DOI
10.1038/npp.2010.110
PMC
PMC2978766
OpenAlex
W2015344919
Semantic Scholar
117ee181e5300d0d01eb7e2b7b024450b8cc5c93
Cited by
97
References
51
Citations by year
2025: 4 · 2024: 6 · 2023: 4 · 2022: 2 · 2021: 5 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 5 · 2016: 4 · 2015: 10 · 2014: 9 · 2013: 12 · 2012: 12
FWCI
16.54
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Neuropsychopharmacology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Figshare (submittedVersion, cc-by)
  • Research Portal (King's College London) (submittedVersion)
Funders
  • Wellcome Trust
  • National Institutes of Health (Z99 MH999999)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
oxytocin, emotional face processing, associative learning, social decision-making, financial decision-making, social feedback, emotional valence, neuropeptides
MeSH terms
Adult, Anger, Association Learning, Choice Behavior, Emotions, Facial Expression, Humans, Male, Oxytocin, Social Behavior, Models, Statistical, Feedback, Psychological

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