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Oxytocin Attenuates Affective Evaluations of Conditioned Faces and Amygdala Activity
Open accessAbstract
Social relations between humans critically depend on our affective experiences of others. Oxytocin enhances prosocial behavior, but its effect on humans' affective experience of others is not known. We tested whether oxytocin influences affective ratings, and underlying brain activity, of faces that have been aversively conditioned. Using a standard conditioning procedure, we induced differential negative affective ratings in faces exposed to an aversive conditioning compared with nonconditioning manipulation. This differential negative evaluative effect was abolished by treatment with oxytocin, an effect associated with an attenuation of activity in anterior medial temporal and anterior cingulate cortices. In amygdala and fusiform gyrus, this modulation was stronger for faces with direct gaze, relative to averted gaze, consistent with a relative specificity for socially relevant cues. The data suggest that oxytocin modulates the expression of evaluative conditioning for socially relevant faces via influences on amygdala and fusiform gyrus, an effect that may explain its prosocial effects.
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“Results indicate that the tested type of intranasal OT delivery -but not peripherally delivered OT that produces similar blood levels -replicates prior findings of reduced right amygdala activation in response to emotional stimuli after OT treatment (Domes et al., 2007;Labuschagne et al., 2010;Petrovic et al., 2008).”
From Low dose intranasal oxytocin delivered with Breath Powered device dampens amygdala response to emotional stimuli: A peripheral effect-controlled within-subjects randomized dose-response fMRI trial (2016) · cites this paper as Petrovic et al., 2008
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In the citing paper
“This finding is in line with the anxiolytic action of OT via inhibiting amygdala responses to threatening stimuli (Kirsch et al., 2005; Petrovic et al., 2008).”
From Oxytocin facilitates approach behavior to positive social stimuli via decreasing anterior insula activity (2018) · cites this paper as Petrovic et al., 2008
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 [30]
In the citing paper
“Intranasal OT administration in FXS may work mechanistically by dampening amygdala reactivity toward socially threatening and anxiety-provoking stimuli (Kirsch et al., 2005; Petrovic et al., 2008), decreasing HPA axis activation, and increasing social motivation (Witt et al., 1992).”
From Effects of intranasal oxytocin on social anxiety in males with fragile X syndrome (2012) · cites this paper as Petrovic et al., 2008
In the citing paper
“Recent functional neuroimaging studies suggest that these effects are mediated through OXT's effects on amygdala reactivity and/or amygdala-frontal connectivity.”
From Modulation of Resting-State Amygdala-Frontal Functional Connectivity by Oxytocin in Generalized Social Anxiety Disorder (2014) · cites this paper as Petrovic et al, 2008
In the citing paper
“In this context, the insula17 as well as the amygdala seem to be key target regions in the brain, with oxytocin modulating amygdala responsiveness to emotional faces18–22 or social stimuli in general23.”
From Randomized clinical trial shows no substantial modulation of empathy-related neural activation by intranasal oxytocin in autism (2021) · cites this paper as [22]
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 Petrovic et al., 2008
In the citing paper
“OT is highly involved in the regulation of social recognition, by facilitating social memory and selective attention to socially-relevant information through action in the medial amygdala (Petrovic et al., 2008; Samuelsen and Meredith, 2011).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Petrovic et al., 2008
In the citing paper
“Petrovic et al. (2008) found that oxytocin reduced the negative evaluation of a face predicting unpleasant electric shocks.”
From Oxytocin enhances pupil dilation and sensitivity to 'hidden' emotional expressions (2013) · cites this paper as Petrovic et al. (2008)
In the citing paper
“possibly through dampening amygdala activation in response to fear-inducing stimuli [16], [17]”
From A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli (2013) · cites this paper as [17]
In the citing paper
“While previous research strongly suggests that intranasal administration of OT can reliably influence socially relevant judgments and ratings, relative to placebo [58], [17], [5]”
From A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli (2013) · cites this paper as [17]
In the citing paper
“its activity here tends to be reduced by OT administration upon exposure to threatening stimuli [18], [16], [17].”
From A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli (2013) · cites this paper as [17]
In the citing paper
“the anxiolytic action of OT via inhibiting amygdala responses to threatening stimuli (Kirsch et al., 2005; Petrovic et al., 2008)”
From Oxytocin facilitates approach behavior to positive social stimuli via decreasing anterior insula activity (2018) · cites this paper as Petrovic et al., 2008
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Citations
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Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690 · cited 6×
“Thus, an oxytocin effect in humans should be evident in altered behavior (Kosfeld et al., 2005) and also in how we affectively experience others.”
BackgroundMethodResultInfluentialThe amygdala: vigilance and emotion
Davis, M., & Whalen, P. J. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000812 · Cited by 2,882 · cited 2×
“One expression of this is augmentation of activity in fusiform face area (FFA) to fearful facial expressions (Vuilleumier and Pourtois, 2007), in addition to influences on subcortical and brainstem structures involved in behavioral fear responses (Davis and Whalen, 2001).”
BackgroundFunctional imaging of brain responses to pain. A review and meta-analysis (2000)
Peyron, R., Laurent, B., & García-Larrea, L. (2000) · Neurophysiologie Clinique/Clinical Neurophysiology · doi:10.1016/s0987-7053(00)00227-6 · Cited by 2,171
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“Oxytocin effects on affective evaluations In line with previous studies in which oxytocin was administrated externally (Pitman et al., 1993; Heinrichs et al., 2003, 2004; Kirsch et al., 2005; Kosfeld et al., 2005; Domes et al., 2007a), we did not observe any significant effect on mood ratings…”
BackgroundMethodEmotion and Cognition: Insights from Studies of the Human Amygdala
Phelps, E. A. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070234 · Cited by 1,798 · cited 11×
“We used a sequence with axial slices tilted by 30° and a flip angle of 90° that reduces signal dropout attributable to susceptibility-induced field inhomogeneities in amygdala and orbitofrontal cortex (Obfc) (Deichmann et al., 2002).”
BackgroundInfluentialPhelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.042 · Cited by 1,753 · cited 2×
“In the placebo group, we observed increased activity in the extended/dorsal amygdala and in other regions previously shown to be involved in fear conditioning and extinction such as insula, Obfc, and ACC (Gottfried and Dolan, 2004; Phelps et al., 2004; Kalisch et al., 2006; Milad et al., 2007).”
Background
Cited by
Sorted by citations
Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3044 · Cited by 1,688
“Additional brain imaging studies using different stimuli and experimental approaches replicated the dampening effect of OXT on amygdala activity in male”
Oxytocin, vasopressin, and the neurogenetics of sociality
Donaldson, Z. R., & Young, L. J. (2008) · Science · doi:10.1126/science.1158668 · Cited by 1,645
Social effects of oxytocin in humans: context and person matter
Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.002 · Cited by 1,581
Oxytocin: The Great Facilitator of Life
Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037
“Similarly, intranasal Oxt attenuates feelings of negativity towards faces conditioned with negative affective ratings, particularly in faces with direct gaze (Petrovic et al., 2008).”
InfluentialThe oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999
Metadata
- Authors
- Petrovic, P., Kalisch, R., Singer, T., & Dolan, R. J.
- Affiliations
- Max Planck Society (DE)
- University College London (GB)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2008-06-25
- Volume
- 28
- Issue
- 26
- Pages
- 6607-6615
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2647078
- OpenAlex
- W1993130604
- Cited by
- 424
- References
- 80
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 8 · 2023: 6 · 2022: 8 · 2021: 17 · 2020: 22 · 2019: 13 · 2018: 25 · 2017: 23 · 2016: 22 · 2015: 44 · 2014: 47 · 2013: 45 · 2012: 38
- FWCI
- 43.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Wellcome Trust (078865)
- Vetenskapsrådet
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- oxytocin, evaluative conditioning, amygdala, fusiform gyrus, gaze direction, anterior cingulate cortex, prosocial behavior, social cognition
- MeSH terms
- Adult, Affect, Amygdala, Conditioning, Psychological, Facial Expression, Fixation, Ocular, Humans, Male, Neuropsychological Tests, Oxytocin, Pattern Recognition, Visual, Photic Stimulation, Social Behavior, Temporal Lobe, Visual Cortex
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