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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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“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
“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
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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Mathews, A., Mackintosh, B., & Fulcher, E. P. (1997) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(97)01092-9 · Cited by 221 · cited 2×
“Slowing of CS relative to CS RTs during a testing phase after conditioning has been reported previously (Kalisch et al., 2006) and is likely to reflect interference of emotion on a simultaneous cognitive task (Mathews et al., 1997).”
BackgroundPredictability modulates the affective and sensory-discriminative neural processing of pain
Carlsson, K., Andersson, J., Petrovic, P., Petersson, K. M., Öhman, A., & Ingvar, M. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.05.027 · Cited by 208
Selective amnesic effects of oxytocin on human memory.
HEINRICHS, M., MEINLSCHMIDT, G., WIPPICH, W., EHLERT, U., & HELLHAMMER, D. (2004) · Physiology & Behavior · doi:10.1016/s0031-9384(04)00346-4 · Cited by 205 · cited 2×
“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…”
MethodThe neurobiology of social recognition, approach, and avoidance
Young, L. J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01268-9 · Cited by 177 · cited 2×
“Oxytocin, a nanopeptide produced within hypothalamic paraventricular nuclei, modulates these processes in animals (Insel et al., 2001; Young, 2002; Debiec, 2005; Lim and Young, 2006) and facilitates prosocial behavior by both increasing approach but also suppressing avoidance (Bartz and Hollander,…”
BackgroundCheng, D. T., Knight, D. C., Smith, C. N., Stein, E. A., & Helmstetter, F. J. (2003) · Behavioral Neuroscience · doi:10.1037//0735-7044.117.1.3 · Cited by 163
Kapp, B. S., Supple, W. F., & Whalen, P. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.81 · Cited by 152
Pitman, R. K., Orr, S. P., & Lasko, N. B. (1993) · Psychiatry Research · doi:10.1016/0165-1781(93)90035-f · Cited by 150 · cited 5×
“Several studies using this method have reported oxytocindependent effects on behavior or brain function (Pitman et al., 1993; Heinrichs et al., 2003, 2004; Kirsch et al., 2005; Kosfeld et al., 2005; Domes et al., 2007a).”
BackgroundMethodResultInfluentialContingency awareness in human aversive conditioning involves the middle frontal gyrus
Carter, R. M., O’Doherty, J. P., Seymour, B., Koch, C., & Dolan, R. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.09.011 · Cited by 149
Self-citationSearch for autism loci by combined analysis of Autism Genetic Resource Exchange and Finnish families
Ylisaukko‐oja, T., Alarcón, M., Cantor, R. M., Auranen, M., Vanhala, R., Kempas, E., von Wendt, L., Järvelä, I. E., Geschwind, D. H., & Peltonen, L. (2005) · Annals of Neurology · doi:10.1002/ana.20722 · Cited by 139 · cited 2×
“, 2001) and an association with specific variants of the oxytocin receptor gene (Wu et al., 2005; Ylisaukko-oja et al., 2006).”
BackgroundTabbert, K., Stark, R. M., Kirsch, P., & Vaitl, D. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.03.038 · Cited by 123
Kapp, B. S., Supple, W. F., & Whalen, P. J. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.81 · Cited by 120
Context-dependent Deactivation of the Amygdala during Pain
Petrović, P., Carlsson, K., Petersson, K. M., Hansson, P. T., & Ingvar, M. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929041920469 · Cited by 102
Intact electrodermal skin conductance responses after bilateral amygdala damage
Tranel, D., & Damásio, H. (1989) · Neuropsychologia · doi:10.1016/0028-3932(89)90046-8 · Cited by 93
Dębiec, J. (2005) · BioEssays · doi:10.1002/bies.20301 · Cited by 90 · cited 5×
“Oxytocin is also implicated in inhibition of fear-related processes (Debiec, 2005).”
BackgroundInfluentialNeuroendocrine mechanisms of stress and social interaction: Implications for mental disorders
Heinrichs, M., & Gaab, J. (2007) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e3280146a13 · Cited by 79 · cited 5×
“It has been suggested that an underlying cause for deficits in social interaction in autistics is a malfunctioning oxytocin system (Bartz and Hollander, 2006; Hammock and Young, 2006; Carter, 2007; Heinrichs and Gaab, 2007), evidenced in lower oxytocin levels than in normal controls (Modahl et al.”
BackgroundInfluentialTabbert, K., Stark, R. M., Kirsch, P., & Vaitl, D. (2005) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.01.007 · Cited by 76
Chapter 4 Oxytocin: who needs it?
Insel, T. R., Gingrich, B., & Young, L. J. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33005-4 · Cited by 62 · cited 2×
“Oxytocin, a nanopeptide produced within hypothalamic paraventricular nuclei, modulates these processes in animals (Insel et al., 2001; Young, 2002; Debiec, 2005; Lim and Young, 2006) and facilitates prosocial behavior by both increasing approach but also suppressing avoidance (Bartz and Hollander,…”
BackgroundTime course of amygdala activation during aversive conditioning depends on attention
Straube, T., Weiß, T., Mentzel, H.-J., & Miltner, W. H. R. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.08.021 · Cited by 60
Compensation of susceptibility induced BOLD sensitivity losses in echo-planar fMRI imaging
Deichmann, R., & Turner, R. (2001) · NeuroImage · doi:10.1016/s1053-8119(01)91351-5 · Cited by 11
Morris, J. S., Buchel, C., & Dolan, R. J. (2001) · NeuroImage · doi:10.1006/nimg.2001.0891 · Cited by 9
Self-citationVeinante, P., & Freund-Mercier, M.-J. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970707)383:3
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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”
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“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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