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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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“Reduced amygdala activation due to OT has been shown in previous fMRI studies using a similar protocol to exogenously apply OT via a nasal spray (Baumgartner et al., 2008; Domes, Heinrichs, Glascher et al., 2007; Kirsch et al., 2005; Petrovic et al., 2008).”
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“Regions in these studies which are affected by oxytocin, such as the amygdala, fusiform gyrus, ventromedial prefrontal cortex, insula, superior temporal gyrus, and inferior frontal gyrus [108], are consistently atypical in conditions where difficulties in social cognition are a defining feature as in ASC [45, 95].”
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“Biological P IN-OT on amygdala functional connectivity (105) or amygdala response involving left (92,98,113,114) or right amygdala laterality (97,100,101).”
Carson, D. S., Berquist, S. W., Trujillo, T. H., Garner, J. P., Hannah, S. L., Hyde, S. A., Sumiyoshi, R. D., Jackson, L. P., Moss, J. K., Strehlow, M. C., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.132 · Cited by 196
Oxytocin, the peptide that bonds the sexes also divides them
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Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications
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“[157-163].”
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Oxytocin increases amygdala reactivity to threatening scenes in females
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“…to threatening scenes following OT treatment in females sharply contrasts with the observation of attenuated amygdala activity in response to threat-related scenes (Kirsch et al., 2005) and faces (Domes et al., 2007a; Gamer et al., 2010; Kirsch et al., 2005; Petrovic et al., 2008) in males.”
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“In addition, variation inOXTR has been implicated in social information processing (Petrovic et al., 2008; Tost et al., 2010) and social communication, with GG individuals being better at detecting some emotions in others (Rodrigues et al., 2009).”
BackgroundOxytocin receptor gene methylation: converging multilevel evidence for a role in social anxiety
Ziegler, C., Dannlowski, U., Bräuer, D., Stevens, S., Laeger, I., Wittmann, H., Kugel, H., Dobel, C., Hurlemann, R., Reif, A., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.2 · Cited by 193
Oxytocin-Induced Analgesia and Scratching Are Mediated by the Vasopressin-1A Receptor in the Mouse
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“The central and peripheral effects of OXT are thought to be mediated by its binding to a single isoform of the OTR (Gimpl and Fahrenholz, 2001), which activates the phospholipase C (PLC ) signal transduction pathway (Arnaudeau et al., 1994; Ku et al., 1995; Phaneuf et al., 1995).”
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“[138, 140–142], fear [143, 144], empathy [145, 146], trust”
Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum
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The effect of intranasal administration of oxytocin on fear recognition
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“001 1182 Left BA 13 (222) Left BA 22 (219) Left BA 38 (174) Left BA 6 (165) Left BA 21 (120) Left BA 43 (70) Left BA 44 (39) Left BA 4 (37) Left BA 47 (31) Left BA 42 (26) Left BA 9 (19) Left BA 20 (12)”
Neurobehavioral foundation of environmental reactivity.
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Borderline personality disorder, mentalization, and the neurobiology of attachment
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Human neuroimaging of oxytocin and vasopressin in social cognition
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“When considering the eye gaze of the face stimuli, the activity in the right amygdala was found to be diminished by oxytocin only to aversely conditioned faces of high social relevance (direct gaze), which strongly activated amygdala under placebo (Petrovic et al., 2008).”
BackgroundInfluentialMaking room for oxytocin in understanding depression
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Association between the oxytocin receptor gene and amygdalar volume in healthy adults
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“ics and, in general, the pro-social features of the neuropeptide [166].”
Oxytocin, cortisol, and triadic family interactions
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Anxiolytic-like effect of oxytocin in the simulated public speaking test
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“OT attenuates negative affective evaluations associated with aversively conditioned faces through modulation of the amygdala and fusiform gyrus in non-clinical adults (Petrovic et al., 2008).”
BackgroundResultNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157
“Intranasal OT reliably modulates hemodynamic activity in the amygdala in healthy humans (28, 29, 31), children with autism (32), and rhesus macaques (30).”
BackgroundOxytocin enhances pupil dilation and sensitivity to 'hidden' emotional expressions
Leknes, S., Wessberg, J., Ellingsen, D.-M., Chelnokova, O., Olausson, H., & Laeng, B. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss062 · Cited by 151
“Petrovic et al. (2008) found that oxytocin reduced the negative evaluation of a face predicting Oxytocin, pupils and emotional sensitivity unpleasant electric shocks.”
BackgroundQuintana, D. S., Alvares, G. A., Hickie, I. B., & Guastella, A. J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.011 · Cited by 149
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“These studies showed that OT modulates amygdala activity when viewing human face stimuli in a sexually dimorphic manner, with OT generally decreasing amygdala activation to emotional faces in men (Kirsch et al., 2005; Domes et al., 2007b; Petrovic et al., 2008) but increasing it in women (Domes et al.”
BackgroundEffects of intranasal oxytocin on 'compassion focused imagery'
Rockliff, H., Karl, A., McEwan, K., Gilbert, J., Matos, M., & Gilbert, P. (2011) · Emotion · doi:10.1037/a0023861 · Cited by 147
Mattie Tops, A., Koole, S. L., IJzerman, H., & Buisman‐Pijlman, F. T. A. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.07.015 · Cited by 146
“Moreover, intranasal oxytocin abolished negative affective ratings of neutral faces induced by aversive conditioning, decreased right IFG responses and increased left IFG responses to the faces (Petrovic et al., 2008).”
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139
Effects of intranasal oxytocin on social anxiety in males with fragile X syndrome
Hall, S. S., Lightbody, A. A., McCarthy, B. E., Parker, K. J., & Reiss, A. L. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.020 · Cited by 143
“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.”
Gur, R., Tendler, A., & Wagner, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.022 · Cited by 144
Neuropeptides and central control of sexual behaviour from the past to the present: A review
Argiolas, A., & Melis, M. R. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.06.006 · Cited by 141
Emotion recognition and oxytocin in patients with schizophrenia
Averbeck, B. B., Bobin, T., Evans, S., & Shergill, S. S. (2011) · Psychological Medicine · doi:10.1017/s0033291711001413 · Cited by 148
“Related to this, oxytocin has also been shown to decrease negative affective evaluation of faces that have been negatively conditioned with shock, an effect also mediated by the amygdala (Petrovic et al. 2008).”
BackgroundTranslating mouse vocalizations: prosody and frequency modulation1
Lahvis, G. P., Alleva, E., & Scattoni, M. L. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00603.x · Cited by 149
“For instance, mice that lack a functional oxytocin allele, a molecule that plays a role in social bonding (Ferguson et al. 2000, 2002, Kavaliers et al. 2004, Mahler & Berridge 2009, Petrovic et al. 2008), emit fewer separation calls than their wild-type littermates (Winslow et al. 2000).”
BackgroundAcheson, D., Feifel, D., de Wilde, S., Mckinney, R., Lohr, J., & Risbrough, V. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3099-4 · Cited by 141
“…initial extinction training in this study is somewhat surprising given the evidence for acute reductions in amygdala activation and anxiolytic effects after IN OT treatment in humans (Petrovic et al. 2008; de Oliveira et al. 2012; Labuschagne et al. 2010; Domes et al. 2007; Kirsch et al. 2005).”
BackgroundInfluentialInterplay between Oxytocin and Sensory Systems in the Orchestration of Socio-Emotional Behaviors
Grinevich, V., & Stoop, R. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.016 · Cited by 139
“have emerged during evolution (Hodos and Butler, 1997; Kaas, 1989, 2008; Niven and Laughlin, 2008) and a number of recent break-through studies reported modulatory effects of OT visual and auditory signals in different orders of mammals (Domes et al., 2013; Freeman and Young, 2016; Kirsch et al., 2005; Marlin et al.,…”
The social brain: Neurobiological basis of affiliative behaviours and psychological well-being
Walker, S. C., & McGlone, F. P. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.008 · Cited by 145
“Neurally, part of OT’s effect appears to be a reduction in amygdala response to fear related stimuli (Petrovic et al., 2008).”
BackgroundHarari-Dahan, O., & Bernstein, A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.007 · Cited by 143
A psychobiological rationale for oxytocin in the treatment of posttraumatic stress disorder
Olff, M., Langeland, W., Witteveen, A., & Denys, D. (2010) · CNS Spectrums · doi:10.1017/s109285290000047x · Cited by 135
The past, present and future of social neuroscience: A European perspective
Singer, T. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.109 · Cited by 141
“…2008; Knoch et al., 2006), as well as the use of intranasal administration of oxytocin to measure trust (Kosfeld et al., 2005) and other social capacities such as social learning (Petrovic et al., 2008a; Petrovic et al., 2008b), mind reading and empathy (Domes et al., 2007; Singer et al., 2008).”
BackgroundSelf-citationOxytocin blunts social vigilance in the rhesus macaque
Ebitz, R. B., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305230110 · Cited by 132
“For example, OT reduces amygdala responses (12–14), self-reported affective responses (13), and self-reported arousal (15) following threat cues in humans.”
BackgroundMa, Y., Shamay-Tsoory, S., Han, S., & Zink, C. F. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.10.009 · Cited by 131
“By contrast, IN-OT may increase the capacity to regulate negative affect by increasing activity in the medial prefrontal cortex (mPFC [19,48,49]), ventral lateral prefrontal cortex (vlPFC [13,48,50,52,70]), and dorsal lPFC [49,70], which comprise the neural circuits for automatic and effortful regulation of emotion [6…”
BackgroundInfluentialMelis, M. R., & Argiolas, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.014 · Cited by 129
Wong, R. Y., Oxendine, S. E., & Godwin, J. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-348 · Cited by 132
“Oxytocin is thought to affect many social behaviors in humans [73] including having anxiolytic effects [74,75].”
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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