Intranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions
Open accessAbstract
Intranasal oxytocin (IN-OT) modulates social perception and cognition in humans and could be an effective pharmacotherapy for treating social impairments associated with neuropsychiatric disorders, like autism. However, it is unknown how IN-OT modulates social cognition, its effect after repeated use, or its impact on the developing brain. Animal models are urgently needed. This study examined the effect of IN-OT on social perception in monkeys using tasks that reveal some of the social impairments seen in autism. Six rhesus macaques (Macaca mulatta, 4 males) received a 48 IU dose of OT or saline placebo using a pediatric nebulizer. An hour later, they performed a computerized task (the dot-probe task) to measure their attentional bias to social, emotional, and nonsocial images. Results showed that IN-OT significantly reduced monkeys' attention to negative facial expressions, but not neutral faces or clip art images and, additionally, showed a trend to enhance monkeys' attention to direct vs. averted gaze faces. This study is the first to demonstrate an effect of IN-OT on social perception in monkeys, IN-OT selectively reduced monkey's attention to negative facial expressions, but not neutral social or nonsocial images. These findings complement several reports in humans showing that IN-OT reduces the aversive quality of social images suggesting that, like humans, monkey social perception is mediated by the oxytocinergic system. Importantly, these results in monkeys suggest that IN-OT does not dampen the emotional salience of social stimuli, but rather acts to affect the evaluation of emotional images during the early stages of information processing.
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IN-OXT treatment increases gaze following, increases socially oriented gaze, and alters social attention in a wide variety of contexts in macaques.
“This work provides anatomical support for other findings in macaques, which indicate that IN-OXT treatment increases gaze following67, increases socially oriented gaze68, and alters social attention in a wide variety of contexts69–74.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [69]
The dose of 50 IU oxytocin has been used previously for rhesus monkeys.
“This dose has been used previously used for rhesus monkeys (Dal Monte et al., 2014b; Parr et al., 2013).”
From Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys (2016) · cites this paper as Parr et al., 2013
In rhesus macaques, three studies found that intranasal oxytocin treatment impacts social visual attention and looking behaviours across a variety of tasks.
“In rhesus macaques, three studies have found that treatment with IN-OT impacts social visual attention and looking behaviours in a variety of tasks (77-79).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [78]
Inhaled oxytocin affected monkeys' social perceptions by reducing their attention to negative but not neutral facial expressions.
“Parr et al. (2013) found that inhaled oxytocin affected the monkeys' social perceptions by reducing their attention to negative but not neutral facial expressions.”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Parr et al., 2013
Oxytocin release may depend more on an individual's social perception of an interaction than on the properties of the interaction itself.
“That oxytocin release may depend more on an individuals' social perception of an interaction than on the properties of the interaction itself mirrors other studies on human and non-human primates which suggest that inhaled oxytocin changes individuals' perception or motivation toward a social context (Chang et al., 2012; Parr et al., 2013, for reviews see: Bartz et al., 2011; Olff et al., 2013).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Parr et al., 2013
Studies using exogenous oxytocin have highlighted that a possible effect of oxytocin is to change individuals' social motivations or perceptions of a current social context, such that individuals that inhale oxytocin compared with those that do not become more affiliative, attentive, prosocial or empathetic to the same social stimuli.
“Studies using exogenous oxytocin have highlighted how a possible effect of oxytocin is to change individuals' social motivations or perceptions of a current social context, such that individuals that inhale oxytocin compared with those that do not, become more affiliative, attentive, prosocial or empathetic to the same social stimuli (e.g., Bartz et al., 2011; Chang et al., 2012; Parr et al., 2013”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Parr et al., 2013
Inhaled OT selectively reduces attention to emotional facial expressions while enhancing attention to faces with direct gaze in rhesus macaques.
“Consistent with the role of OT in reducing social vigilance state, another recent study in rhesus macaques reported that inhaled OT selectively reduces attention to emotional facial expressions while enhancing attention to faces with direct gaze (Parr et al., 2013) (Fig. 3D), which is a threatening gesture in macaques.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Parr et al., 2013
Preclinical studies demonstrated that exogenous intravenous and intranasal oxytocin can influence fear related responses in rodents and monkeys respectively, reducing hiding behaviour during an open field test and attentional bias towards threatening facial expressions.
“Preclinical studies demonstrated that exogenous intravenous and intranasal oxytocin can influence fear related responses in rodents and monkeys respectively, reducing hiding behaviour during an open field test and attentional bias towards threatening facial expressions (Parr et al., 2013;Rotzinger et al., 2010).”
From Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans (2018) · cites this paper as Parr et al., 2013
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Self-citationIntranasal oxytocin enhances socially-reinforced learning in rhesus monkeys
Parr, L. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00278 · Cited by 23 · see citing works
Self-citationEffects of chronic oxytocin on attention to dynamic facial expressions in infant macaques
Parr, L. A., Brooks, J. M., Jonesteller, T., Moss, S., Jordano, J. O., & Heitz, T. R. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.08.028 · Cited by 23 · see citing works
Self-citation
- Authors
- Parr, L. A., Modi, M., Siebert, E., & Young, L. J.
- Affiliations
- Emory University (US)
- Emory National Primate Research Center (US)
- Corresponding author
- Parr, Lisa A.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 38
- Issue
- 9
- Pages
- 1748-1756
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3743934
- OpenAlex
- W2168647678
- Cited by
- 124
- References
- 51
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 6 · 2023: 3 · 2022: 10 · 2021: 13 · 2020: 7 · 2019: 9 · 2018: 16 · 2017: 11 · 2016: 8 · 2015: 10 · 2014: 18 · 2013: 7
- FWCI
- 21.45
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (P51OD011132)
- U.S. Public Health Service (MHR01068791)
- National Institute of Mental Health (K02MH096084, R01MH068791)
- National Center for Research Resources (P51RR000165)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- intranasal oxytocin, rhesus monkeys, social perception, attentional bias, negative facial expressions, autism spectrum disorder, dot-probe task, gaze direction, emotional salience, oxytocinergic system, social cognition
- MeSH terms
- Administration, Intranasal, Aerosols, Animals, Attention, Emotions, Equipment Design, Facial Expression, Female, Macaca mulatta, Male, Nebulizers and Vaporizers, Oxytocin, Social Perception, Species Specificity
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