Oxytocin blunts social vigilance in the rhesus macaque
Open accessAbstract
Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.
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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 [70]
When administered intranasally, OT increases the time that rhesus monkeys spend viewing the eyes of conspecifics in static images.
“When administered intranasally, OT increases the time that rhesus monkeys spend viewing the eyes of conspecifics in static images (Dal Monte et al., 2014a; Ebitz et al., 2013) and communicative gesturing in rhesus infants (Simpson et al., 2014).”
From Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys (2016) · cites this paper as Ebitz 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 [79]
Acute OXT aerosol in male monkeys reduced social vigilance for unfamiliar dominant faces.
“acute OXT aerosol in male monkeys reduced social vigilance for unfamiliar dominant faces (Ebitz et al, 2013).”
From Chronic and acute intranasal oxytocin produce divergent social effects in mice (2014) · cites this paper as Ebitz et al, 2013
Reducing social vigilance state could free up cognitive resources and promote social exploration.
“Reducing social vigilance state in turn could free up cognitive resources and promote social exploration (Ebitz et al., 2013).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
OT substantially attenuates species-typical distraction by the peripheral flash of images of unfamiliar monkey faces, indexed by a reduction in gaze deflection towards them.
“Moreover, OT substantially attenuates species-typical distraction by the peripheral flash of images of unfamiliar monkey faces, indexed by a reduction in gaze deflection towards them (Fig. 3C).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
OT helps regulate species-typical social vigilance.
“These findings endorse the idea that OT helps regulate species-typical social vigilance.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
OT selectively reduces species-typical tendencies to view the faces of dominant monkeys, a threatening but highly informative stimulus, in male rhesus macaques.
“When monkeys choose whether to acquire different types of visual information about the local social context (viewing different social images), OT selectively reduces species-typical tendencies to view the faces of dominant monkeys, a threatening but highly informative stimulus (Fig. 3A).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
Inhaled OT eliminates the privileged processing for dominant faces over other images, effectively slowing monkeys down when making this particular decision.
“Inhaled OT also eliminates the privileged processing for dominant faces over other images, effectively slowing monkeys down when making this particular decision (Fig. 3B).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
Reduced vigilance might play a permissive role in social approach behavior, favoring increased attention to faces and eyes and subsequent enhancements in social cognition.
“Based on these results, we conjecture that reduced vigilance might play a permissive role in social approach behavior, favoring increased attention to faces and eyes and subsequent enhancements in social cognition.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
OT may facilitate social interactions by lowering social vigilance and reducing social stress.
“Taken together, these findings suggest that OT may facilitate social interactions by lowering social vigilance and reducing social stress (Carter, 1998; Chang et al., 2013b; Ebitz et al., 2013; Neumann et al., 2000b; Uvnäs-Moberg et al., 1994).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Ebitz et al., 2013
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Bradley, E. R., Seitz, A., Niles, A. N., Rankin, K. P., Mathalon, D. H., O'Donovan, A., & Woolley, J. D. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.07.039 · Cited by 22 · see citing works
- Authors
- Ebitz, R. B., Watson, K. K., & Platt, M. L.
- Affiliations
- Duke University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-06-24
- Volume
- 110
- Issue
- 28
- Pages
- 11630-11635
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3710816
- OpenAlex
- W2028239280
- Cited by
- 132
- References
- 55
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 7 · 2023: 6 · 2022: 10 · 2021: 8 · 2020: 4 · 2019: 10 · 2018: 18 · 2017: 15 · 2016: 9 · 2015: 12 · 2014: 17 · 2013: 7 · 2012: 1
- FWCI
- 22.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH086712, R01MH086712, R01MH089484, R01MH096875, R01MH095894)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- oxytocin, social vigilance, rhesus monkeys, prosocial behavior, social attention, face attention, emotional facial expressions, social danger
- MeSH terms
- Animals, Behavior, Animal, Macaca mulatta, Oxytocin, Saccades, Social Behavior
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