Intranasal oxytocin modulates neural functional connectivity during human social interaction
Open accessAbstract
Oxytocin (OT) modulates social behavior in primates and many other vertebrate species. Studies in non‐primate animals have demonstrated that, in addition to influencing activity within individual brain areas, OT influences functional connectivity across networks of areas involved in social behavior. Previously, we used fMRI to image brain function in human subjects during a dyadic social interaction task following administration of either intranasal oxytocin (INOT) or placebo, and analyzed the data with a standard general linear model. Here, we conduct an extensive re‐analysis of these data to explore how OT modulates functional connectivity across a neural network that animal studies implicate in social behavior. OT induced widespread increases in functional connectivity in response to positive social interactions among men and widespread decreases in functional connectivity in response to negative social interactions among women. Nucleus basalis of Meynert, an important regulator of selective attention and motivation with a particularly high density of OT receptors, had the largest number of OT‐modulated connections. Regions known to receive mesolimbic dopamine projections such as the nucleus accumbens and lateral septum were also hubs for OT effects on functional connectivity. Our results suggest that the neural mechanism by which OT influences primate social cognition may include changes in patterns of activity across neural networks that regulate social behavior in other animals.
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No effects of intranasal OXT treatment were observed in women when they were not cooperating.
“Conversely, no effects of intranasal OXT treatment were observed in women when they were not cooperating.”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Rilling et al., 2018
Results §3.1 reports no effect on individual-region activation in women for CD outcomes, but Results §3.2 reports 19 oxytocin-modulated functional connections in women for those outcomes. Methods §2.3 defines CD as the woman cooperating while her partner defects, so it does not describe women themselves not cooperating. The paper therefore does not support the unqualified claim of no effects. (LLM, conf=0.85)
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Experimental — accuracy not yet measuredIntranasal OXT treatment had no discernible impact on brain activity in men when they were cooperating.
“However, intranasal OXT treatment had no discernible impact on brain activity in men when they were cooperating.”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Rilling et al., 2018
Results §3.1 reports no effect of oxytocin on activation in any individual region in men following reciprocated cooperation (CC outcomes). But Results §3.2 reports that oxytocin altered 23 functional connections in men following those outcomes, so the broader claim of no discernible impact on brain activity overstates the finding. Page numbers were not available in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIntraperitoneal OXT injection significantly influenced trial outcomes, leading to a decrease in defection and an increase in cooperation.
“Notably, an intraperitoneal OXT injection significantly influenced the trial outcomes, leading to a decrease in defection and an increase in cooperation (Donovan et al., 2020), a pattern similar to what has been observed in humans (Rilling et al., 2018).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Rilling et al., 2018
The Introduction reports that intranasal oxytocin has been associated with trust and cooperation in humans, supporting the broad comparison. But this paper’s Discussion reports sex-dependent neural responses to cooperation and defection outcomes, not a demonstrated decrease in defection and increase in cooperation in its participants. Its human treatment was intranasal, not intraperitoneal. (LLM, conf=0.84)
Experimental — accuracy not yet measuredReduced AMY and VTA activation after a non-cooperative outcome was found in men.
“In addition, reduced AMY and VTA activation after a non-cooperative outcome was found in this group (Rilling et al., 2018).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Rilling et al., 2018
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- Chen X Hackett PD DeMarco AC Feng C Stair S Haroon E … Rilling JK 2016 Effects of oxytocin and vasopressin on the neural response to unreciprocated cooperation within brain regions involved in stress and anxiety in men and women Brain Imaging Behav 10 2 581 593 10.1007/s11682-015-9411-7 26040978 PMC4670292 · DOI · Paper page
- Feng C Hackett PD DeMarco AC Chen X Stair S Haroon E … Rilling JK 2015 Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans Brain Imaging Behav 9 4 754 764 10.1007/s11682-014-9333-9 25416642 · DOI · Paper page
- Mai Jurgen K Paxinos George Voss Thomas 2008 Atlas of the Human Brain 3 Boston Elsevier
Cited by
Sorted by citations
Waller, R. E., & Wagner, N. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.005 · Cited by 138 · see citing works
Sex-dependent regulation of social reward by oxytocin: an inverted U hypothesis
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Self-citationNeurobiology of Loneliness, Isolation, and Loss: Integrating Human and Animal Perspectives
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“Notably, an intraperitoneal OXT injection significantly influenced the trial outcomes, leading to a decrease in defection and an increase in cooperation (Donovan et al., 2020), a pattern similar to what has been observed in humans (Rilling et al., 2018).”
BackgroundResultOxytocin Modulates the Intrinsic Dynamics Between Attention-Related Large-Scale Networks
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- Authors
- Rilling, J. K., Chen, X., Chen, X., & Haroon, E.
- Affiliations
- Emory University (US)
- Corresponding author
- Rilling, James K.
- Venue
- American Journal of Primatology
- Publisher
- Wiley
- Published
- 2018-02-10
- Volume
- 80
- Issue
- 10
- Pages
- e22740-e22740
- ISSN
- 0275-2565 (ISSN-L)
- 1098-2345
- PMC
- PMC6086772
- OpenAlex
- W2789734967
- Cited by
- 40
- References
- 79
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 7 · 2023: 3 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 5 · 2018: 5
- FWCI
- 5.75
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Primatology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (MH084068)
- National Institutes of Health (UL1TR000454377)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- intranasal oxytocin, functional connectivity, social interaction, dyadic interaction, nucleus basalis of Meynert, nucleus accumbens, lateral septum, mesolimbic dopamine system, social cognition, sex differences, artificial neural networks, primate social behavior
- MeSH terms
- Prisoner Dilemma, Administration, Intranasal, Adolescent, Brain, Female, Humans, Interpersonal Relations, Male, Oxytocin, Sex Factors, Young Adult, Functional Neuroimaging
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