Intranasal oxytocin modulates neural functional connectivity during human social interaction

• Authors: James K Rilling, Emory University; Xiangchuan Chen, Emory University; Xu Chen, Emory University; Ebrahim Haroon, Emory University
• Journal Title: American Journal of Primatology
• Volume: Volume 80, Number 10
• Publisher: Wiley: 12 months | 2018-10-01, Pages e22740-e22740
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1002/ajp.22740
• Subjects: Biology, Neuroscience; Anthropology, Medical and Forensic; Psychology, Behavioral
• Keywords: Science & Technology; Life Sciences & Biomedicine; Zoology; fMRI; functional connectivity; network; oxytocin; sex differences; MALE PRAIRIE VOLES; HUMAN CEREBRAL-CORTEX; PAIR BOND FORMATION; ANXIETY DISORDER; SEX-DIFFERENCES; MICROTUS-OCHROGASTER; CALLICEBUS-CUPREUS; EMOTIONAL STIMULI; NONHUMAN PRIMATE; DECISION-MAKING

Abstract

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.