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Within vs. between-subject effects of intranasal oxytocin on the neural response to cooperative and non-cooperative social interactions.

ABSTRACT: The neuropeptide oxytocin (OT) plays a critical role in modulating social behavior across a wide range of vertebrate species. In humans, intranasal oxytocin (INOT) has been shown to modulate various aspects of social behavior, such as empathy, trust, in-group preference, and memory of socially relevant cues. Most INOT studies employ cross-sectional designs despite the enhanced statistical power and reduction in error variance associated with individual differences characteristic of within-subject designs. Using the Prisoner Dilemma task, which models a real-life dyadic social interaction, our group has systematically explored the effect of INOT on social cooperation and non-cooperation using a cross-sectional design. In the current study, we investigated if the main findings from our cross-sectional study could be replicated in a within-subject design using the same paradigm and whether new findings would emerge. We found OT to attenuate the ventral tegmental area response to reciprocated cooperation in women, an effect that is also present in our cross-sectional sample. However, other cross-sectional findings, especially those found in men, were not observed in this within-subject study. We hypothesize that the discrepancy can be explained by differing OT effects based on the degree of stimulus novelty/familiarity. Our within-subject study also revealed new effects not found previously in our cross-sectional study. Most importantly, OT treatment on scan 2 blocked amygdala habituation to unreciprocated cooperation found in a group that received placebo on both scans among men. Our results suggest that exogenous OT reduces the salience of positive social interactions among women and prevents habituation to negative social interactions among men. These findings may have implications for the potential clinical utility of OT as a treatment for psychiatric disorders.

SUBMITTER: Chen X

PROVIDER: S-EPMC5362337 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Within vs. between-subject effects of intranasal oxytocin on the neural response to cooperative and non-cooperative social interactions.

Chen Xu X Gautam Pritam P Haroon Ebrahim E Rilling James K JK

Psychoneuroendocrinology 20170116

The neuropeptide oxytocin (OT) plays a critical role in modulating social behavior across a wide range of vertebrate species. In humans, intranasal oxytocin (INOT) has been shown to modulate various aspects of social behavior, such as empathy, trust, in-group preference, and memory of socially relevant cues. Most INOT studies employ cross-sectional designs despite the enhanced statistical power and reduction in error variance associated with individual differences characteristic of within-subjec ...[more]

PMID: 28142074

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Project description:Both oxytocin (OT) and vasopressin (AVP) are known to modulate social behavior, and dysfunction in both systems has been postulated as a potential cause of certain psychiatric disorders that involve social behavioral deficits. In particular, there is growing interest in intranasal OT as a potential treatment for certain psychiatric disorders, and preliminary pre-clinical and clinical studies suggest efficacy in alleviating some of the associated symptoms. However, the vast majority of research participants in these studies have been male, and there is evidence for sexually differentiated effects of nonapeptides in both humans and non-human animals. To date, no study has investigated the effect of intranasal OT on brain function in human males and females within the same paradigm. Previously, in a randomized, placebo-controlled, double-blind fMRI study, we reported effects of intranasal OT and AVP on behavior and brain activity of human males as they played an interactive social game known as the Prisoner's Dilemma Game. Here, we present findings from an identical study in human females, and compare these with our findings from males. Overall, we find that both behavioral and neural responses to intranasal OT and AVP are highly sexually differentiated. In women, AVP increased conciliatory behavior, and both OT and AVP caused women to treat computer partners more like humans. In men, AVP increased reciprocation of cooperation from both human and computer partners. However, no specific drug effects on behavior were shared between men and women. During cooperative interactions, both OT and AVP increased brain activity in men within areas rich in OT and AVP receptors and in areas playing a key role in reward, social bonding, arousal and memory (e.g., the striatum, basal forebrain, insula, amygdala and hippocampus), whereas OT and AVP either had no effect or in some cases actually decreased brain activity in these regions in women. OT treatment rendered neural responses of males more similar to responses of females in the placebo group and vice versa, raising the prospect of an inverted u-shaped dose response to central OT levels. These findings emphasize the need to fully characterize the effects of intranasal OT and AVP in both males and females and at multiple doses before widespread clinical application will be warranted.

Dataset Information

Within vs. between-subject effects of intranasal oxytocin on the neural response to cooperative and non-cooperative social interactions.

Publications

Within vs. between-subject effects of intranasal oxytocin on the neural response to cooperative and non-cooperative social interactions.

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