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Sex Differences in Neural Responses to the Perception of Social Interactions

ABSTRACT: Social interaction is critical to emotional well-being. Previous studies have suggested sex differences in the perception of social interaction. However, the findings depend on the nature of interactions and whether it involves facial emotions. Here, we explored sex differences in neural responses to the perception of social interaction using the Human Connectome Project data. Participants (n = 969, 505 women) were engaged in a social cognition task with geometric objects moving and colliding to simulate social interaction. Behaviorally, men relative to women demonstrated higher accuracy in perceiving social vs. random interactions. Men vs. women showed higher activation in the right superior temporal gyrus, bilateral occipital and posterior cingulate cortex and precuneus, and women vs. men showed higher activation in the right inferior frontal cortex, during exposure to social vs. random interactions. In whole-brain regressions, the differences in accuracy rate in identifying social vs. random interactions (ARSOC – ARRAN) were associated with higher activation in the paracentral lobule (PCL) and lower activation in bilateral anterior insula (AI), pre-supplementary motor area (preSMA), and left middle frontal gyrus (MFG) in men and women combined, lower activation in bilateral AI, preSMA and left MFG in men alone, and higher activation in the PCL and the medial orbitofrontal cortex in women alone. The latter sex differences were confirmed by slope tests. Further, the PCL activity mediated the correlation between an internalizing syndromal score, as assessed by the Achenbach Self-Report, and (ARSOC – ARRAN) across all subjects. These findings highlighted sex differences in the behavioral and neural processes underlying the perception of social interaction, as well as the influence of internalizing traits on these processes.

SUBMITTER: Li G

PROVIDER: S-EPMC7518190 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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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.

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Sex Differences in Neural Responses to the Perception of Social Interactions

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