Functional selectivity for naturalistic social interaction perception in the human superior temporal sulcus

Abstract

Recognizing others social interactions is a crucial human ability. Using simple stimuli, previous studies have shown that social interactions are selectively processed in the superior temporal sulcus (STS), but prior work with movies has suggested that social interactions are processed in the medial prefrontal cortex (mPFC), part of the theory of mind network. It remains unknown to what extent social interaction selectivity is observed in real world stimuli when controlling for other covarying perceptual and social information, such as faces, voices, and theory of mind. The current study utilizes a functional magnetic resonance imaging (fMRI) movie paradigm and advanced machine learning methods to uncover the brain mechanisms uniquely underlying naturalistic social interaction perception. We analyzed two publicly available fMRI datasets, collected while both male and female human participants (n = 17 and 18) watched two different commercial movies in the MRI scanner. By performing voxel-wise encoding and variance partitioning analyses, we found that broad social-affective features predict neural responses in social brain regions, including the STS and mPFC. However, only the STS showed robust and unique selectivity specifically to social interactions, independent from other covarying features. This selectivity was observed across two separate fMRI datasets. These findings suggest that naturalistic social interaction perception recruits dedicated neural circuity in the STS, separate from the theory of mind network, and is a critical dimension of human social understanding. Significance StatementSocial interaction perception guides our daily behavior, yet it is unknown how our brain processes real-world social interaction scenes. Here, we demonstrate that social brain areas, including the superior temporal sulcus (STS) and medial prefrontal cortex (mPFC), are sensitive to broad social-affective information in naturalistic movies, replicating prior results with controlled paradigms. We show for the first time however, that the STS, but not mPFC, selectively processes social interactions in natural movies, independent of other co-occurring perceptual and social features, including motion, presence of faces, speech, and mentalizing about others. Our results suggest that social interaction perception is a crucial dimension of social understanding represented in the human brain.