Representational geometry of emotional empathy in the ventromedial prefrontal cortex and in the mid-posterior insula

Abstract Facial expressions provide rapid and informative cues about others’ emotional and mental states, playing a critical role in social interactions. However, whether distinct emotional expressions reflect discrete neural processes or arise from varying combinations of underlying affective dimensions such as arousal and valence remains a subject of investigation. Crucially, these accounts need not be mutually exclusive: different brain regions may encode emotional expressions along both categorical and dimensional axes to varying degrees. To test this hypothesis, we probed different brain systems involved in emotion recognition - the ventral attentional network and the cortical limbic system centered on the ventromedial prefrontal cortex (vmPFC) - to investigate the extent to which these networks and their subregions encode emotional facial expressions in terms of (1) perceived arousal, (2) arousal+valence, or (3) six discrete emotion categories (anger, disgust, fear, happiness, pain, sadness). To this aim, we modelled the fMRI signal from perceiving movies of facial emotional expressions with ratings for either arousal, arousal+valence or emotion category using representational similarity analysis (RSA) - a method that aims at assessing which ratings model better represents how the perception of facial expressions is reflected by the fMRI parameter estimates across all the voxels within a brain region. This analysis showed that regions in the vmPFC network, including the subgenual cingulate and the medial OFC, are sensitive to ratings for distinct emotion category and for arousal+valence - significantly more so for the former - while they fail to show sensitivity for arousal ratings alone. In the ventral attentional network, the mid-posterior insula showed a similar profile, while the most posterior and ventral insular show evidence of encoding arousal+valence, but not for emotion category or arousal alone. Our findings support the idea that the vmPFC and the mid-posterior insula play a role in encoding emotion-specific and valence representations beyond general arousal processing. These results contribute to understanding how integrative brain regions support emotional empathy and social cognition.