Remembering unexpected beauty: Contributions of the ventral striatum to the processing of reward prediction errors regarding the facial attractiveness in face memory

Abstract

The COVID-19 pandemic has led people to predict facial attractiveness from partially covered faces. Differences in the predicted and observed facial attractiveness (i.e., masked and unmasked faces, respectively) are defined as reward prediction error (RPE) in a social context. Cognitive neuroscience studies have elucidated the neural mechanisms underlying RPE-induced memory improvements in terms of monetary rewards. However, little is known about the mechanisms underlying RPE-induced memory modulation in terms of social rewards. To elucidate this, the present functional magnetic resonance imaging (fMRI) study investigated activity and functional connectivity during face encoding. In encoding trials, participants rated the predicted attractiveness of faces covered except for around the eyes (prediction phase) and then rated the observed attractiveness of these faces without any cover (outcome phase). The difference in ratings between these phases was defined as RPE in facial attractiveness, and RPE was categorized into positive RPE (increased RPE from the prediction to outcome phases), negative RPE (decreased RPE from the prediction to outcome phases), and non-RPE (no difference in RPE between the prediction and outcome phases). During retrieval, participants were presented with individual faces that had been seen and unseen in the encoding trials, and were required to judge whether or not each face had been seen in the encoding trials. Univariate activity in the ventral striatum (VS) exhibited a linear increase with increased RPE in facial attractiveness. In the multivariate pattern analysis (MVPA), activity patterns in the VS and surrounding areas (extended VS) significantly discriminated between positive/negative RPE and non-RPE. In the functional connectivity analysis, significant functional connectivity between the extended VS and the hippocampus was observed most frequently in positive RPE. Memory improvements by face-based RPE could be involved in functional networks between the extended VS (representing RPE) and the hippocampus, and the interaction could be modulated by RPE values in a social context.