Medial prefrontal and occipito-temporal activity at encoding determines enhanced recognition of threatening faces after 1.5 years

Abstract

Studies demonstrated that faces with threatening emotional expressions are better remembered than non-threatening faces. However, whether this memory advantage persists over years and which neural systems underlie such an effect remains unknown. Here, we employed an individual difference approach to examine whether the neural activity during incidental encoding was associated with differential recognition of faces with emotional expressions (angry, fearful, happy, sad and neutral) after a retention interval of > 1.5 years (N = 89). Behaviorally, we found a better recognition for threatening (angry, fearful) versus non-threatening (happy and neutral) faces after a delay of > 1.5 years, which was driven by forgetting of non-threatening faces compared with immediate recognition after encoding. Multivariate principal component analysis (PCA) on the behavioral responses further confirmed the discriminative recognition performance between threatening and non-threatening faces. A voxel-wise whole-brain analysis on the concomitantly acquired functional magnetic resonance imaging (fMRI) data during incidental encoding revealed that neural activity in bilateral inferior occipital gyrus (IOG) and ventromedial prefrontal/orbitofrontal cortex (vmPFC/OFC) was associated with the individual differences in the discriminative emotional face recognition performance measured by an innovative behavioral pattern similarity analysis (BPSA). The left fusiform face area (FFA) was additionally determined using a regionally focused analysis. Overall, the present study provides evidence that threatening facial expressions lead to persistent face recognition over periods of > 1.5 years, and that differential encoding-related activity in the medial prefrontal cortex and occipito-temporal cortex may underlie this effect.