Neural network dynamics underlying the bottom-up perception and top-down regulation processes of empathy

Contemporary theoretical models of empathy propose that it involves both bottom-up perception and top-down regulation processes. Although previous studies have explored brain regions involved in empathy, direct evidence for a hierarchical organization in empathy processing remains limited. In this functional magnetic resonance imaging study, we sought to address this gap by using positive, negative, and neutral stimuli to explore whether shared or valence-specific processing underlies positive and negative empathy. Our results indicate that the bottom-up perception process involves the bilateral triangular part of the inferior frontal gyrus (IFGtri) and the superior temporal sulcus (STS), with the IFGtri initiating information flow to the STS. Moreover, while bilateral IFGtri only shows excitatory effects on bilateral STS, bilateral STS only shows inhibitory effects on bilateral IFGtri. The right IFGtri appears to be more involved in external information processing, whereas the left IFGtri focuses more on internal information communication. The top-down regulation process involves information flow from the left dorsolateral superior frontal gyrus (dlSFG) to the medial prefrontal gyrus (mPFC), and then to the precuneus. Moreover, positive stimuli show an inhibitory effect from dlSFG to mPFC and from mPFC to precuneus, whereas negative stimuli only inhibit the flow from mPFC to precuneus. This finding suggests that more regulatory neural mechanisms occur to others' positive emotions than negative ones. In conclusion, our study provides direct evidence of a hierarchical neural network supporting theoretical models of empathy, offering novel insights into how bottom-up perception and top-down regulation processes are instantiated in the brain.