Causal Dynamics of Social Gaze in Primate Prefrontal-Amygdala Networks Revealed by Dynamic Bayesian Modeling

Abstract

Social gaze is a fundamental channel of primate communication, shaping dynamic interactions and fostering mutual understanding. While prior studies have mapped the behavioral correlates of social gaze across the prefrontal-amygdala circuits, the causal architecture of these interactions remains poorly understood. Here, we introduce a novel algorithm to integrate independently recorded sessions into "super-sessions", validated using ground-truth synthetic data, enabling the reconstruction of simultaneous multi-area recordings aligned to matched gaze sequences. Applying Dynamic Bayesian Network analysis to these super-sessions, we uncover temporally structured, behavior-dependent causal interactions among the amygdala, orbitofrontal cortex, dorsomedial prefrontal cortex (dmPFC), and anterior cingulate cortex. When macaques were the targets of social gaze, the brain-behavior network exhibited positive temporal modulations, with the dmPFC emerging as the dominant source and the amygdala as a primary recipient of influence. When macaques directed their gaze toward their partners, the dmPFC and amygdala retained their respective roles. Prefrontal regions positively modulated one another, while the amygdala acted solely as a downstream target receiving exclusively negatively modulated prefrontal inputs. These findings reveal previously unknown directional interactions in the primate social brain and highlight distinct causal architectures underlying the bidirectional dynamics of social attention.