Human Lateral Frontal Pole Contributes to Control over Emotional Approach Avoidance Actions

Regulation of emotional behavior is essential for human social interactions. Recent work has exposed its cognitive complexity, as well as its unexpected reliance on portions of the anterior PFC (aPFC) also involved in exploration, relational reasoning, and counterfactual choice, rather than on dorsolateral and medial prefrontal areas involved in several forms of cognitive control. This study anatomically qualifies the contribution of aPFC territories to the regulation of prepotent approach-avoidance action tendencies elicited by emotional faces, and explores a possible structural pathway through which this emotional action regulation might be implemented. We provide converging evidence from task-based fMRI, diffusion-weighted imaging, and functional connectivity fingerprints for a novel neural element in emotional regulation. Task-based fMRI in human male participants (N = 40) performing an emotional approach-avoidance task identified aPFC territories involved in the regulation of action tendencies elicited by emotional faces. Connectivity fingerprints, based on diffusion-weighted imaging and rest ing-state connectivity, localized those task-defined frontal regions to the lateral frontal pole (FPI), an anatomically defined portion of the aPFC that lacks a homologous counterpart in macaque brains. Probabilistic tractography indicated that 10%-20% of interindividual variation in emotional regulation abilities is accounted for by the strength of structural connectivity between FPI and amygdala. Evidence from an independent replication sample (N = 50; 10 females) further substantiated this result. These findings provide novel neuroanatomical evidence for incorporating FPI in models of control over human action tendencies elicited by emotional faces.