Endogenous Testosterone Modulates Prefrontal-Amygdala Connectivity during Social Emotional Behavior

It is clear that the steroid hormone testosterone plays an important role in the regulation of social emotional behavior, but it remains unknown which neural circuits mediate these hormonal influences in humans. We investigated the modulatory effects of endogenous testosterone on the control of social emotional behavior by applying functional magnetic resonance imaging while healthy male participants performed a social approach-avoidance task. This task operationalized social emotional behavior by having participants approach and avoid emotional faces by pulling and pushing a joystick, respectively. Affect-congruent trials mapped the automatic tendency to approach happy faces and avoid angry faces. Affect-incongruent trials required participants to override those automatic action tendencies and select the opposite response (approach-angry, avoid-happy). The social emotional control required by affect-incongruent responses resulted in longer reaction times (RTs) and increased activity at the border of the ventrolateral prefrontal cortex and frontal pole (VLPFC/FP). We show that endogenous testosterone modulates these cerebral congruency effects through 2 mechanisms. First, participants with lower testosterone levels generate larger VLPFC/FP responses during affect-incongruent trials. Second, during the same trials, endogenous testosterone modulates the effective connectivity between the VLPFC/FP and the amygdala. These results indicate that endogenous testosterone influences local prefrontal activity and interregional connectivity supporting the control of social emotional behavior.