Developmental shift in testosterone influence on prefrontal emotion control

A paradox of testosterone effects is seen in adolescents versus adults in social emotional approach-avoidance behavior. During adolescence, high testosterone levels are associated with increased anterior prefrontal (aPFC) involvement in emotion control, whereas during adulthood this neuro-endocrine relation is reversed. Rodent work shows that, during puberty, testosterone transitions from a neuro-developmental to a social-sexual activating hormone. In this study, we explored whether this functional transition is also present in human adolescents and young adults. Using a prospective longitudinal design, we investigated the role of testosterone on neural control of social emotional behavior during the transitions from middle to late adolescence and into young adulthood. Seventy-one individuals (tested at ages 14, 17, and 20 years) performed an fMRI-adapted approach-avoidance (AA) task involving automatic and controlled actions in response to social emotional stimuli. In line with predictions from animal models, the effect of testosterone on aPFC engagement decreased between middle and late adolescence, and shifted into an activational role by young adulthood-impeding neural control of emotions. This change in testosterone function was accompanied by increased testosterone-modulated amygdala reactivity. These findings qualify the testosterone-dependent maturation of the prefrontal-amygdala circuit supporting emotion control during the transition from middle adolescence into young adulthood.

Automated summary

A paradoxical effect of testosterone is observed in social emotional behavior between adolescents and adults. While high testosterone levels are associated with increased emotion control in the prefrontal cortex during adolescence, this neuro-endocrine relationship is reversed in adulthood. This study investigated whether this functional transition also occurs in human adolescents and young adults. The findings suggest that testosterone-dependent maturation of the prefrontal-amygdala circuit supporting emotion control changes during the transition from middle adolescence into young adulthood, with a decrease in prefrontal cortex engagement and an increase in testosterone-modulated amygdala reactivity.