Karin Roelofs

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.

Evolutionary threats (ETs), such as predatory animals and heights, elicit stronger fear responses and are more often the subject of specific phobias, as compared to modern threats (MTs, such as guns and motorcycles). Since processing of ET depends on lower‐order, phylogenetically conserved neural fear circuits, it may be less susceptible to higher‐order (vs. simpler) cognitive emotion regulation. Given the relevance for treatment of specific phobias, we tested this hypothesis in an ERP study. Sixty‐one female participants passively watched high‐ and low‐threat pictures of evolutionary (snakes, lizards) and modern (guns, water‐guns) origin, and downregulated responses to the high‐threat pictures (snakes and guns) using either cognitive reappraisal or a simpler cognitive distraction strategy. ET elicited stronger early (EPN) and sustained (LPP) attention processing compared to MT. Both strategies successfully downregulated subjective and LPP (but not EPN) responses compared to passive watching. Although reappraisal was more effective subjectively, distraction downregulated the LPP earlier and stronger than reappraisal, irrespective of the threat type. These findings provide novel evidence that neural responses to physical threat might be less susceptible to cognitive emotion regulation via higher‐order (reappraisal) versus simpler (distraction) strategies, irrespective of the evolutionary or modern relevance of threat. Combining both strategies could be beneficial for the emotion regulation‐enhancing interventions for specific phobias. Distraction could be used during initial exposure, to reduce immediate emotion responding and help endure the contact with the feared stimulus, whereas reappraisal could be used subsequently, when emotions are less intense, to change maladaptive thoughts about the stimulus for future encounters.