Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex

Abstract

Increased limbic and striatal activation in adolescence has been attributed to a relative delay in the maturation of prefrontal areas, resulting in the increase of impulsive reward-seeking behaviors that are often observed during puberty. However, it remains unclear whether and how this general developmental pattern applies to the control of social emotional actions, a fundamental adult skill refined during adolescence. This domain of control pertains to decisions involving emotional responses. When faced with a social emotional challenge (e.g., an angry face), we can follow automatic response tendencies and avoid the challenge or exert control over those tendencies by selecting an alternative action. Using an fMRI-adapted social approach-avoidance task, this study identifies how the neural regulation of emotional action control changes as a function of human pubertal development in 14-year-old adolescents (n ϭ 47). Pubertal maturation, indexed by testosterone levels, shifted neural regulation of emotional actions from the pulvinar nucleus of the thalamus and the amygdala to the anterior prefrontal cortex (aPFC). Adolescents with more advanced pubertal maturation showed greater aPFC activity when controlling their emotional action tendencies, reproducing the same pattern consistently observed in adults. In contrast, adolescents of the same age, but with less advanced pubertal maturation, showed greater pulvinar and amygdala activity when exerting similarly effective emotional control. These findings qualify how, in the domain of social emotional actions, executive control shifts from subcortical to prefrontal structures during pubertal development. The pulvinar and the amygdala are suggested as the ontogenetic precursors of the mature control system centered on the anterior prefrontal cortex.

Puberty and structural brain development in humans

“…As previously alluded to, timing and tempo of pubertal maturation has been linked with various psychological outcomes, including internalizing behaviors (Mendle, Leve et al 2014) and depression (Angold, Costello et al 1998, Angold, Costello et al 1999). Additional evidence for this idea stems from functional MRI studies linking pubertal development and sex steroids to emotional and social processing (Pfeifer, Kahn et al 2013, Spielberg, Olino et al 2014, Pagliaccio, Luby et al 2015, Spielberg, Forbes et al 2015), emotional-cognitive interactions (Cservenka, Stroup et al 2015, Tyborowska, Volman et al 2016), and risk and reward processing (Op de Macks, Gunther Moor et al 2011, Braams, van Duijvenvoorde et al. 2015, LeMoult, Colich et al 2015).…”

Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?

“…Increased neural capacity to represent rules of the task and multiple actions may drive age related increases in task performance. A recent study by Tyborowska et al (2016) was able to further parse the role of testosterone levels in 14 year-old adolescents’ ability to avoid impulsive actions in an emotional approach-avoidance task. Higher testosterone levels were associated with greater control over emotional actions and increased recruitment of the anterior prefrontal cortex.…”

Animal to human translational paradigms relevant for approach avoidance conflict decision making

“…Please refer to related reviews in this regard (e.g., Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & Van Ijzendoorn, 2007). However, it is interesting to note that research with such tasks implicates the lateral anterior PFC in overriding automatic responses to emotionally laden stimuli (Tyborowska, Volman, Smeekens, Toni, & Roelofs, 2016; Volman, Roelofs, Koch, Verhagen, & Toni, 2011; Volman et al, 2013). Other translational paradigms, although not directly tapping into approach-avoidance conflict, are relevant for our understanding of conflict and anxious avoidance and lend themselves well to multiple methodological approaches.…”