<p class="first" id="d10376590e214">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 (
<i>n</i> = 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.
</p><p id="d10376590e219">
<b>SIGNIFICANCE STATEMENT</b> Adolescents can show distinct behavioral problems when
emotionally aroused. This
could be related to later development of frontal regions compared with deeper brain
structures. This study found that when the control of emotional actions needs to be
exerted, more mature adolescents, similar to adults, recruit the anterior prefrontal
cortex (aPFC). Less mature adolescents recruit specific subcortical regions, namely
the pulvinar and amygdala. These findings identify the subcortical pulvino–amygdalar
pathway as a relevant precursor of a mature aPFC emotional control system, opening
the way for a neurobiological understanding of how emotion control-related disorders
emerge during puberty.
</p>