A neural basis for difficulties in regulating behavior in emotional contexts in adolescents was tested. The findings are consistent with a neurobiological model (20
) of competition between enhanced activity in subcortical emotional processing systems and less mature top-down prefrontal systems. The ability to engage in top-down regulation of emotional centers such as the amygdala is likely to be important during adolescence in guiding behavior in highly emotional contexts. Our findings suggest elevated amygdala activity in such situations in adolescents relative to children and adults. Differences in the strength of connectivity between top-down control and bottom-up emotion processing regions may underlie individual differences in emotion regulation especially during adolescence when these bottom up systems appear to be elevated in activity. Anatomical studies of brain development have shown protracted development of prefrontal regions in terms of both local decreases in gray matter density and increases in the myelination of fibers linking prefrontal cortex to other brain regions (27
). Both local refinements and increased connectivity are likely to improve the efficiency of emotion regulation based on our findings showing that the strength of coupling between ventral prefrontal cortex and the amygdala is correlated with greater habituation of amygdala activity during adolescence. Despite the relative immaturity of prefrontal cortex during adolescence, amygdala activity decreased to near or even below baseline with repeated exposure to empty threat (fearful faces) in both adults and adolescents. These data are consistent with previous neuroimaging studies of cognitive control showing that adolescents can suppress a competing response, but must recruit prefrontal regions more than adults to do so (28
). The fact that adolescents respond more slowly to fear targets and show less prefrontal relative to amygdala activity for these trials than adults suggests that adolescents might be more susceptible to emotional interference relative to adults. Greater initial reactivity in subcortical limbic regions in adolescents relative to adults may explain why poor decisions may be made in the heat of the moment even though adolescents know better. Given the role of prefrontal regions in guiding appropriate actions, immature prefrontal activity might hinder decisions within an emotional context (i.e., heat of the moment).
Differences in the efficiency of prefrontal regulation may also explain the lower levels of vPFC activity in less anxious adults in the current study. Whereas less anxious teens showed greater vPFC activity in early versus late trials mirroring the decrease in amygdala activity, less anxious adults showed little activity in vPFC regions for fear targets. However, less anxious adults also showed rapid habituation (decrease from early to late trials) of amygdala activity to levels below baseline. Less anxious adults may be more efficient in regulating amygdala activity and, therefore require less vPFC activity.
Theories of the neurobiological basis of affective disorders emphasize the role of circuits including the amygdala and ventral prefrontal cortex(29
). The current study showed differences in the amygdala and ventral prefrontal cortex as a function of variance in trait anxiety within the normal range and these differences may be even greater in clinically anxious populations. Functional magnetic resonance imaging studies have found greater amygdala activity in response to negatively valenced information (often fearful faces) and diminished activation of ventral prefrontal cortex(16
) in clinically anxious children and adults relative to controls. We, and others(18
), have shown that less functional connectivity between amygdala and ventral prefrontal cortex is associated with higher anxiety. Functional coupling between the amygdala and ventral prefrontal cortex is influenced by emotional context (35
). This association may be especially important during adolescence when transitions from childhood to adulthood result in increased independence (separation from care-givers) and require more self-regulation of emotion.
Increased amygdala activity has been shown during initial fear conditioning in healthy controls that diminishes with extinction (37
). There is evidence for less habituation of amygdala activity (ie., diminished activity with repeated exposures to empty threat) in clinically anxious populations than in healthy controls. A recent meta-analysis of studies utilizing fear conditioning paradigms in participants with anxiety disorders revealed consistent deficits in extinction following simple fear conditioning relative to controls (39
). A similar study directly examining amygdala habituation to signals of threat (fearful faces) found a trend for less habituation in patients with PTSD compared to healthy controls (40
). These results are consistent with our data showing a correlation between amygdala habituation and trait anxiety in healthy adolescents and adults.
The current study required subjects to make a response that was in opposition to an affective signal (i.e. approach fearful expressions that are associated with threat), and to do so as fast as they could. Thus, optimal performance required emotion regulation and allowed us to examine individual and age-related differences in sensitivity to affective interference. Adolescents and children were relatively slower than adults when responding to fearful target faces suggesting that adolescents and children were less efficient at overriding affective interference compared to adults. We have now shown in two separate experiments that, in the context of a go-nogo task, mean reaction times for fearful facial expressions as targets are positively correlated with amygdala activity(25
). Ventral PFC activity was associated with both faster reaction times to fear targets and greater amygdala habituation. Together these findings suggest that ventral prefrontal regions are engaged to regulate affective processing and facilitate appropriate responses in the presence of affective interference. Prefrontal regulation may be especially important during adolescence due to increased reactivity of affective processing systems like the amygdala in response to emotional information compared to children and adults. Furthermore, adolescents must deal with dramatic changes in their social environment and interactions that may serve as stressors driving activity in hypersensitive affective systems that immature prefrontal control circuitry cannot effectively regulate. Therefore, the combination of biological susceptibility and environmental context may underlie the prevalence of affective disorder onset during adolescence.