Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task

Abstract

Background: Adolescence is a transition period from childhood to adulthood that is often characterized by emotional instability. This period is also a time of increased incidence of anxiety and depression, underscoring the importance of understanding biological substrates of behavioral and emotion regulation during adolescence. Developmental changes in the brain in concert with individual predispositions for anxiety might underlie the increased risk for poor outcomes reported during adolescence. We tested the hypothesis that difficulties in regulating behavior in emotional contexts in adolescents might be due to competition between heightened activity in subcortical emotional processing systems and immature top-down prefrontal systems. Individual differences in emotional reactivity might put some teens at greater risk during this sensitive transition in development.

Methods: We examined the association between emotion regulation and frontoamygdala circuitry in 60 children, adolescents, and adults with an emotional go-nogo paradigm. We went beyond examining the magnitude of neural activity and focused on neural adaptation within this circuitry across time with functional magnetic resonance imaging.

Results: Adolescents showed exaggerated amygdala activity relative to children and adults. This age-related difference decreased with repeated exposures to the stimuli, and individual differences in self-ratings of anxiety predicted the extent of adaptation or habituation in amygdala. Individuals with higher trait anxiety showed less habituation over repeated exposures. This failure to habituate was associated with less functional connectivity between ventral prefrontal cortex and amygdala.

Conclusions: These findings suggest that exaggerated emotional reactivity during adolescence might increase the need for top-down control and put individuals with less control at greater risk for poor outcomes.

Figure 1

Task Design. Shown is the temporal layout of stimulus presentations within a scan where fear expressions where the target and calm expressions were the non-targets. Stimuli were presented for 500 ms and followed by a variable ISI of 2000 – 14,500 ms.

Figure 2

Greater amygdala reactivity in adolescents. Mean amygdala activity for both target and non-target expressions was greater for adolescents than adults and children. Scatter plot shows mean MR signal in the amygala on the y-axis. The x-axis represents age in years. Age group is coded with adults as squares, adolescents as circles and children as triangles.

Figure 3

Neural correlates of reaction time for fear targets. Activity in the left amygdala was positively correlated with reaction time for fear relative to happy targets (r = .418; p< .001) while activity in the ventral prefrontal cortex vPFC was negatively correlated with reaction time (r = −.411 p< .001 a) region of the left amygdala that correlated with reaction time b) Scatter plot of the correlation between reaction time and amgdala activity. The y-axis represents the difference in reaction time between fear and happy targets as calculated by dividing the difference between mean reaction times for fear and happy by overall mean reaction time. The x-axis represents amount of activity in the amygdala for fear minus happy targets. c) region of ventral prefrontal cortex that was negatively correlated with reaction time.d) Scatter plot of the correlation between vPFC activity and reaction time. The y-axis represents the difference in reaction time between fear and happy targets as calculated by dividing the difference between mean reaction times for fear and happy by overall mean reaction time. The x-axis represents amount of activity in the vPFC for fear minus happy targets after removing the variance associated with left amygdala activity and target accuracy using linear regression. Age group is coded with adults as squares, adolescents as circles and children as triangles.

Figure 4

Amygdala habituation and trait anxiety. Trait anxiety scores were negatively correlated with habituation (decrease from early to late trials) of amygdala activity (r = −.447; p< .001) Amygdala habituation was calculated by subtracting activity in late trials from activity in early trials a) region of the left amygdala that correlated with trait anxiety. b) Scatter plot of the correlation between trait anxiety and amygdala habituation. The y-axis represents MR Signal in the left amygdala for early minus late trials. The x-axis represents trait anxiety score.

Figure 5

Ventral prefrontal – amygdala connectivity and habituation. There was negative functional connectivity between the amygdala and the vPFC. The magnitude of activity in vPFC and the strength of the connectivity between vPFC and the amygdala were negatively correlated with amygdala habituation (r = −.559 p< .001). Amygdala habituation was calculated by subtracting activity in late trials from activity in early trials.a) shows the conjunction analysis for a vPFC region displaying a significant interaction between age group, emotion, trial, and anxiety and where stronger functional connectivity predicted greater amygdala habituation d) Scatterplot of vPFC-amygdala connectivity values versus amygdala habituation. The y-axis represents MR Signal in the leftamygdala for early minus late trials. The x-axis represents z-scored vPFC-amygdala connectivity values.