Age‐related changes in amygdala–frontal connectivity during emotional face processing from childhood into young adulthood

Abstract

The ability to process and respond to emotional facial expressions is a critical skill for healthy social and emotional development. There has been growing interest in understanding the neural circuitry underlying development of emotional processing, with previous research implicating functional connectivity between amygdala and frontal regions. However, existing work has focused on threatening emotional faces, raising questions regarding the extent to which these developmental patterns are specific to threat or to emotional face processing more broadly. In the current study, we examined age-related changes in brain activity and amygdala functional connectivity during an fMRI emotional face matching task (including angry, fearful and happy faces) in 61 healthy subjects aged 7–25 years. We found age-related decreases in ventral medial prefrontal cortex (vmPFC) activity in response to happy faces but not to angry or fearful faces, and an age-related change (shifting from positive to negative correlation) in amygdala-anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC) functional connectivity to all emotional faces. Specifically, positive correlations between amygdala and ACC/mPFC in children changed to negative correlations in adults, which may suggest early emergence of bottom-up amygdala excitatory signaling to ACC/mPFC in children and later development of top-down inhibitory control of ACC/mPFC over amygdala in adults. Age-related changes in amygdala-ACC/mPFC connectivity did not vary for processing of different facial emotions, suggesting changes in amygdala-ACC/mPFC connectivity may underlie development of broad emotional processing, rather than threat-specific processing.

A dimensional approach to determine common and specific neurofunctional markers for depression and social anxiety during emotional face processing

“…In the present sample of healthy subjects, increased GP and PUT reactivity towards negative faces was found to be positively associated with both depression and social anxiety symptoms. This is consistent with previous meta-analyses on depression and social anxiety disorders showing increased reactivity in these regions during emotional face processing (Binelli et al, 2014;Delvecchio et al, 2012;Gee et al, 2013;Kanske and Kotz, 2011a,b;MacQueen, 2012;Wu et al, 2016).…”

“…In the present sample of healthy subjects, increased GP and PUT reactivity towards negative faces was found to be positively associated with both depression and social anxiety symptoms. This is consistent with previous meta‐analyses on depression and social anxiety disorders showing increased reactivity in these regions during emotional face processing (Binelli et al, ; Delvecchio et al, ; Gee et al, ; Kanske and Kotz, ; MacQueen, ; Wu et al, ). As core regions of the dorsal striatum and the basal ganglia, both GP and PUT, are not only involved in motor functions, but also play important roles in other domains, such as emotional regulation (Frank et al, ; Sztainberg, Kuperman, Justice, & Chen, ), salience processing (Gentili et al, ; Menon, ; Smith, Berridge, & Aldridge, ) and social‐cognitive functions (MacQueen, ).…”

Altered Development of Amygdala-Anterior Cingulate Cortex Connectivity in Anxious Youth and Young Adults

“…Adult participants and parents of children under the age of 18 provided written informed consent and verbal assent was obtained from minors. We previously reported on typical age-related changes in brain activation and amygdala connectivity during emotional face processing in this sample of healthy volunteers (23) and on neural processing of emotional faces in separate studies of anxious youth (18) and young adults (24; 25). In this paper, we extend this work by combining pediatric and adult samples to examine age-related changes in amygdala connectivity in anxiety.…”

The developing amygdala: a student of the world and a teacher of the cortex

“…Unlike in the adult, these regulatory influences from the medial PFC are not available to the young child. Several studies have now shown that functional connections between the amygdala and the medial PFC are immature in childhood[30, 32, 55]and switch to the adult-like state in adolescence (Fig 2, bottom)[29, 56–59]. That is, during childhood the amygdala is less likely to be regulated by the mPFC than after childhood.…”