Functional brain activation to emotional and nonemotional faces in healthy children: evidence for developmentally undifferentiated amygdala function during the school-age period

Abstract

The amygdala is a key region in emotion processing. In particular, fMRI studies have demonstrated that the amygdala is active during the viewing of emotional faces. Previous research has consistently found greater amygdala responses to fearful than to neutral faces in adults, convergent with a focus in the animal literature on the amygdala's role in fear processing. Studies have shown that the amygdala also responds differentially to other facial emotion types in adults. Yet the literature regarding when this differential amygdala responsivity develops is limited and mixed. Thus, the goal of the present study was to examine amygdala responses to emotional and neutral faces in a relatively large sample of healthy school-age children (N = 52). Although the amygdala was active in response to emotional and neutral faces, the results did not support the hypothesis that the amygdala responds differentially to emotional faces in 7- to 12-year-old children. Nonetheless, amygdala activity was correlated with the severity of subclinical depression symptoms and with emotional regulation skills. Additionally, sex differences were observed in frontal, temporal, and visual regions, as well as effects of pubertal development in visual regions. These findings suggest important differences in amygdala reactivity in childhood.

Figure 1. Functionally and anatomically defined amygdala ROIs

A) Functionally defined amygdala ROIs isolated from the whole-brain main effect of time B) Anatomically defined amygdala ROIs isolated by FreeSurfer segmentation. Heat map values indicate the number of participants with overlapping ROIs at each voxel. C) Timecourses (average of all face types) for left and right anatomically defined ROIs with 95% confidence intervals. * = significant difference from zero at a given timepoint (p < 0.05)

Figure 2. Brain regions showing a main effect of time (timepoint within trial)

Surface renderings of the thresholded main effect of time from the whole-brain ANOVA results. The color scale indicates z-score values.

Figure 3. Example timecourses in brain regions showing three different types of interactions between sex and time

Lines indicate average timecourses for each sex. A) Fusiform gyrus shows greater activity in females than males (F>M,act). B) Precuneus shows deactivation in females and no significant effect of time in males (F>M deact; M:ns). C) Putamen shows activation in males and no significant effect of time in females (M>F act; F:ns).

Figure 4. Timecourse for inferior frontal gyrus region showing emotion × sex × time interaction

A) Surface rendering of region showing emotion × sex × time interaction. Color scale represents z-score values from whole-brain ANOVA. B) Lines indicate average timecourse for happy and fearful face trials (the only emotion types showing sex × time interaction, F and p-values indicated) split by sex.

Figure 5. Brain regions showing interactions with pubertal status

Colors indicate interaction type. Inset shows ventral posterior right hemisphere to highlight region of greatest overlap. Red: puberty × time; Green: puberty × sex × time; Blue: emotion × puberty × time; Yellow: overlap of puberty × sex × time and puberty × time; Purple: overlap of emotion × puberty × time and puberty × time; Pink: overlap between all three contrasts