The changing face of emotion: age-related patterns of amygdala activation to salient faces

Abstract

The present study investigated age-related differences in the amygdala and other nodes of face-processing networks in response to facial expression and familiarity. fMRI data were analyzed from 31 children (3.5-8.5 years) and 14 young adults (18-33 years) who viewed pictures of familiar (mothers) and unfamiliar emotional faces. Results showed that amygdala activation for faces over a scrambled image baseline increased with age. Children, but not adults, showed greater amygdala activation to happy than angry faces; in addition, amygdala activation for angry faces increased with age. In keeping with growing evidence of a positivity bias in young children, our data suggest that children find happy faces to be more salient or meaningful than angry faces. Both children and adults showed preferential activation to mothers' over strangers' faces in a region of rostral anterior cingulate cortex associated with self-evaluation, suggesting that some nodes in frontal evaluative networks are active early in development. This study presents novel data on neural correlates of face processing in childhood and indicates that preferential amygdala activation for emotional expressions changes with age.

Fig. 1

Experimental design. (A) 16-s blocks of affective faces were alternated with 16-s blocks of phase-scrambled images. There were four types of affective faces: Happy Mother (HM), Angry Mother (AM), Happy Stranger (HS) and Angry Stranger (AS). For each face type there were five photographs rated and matched for intensity and appearance. Each block contained 16 1-second images of each face type presented in random order. (A) cartoon image appeared at random intervals and participants were instructed to press a button when they saw the cartoon. (B) Schematic of block presentation. There were three blocks of each face type for a total of 12 blocks of faces and 12 blocks of scrambled images.

Fig. 2

Amygdala ROI. (A) Example amygdala ROI in a representative participant. Yellow and orange denote masks drawn over left and right amygdala, respectively. (B) Age Group by Expression interaction: Both older (N = 17, mean age =6.9 years) and younger children (N = 14, mean age = 4.8 years) showed significantly greater activation for happy than angry faces. The y-axis shows percent signal change from the scrambled image baseline. (C) Activation for happy and angry mothers and strangers in the 2 groups of children and adults. Both groups of children show greater activation to happy than angry faces. (D) Results of voxelwise analysis of 14 adults and 14 motion-equated children (4.3–8.9 years, mean age = 6.3 years) showing the contrast happy–angry in the children.

Fig. 3

(A) Results of voxelwise analysis of 14 adults and 14 motion-matched children showing the interaction between age group and expression in a region centered on the putamen. (B) Contrast between angry and happy faces in the group of 14 adults revealing greater putamen activation for angry than happy faces at a threshold of P < 0.005. (C) Contrast between angry and happy faces in the group of 14 children revealing greater putamen activation for happy than angry faces at a threshold of P < 0.005. (D) Results of voxelwise analysis of 14 adults and 14 motion-matched children showing greater activation in anterior cingulate cortex for mothers than strangers. (E) Results of voxelwise analysis of 17 older and 14 younger children, showing greater activation in anterior cingulate cortex for mothers than strangers. (F) Results of voxelwise analysis with 14 adults and 14 motion-matched children showing greater activation in the right fusiform gyrus and inferior parietal lobule for adults than children. (G) Results of voxelwise analysis with 17 older children and 14 younger children showing greater activation in the left fusiform gyrus for younger than older children.