Neural circuitry of emotional face processing in autism spectrum disorders

Abstract

Background: Autism spectrum disorders (ASD) are associated with severe impairments in social functioning. Because faces provide nonverbal cues that support social interactions, many studies of ASD have examined neural structures that process faces, including the amygdala, ventromedial prefrontal cortex and superior and middle temporal gyri. However, increases or decreases in activation are often contingent on the cognitive task. Specifically, the cognitive domain of attention influences group differences in brain activation. We investigated brain function abnormalities in participants with ASD using a task that monitored attention bias to emotional faces.

Methods: Twenty-four participants (12 with ASD, 12 controls) completed a functional magnetic resonance imaging study while performing an attention cuing task with emotional (happy, sad, angry) and neutral faces.

Results: In response to emotional faces, those in the ASD group showed greater right amygdala activation than those in the control group. A preliminary psychophysiological connectivity analysis showed that ASD participants had stronger positive right amygdala and ventromedial prefrontal cortex coupling and weaker positive right amygdala and temporal lobe coupling than controls. There were no group differences in the behavioural measure of attention bias to the emotional faces.

Limitations: The small sample size may have affected our ability to detect additional group differences.

Conclusion: When attention bias to emotional faces was equivalent between ASD and control groups, ASD was associated with greater amygdala activation. Preliminary analyses showed that ASD participants had stronger connectivity between the amygdala ventromedial prefrontal cortex (a network implicated in emotional modulation) and weaker connectivity between the amygdala and temporal lobe (a pathway involved in the identification of facial expressions, although areas of group differences were generally in a more anterior region of the temporal lobe than what is typically reported for emotional face processing). These alterations in connectivity are consistent with emotion and face processing disturbances in ASD.

Fig. 1

The visual task presented to the autism spectrum disorder (ASD) and control participants. The columns on the far left and right show the screens that participants saw for the 2 trial types with happy faces. In the left column, the happy face and probe are presented on different sides of the screen (incongruent). In the right column, the happy face and probe are presented on the same side of the screen (congruent). Participants also viewed sad–neutral, angry–neutral and neutral–neutral trials.

Fig. 2

Right amygdala activation in the autism spectrum disorder (ASD) and control groups. (A) In the comparison of happy–neutral face pair trials versus neutral–neutral face pair trials, the ASD group showed greater right amygdala activation relative to the control group. The threshold for the illustration was set at p = 0.02 with a minimum cluster size of 90 voxels. To further evaluate group differences in amygdala function, mean contrast values for the whole right amygdala were extracted for the contrast of happy–neutral face pair trials versus neutral–neutral face pair trials. Contrast values represent the difference in mean activation in the whole right amygdala for the given contrast for all participants averaged together in each group. (B) Relative to controls, those in the ASD group showed greater activation in the whole right amygdala. Error bars are standard errors of the mean. (C) For the sad–neutral face pair trials vs. neutral–neutral face pair trials, the ASD group showed greater right amygdala activation relative to the control group. Group differences in amygdala function were evaluated by extracting the mean contrast values for the whole right amygdala for the contrast of sad–neutral face pair trials vs. neutral–neutral face pair trials. (D) Compared to controls, those in the ASD group also showed greater activation in the whole right amygdala. (E) There were no group differences in activation for the angry–neutral face pair trials vs. the neutral–neutral face pair trials.

Fig. 3

Differences between the autism spectrum disorder (ASD) and control groups in the psychophysiological interaction connectivity analysis. (A) In the analysis of happy–neutral face pair trials versus neutral–neutral face pair trials, the ASD group showed greater positive connectivity between the right amygdala and ventromedial prefrontal cortex than did the control group. The threshold for the illustration was set at p = 0.02 with a minimum of 60 voxels. Contrast values represent the difference in mean activation in the whole right amygdala for the given contrast for all participants averaged together in each group. (B) The bar graph illustrates average contrast values within an 8-mm sphere around the peak ventromedial pre-frontal cortex activation. Error bars are standard errors of the mean. (C) For the same analysis of happy–neutral face pair trials versus neutral–neutral face pair trials, the control relative to the ASD group showed greater positive connectivity between the right amygdala and left middle temporal gyrus. (D) The bar graph illustrates average contrast values within an 8-mm sphere around the peak left middle temporal lobe activation.