Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes

Abstract

Previous studies that showed decreased brain activation in people with autism spectrum disorder (ASD) viewing expressive faces did not control that participants looked in the eyes. This is problematic because ASD is characterized by abnormal attention to the eyes. Here, we collected fMRI data from 48 participants (27 ASD) viewing pictures of neutral faces and faces expressing anger, happiness, and fear at low and high intensity, with a fixation cross between the eyes. Group differences in whole brain activity were examined for expressive faces at high and low intensity versus neutral faces. Group differences in neural activity were also investigated in regions of interest within the social brain, including the amygdala and the ventromedial prefrontal cortex (vmPFC). In response to low intensity fearful faces, ASD participants showed increased activation in the social brain regions, and decreased functional coupling between the amygdala and the vmPFC. This oversensitivity to low intensity fear coupled with a lack of emotional regulation capacity could indicate an excitatory/inhibitory imbalance in their socio-affective processing system. This may result in social disengagement and avoidance of eye-contact to handle feelings of strong emotional reaction. Our results also demonstrate the importance of careful control of gaze when investigating emotional processing in ASD. Hum Brain Mapp 38:5943-5957, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: amygdala; autism; eye contact; fMRI; facial expressions; fear.

Figure 1

Map of activation showing the brain areas that are more activated for ASD than CON participants, for the low intensity fearful condition. The rightmost image is a transverse view of the brain showing increased activation in the amygdala for ASD vs. CON participants, in this condition. Data are shown for P < 0.05 (unclustered). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Map of activation showing the brain areas that are more activated for CON than ASD participants, for the high intensity happy condition. Data are shown for P < 0.05 (unclustered). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Partial correlations (with age being controlled for) between the amygdala activity (displayed on the x‐axis) and the vmPFC activity (displayed on the y‐axis) for angry (leftmost panel), happy (central panel), and fearful faces (rightmost panel). Low intensity emotions are featured in the upper part of the figure while high intensity emotions are featured in the lower part of the picture. ASD data is represented in blue and CON data is represented in orange. Significant correlation P < 0.05 are indicated with an asterisk (*), P < 0.01 with two asterisks (**), and trending correlations P < 0.07 with a tilde (∼). [Color figure can be viewed at http://wileyonlinelibrary.com]