Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism

Abstract

Individuals with Autism Spectrum Disorder (ASD) seem to have difficulties looking others in the eyes, but the substrate for this behavior is not well understood. The subcortical pathway, which consists of superior colliculus, pulvinar nucleus of the thalamus, and amygdala, enables rapid and automatic face processing. A specific component of this pathway - i.e., the amygdala - has been shown to be abnormally activated in paradigms where individuals had to specifically attend to the eye-region; however, a direct examination of the effect of manipulating the gaze to the eye-regions on all the components of the subcortical system altogether has never been performed. The subcortical system is particularly important as it shapes the functional specialization of the face-processing cortex during development. Using functional MRI, we investigated the effect of constraining gaze in the eye-region during dynamic emotional face perception in groups of participants with ASD and typical controls. We computed differences in activation in the subcortical face processing system (superior colliculus, pulvinar nucleus of the thalamus and amygdala) for the same stimuli seen freely or with the gaze constrained in the eye-region. Our results show that when constrained to look in the eyes, individuals with ASD show abnormally high activation in the subcortical system, which may be at the basis of their eye avoidance in daily life.

Figure 1

Descriptive plots of the ANOVA for each of the four ROIs. Panel A: Superior colliculus; Panel B: Pulvinar; Panel C: Left amygdala; Panel D: Right amygdala. Each panel shows the results obtained for neutral, happy, angry and fear faces. ASD participants are shown in white, controls (CON) in black. Values represented indicate mean ± SEM. Significant differences are indicated by red symbols (~trend, *p < 0.05; **p < 0.01; ***p < 0.001).