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.
Highlights
Individuals with autism spectrum disorder (ASD) often report that looking in the eyes of others is uncomfortable for them, that it is terribly stressful, or even that ‘it burns’
This pathway has been thought to be specific for threat, and fearful face stimuli may serve as optimal stimuli for the subcortical face processing network[19], it was shown in a blindsight patient that it could convey other, positive emotions[20]
Tottenham et al.[28] demonstrated using an elegant paradigm that when Autism Spectrum Disorder (ASD) participants had to engage in a task that involved detecting a shape placed in the left or the right eye of faces, they showed heightened amygdala activity compared with controls, and that those who in natural settings had the least eye-movements towards the eyes were exhibiting the highest amygdala response when gaze was experimentally driven towards the eyes
Summary
Individuals with autism spectrum disorder (ASD) often report that looking in the eyes of others is uncomfortable for them, that it is terribly stressful, or even that ‘it burns’ (e.g. ref. 1). Newborns’ looking preferences are presumed to be mediated by the subcortical pathway over the first months, and help the normal maturation of the visual cortical areas involved in face perception This pathway has been thought to be specific for threat, and fearful face stimuli may serve as optimal stimuli for the subcortical face processing network[19], it was shown in a blindsight patient that it could convey other, positive emotions[20]. Dalton et al showed that amygdala activation in ASD children was correlated with spontaneous variations in time spent looking in the eyes of the face[26] This suggests that some level of experimental control over participants’ gaze patterns may be critical for characterizing the neural substrate of emotional face processing in ASD27. Perlman et al.[29] found, in a study conducted with 12 participants with ASD and 7 controls, that the level of amygdala activity in ASD participants was lower in a free viewing mode compared to controls, but that activity was modulated by experimental manipulation of gaze pattern towards the nose and eyes
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