Neural Correlates of Eye Contact and Social Function in Autism Spectrum Disorder

Abstract

Reluctant eye contact and reduced social interactions characteristic of autism spectrum disorder (ASD) are consistent with deficits in oculomotor and face processing systems. We test the hypothesis that these deficits are interrelated ASD. Eye-tracking and hyperscanning with functional near-infrared spectroscopy (fNIRS) were used to acquire neuroimaging data during live, dynamic eye-to-eye contacts in 17 ASD and 19 typically-developed (TD) adults. Real eye contact conditions were contrasted with conditions where eye gaze was directed at a comparable dynamic face video. These findings were regressed with eye-contact dwell-time, i.e., times when gaze of both partners was in the eye-box of the other, to confirm the relationship between visual sensing and neural coding. Visual fixations and positional variance were also determined. Average gaze dwell-times in the “eye-box” did not vary between ASD and TD participants but were longer for the Real Eye than Video Eye condition for both groups. However, positional gaze variability, “jitter”, was higher for ASD in both conditions. Neural findings for TD [Real Eye > Video Eye] were consistent with previous findings for interactive face-gaze with activity in right temporal and dorsal parietal regions. However, in ASD ventral temporal regions were observed for this contrast without evidence for dorsal parietal activity. This neural difference was enhanced when regressed by eye-contact dwell-times. Together findings are consistent with the hypothesis that unstable bottom-up oculomotor signals contribute to deficits in live face processing and reduced dorsal stream activity in ASD. Significance Eye contact avoidance is a diagnostic feature of autism spectrum disorder (ASD). However, the underlying neural mechanisms are unknown. Using a two-person neural imaging system and a face-to-face paradigm with eye tracking, we found that the neural systems activated by live eye contact differed between typically developed (TD) and ASD groups. In ASD, the ventral occipital parietal systems were engaged, whereas in TD, the dorsal posterior parietal systems were engaged. Positional variation of eye gaze, “jitter”, was higher in ASD than TD. These findings are consistent with the hypothesis that bottom-up variations in visual sensing are components of altered interactive face processing and dorsal stream mechanisms and may contribute to the neural underpinnings of reluctant eye contact behaviors in ASD.