Neural Mechanisms Underlying Conscious and Unconscious Gaze-Triggered Attentional Orienting in Autism Spectrum Disorder.

Wataru Sato,Shota Uono,Takanori Kochiyama,Sayaka Yoshimura,Motomi Toichi

doi:10.3389/fnhum.2017.00339

Abstract

Impaired joint attention represents the core clinical feature of autism spectrum disorder (ASD). Behavioral studies have suggested that gaze-triggered attentional orienting is intact in response to supraliminally presented eyes but impaired in response to subliminally presented eyes in individuals with ASD. However, the neural mechanisms underlying conscious and unconscious gaze-triggered attentional orienting remain unclear. We investigated this issue in ASD and typically developing (TD) individuals using event-related functional magnetic resonance imaging. The participants viewed cue stimuli of averted or straight eye gaze direction presented either supraliminally or subliminally and then localized a target. Reaction times were shorter when eye-gaze cues were directionally valid compared with when they were neutral under the supraliminal condition in both groups; the same pattern was found in the TD group but not the ASD group under the subliminal condition. The temporo–parieto–frontal regions showed stronger activation in response to averted eyes than to straight eyes in both groups under the supraliminal condition. The left amygdala was more activated while viewing averted vs. straight eyes in the TD group than in the ASD group under the subliminal condition. These findings provide an explanation for the neural mechanisms underlying the impairment in unconscious but not conscious gaze-triggered attentional orienting in individuals with ASD and suggest possible neurological and behavioral interventions to facilitate their joint attention behaviors.

Highlights

Individuals with autism spectrum disorder (ASD) are characterized by qualitative impairments in social interaction (American Psychiatric Association, 2013)
A series of t-tests on the data from the ASD group was conducted and no significant differences were identified among the cue-validity conditions (t < 1.57, p > 0.1)
The conjunction analysis testing the commonality across groups for the main effect of direction with an exclusive mask of the group × direction interaction for the supraliminal condition revealed that averted eyes activated the bilateral inferior parietal lobules, which covered parts of the posterior superior temporal gyri, and the right inferior frontal gyrus significantly more than the straight eyes in both the typically developing (TD) and ASD groups (Table 2; Figure 2)

Summary

Introduction

Individuals with autism spectrum disorder (ASD) are characterized by qualitative impairments in social interaction (American Psychiatric Association, 2013). The reaction time (RT) for detecting the target was shorter after a face with a valid averted gaze (i.e., directionally congruent with target location) than a face with straight eyes or an invalid averted gaze in both ASD and TD participants. Another previous study (Sato et al, 2010) presented subliminal eye-gaze cues using a cueing paradigm and reported that the cueing effect was evident in the TD group, which is similar to previous studies (Sato et al, 2007; Xu et al, 2011; Al-Janabi and Finkbeiner, 2012; Bailey et al, 2014), but not in the ASD group. Even though findings under the supraliminal condition are inconsistent and those under the subliminal condition are scarce, these data suggest that gaze-triggered attentional orienting is intact in response to supraliminally presented eyes but impaired in response to subliminally presented eyes in individuals with ASD

Methods

Results

Conclusion