Unconscious avoidance of eye contact in autism spectrum disorder

Abstract

Atypical responses to direct gaze are one of the most characteristic hallmarks of autism spectrum disorder (ASD). The cause and mechanism underlying this phenomenon, however, have remained unknown. Here we investigated whether the atypical responses to eye gaze in autism spectrum disorder is dependent on the conscious perception of others' faces. Face stimuli with direct and averted gaze were rendered invisible by interocular suppression and eye movements were recorded from participants with ASD and an age and sex matched control group. Despite complete unawareness of the stimuli, the two groups differed significantly in their eye movements to the face stimuli. In contrast to the significant positive saccadic index observed in the TD group, indicating an unconscious preference to the face with direct gaze, the ASD group had no such preference towards direct gaze and instead showed a tendency to prefer the face with averted gaze, suggesting an unconscious avoidance of eye contact. These results provide the first evidence that the atypical response to eye contact in ASD is an unconscious and involuntary response. They provide a better understanding of the mechanism of gaze avoidance in autism and might lead to new diagnostic and therapeutic interventions.While verbal communication is the predominant means to deliver messages in social contexts, nonverbal signals play an essential role in paving the way for social interactions. The eyes in particular deliver a multitude of social cues. Adults 1 and already neonates 2 shift their attention preferably and reflexively towards others' direct gaze to establish mutual eye contact. This preference for direct gaze is not limited to conscious perception, but occurs even when individuals are completely unaware of being looked at 3 , accentuating the rapid and automatic processing of direct gaze in typically developed (TD) individuals. In contrast, individuals with autism spectrum disorder (ASD) show atypical responses to eye gaze -in particular an avoidance of mutual eye contact 4 . This striking and well-documented feature of ASD is directly related to deficits in social interactions and occurs early in the course of the disorder 5 . The cause and the mechanisms underlying eye contact avoidance in autism, however, have remained elusive 6 . On the one hand, it could be the consequence of a fast, yet conscious evaluation process involving high-level cortical processing stages, that is, an active avoidance of the eye region 7 . On the other hand and what remains unknown, is whether this avoidance of eye contact could proceed automatically and even unconsciously. Such an unconscious avoidance of eye contact would imply a mechanism implemented at low levels of the processing hierarchy and differences in the neurodevelopmental pathway of gaze processing 6 . A deeper understanding of the degree of the automaticity of gaze avoidance in autism is not only relevant for a refinement of the psychopathological model of autism but could also aid the development of effective treatments.To...

Towards the automatic detection of social biomarkers in autism spectrum disorder: introducing the simulated interaction task (SIT)

“…26 Atypical gaze patterns 27,28 are furthermore characteristic of ASD-especially the avoidance of direct eye contact. [29][30][31] Moreover, ASD involves aberrant voice intonation, 32 especially in naturalistic settings. 33 The SIT aims at reliably capturing those social biomarkers, which may aid earlier diagnosis as well as monitoring of the course of the disorder and treatment outcome.…”

Communicative Misalignment in Autism Spectrum Disorder

“…Second, those failures might affect the resolution of the ambiguity intrinsic in those signals. It remains to be seen whether other social deficits observed in ASD (and controlled for in this study), such as abnormalities in eye contact, facial expressions, speech, and turn-taking (Madipakkam, Rothkirch, Dziobek, & Sterzer, 2017;Shriberg et al, 2001;Tager-Flusberg & Anderson, 1991) , could in fact be downstream consequences of difficulties in predicting and monitoring mutual understanding (Stolk et al, 2016) . It will also be of interest to know whether and how conceptual alignment deficits interact with cognitive traits and environmental factors to…”

Communicative misalignment in Autism Spectrum Disorder

“…Second, those failures might affect the resolution of the ambiguity intrinsic in those signals. It remains to be seen whether other social deficits observed in ASD (and controlled for in this study), such as abnormalities in eye contact, facial expressions, speech, and turn-taking (Madipakkam, Rothkirch, Dziobek, & Sterzer, 2017;Shriberg et al, 2001;Tager-Flusberg & Anderson, 1991) , could in fact be downstream consequences of difficulties in predicting and monitoring mutual understanding (Stolk et al, 2016) . It will also be of interest to know whether and how conceptual alignment deficits interact with cognitive traits and environmental factors to give rise to the considerable behavioral and developmental variability observed in ASD, opening the way for principled interventions to improve communication between autistic and neurotypical individuals (Edey et al, 2016;Fusaroli, Weed, Fein, & Naigles, 2018;Greenberg, Warrier, Allison, & Baron-Cohen, 2018;Perry, Levy-Gigi, Richter-Levin, & Shamay-Tsoory, 2015;Stolk, Hunnius, et al, 2013; .…”