Atypical scan paths on emotional faces and reduced eye contact represent a prominent feature of autism symptomatology, yet the reason for these abnormalities remains a puzzle. Do individuals with autism spectrum disorders (ASDs) fail to orient toward the eyes or do they actively avoid direct eye contact? Here, we used a new task to investigate reflexive eye movements on fearful, happy, and neutral faces. Participants (ASDs: 12; controls: 11) initially fixated either on the eyes or on the mouth. By analyzing the frequency of participants' eye movements away from the eyes and toward the eyes, respectively, we explored both avoidance and orientation reactions. The ASD group showed a reduced preference for the eyes relative to the control group, primarily characterized by more frequent eye movements away from the eyes. Eye-tracking data revealed a pronounced influence of active avoidance of direct eye contact on atypical gaze in ASDs. The combination of avoidance and reduced orientation into an individual index predicted emotional recognition performance. Crucially, this result provides evidence for a direct link between individual gaze patterns and associated social symptomatology. These findings thereby give important insights into the social pathology of ASD, with implications for future research and interventions.

Reduced focus toward the eyes is a characteristic of atypical gaze on emotional faces in autism spectrum disorders (ASD). Along with the atypical gaze, aberrant amygdala activity during face processing compared with neurotypically developed (NT) participants has been repeatedly reported in ASD. It remains unclear whether the previously reported dysfunctional amygdalar response patterns in ASD support an active avoidance of direct eye contact or rather a lack of social attention. Using a recently introduced emotion classification task, we investigated eye movements and changes in blood oxygen level-dependent (BOLD) signal in the amygdala with a 3T MRI scanner in 16 autistic and 17 control adult human participants. By modulating the initial fixation position on faces, we investigated changes triggered by the eyes compared with the mouth. Between-group interaction effects revealed different patterns of gaze and amygdalar BOLD changes in ASD and NT: Individuals with ASD gazed more often away from than toward the eyes, compared with the NT group, which showed the reversed tendency. An interaction contrast of group and initial fixation position further yielded a significant cluster of amygdala activity. Extracted parameter estimates showed greater response to eyes fixation in ASD, whereas the NT group showed an increase for mouth fixation.The differing patterns of amygdala activity in combination with differing patterns of gaze behavior between groups triggered by direct eye contact and mouth fixation, suggest a dysfunctional profile of the amygdala in ASD involving an interplay of both eye-avoidance processing and reduced orientation.

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Deviant gaze behavior is a defining characteristic of autism. Its relevance as a pathophysiological mechanism, however, remains unknown. In the present study, we compared eye fixations of 20 adults with autism and 21 controls while they were engaged in taking the Multifaceted Empathy Test (MET). Additional measures of face emotion and identity recognition were also obtained. While both groups fixated more on the face and mouth in the emotion recognition than in the face identity condition of the MET, individuals with autism fixated less on the face across MET conditions. Correlation analysis revealed associations between fixation time on the eyes and face processing abilities. Our results suggest that eye fixation patterns are an important characteristic of the social phenotype of autism.