Comparing social attention in autism and amygdala lesions: Effects of stimulus and task condition

Abstract

The amygdala plays a critical role in orienting gaze and attention to socially salient stimuli. Previous work has demonstrated that SM a patient with rare bilateral amygdala lesions, fails to fixate and make use of information from the eyes in faces. Amygdala dysfunction has also been implicated as a contributing factor in autism spectrum disorders (ASD), consistent with some reports of reduced eye fixations in ASD. Yet, detailed comparisons between ASD and patients with amygdala lesions have not been undertaken. Here we carried out such a comparison, using eye tracking to complex social scenes that contained faces. We presented participants with three task conditions. In the Neutral task, participants had to determine what kind of room the scene took place in. In the Describe task, participants described the scene. In the Social Attention task, participants inferred where people in the scene were directing their attention. SM spent less time looking at the eyes and much more time looking at the mouths than control subjects, consistent with earlier findings. There was also a trend for the ASD group to spend less time on the eyes, although this depended on the particular image and task. Whereas controls and SM looked more at the eyes when the task required social attention, the ASD group did not. This pattern of impairments suggests that SM looks less at the eyes because of a failure in stimulus-driven attention to social features, whereas individuals with ASD look less at the eyes because they are generally insensitive to socially relevant information and fail to modulate attention as a function of task demands. We conclude that the source of the social attention impairment in ASD may arise upstream from the amygdala, rather than in the amygdala itself.

Keywords:

• Social attention
• Amygdala
• Autism
• Scene perception
• Gaze selection

Acknowledgments

Special thanks to Brian Cheng and Catherine Holcomb for helping with subject recruitment and data analysis, to Prof. Christof Koch for use of the Eyelink 1000, and to Drs Lynn Paul and Dan Kennedy for help with diagnoses and assessments of the participants. This work was supported in part by grants from the Simons Foundation and the National Institute of Mental Health to R.A.; and a fellowship from the Natural Sciences and Engineering Research Council of Canada to E.B.