Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search

Shuo Wang, Juan Xu, Ming Jiang, Qi Zhao, Rene Hurlemann, Ralph Adolphs

Research output: Contribution to journalArticlepeer-review

25 Scopus citations

Abstract

People with autism spectrum disorders (ASD) have pervasive impairments in social interactions, a diagnostic component that may have its roots in atypical social motivation and attention. One of the brain structures implicated in the social abnormalities seen in ASD is the amygdala. To further characterize the impairment of people with ASD in social attention, and to explore the possible role of the amygdala, we employed a series of visual search tasks with both social (faces and people with different postures, emotions, ages, and genders) and non-social stimuli (e.g., electronics, food, and utensils). We first conducted trial-wise analyses of fixation properties and elucidated visual search mechanisms. We found that an attentional mechanism of initial orientation could explain the detection advantage of non-social targets. We then zoomed into fixation-wise analyses. We defined target-relevant effects as the difference in the percentage of fixations that fell on target-congruent vs. target-incongruent items in the array. In Experiment 1, we tested 8 high-functioning adults with ASD, 3 adults with focal bilateral amygdala lesions, and 19 controls. Controls rapidly oriented to target-congruent items and showed a strong and sustained preference for fixating them. Strikingly, people with ASD oriented significantly less and more slowly to target-congruent items, an attentional deficit especially with social targets. By contrast, patients with amygdala lesions performed indistinguishably from controls. In Experiment 2, we recruited a different sample of 13 people with ASD and 8 healthy controls, and tested them on the same search arrays but with all array items equalized for low-level saliency. The results replicated those of Experiment 1. In Experiment 3, we recruited 13 people with ASD, 8 healthy controls, 3 amygdala lesion patients and another group of 11 controls and tested them on a simpler array. Here our group effect for ASD strongly diminished and all four subject groups showed similar target-relevant effects. These findings argue for an attentional deficit in ASD that is disproportionate for social stimuli, cannot be explained by low-level visual properties of the stimuli, and is more severe with high-load top-down task demands. Furthermore, this deficit appears to be independent of the amygdala, and not evident from general social bias independent of the target-directed search.

Original languageEnglish (US)
Pages (from-to)259-274
Number of pages16
JournalNeuropsychologia
Volume63
DOIs
StatePublished - Oct 1 2014
Externally publishedYes

Bibliographical note

Funding Information:
We thank Jed Elison and Noah Sasson for providing the original stimuli, Ty Basinger for creating some of the stimuli, Lynn Paul for psychological assessments, and Mike Tyszka for providing the anatomical scans of the amygdala lesion patients. This research was supported in part by an R01 Grant from NIMH , an NIMH Conte Center, and the Singapore Ministry of Education Academic Research Fund Tier 1 (No. R-263-000-A49-112 ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
© 2014 Elsevier Ltd.

Keywords

  • Amygdala
  • Autism
  • Saliency
  • Social
  • Visual search

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