Puzzle of Reduced Attention to Eyes in Autism Solved?

Liam Davenport

January 17, 2017

The reduced attention to other people's eyes in children with autism spectrum disorder (ASD) is due to passive insensitivity to social signals in others' eyes, rather than gaze aversion, conclude US investigators in findings that could ultimately point to novel therapies for the condition.

In two experiments, researchers showed that children with ASD did not look away faster than typically developing children from direct gaze but reacted less to implicit social cues for eye-looking.

"These results contradict the hypothesis that children with ASD actively avoid looking at the eyes in early life. Instead, the results are consistent with gaze indifference and indicate passive insensitivity to social signals in others' eyes coupled with intact sensitivity to nonsocial, physical cues," the investigators, led by Warren Jones, PhD, assistant professor of pediatrics, Emory University, Atlanta, Georgia, write.

The study was published in the January issue of the American Journal of Psychiatry.

Opposing Hypotheses

Diminished attention gaze is one of the earliest emerging features of ASD and plays a key role in deficits in initiating and modulating reciprocal social interaction.

Two opposing hypotheses attempt to explain this early hallmark of autism. They point to different pathogenic models of disability and to different potential treatments. One is that children are purposely looking away, owing to gaze aversion; the other is that the children are indifferent to gaze.

To examine the two hypotheses, the researchers gathered eye-tracking data on 86 children (mean age, 24.9 months). Of those 86 children, 26 had ASD, 38 were developing typically, and 22 had nonautistic developmental delay.

The team conducted two experiments. The first measured the response to direct cueing to eye-looking using a standardized target. Specifically, the researchers measured the latency to look away and assessed sustained levels of continued eye-looking after caring and initial shifts gaze.

The second experiment determined the children's response to implicit cueing for eye-looking using video stimuli designed on the basis of data from typically developing children. For this, the researchers measured the probability of eye-looking and the density of fixation locations.

In response to direct cueing for eye-looking, there were no significant differences between children with ASD and typically developing children in terms of the success of direct cueing, the time spent freely watching the stimuli, and the integrity of extraocular muscle movements.

There were also no significant differences in latency to first saccade, suggesting that children with ASD and typically developing children are equally capable of rapidly shifting their gaze. The findings were not altered when measuring latency as a function of cueing target location.

However, the team found that there was a significantly greater association between the degree of initial cueing and the level of eye-looking in autistic children than their typically developing counterparts. This association persisted up to 1233 ms in autistic children, as compared with 500 ms in typically developing children, a greater than twofold increase.

"The persistence of this association required both additional fixations on the eyes when cued for eye-looking, as well as additional fixations on the mouth when cued for mouth-looking, an indication of relative insensitivity to the content of either cued target location," the authors write.

In response to implicit cueing for eye-looking, typically developing children were significantly more likely to look at the eyes when there was stronger implicit cueing (P < .001).

"Critically, however, children with autism spectrum disorder were not less likely to look at the eyes in response to the strongest cueing for eye-looking, evidence that is inconsistent with the gaze aversion hypothesis," the investigators note.

Although there was a significant association between fixation density and the strength of implicit cueing in typically developing children (P < .001), this was not seen in children with ASD.

"Our results indicate that reduced eye-looking in autism spectrum disorder at the time of initial diagnosis is not an anxiety-related response and that it is unlikely to be caused by hyperarousal or amygdala hyperactivation," the investigators write.

"Instead, because reduced attention to the eyes appears to be due to passive insensitivity to the social signals of a conspecific, observed amygdala dysfunction in ASD, it is more likely due to atypical development of neural networks involving the basolateral amygdala, including circuits associated with social gaze perception and with frontal cortex-associated attribution of reward value to social interaction," they add.

Window to the Mind

In an accompanying editorial, Simon Baron-Cohen, PhD, Autism Research Center, Cambridge University, the United Kingdom, notes that the study authors "pit two theories against each other: gaze aversion and gaze indifference. Their results point to the latter, not the former, although the question of why remains."

Dr Baron-Cohen notes there are a number of possible explanations, including neuronal deficits potentially arising from genetic alterations, as well as prenatal hormone levels.

"Naturally, individual differences in reading the mind in the eyes are not just a function of our biology, as postnatal social experience likely amplifies these prenatal determinants," Dr Baron-Cohen notes.

"For this reason, we should expect that impaired performance on this test might be observed in a range of clinical groups, not just in autism, for diverse reasons."

The study was supported by grants from the National Institute of Mental Health, the Autism Science Foundation, the Marcus Foundation, the Whitehead Foundation, and the Georgia Research Alliance. The authors have disclosed no relevant financial relationships.

Am J Psychiatry. 2017;174:26-35, 1-2. Abstract, Editorial

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