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. 2014 Jan;9(1):106-17.
doi: 10.1093/scan/nst050. Epub 2013 Apr 16.

Elevated amygdala response to faces and gaze aversion in autism spectrum disorder

Nim Tottenham  1 , Margaret E Hertzig, Kristen Gillespie-Lynch, Tara Gilhooly, Alexander J Millner, B J Casey
Affiliations

Elevated amygdala response to faces and gaze aversion in autism spectrum disorder

Nim Tottenham et al. Soc Cogn Affect Neurosci. 2014 Jan.

Abstract

Autism spectrum disorders (ASD) are often associated with impairments in judgment of facial expressions. This impairment is often accompanied by diminished eye contact and atypical amygdala responses to face stimuli. The current study used a within-subjects design to examine the effects of natural viewing and an experimental eye-gaze manipulation on amygdala responses to faces. Individuals with ASD showed less gaze toward the eye region of faces relative to a control group. Among individuals with ASD, reduced eye gaze was associated with higher threat ratings of neutral faces. Amygdala signal was elevated in the ASD group relative to controls. This elevated response was further potentiated by experimentally manipulating gaze to the eye region. Potentiation by the gaze manipulation was largest for those individuals who exhibited the least amount of naturally occurring gaze toward the eye region and was associated with their subjective threat ratings. Effects were largest for neutral faces, highlighting the importance of examining neutral faces in the pathophysiology of autism and questioning their use as control stimuli with this population. Overall, our findings provide support for the notion that gaze direction modulates affective response to faces in ASD.

Keywords: amygdala; autism spectrum disorders; eye-tracking; fMRI; face expressions.

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Figures

Fig. 1
Fig. 1
(A) Eye tracking indicates that saccades toward the eye region are less frequent in the ASD group for neutral faces. (B) Within the ASD group, greater perceived threat ratings for neutral faces were associated with fewer eye movements directed toward the eye region for neutral faces; residuals plotted controlling for age and sex. TD, typically developing; ASD, autism spectrum disorder; **between-group difference, P < 0.01.
Fig. 2
Fig. 2
Face labeling errors associated with threat endorsement. (A) Accuracy was significantly lower in the ASD group when labeling neutral faces. (B) The ASD group was more likely to mistakenly label neutral as a negative emotion. (C) Higher ratings of threat for neutral faces were associated with a tendency to mislabel neutral faces as a negative expression, with TD represented with open circles and ASD represented with filled circles. Residuals plotted, controlling for group and age group. TD, typically developing; ASD, autism spectrum disorder; ***between-group difference, P < 0.005.
Fig. 3
Fig. 3
Natural viewing condition. (A) Illustration of condition. During an essentially passive viewing task, participants were instructed to provide a single button press for each trial. They were instructed to alternate the finger used on each trial (either index or middle finger). (B) Individuals in the ASD group showed elevated amygdala activity (Faces > baseline) compared with the TD group. TD, typically developing; ASD, autism spectrum disorder; *between-group difference, P < 0.025.
Fig. 4
Fig. 4
Experimental gaze-manipulation condition. (A) Illustration of condition. Participants were instructed to press the button on each trial that corresponded to the location of a visually degraded cue (accentuated here for visualization) placed in either the right or left eye of each face trial. (B) Experimental gaze manipulation increased looks toward the eye region. When gaze was directed toward the eye region, a Group × Emotion interaction emerged (C), where individuals in the ASD group showed elevated amygdala response to neutral faces, averaged over both hemispheres for this figure (D). TD, typically developing; ASD, autism spectrum disorder; *between-group difference, P < 0.05; **within-group difference P < 0.01.
Fig. 5
Fig. 5
Effect of experimental gaze manipulation with ASD group. When gaze was directed to the eye region, amygdala response was potentiated for neutral faces in the ASD group. Panel (A) shows effect of Emotion × Face viewing condition interaction in the right and left amygdala, and panel (B) explains the source of the interaction, where the experimental gaze manipulation condition resulted in a potentiated amygdala response to neutral faces, averaged across both hemispheres for this figure. Panel (C) shows an inverse association between gaze directed toward the eye region of neutral faces under natural viewing conditions and amygdala potentiation by experimental eye gaze (experimental eye-gaze condition minus natural viewing); residuals controlling for age and sex are plotted. ASD, autism spectrum disorder; ns, not significant; *within-group difference, P < 0.025.
Fig. 6
Fig. 6
Amygdala response to neutral faces during experimental gaze manipulation was positively associated with increased threat appraisals of neutral faces. Plotted here are the residuals for amygdala response controlling for age, sex and group.
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