Perception of social cues of danger in autism spectrum disorders

Abstract

Intuitive grasping of the meaning of subtle social cues is particularly affected in autism spectrum disorders (ASD). Despite their relevance in social communication, the effect of averted gaze in fearful faces in conveying a signal of environmental threat has not been investigated using real face stimuli in adults with ASD. Here, using functional MRI, we show that briefly presented fearful faces with averted gaze, previously shown to be a strong communicative signal of environmental danger, produce different patterns of brain activation than fearful faces with direct gaze in a group of 26 normally intelligent adults with ASD compared with 26 matched controls. While implicit cue of threat produces brain activation in attention, emotion processing and mental state attribution networks in controls, this effect is absent in individuals with ASD. Instead, individuals with ASD show activation in the subcortical face-processing system in response to direct eye contact. An effect of differences in looking behavior was excluded in a separate eye tracking experiment. Our data suggest that individuals with ASD are more sensitive to direct eye contact than to social signals of danger conveyed by averted fearful gaze.

Figure 1. Face and gaze interactions depend on the degree of biological relevance conveyed.

(1) For neutral faces, humans are more sensitive to direct gaze than averted gaze , as direct gaze reflects interest from a social partner and the beginning of a social exchange. (2) A face looking at us with a fearful expression is more arousing than a face with a neutral expression, due to the strong emotion it conveys . (3) For fearful facial expressions, averted gaze is the most biologically self-relevant condition, with the social partner using non-verbal communicative cues to alert us to potential environmental danger .

Figure 2. Cortical activation for averted gaze.

Statistical maps of differences in fMRI activation for CON>ASD for the contrast averted>direct gaze (depicted in red to yellow). Group differences reflect increased activation for averted gaze in CON and lack of activation in ASD. Statistical maps are displayed on the lateral, medial and ventral views of both hemispheres, at p _FWE <0.05. The light grey mask covers subcortical regions in which activity cannot be expressed in surface rendering.

Figure 3. Region of interest analysis.

Percent BOLD signal change (± SEM), for averted vs. direct gaze in selected subcortical ROIs. The thalamus (THAL) (p = 0.01), and superior colliculus (SC) (p = 0.04) were significantly different between ASD and CON while a strong trend was found for the amygdala (AMY) (p = 0.056).

Figure 4. Atypical reactivity to social stimuli in ASD.

Individuals with ASD show increased response to direct as opposed to averted gaze ((1) - Kylliainen 2006) but show atypical eye contact. While deficits in fearful face processing have been described in ASD, no study to our knowledge has specifically investigated fearful vs. neutral faces and it is unclear if individuals with ASD would show more activation in response to direct fearful gaze as opposed to direct neutral gaze. Finally, unlike controls, individuals with ASD do not show more activation for fearful averted gaze.