Autism is a pervasive neurodevelopmental disorder characterized by pronounced impairments in social interactions [1
]. From the first year of life, individuals with autism spectrum disorders (ASD) show a lack of interest in the human face, and typically show reduced eye contact [2
]. The failure to attend to social stimuli such as the human face may have extensive negative consequences for later development. For instance, individuals with ASD may not develop expertise in processing information from faces [3
] and may fail to appreciate their emotional salience [5
Why individuals with ASD tend to look away from the eyes and appear to fixate on the local features of the face, such as the mouth and chin, compared to typically developing (TD) counterparts [6
] remains controversial. One possibility is that they find looking at the eyes over-stimulating or emotionally distressing [10
]. In support of this “aversion” hypothesis, one study found that in individuals with ASD, eye fixation correlated with activation in the amygdala, an area associated with processing fear [6
]. On the other hand, it is also possible that the eyes may simply be uninteresting to individuals with ASD, if they fail to appreciate the information the eye region may convey. According to the social motivation hypothesis, individuals with ASD may not attend to social stimuli—such as faces and the eye region in particular—because they have difficulty forming representations of the reward value of these social stimuli [12
]. As these individuals may not find faces and eye contact rewarding, they may not be motivated to interact socially. In contrast, a happy face may be socially rewarding for neurotypical individuals. Indeed, happy [14
] and attractive faces [15
] have been shown to activate reward circuitry, such as the ventral striatum and orbitofrontal cortex, using functional MRI (fMRI). Further, Kampe et al. (2001) showed that fMRI activation in the ventral striatum is modulated both by reward magnitude (degree of facial attractiveness) and direction of the gaze (direct vs. averted), indicating that reward circuits are engaged when looking at people’s faces and that this network is also sensitive to eye contact. These findings suggest that, for neurotypical individuals, direct eye contact during social interactions may be intrinsically rewarding.
The aim of this study was to investigate whether children and adolescents with ASD find looking at the eye region aversive or simply unrewarding, using pupillometry as an index of emotional responsiveness. Task-evoked pupillary responses have been shown to reflect variations in processing load, or arousal level, across various cognitive domains including short-term memory, language, arithmetic and perception tasks (see [17
] for a review). Importantly, emotional arousal, regardless of valence, is also related to the pupillary dilation response [18
]. In fact, the largest pupillary dilations are evoked by stimuli reported as most aversive or most pleasant [20
]. Some studies of pupil dilation in children and adolescents have demonstrated greater pupil dilation to negative stimuli (words, interactions) than to neutral or positive stimuli [23
]. Further, pupillary changes have been found to co-vary with skin conductance change [20
], indicating that pupillary responses reflect emotional arousal associated with increased sympathetic activity. Importantly, several studies have reported increases in pupil dilation in response to rewarding stimuli. In adults, sexually arousing stimuli, whether visual or auditory, lead to increases in pupil diameter [25
]. Increasing levels of reward led to corresponding increases in pupil diameter [28
], whether the reward cues were apparent or subliminal. Craving-related visual cues in smokers produced increased pupil diameters [29
]; these same cues were also associated with increased fMRI signal in the ventral striatum [30
], suggesting that the pupil dilation during craving is related to reward anticipation. However, anticipation of a potential reward or loss in a gambling task caused an increase in pupil diameter, while actually receiving a reward resulted in pupil reduction more than losing a reward, suggesting that pupil dilation may be related to anticipation of reward outcomes rather than the attainment of the reward per se.
Despite the utility of pupillary response as a measure of autonomic arousal, very few studies to date have reported on pupillary response to facial stimuli in developmental disorders, such as autism [32
]. While one study [32
] found overall pupillary constriction when the ASD group viewed faces as compared to the TD group, another study [33
] did not show differences in pupillary responses to upright faces between the ASD and TD group. However, this latter study found that the ASD group showed increased pupil dilation to the inverted faces (compared to upright faces), whereas this effect was not seen in the TD group. Overall, little is known about the nature of the pupillary response to faces in individuals with ASD, and the few existing studies have reported discrepant results.
In the current study, we presented emotional faces with averted gaze (the eyes of the faces presented are looking to the side of the subject) and faces with direct gaze (the eyes of the faces presented are gazing directly at the subject). Direct gaze in humans communicates the intent to engage with another person and maintain social interaction [34
]. In neurotypical individuals, direct gaze compared to averted gaze is associated with increased activation of the fusiform face area [35
]; in contrast, in one study in children with ASD [36
], gaze direction was not found to modulate brain activity.
Therefore, in the present study we investigated pupillary response and fixation behavior in children with ASD and age-matched TD controls while they were presented with emotional faces (angry, afraid, happy or neutral) displaying either direct or averted gaze. To examine the aversion hypothesis, we compared pupillary response to emotional faces in the ASD and TD groups. If individuals with ASD avoid looking at faces (and the eye region in particular) because they find this aversive, then children and adolescents with ASD should show an overall increased pupillary response to faces compared to the TD group. However, it is also possible that between-group differences in pupillary responses may only be observed for faces displaying direct eye gaze, irrespective of emotion, or for faces displaying negative affect.
To examine the social motivation hypothesis, we examined pupillary response to faces displaying positive affect (a happy expression) in the ASD and TD groups, with the underlying assumption that a happy face with direct eye gaze would be most rewarding for neurotypical individuals [14
]. We hypothesized that TD children would show increased pupil dilation to happy faces with direct gaze compared to averted gaze. If individuals with ASD avoid looking at faces, and the eyes in particular, because they find them unrewarding, then our sample of children with ASD should not show this effect.