The pupil: a window on social automatic processing in autism spectrum disorder children

Abstract

BackgroundFaces are crucial social stimuli, eliciting automatic processing associated with increased physiological arousal in observers. The level of arousal can be indexed by pupil diameter (the ‘Event‐Related Pupil Dilation’, ERPD). However, many parameters could influence the arousal evoked by a face and its social saliency (e.g. virtual vs. real, neutral vs. emotional, static vs. dynamic). A few studies have shown an atypical ERPD in autism spectrum disorder (ASD) patients using several kinds of faces but no study has focused on identifying which parameter of the stimulus is the most interfering with face processing in ASD.MethodsIn order to disentangle the influence of these parameters, we propose an original paradigm including stimuli along an ecological social saliency gradient: from static objects to virtual faces to dynamic emotional faces. This strategy was applied to 186 children (78 ASD and 108 typically developing (TD) children) in two pupillometric studies (22 ASD and 47 TD children in the study 1 and 56 ASD and 61 TD children in the study 2).ResultsStrikingly, the ERPD in ASD children is insensitive to any of the parameters tested: the ERPD was similar for objects, static faces or dynamic faces. On the opposite, the ERPD in TD children is sensitive to all the parameters tested: the humanoid, biological, dynamic and emotional quality of the stimuli. Moreover, ERPD had a good discriminative power between ASD and TD children: ASD had a larger ERPD than TD in response to virtual faces, while TD had a larger ERPD than ASD for dynamic faces.ConclusionsThis novel approach evidences an abnormal physiological adjustment to socially relevant stimuli in ASD.

Autism spectrum disorder and pupillometry: A systematic review and meta-analysis

“…However, the responses of the ASD group did not differ significantly from the mental age matched TD group. Aguillon-Hernandez et al (2019) found that only dilation in response to virtual faces was stronger in ASD than in the TD group, and further confirmed the undifferentiated responses in the ASD group that were also found by Martineau et al (2011b). They hypothesise that dynamic emotional faces might elicit a larger response than static ones because of the larger emotional contagion in a dynamic or action context.…”

“…In their study, the ASD group showed inflexibility of regulation of the LC activity, they conclude based on a lower pupil reactivity in the presence of distractions, which is not expected when the LC would be regulated correctly. In toddlers with ASD, this LC-NE system is more often in a phasic state, which could be advantageous in a visual search task as performed by Blaser et al and could be a starting point for other cascading ASD characteristics (Blaser et al, 2014) The LC provides NE to the amygdala, thalamus and superior colliculi which are implied to be part of the low frequency face detector system, which would provide an automatic face processing (Aguillon--Hernandez et al, 2019). This system could be impaired in ASD hypothesise (Aguillon-Hernandez et al, 2019), because of their findings of reduced reactivity to faces.…”

“…In toddlers with ASD, this LC-NE system is more often in a phasic state, which could be advantageous in a visual search task as performed by Blaser et al and could be a starting point for other cascading ASD characteristics (Blaser et al, 2014) The LC provides NE to the amygdala, thalamus and superior colliculi which are implied to be part of the low frequency face detector system, which would provide an automatic face processing (Aguillon--Hernandez et al, 2019). This system could be impaired in ASD hypothesise (Aguillon-Hernandez et al, 2019), because of their findings of reduced reactivity to faces. Another structure receiving NE from the LC is the hippocampus, which is important in memory (Ring et al, 2020).…”

Emotional vs. Neutral Face Exploration and Habituation: An Eye-Tracking Study of Preschoolers With Autism Spectrum Disorders

“…This could suggest that emotional faces are perceived as less appealing and less salient for children with ASD. This finding is in line with a recent pupillometry study, in which a lack of pupil dilatation was reported in children with ASD while looking at objects, as well as static and dynamic faces (54). The authors attributed this lack of difference to an insensitivity toward event-related pupil dilatation, suggesting an abnormal physiological reaction and reduced arousal to socially salient stimuli in ASD.…”

Uncharacteristic Task-Evoked Pupillary Responses Implicate Atypical Locus Ceruleus Activity in Autism

“…A recent review from Bast et al (2018) suggests that LC dysfunction might be associated with attentional differences in ASD, but there has been little prior empirical evidence to support this hypothesis. Several studies have shown phasic pupillary response differences in ASD (Martineau et al, 2011;Blaser et al, 2014;Nuske et al, 2014a,b;Krach et al, 2015;Lawson et al, 2017;Aguillon-Hernandez et al, 2019;Boxhoorn et al, 2019). However, in these studies, participants with ASD exhibited differences in task performance compared with controls; thus, differences in pupil dilations may be attributable to differences in task performance.…”