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

BACKGROUND: Faces 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. METHODS: In 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). RESULTS: Strikingly, 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. CONCLUSIONS: This novel approach evidences an abnormal physiological adjustment to socially relevant stimuli in ASD.

Eye Movement Monitoring and Maturation of Human Face Exploration.

OBJECTIVE: The aim of this study was to characterize ocular exploration of neutral and emotional faces in the typical development of a child. SUBJECTS AND METHOD: In this eye-tracking study, visual exploration of faces (with neutral or emotional expressions: happiness or sadness) was characterized in a population of 52 children (24 girls and 28 boys from 4 to 15 years of age) and 44 adults (22 women and 22 men from 18 to 35 years of age). The time spent on the eyes, nose and mouth of the faces was measured. RESULTS: All participants spent more time on the eyes (13%) rather than the nose and mouth (6%). The youngest participants spent less time exploring the eyes than the older participants, suggesting the progressive establishment of interest in these informative regions of the face during maturation. This process seemed to occur later in females (7-9 years) than males (4-6 years). CONCLUSION: These results confirm the importance of the eye area and the capacity of this region to capture attention. In addition, this study shows that the exploration of this region increases with age and is lower among girls aged 4-6 years compared with boys of the same age.

An odor identification approach based on event-related pupil dilation and gaze focus.

Olfactory disorders constitute a potential marker of many diseases and are considered valuable clues to the diagnosis and evaluation of progression for many disorders. The most commonly used test for the evaluation of impairments of olfactory identification requires the active participation of the subject, who must select the correct name of the perceived odor from a list. An alternative method is required because speech may be impaired or not yet learned in many patients. As odor identification is known to be facilitated by searching for visual clues, we aimed to develop an objective, vision-based approach for the evaluation of odor identification. We used an eye tracking method to quantify pupillary and ocular responses during the simultaneous presentation of olfactory and visual stimuli, in 39 healthy participants aged from 19 to 77years. Odor presentation triggered an increase in pupil dilation and gaze focus on the picture corresponding to the odor presented. These results suggest that odorant stimuli increase recruitment of the sympathetic system (as demonstrated by the reactivity of the pupil) and draw attention to the visual clue. These results validate the objectivity of this method.

Human infants detect other people's interactions based on complex patterns of kinematic information.

Do infants perceive other people's interactions by means of a mechanism that integrates biological motion information across the observed individuals? In support of this view, the present study demonstrates that infants (N = 28, Age  = 14 months) discriminate between point light displays representing disrupted and non-disrupted interactions between people, even though the two interaction types are identical at the level of individual point light agents. Moreover, a second experiment (sample 2: N = 28, Age  = 14 months) indicated that visual preference in this context is influenced by an audiovisual integration processes that takes into account the presence of an interaction between people. All these results were found exclusively for upright displays--when stimuli were shown upside-down (disrupting biological motion processing), performance was random. Collectively, these findings point to an important role for biological motion in social perception in human infants.

Back to basic: do children with autism spontaneously look at screen displaying a face or an object?

Eye-tracking studies on exploration of faces and objects in autism provided important knowledge but only in a constraint condition (chin rest, total time looking at screen not reported), without studying potential differences between subjects with autism spectrum disorder (ASD) and controls in spontaneous visual attention toward a screen presenting these stimuli. This study used eye tracking to compare spontaneous visual attention to a screen displaying a face or an object between children with autism and controls in a nonconstraint condition and to investigate the relationship with clinical characteristics in autism group. Time exploring screen was measured during passive viewing of static images of faces or objects. Autistic behaviors were assessed by the CARS and the BSE-R in autism group. In autism group, time exploring face screen and time exploring object screen were lower than in controls and were not correlated with degree of distractibility. There was no interaction between group and type of image on time spent exploring screen. Only time exploring face screen was correlated with autism severity and gaze impairment. Results highlight particularities of spontaneous visual attention toward a screen displaying faces or objects in autism, which should be taken into account in future eye-tracking studies on face exploration.

Can pupil size and pupil responses during visual scanning contribute to the diagnosis of autism spectrum disorder in children?

The purpose of this study was to determine whether baseline pupil size and pupil responses during visual scanning with eye-tracking technology could discriminate children with autism spectrum disorder (ASD) from mental age-matched and chronological age-matched controls. To this end, we used stimuli consisting in still color photographs presented centrally to the participant's midline on a stimulus monitor. Each child was presented with a series of neutral faces, virtual faces (avatars) and different objects, separated by black slides. We recorded the mean pupil size and pupil size changes over time in each of the three categories of stimuli and during exposure to the black slides. Fifty-seven children participated in study (19 ASD, mean age 118 months; 19 mental age-matched controls, mean age 87 months; and 19 chronological age-matched controls, mean age 118 months). We compared the baseline pupil size and pupil responses during visual scanning among the three diagnostic groups. During the presentation of slides, the mean pupil size in the ASD group was clearly smaller than in the MA-matched and CA-matched groups. Discriminate analysis of pupil size during the presentation of black slides and slides with visual stimuli successfully predicted group membership in 72% of the participants. Group membership was correctly classified in 89% of the participants in the ASD group, in 63% in the MA-matched group and in 63% in the CA-matched group. These potential biomarkers may contribute to our understanding of the differences in neurological development in the brain in autism and could prove useful as indicators of ASD.