Idiosyncratic pupil regulation in autistic children

Abstract

Recent neuroimaging and eye-tracking studies have suggested that children with autism exhibit more variable and idiosyncratic brain responses and eye movements than typically developing (TD) children. Here, we extended this research to pupillometry recordings. We successfully acquired pupillometry recordings from 111 children (74 with autism), 4.5-years-old on average, who viewed three 90 s movies, twice. We extracted their pupillary time-course for each movie, capturing their stimulus evoked pupillary responses. We then computed the correlation between the time-course of each child and those of all others in their group as well as between each autistic child and all children in the TD group. This yielded an average inter-subject correlation value per child, representing how similar their pupillary responses were to all others in their group or the comparison group. Children with autism exhibited significantly weaker inter-subject correlations than TD children in all comparisons. These differences were independent of previously reported differences in gaze inter-subject correlations and were largest in responses to a naturalistic movie containing footage of a social interaction between two TD children. The results demonstrate the utility of measuring the idiosyncrasy of pupil regulation, which can be performed with passive viewing of movies even by young children with co-occurring intellectual disability. These findings reveal that a considerable number of children with autism have significantly less stable, idiosyncratic pupil regulation than TD children, indicative of more variable, weakly regulated, underlying neural activity.

Keywords: Autism; idiosyncrasy; inter‐subject; naturalistic; pupil; pupillometry.

FIGURE 1

Tonic pupil diameter (mm) in each of the six movies. (a) Scatter plot demonstrating tonic pupil diameter for each individual, across both groups, per movie. Black line: mean tonic pupil diameter per group. There were no significant differences across groups. (b–d) Scatter plots demonstrating stability of tonic pupil diameter per participant across two presentations of each movie. Each point represents a single child. Solid lines: Least squares fit. Dotted line: unity line. Blue: autism, Gray: TD.

FIGURE 2

Time‐courses of pupil diameter from each presentation of the three movies. (a, c, e) First presentation. (b, d, f) Second presentation. Solid line: average pupil diameter across participants per group. Shaded area: standard error of the mean. Blue: autism. Gray: TD.

FIGURE 3

Comparison of inter‐SC values across groups for each movie and presentation. (a) First presentation. (b) Second presentation. Gray: inter‐SC within the TD group. Dark blue: inter‐SC within the autism group. Light blue: inter‐SC of children with autism relative to TD controls (i.e., AC). Asterisks: Significant differences across groups according to ANCOVA tests (*p < 0.05, **p < 0.01, ***p < 0.001).

FIGURE 4

Scatter plots of inter‐SC values demonstrating their correlation across the two presentations of Jack‐Jack Attack (a), Jungle Book (b), and Naturalistic (c) movies. Gray: inter‐SC within the TD group. Light Blue: inter‐SC of children with autism relative to controls (AC). Solid lines: Least squares fit. Dotted line: unity line. Inter‐SC, inter‐subject correlation.

FIGURE 5

ROC analyses using inter‐SC to classify autistic and TD participants. (a) First presentation. (b) Second presentation. Purple: Jack‐Jack Attack, Yellow: Jungle Book, Red: Naturalistic movie. Black dashed line: unity line. Inter‐SC, inter‐subject correlation; ROC, receiver operating characteristic.