A constellation of eye-tracking measures reveals social attention differences in ASD and the broad autism phenotype

Abstract

Background: Social attention differences, expressed through gaze patterns, have been documented in autism spectrum disorder (ASD), with subtle differences also reported among first-degree relatives, suggesting a shared genetic link. Findings have mostly been derived from standard eye-tracking methods (total fixation count or total fixation duration). Given the dynamics of visual attention, these standard methods may obscure subtle, yet core, differences in visual attention mechanisms, particularly those presenting sub-clinically. This study applied a constellation of eye-tracking analyses to gaze data from individuals with ASD and their parents.

Methods: This study included n = 156 participants across groups, including ASD (n = 24) and control (n = 32) groups, and parents of individuals with ASD (n = 61) and control parents (n = 39). A complex scene with social/non-social elements was displayed and gaze tracked via an eye tracker. Eleven analytic methods from the following categories were analyzed: (1) standard variables, (2) temporal dynamics (e.g., gaze over time), (3) fixation patterns (e.g., perseverative or regressive fixations), (4) first fixations, and (5) distribution patterns. MANOVAs, growth curve analyses, and Chi-squared tests were applied to examine group differences. Finally, group differences were examined on component scores derived from a principal component analysis (PCA) that reduced variables to distinct dimensions.

Results: No group differences emerged among standard, first fixation, and distribution pattern variables. Both the ASD and ASD parent groups demonstrated on average reduced social attention over time and atypical perseverative fixations. Lower social attention factor scores derived from PCA strongly differentiated the ASD and ASD parent groups from controls, with parent findings driven by the subset of parents demonstrating the broad autism phenotype.

Limitations: To generalize these findings, larger sample sizes, extended viewing contexts (e.g., dynamic stimuli), and even more eye-tracking analytical methods are needed.

Conclusions: Fixations over time and perseverative fixations differentiated ASD and the ASD parent groups from controls, with the PCA most robustly capturing social attention differences. Findings highlight their methodological utility in studies of the (broad) autism spectrum to capture nuanced visual attention differences that may relate to clinical symptoms in ASD, and reflect genetic liability in clinically unaffected relatives. This proof-of-concept study may inform future studies using eye tracking across populations where social attention is impacted.

Keywords: Autism spectrum disorder; Broad autism phenotype; Endophenotype; Eye tracking; Social attention; Visual processing.

Fig. 1

A TAT image examined—Card 2; Farmland Scene; B Two primary areas of interest (AOIs) were generated—Social AOI, which included all the characters in the image; and Non-social AOI, which included everything else such as the book, barn, field

Fig. 2

Schematic representing fixation spatial distribution/coverage analysis AOIs. A Large areas (5 × 4 grid) and B small areas (10 × 8 grid)

Fig. 3

Overall gaze variables depicting A fixation count and B dwell time. Significant differences between BAP(+) and Control parent groups emerged in dwell time across social and non-social visual attention

Fig. 4

Dwell time patterns depicting A proportion of fixations over time (higher value indicates greater social attention) and B a schematic representing divergence time-bin analyses, where individuals with ASD were observed to attend less to social information than the control group half way into the stimulus presentation. Both BAP(−) and BAP(+) parents showed a spike in social attention around 5 s, with the BAP(+) group showing a striking decrease in social attention towards the end of the stimulus presentation compared to BAP(−) and Control parent groups

Fig. 5

Fixation patterns depicting A Percentage of perseverative fixations and B Percentage of regressive fixations. Significant differences between ASD and control groups, and BAP(+) and Control parent groups emerged in perseverative fixation patterns, showing elevated non-social and reduced social perseverative fixations, respectively

Fig. 6

Fixation patterns depicting transition analysis (i.e., the percentage of fixations characterized as transitions from one AOI to another) as follows: social to social AOI, non-social to non-social AOI, social to non-social AOI, and non-social to social AOI transitions

Fig. 7

A First fixation duration, and B First fixation AOI showing both percentage of first fixations that were made towards social information (lighter shade) and non-social information (darker shade)

Fig. 8

Distribution analyses depicting both A Fixation rate (exploration) overall and by AOI (social and non-social), and B fixation spatial distribution/coverage across larger (5 × 4) and smaller (10 × 8) boxes

Fig. 9

Group differences in factor scores from principal component analysis. Factor 1 = social/non-social attention (higher scores indicate greater social looking); factor 2 = efficiency of exploration