Variation in Social Visual Engagement - a Putative Autism Endophenotype - Reflects Stringent Genetic Control in Early Childhood

Background:  Diminished eye contact—and more specifically, atypical development of social visual engagement (SVE)—has been shown to predict autism spectrum disorder (ASD) by as early as 6 months-of-age among infants at elevated familial risk for ASD. Deviations in visual orientation to socially-salient cues in the course of moment-to-moment life experience are a target of early intervention for ASD, but the nature of causal influence on variation in SVE in early childhood , as well as the genetic structure, is unknown.

Objectives:  This study aims to examine the genetic structure of early SVE in an epidemiologically-ascertained sample of normal, like-sex toddler twins.

Methods:  We examined patterns of concordance in how children visually engage a caregiver's face and how they observe and seek information in the actions and reactions of peers. By collecting eye-tracking data from 338 toddlers, we first examined pairwise concordance in social visual engagement as a function of genetic and environmental variation in 82 monozygotic twins (MZ, 41 pairs), 84 dizygotic twins (DZ, 42 pairs), and 84 non-biologically-related toddlers (42 randomized pairs, matched by age and sex). Our experiments measured both macro-level indices of SVE (e.g. percentage of time spent looking at eye regions), as well as micro-level indices (e.g. timing of individual eye movements, direction of eye movements, etc.).

Results:  For concordance in eye- and mouth-looking, MZ twin-twin intraclass correlations (ICCs) were remarkably high: 0.91 for eyes (95% CI: 0.85-0.95) and 0.86 for mouth (95% CI: 0.76-0.92). This markedly contrasted with correlations for DZ twins: eyes, 0.35 (95% CI: 0.07-0.59) and mouth, 0.44 (95% CI: 0.16-0.65). We also found similar striking concordance among MZ twins compared to DZ twins for micro-level, moment-by-moment SVE. MZ twins demonstrated greater probability of moving their eyes at the same times: for each movement made by twin 1, within 350 milliseconds, there was an 18.6% increase in twin 2’s probability of also making an eye movement. When analyses were restricted to moments of motor initiationof the saccade, we observed a 21.1% increase in probability of time-locked eye movements: within +/-16.7 msec, MZ twins, but not DZ twins, initiated saccades at the same moments.

Conclusions:  MZ twins exhibit strikingly high concordance in overall levels of eye-looking; greater probability of shifting their eyes at the same moments in time; greater probability of shifting their eyes in the same subsequent directions; and greater probability of contemporaneously fixating on the same semantic content. These high levels of MZ concordance, observed at both macro- and micro-levels, indicate strong biological basis for variation in social visual engagement, with a substantial amount of that variation accounted for by genetic influence.