Infant viewing of social scenes is under genetic control and is atypical in autism

Abstract

Long before infants reach, crawl, or walk, they explore the world by looking: they look to learn and to engage1, giving preferential attention to social stimuli including faces2, face-like stimuli3, and biological motion4. This capacity—social visual engagement—shapes typical infant development from birth5 and is pathognomonically impaired in children affected by autism6. Here we show that variation in viewing of social scenes—including levels of preferential attention and the timing, direction, and targeting of individual eye movements—is strongly influenced by genetic factors, with effects directly traceable to the active seeking of social information7. In a series of eye-tracking experiments conducted with 338 toddlers—including 166 epidemiologically-ascertained twins, 88 non-twins with autism, and 84 singleton controls—we find high monozygotic twin-twin concordance (0.91) and relatively low dizygotic concordance (0.35). Moreover, the measures that are most highly heritable, preferential attention to eye and mouth regions of the face, are also those that are differentially diminished in children with autism (Χ2=64.03, P<0.0001). These results—which implicate social visual engagement as a neurodevelopmental endophenotype—not only for autism, but for population-wide variation in social-information-seeking8—reveal a means of human biological niche construction, with phenotypic differences emerging from the interaction of individual genotypes with early life experience7.

Genetic Influence on Eye Movements to Complex Scenes at Short Timescales

“…Our findings serve as a robust initial replication and important extension of recently published work identifying heritable effects on gaze to social videos in toddlers [14], but, importantly, we do so using different analytical methods, different populations (24 and 36 month olds vs. later childhood), and qualitatively different stimuli (dynamic social videos with sound vs. static images of highly varied complex scenes, both social and non-social). Our results extend these initial findings by demonstrating that genes still influence human gaze well beyond infancy and toddlerhood, continuing into at least into later childhood and likely beyond, and influence viewing of highly varied environments, including both social and non-social environments.…”

“…Importantly, this is not a deterministic perspective, in that we do not believe that genes define an outcome (in this case, spatiotemporal patterns of gaze to complex scenes), but rather that genes contribute (in a probabilistic sense) to a developmental process that gives rise to particular gaze behavior as a consequence of a continually and reciprocally reinforcing biology-environment interaction. Infants gain control over their eye movements earlier than most other exploratory actions (e.g., effective reaching for or crawling towards objects) [20, 21], suggesting that a genetic influence on eye movements may play a particularly important role early in life [14]. Furthermore, not only do these results have implications for our understanding of the emergence of individual differences within the range of typical development, but also for understanding atypical development.…”

“…While there is a high degree of similarity across individuals with regard to which features of a scene are fixated [6–8], large individual differences are also present, especially in disorders of development [9–13], and clarifying the origins of these differences are essential to understand the processes by which individuals develop within the complex environments in which they exist and interact. Toward this end, a recent paper [14] found that ‘social visual engagement’ – namely, gaze to eyes and mouths of faces – is strongly influenced by genetic factors. However, whether genetic factors influence gaze to complex visual scenes more broadly, impacting how both social and non-social scene content are fixated, as well as general visual exploration strategies, has yet to be determined.…”

Autism spectrum disorder: advances in diagnosis and evaluation

“…Change in eye gaze duration between 2 months and 6 months differentiated the ASD and typically developing groups with near 100% accuracy; however, other high risk infants (particularly those with subthreshold “broader phenotype” symptoms) had intermediate fixation times. In a recent cross sectional study, eye versus mouth fixation times showed greater concordance in monozygotic versus dizygotic twins,101 which suggests that this attentional bias has a genetic basis. An overview of Klin, Jones, and colleagues’ work argues that eye versus mouth fixation is a strong translational candidate as a universal screener for ASD, but that large scale clinical trials would be needed to assess its potential utility in the general community 102…”

Facilitating Autism Research

“…For example, social attention in infancy is strongly correlated with genetic factors (Constantino et al, 2017); however, environmentally determined factors such as amount of face to face interaction (affected by parenting and intervention) will probably play a larger and larger role in their social attention as development unfolds and so will only be likely to yield more genetically homogenous groups if measured early in development (e.g., Jones and Klin, 2013).…”