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

• Type of Material: Article
• Authors: John N. Constantino, Washington University; Stefanie Kennon-McGill, Washington University; Clarie Weichselbaum, Washington University; Natasha Marrus, Washington University; Alyzeh Haider, Washington University; Anne L. Glowinski, Washington University; Scott Gillespie, Emory University; Cheryl Klaiman, Emory University; Ami Klin, Emory University; Warren R Jones, Emory University
• Language: English
• Date: 2017-07-20
• Publisher: Nature Publishing Group
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
• Final Published Version (URL): http://dx.doi.org/10.1038/nature22999
• Title of Journal or Parent Work: Nature
• ISSN: 0028-0836
• Volume: 547
• Issue: 7663
• Start Page: 340
• End Page: +
• Grant/Funding Information: Research was supported by grants from the National Institute of Child Health & Human Development, HD068479 (JNC) and U54 HD087011 (Intellectual and Developmental Disabilities Research Center at Washington University, JNC PI); and by the National Institute of Mental Health, MH100019 (NM) and MH100029 (AK, WJ). Additional support provided by the Marcus Foundation, the Whitehead Foundation, and the Georgia Research Alliance.
• Keywords: SALIENCE; VISUAL-ATTENTION; INTRACLASS CORRELATION-COEFFICIENT; GENERAL-POPULATION; TRAITS; TODDLERS; Science & Technology - Other Topics; Multidisciplinary Sciences; FRONTAL EYE FIELD; TWIN; BEHAVIOR; Science & Technology; SPECTRUM DISORDER
• Research Categories: Health Sciences, Medicine and Surgery; Biology, Neuroscience

Abstract

Long before infants reach, crawl or walk, they explore the world by looking: they look to learn and to engage, giving preferential attention to social stimuli, including faces, face-like stimuli and biological motion. This capacity - social visual engagement - shapes typical infant development from birth and is pathognomonically impaired in children affected by autism. 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 information. In a series of eye-tracking experiments conducted with 338 toddlers, including 166 epidemiologically ascertained twins (enrolled by representative sampling from the general population), 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 characteristics that are the most highly heritable, preferential attention to eye and mouth regions of the face, are also those that are differentially decreased in children with autism (χ 2 = 64.03, P < 0.0001). These results implicate social visual engagement as a neurodevelopmental endophenotype not only for autism, but also for population-wide variation in social-information seeking. In addition, these results reveal a means of human biological niche construction, with phenotypic differences emerging from the interaction of individual genotypes with early life experience.