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

Nature volume 547, pages 340–344 (2017)Cite this article

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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 (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 (χ2 = 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 seeking8. 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 experience7.

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Figure 1: Monozygotic twins exhibit high twin–twin concordance for eye- and mouth-looking, significantly greater than dizygotic twins or age- and sex-matched non-siblings.
Figure 2: Monozygotic twins exhibit greater probability of shifting their eyes at the same moments, in the same directions, and onto the same semantic content when viewing scenes of social interaction.
Figure 3: Monozygotic twins exhibit high twin–twin concordance in eye-looking, whether watching the same or different video stimuli, evidence of active niche-picking in the goal-directed seeking of social information.
Figure 4: Comparison of social visual engagement in epidemiologically ascertained toddlers from the general population relative to two cohorts of toddlers diagnosed with autism spectrum disorder.

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Acknowledgements

We thank the families and children for their participation. Research was supported by grants from the National Institute of Child Health & Human Development, HD068479 (J.N.C.) and U54 HD087011 (Intellectual and Developmental Disabilities Research Center at Washington University, J.N.C., principal investigator); and by the National Institute of Mental Health, MH100019 (N.M.) and MH100029 (A.K., W.J.). Additional support was provided by the Marcus Foundation, the Whitehead Foundation and the Georgia Research Alliance. Epidemiologic ascertainment of twins was made possible by the Missouri Family Register, a joint program of Washington University and the Missouri Department of Health and Senior Services; authorization to access was approved by the MO DHSS Institutional Review Board (S. Ayers, Chair) under auspices of the project entitled Early Quantitative Characterization of Reciprocal Social Behavior. We thank E. Mortenson, S. Sant, T. Gray, Y. Zhang, L. Campbell, L. Malik, A. Khan and E. McGarry for data collection and analysis; A. C. Heath and A. Agrawal for discussions of data analysis and statistics; C. Gunter for helpful comments on the manuscript; C. Drain and D. Hopper for project coordination and data collection; D. Jovanovic and R. Todorovic for contributions to twin family ascertainment; M. Panther for administrative support; and S. Kovar, J. Paredes, and M. Ly for designing and building the eye-tracking laboratory.

Author information

Authors and Affiliations

  1. Department of Psychiatry, Washington University, St Louis, 63110, Missouri, USA

    John N. Constantino, Stefanie Kennon-McGill, Claire Weichselbaum, Natasha Marrus, Alyzeh Haider & Anne L. Glowinski

  2. Department of Pediatrics, Washington University, St Louis, 63110, Missouri, USA

    John N. Constantino

  3. Intellectual and Developmental Disabilities Research Center, Washington University, St Louis, 63110, Missouri, USA

    John N. Constantino & Natasha Marrus

  4. Pediatric Biostatistics Core, Emory University School of Medicine, Atlanta, 30307, Georgia, USA

    Scott Gillespie

  5. Marcus Autism Center, Children’s Healthcare of Atlanta, Atlanta, 30329, Georgia, USA

    Cheryl Klaiman, Ami Klin & Warren Jones

  6. Division of Autism & Related Disabilities, Department of Pediatrics, Emory University School of Medicine, Atlanta, 30329, Georgia, USA

    Cheryl Klaiman, Ami Klin & Warren Jones

  7. Center for Translational Social Neuroscience, Emory University, Atlanta, 30329, Georgia, USA

    Ami Klin & Warren Jones

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Contributions

J.N.C., A.L.G., A.K. and W.J. developed the initial idea and study design. J.N.C. and W.J. had full access to all data and take responsibility for data integrity and accuracy of analyses. J.N.C. supervised participant characterization. W.J. supervised technology development, data acquisition and analysis. S.K.-M., C.W., N.M. and A.H. collected data, ensured quality control at Washington University, conducted sub-analyses and participated in manuscript writing and revision. S.G., C.K. and W.J. performed data processing at Emory, ensured quality control across sites and participated in manuscript revision. W.J., A.K. and J.N.C. interpreted data and wrote the manuscript.

Corresponding authors

Correspondence to John N. Constantino or Warren Jones.

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The authors declare no competing financial interests.

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Reviewer Information Nature thanks R. Adolphs, J. P. McCleery, C. Nelson and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 Measuring genetic structure of social visual engagement in 250 paired toddlers.

Data consisted of measurements in dizygotic twins (n = 84, 42 pairs), monozygotic twins (n = 82, 41 pairs), and non-sibling comparison children (n = 84, randomized to 42 pairs). a, Example still images from dyadic mutual gaze video stimuli. b, Data from two typically developing 18-month-old dizygotic (DZ) twins. c, Data from two typically developing 18-month-old monozygotic (MZ) twins. Plots (b, c) show two seconds of eye-tracking data, corresponding to each image in a (the onscreen image at midpoint of the two-second data sample). Data are overlaid on the corresponding regions of interest for each image, shaded to indicate eyes (dark grey), mouth (light grey), body (black), and object regions (white). Saccades are plotted as thin white lines with white dots; fixation data are plotted as larger coloured dots. d–f, Fixation time summaries for each comparison group for percentage of total fixation time on eye region (d), percentage of total fixation time on mouth region (e), and percentage of total time spent fixating (f). Box plots span full range of data collected, with vertical lines extending from minimum to maximum values, boxes spanning the 25th to 75th percentiles, and horizontal black lines marking medians.

Extended Data Figure 2 Between-group controls for calibration accuracy and oculomotor function.

To test for group-wise differences unrelated to subsequent paired comparisons in the main study experiments we measured calibration accuracy and oculomotor function. a–c, Total variance in calibration accuracy for age- and sex-matched non-sibling controls (a), dizygotic twins (b), and monozygotic twins (c). Plots show kernel density estimates of the distribution of measured fixation locations relative to calibration accuracy verification targets. d–f, Average calibration accuracy (in degrees) for non-sibling controls (d), dizygotic twins (e), and monozygotic twins (f). Crosses mark the location of mean calibration accuracy, while annuli mark 95% confidence intervals (95% CI). g–i, Concordance in calibration accuracy measurements for non-sibling controls (g), dizygotic twins (h), and monozygotic twins (i). Measurements in (g–i) are average accuracy per child across all accuracy verification trials. j, ICCs, plotted with 95% confidence intervals. k–m, Oculomotor relationship between maximum saccade velocity (Vmax) and amplitude (in degrees) for non-sibling controls (k), dizygotic twins (l), and monozygotic twins (m).

Extended Data Figure 3 Within-subject stability versus between-subject concordance.

For heritable traits, one expects to observe substantial within-subject stability contrasting with marked differences, varying by zygosity, in between-subject (twin–twin) concordance. a–d, Within-subject stability of observed levels of eye-looking for non-siblings (a, b), dizygotic twins (c), and monozygotic twins (d). Dots are each child’s measured level on the test comparison (x-axis) versus measured level on the retest comparison (y-axis)). (Scatter plots in a and b are repeated for comparison with plots f and g.) e, Group-wise summary of within-subject stability (test–retest reliability) of measurements of eye-looking quantified by ICC with two-way random effects model (ICC (2,1)). Error bars are 95% confidence intervals. Note that estimates assuming fixed rather than random effects of testing (ICC (3,k), not plotted) yield ICC values greater than 0.9 for each group, evidence that the analyses of inter-individual variation—the difference between individuals—are also highly reliable. f–i, Plots repeated from main text Fig. 1a–e, showing paired measurements of eye-looking in randomly paired non-siblings (f), in age- and sex-matched non-siblings (g), in dizygotic twins (h), and in monozygotic twins (i). Dots are measured levels per child, paired so that one child’s level of eye-looking is on the x-axis versus the paired child on the y-axis. j, ICCs and 95% confidence intervals for twin–twin concordance in eye-looking.

Extended Data Figure 4 Monozygotic twins maintain high twin–twin concordance, which is significantly greater than that observed in dizygotic twins, when tested again at 36 months.

a–c, Paired measurements of eye-looking in randomly assigned pairs (a), in dizygotic twins (b), and in monozygotic twins (c). d, ICCs and 95% confidence intervals across groups for eye-looking. e–h, Paired measurements of concordance in mouth-looking. i–l, Paired measurements of concordance in percentage of time spent attending to task (maintaining stable onscreen fixation). In all plots, randomly matched controls in white, dizygotic twins in orange, and monozygotic twins in blue. Error estimates are 95% confidence intervals. Dots are individual values for paired children, as in Extended Data Fig. 3f–i. m, n, Summary of results for monozygotic (m) and dizygotic (n) twins at initial time of testing (21 months, summary data from Fig. 1) relative to results at time of longitudinal follow-up (36 months, summary from d, h, l). Monozygotic twins exhibit marginally, though not significantly, increased concordance values when tested again at 36 months. By contrast, dizygotic twins exhibit marginally, though not significantly, decreased concordance values. Plotted data in a, e, and i are representative random pairings, selected to match the mean ICC value of all 10,000 re-samplings.

Extended Data Figure 5 Longitudinal within-subject stability versus longitudinal twin–twin concordance, from 21 until 36 months.

Dizygotic and monozygotic twins both show high levels of longitudinal within-subject stability when tested again 15 months after initial data were collected, but only monozygotic twins show high levels of longitudinal twin–twin concordance, with twin 1’s results at 21 months being highly concordant with twin 2’s at 36 months. a–d, Within-subject stability of observed levels of eye-looking (a) and mouth-looking (b) for dizygotic twins, and within-subject stability of eye-looking (c) and mouth-looking (d) for monozygotic twins. e, Summary of longitudinal within-subject stability quantified by ICC with two-way random effects model. Error bars are 95% confidence intervals. f–i, Longitudinal twin–twin concordance (twin 1 at 21 months paired with twin 2 at 36 months) for eye- (f) and mouth-looking (g) in dizygotic twins, and for eye- (h) and mouth-looking (i) in monozygotic twins. j, ICCs and 95% confidence intervals.

Extended Data Figure 6 Social visual engagement when watching triadic peer interaction stimuli in 250 paired toddlers.

Data consisted of measurements in dizygotic twins (n = 84, 42 pairs), monozygotic twins (n = 82, 41 pairs), and non-sibling comparison children (n = 84, randomized to 42 pairs). a, Example still images from triadic peer interaction stimuli. b, Data from two typically developing 18-month-old dizygotic twins. c, Data from two typically developing 18-month-old monozygotic twins. b, c, Two seconds of eye-tracking data are plotted, corresponding to each image in a (the onscreen image at midpoint of the two-second data sample). Data are overlaid on each image’s corresponding regions of interest, shaded to indicate eyes, mouth, body, and object regions. Saccades are plotted as thin white lines with white dots; fixation data are plotted as larger coloured dots. d–f, Fixation time summaries for each comparison group for percentage of total fixation time on eyes region (d), percentage of total fixation time on mouth region (e), and percentage of total time spent fixating (f). Boxplots span full range of data collected, with vertical lines extending from minimum to maximum values, boxes spanning the 25th to 75th percentiles, and horizontal black lines marking medians.

Extended Data Figure 7 Physical image properties that constitute eyes vary significantly from video stimulus to video stimulus in lightness, colour, contrast, orientation gradients, and motion.

a, Still images sampled from videos depicting dyadic mutual gaze stimuli (an entreating caregiver, engaging the child in mutual gaze and play routines). Still images from 5 out of 15 videos are shown (all 15 dyadic mutual gaze videos included in actual analyses). b, Eye region demarcated from each still image in a. Across all demarcated eye regions, across all frames of videos presented, physical image property profiles were analysed. c–h, In the rows to the right of each representative still image and corresponding eye region, physical image property profiles, analysed across all video frames, are given as histograms. c, Lightness. d, Red–green colour opponency. e, Yellow–blue colour opponency. f, Contrast. g, Orientation gradients. h, Motion. i, For each physical image property analysed in columns (a–h), i gives corresponding comparison plots across the five histograms located in the column directly above. j, Statistical comparisons of the measured image property distributions by two-sample Kolmogorov–Smirnov test. P values are corrected for multiple comparisons by the Bonferroni method. For each of the physical image properties analysed in columns (a–h), j presents the corresponding matrix of statistical comparisons (that is, the 1st row of coloured circles presents comparisons for Video 1 versus Video 2, Video 1 versus Video 3, and so on; while the 2nd row presents comparisons for Video 2 versus Video 3, Video 2 versus Video 4, and so on). k, Still images sampled from videos depicting triadic peer interaction stimuli (scenes of children interacting in a childcare setting). Still images from 5 out of 12 videos are shown (all 12 triadic peer interaction videos are included in the actual analyses). l, Eye regions demarcated from each still image in k. m–t, All parts of m–t are as in c–j.

Extended Data Table 1 Participant demographics
Full size table
Extended Data Table 2 Concordance in social visual engagement at 21 months, at 36 months, and from 21 until 36 months
Full size table
Extended Data Table 3 Size of experimental stimuli and viewing time summaries
Full size table

Related audio

Supplementary information

Data from one DZ twin pair watching an actress portraying the role of a caregiver engaging in dyadic interaction with the viewer (“Dyadic Mutual Gaze Video”)

Videos show example eye-tracking data for twin pairs. In each video, crosshairs mark the point-of-regard and eye movements of each of the two twins, overlaid on top of the stimulus video. The video stimuli shown to children contained audio, although the data videos shown here do not include audio. The changing color of each crosshair over time signifies eye movement events: on-screen fixations to regions of interest (red, eyes; green, mouth; blue, body; yellow, object); saccades (white), blinks (black crosshair followed by black square in upper left corner of the video); and off-screen fixations (no crosshair, gray square in upper left corner of the video). (MOV 953 kb)

Data from one MZ twin pair watching an actress portraying the role of a caregiver engaging in dyadic interaction with the viewer (“Dyadic Mutual Gaze Video”).

Videos show example eye-tracking data for twin pairs. In each video, crosshairs mark the point-of-regard and eye movements of each of the two twins, overlaid on top of the stimulus video. The video stimuli shown to children contained audio, although the data videos shown here do not include audio. The changing color of each crosshair over time signifies eye movement events: on-screen fixations to regions of interest (red, eyes; green, mouth; blue, body; yellow, object); saccades (white), blinks (black crosshair followed by black square in upper left corner of the video); and off-screen fixations (no crosshair, gray square in upper left corner of the video). (MOV 924 kb)

Data from one DZ twin pair watching scenes of children at play (“Triadic Peer Interaction Video”)

Videos show example eye-tracking data for twin pairs. In each video, crosshairs mark the point-of-regard and eye movements of each of the two twins, overlaid on top of the stimulus video. The video stimuli shown to children contained audio, although the data videos shown here do not include audio. The changing color of each crosshair over time signifies eye movement events: on-screen fixations to regions of interest (red, eyes; green, mouth; blue, body; yellow, object); saccades (white), blinks (black crosshair followed by black square in upper left corner of the video); and off-screen fixations (no crosshair, gray square in upper left corner of the video). (MOV 15346 kb)

Data from one MZ twin pair watching scenes of children at play (“Triadic Peer Interaction Video”)

Videos show example eye-tracking data for twin pairs. In each video, crosshairs mark the point-of-regard and eye movements of each of the two twins, overlaid on top of the stimulus video. The video stimuli shown to children contained audio, although the data videos shown here do not include audio. The changing color of each crosshair over time signifies eye movement events: on-screen fixations to regions of interest (red, eyes; green, mouth; blue, body; yellow, object); saccades (white), blinks (black crosshair followed by black square in upper left corner of the video); and off-screen fixations (no crosshair, gray square in upper left corner of the video). (MOV 15339 kb)

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Constantino, J., Kennon-McGill, S., Weichselbaum, C. et al. Infant viewing of social scenes is under genetic control and is atypical in autism. Nature 547, 340–344 (2017). https://doi.org/10.1038/nature22999

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