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Two-year-olds with autism orient to non-social contingencies rather than biological motion

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Abstract

Typically developing human infants preferentially attend to biological motion within the first days of life1. This ability is highly conserved across species2,3 and is believed to be critical for filial attachment and for detection of predators4. The neural underpinnings of biological motion perception are overlapping with brain regions involved in perception of basic social signals such as facial expression and gaze direction5, and preferential attention to biological motion is seen as a precursor to the capacity for attributing intentions to others6. However, in a serendipitous observation7, we recently found that an infant with autism failed to recognize point-light displays of biological motion, but was instead highly sensitive to the presence of a non-social, physical contingency that occurred within the stimuli by chance. This observation raised the possibility that perception of biological motion may be altered in children with autism from a very early age, with cascading consequences for both social development and the lifelong impairments in social interaction that are a hallmark of autism spectrum disorders8. Here we show that two-year-olds with autism fail to orient towards point-light displays of biological motion, and their viewing behaviour when watching these point-light displays can be explained instead as a response to non-social, physical contingencies—physical contingencies that are disregarded by control children. This observation has far-reaching implications for understanding the altered neurodevelopmental trajectory of brain specialization in autism9.

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Figure 1: Two-year-olds with autism show no preferential attention to biological motion, whereas control children show significant preferences.
Figure 2: When the animation contains a physical contingency, two-year-olds with autism do show significant viewing preferences.
Figure 3: Quantification of audiovisual synchrony.
Figure 4: The level of AVS is highly correlated with preferential viewing in two-year-olds with autism, is uncorrelated with viewing in control children, and can predict ASD viewing patterns in new animations.

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Change history

  • 14 May 2009

    The Y axis label on Fig. 3c was changed on 14 May 2009.

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Acknowledgements

This work was supported by a grant from the National Institutes of Mental Health (U54-MH66494), by Autism Speaks (piloting of methods), and by the Simons Foundation (current methodological developments). We wish to thank the families of the children included in this study for their time and participation. We would also like to thank F. Shic for conceptual discussions and thoughts on methods. We would like to thank L. Dickholtz, A. Kord, L. Else and M. Campisi for their assistance in creating the biological motion stimuli. We also wish to thank K. Carr, A. Blank, A. Bhatt, S. Shultz and K. Knoch for their help in this research project, and our colleagues K. Chawarska, R. Paul and F. Volkmar for conceptual discussions and for their contributions to the clinical characterization of the samples.

Author Contributions A.K. and W.J. developed the initial idea and design of the study, interpreted data, wrote the final manuscript, and take full responsibility for the integrity of data and the accuracy of data analysis. A.K. supervised participant characterization. W.J. supervised all technical aspects of experimental procedure, data acquisition and analysis. P.G. contributed to initial development of AVS methods and data analysis. D.J.L., with W.J. and G.R., developed the final AVS methods. G.R., with W.J. and A.K., helped develop new animations for the second experiment. W.J. created the figures. A.K. and W.J. performed the final revision of the manuscript for intellectual content.

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Correspondence to Ami Klin or Warren Jones.

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This file contains Supplementary Notes for Supplementary Movies 1-2 and Supplementary Video 3, Supplementary Tables 1-2, Supplementary Data and Supplementary References. (PDF 81 kb)

Supplementary Movie 1

This movie complements Figure 1 in the main text (see file s1 for full Legend). (MOV 7132 kb)

Supplementary Movie 2

This movie complements Figure 2 in the main text (see file s1 for full Legend). (MOV 8950 kb)

Supplementary Video 3

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Klin, A., Lin, D., Gorrindo, P. et al. Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature 459, 257–261 (2009). https://doi.org/10.1038/nature07868

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