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Neural responses to affective speech, including motherese, map onto clinical and social eye tracking profiles in toddlers with ASD

Nature Human Behaviour volume 6, pages 443–454 (2022)Cite this article

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Abstract

Affective speech, including motherese, captures an infant’s attention and enhances social, language and emotional development. Decreased behavioural response to affective speech and reduced caregiver–child interactions are early signs of autism in infants. To understand this, we measured neural responses to mild affect speech, moderate affect speech and motherese using natural sleep functional magnetic resonance imaging and behavioural preference for motherese using eye tracking in typically developing toddlers and those with autism. By combining diverse neural–clinical data using similarity network fusion, we discovered four distinct clusters of toddlers. The autism cluster with the weakest superior temporal responses to affective speech and very poor social and language abilities had reduced behavioural preference for motherese, while the typically developing cluster with the strongest superior temporal response to affective speech showed the opposite effect. We conclude that significantly reduced behavioural preference for motherese in autism is related to impaired development of temporal cortical systems that normally respond to parental affective speech.

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Fig. 1: Experimental design and data analysis flow chart.
Fig. 2: Reduced language-related brain activation in toddlers with ASD as compared to TD toddlers.
Fig. 3: Scatterplots showing correlations between brain activation to language and social communication abilities in toddlers.
Fig. 4: Gaze-contingent eye tracking measures of preference for motherese and correlations with neural response to motherese in toddlers with ASD and TD toddlers.
Fig. 5: TD and ASD subgroups with distinct fMRI–clinical patterns and correlations with behavioural preference for motherese.

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Data availability

The tidy data used in this study are publicly available at https://github.com/Yaqiongxiao/asdmotherese_fmriSNF.

Code availability

Completed R code for implementing all analyses reported in this article is available at https://github.com/Yaqiongxiao/asdmotherese_fmriSNF.

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Acknowledgements

We thank the parents and children in San Diego who participated in our research, without whom this would not be possible. We are also fortunate to work with wonderful paediatricians and family practice physicians spanning a range of medical groups including UCSD, Sharp Rees-Stealy, Scripps, Rady-Children’s Primary Care Medical Group, Chula Vista Pediatrics, Graybill Medical Group, Grossmont Pediatrics, Linda Vista Health Care Center, Mills Pediatrics, North County Health Services, San Diego Family Care and Sea Breeze Pediatrics. We are grateful for their support. This work was supported by NIDCD grant 1R01DC016385 awarded to E.C. and K.P.; NIMH grants R01MH118879 and R01MH104446 awarded to K.P.; and 755816 European Research Council awarded to M.V.L. and E.C.. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

  1. Autism Center of Excellence, Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA

    Yaqiong Xiao, Teresa H. Wen, Disha Goel, Karen Pierce & Eric Courchesne

  2. Department of Psychology, University of Miami, Coral Gables, FL, USA

    Lauren Kupis

  3. Department of Psychiatry, University of California, San Diego, La Jolla, CA, USA

    Lisa T. Eyler

  4. VISN 22 Mental Illness Research, Education, and Clinical Center, VA San Diego Healthcare System, San Diego, CA, USA

    Lisa T. Eyler

  5. Point Loma Pediatrics, UC San Diego Health Physician Network, San Diego, CA, USA

    Keith Vaux

  6. Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, Italy

    Michael V. Lombardo

  7. Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK

    Michael V. Lombardo

  8. Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA

    Nathan E. Lewis

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  1. Yaqiong Xiao
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Contributions

E.C., K.P., L.T.E. and L.K. conceived the idea and designed the study. L.K., D.G., T.H.W. and K.V. recruited the participants. L.K., D.G., T.H.W., Y.X., L.T.E. and E.C. collected the data. Y.X. conceived and performed all analyses. E.C., M.V.L. and N.E.L. aided in data analyses. E.C., K.P. and M.V.L. obtained grant funding. Y.X. and E.C. wrote the manuscript. All authors contributed to editing the manuscript.

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Correspondence to Yaqiong Xiao, Karen Pierce or Eric Courchesne.

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The authors declare no competing interests.

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Peer review information Nature Human Behaviour thanks Laura Edwards and Giorgia Silani for their contribution to the peer review of this work. Peer reviewer reports are available.

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Xiao, Y., Wen, T.H., Kupis, L. et al. Neural responses to affective speech, including motherese, map onto clinical and social eye tracking profiles in toddlers with ASD. Nat Hum Behav 6, 443–454 (2022). https://doi.org/10.1038/s41562-021-01237-y

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