Hostname: page-component-77c89778f8-swr86 Total loading time: 0 Render date: 2024-07-19T23:19:53.511Z Has data issue: false hasContentIssue false

Social motivation in infancy is associated with familial recurrence of ASD

Published online by Cambridge University Press:  03 October 2022

Natasha Marrus*
Affiliation:
Department of Psychiatry, Washington University School of Medicine, St Louis, MO, USA
Kelly N. Botteron
Affiliation:
Department of Psychiatry, Washington University School of Medicine, St Louis, MO, USA
Zoë Hawks
Affiliation:
Department of Psychological & Brain Sciences, Washington University in St. Louis, St Louis, MO, USA
John R. Pruett Jr.
Affiliation:
Department of Psychiatry, Washington University School of Medicine, St Louis, MO, USA
Jed T. Elison
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Joshua J. Jackson
Affiliation:
Department of Psychological & Brain Sciences, Washington University in St. Louis, St Louis, MO, USA
Lori Markson
Affiliation:
Department of Psychological & Brain Sciences, Washington University in St. Louis, St Louis, MO, USA
Adam T. Eggebrecht
Affiliation:
Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, USA
Catherine A. Burrows
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Lonnie Zwaigenbaum
Affiliation:
Department of Pediatrics, University of Alberta, Edmonton, Alberta, Canada
Stephen R. Dager
Affiliation:
Department of Radiology, University of Washington, Seattle, WA, USA
Annette M. Estes
Affiliation:
Department of Speech and Hearing Sciences, University of Washington, Seattle, WA, USA
Heather Cody Hazlett
Affiliation:
Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Robert T. Schultz
Affiliation:
Center for Austin Research, The Children’s Hospital of Philadelphia, University of Pennsylvania, Philadelphia, PA, USA
Joseph Piven
Affiliation:
Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
John N. Constantino
Affiliation:
Department of Psychiatry, Washington University School of Medicine, St Louis, MO, USA
*
Corresponding author: Natasha Marrus, email: natasha@wustl.edu

Abstract

Pre-diagnostic deficits in social motivation are hypothesized to contribute to autism spectrum disorder (ASD), a heritable neurodevelopmental condition. We evaluated psychometric properties of a social motivation index (SMI) using parent-report item-level data from 597 participants in a prospective cohort of infant siblings at high and low familial risk for ASD. We tested whether lower SMI scores at 6, 12, and 24 months were associated with a 24-month ASD diagnosis and whether social motivation’s course differed relative to familial ASD liability. The SMI displayed good internal consistency and temporal stability. Children diagnosed with ASD displayed lower mean SMI T-scores at all ages and a decrease in mean T-scores across age. Lower group-level 6-month scores corresponded with higher familial ASD liability. Among high-risk infants, strong decline in SMI T-scores was associated with 10-fold odds of diagnosis. Infant social motivation is quantifiable by parental report, differentiates children with versus without later ASD by age 6 months, and tracks with familial ASD liability, consistent with a diagnostic and susceptibility marker of ASD. Early decrements and decline in social motivation indicate increased likelihood of ASD, highlighting social motivation’s importance to risk assessment and clarification of the ontogeny of ASD.

Type
Regular Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Joseph Piven and John N. Constantino contributed equally.

References

Abrams, D. A., Lynch, C. J., Cheng, K. M., Phillips, J., Supekar, K., Ryali, S., Uddin, L. Q., & Menon, V. (2013). Underconnectivity between voice-selective cortex and reward circuitry in children with autism. Proceedings of the National Academy of Sciences, 110(29), 1206012065. https://doi.org/10.1073/pnas.1302982110 CrossRefGoogle ScholarPubMed
Albert, R. R., Schwade, J. A., & Goldstein, M. H. (2018). The social functions of babbling: Acoustic and contextual characteristics that facilitate maternal responsiveness. Developmental Science, 21(5), e12641. https://doi.org/10.1111/desc.12641 CrossRefGoogle ScholarPubMed
American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Author.Google Scholar
Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012). The social motivation theory of autism. Trends in Cognitive Sciences, 16(4), 231239. https://doi.org/10.1016/j.tics.2012.02.007 CrossRefGoogle ScholarPubMed
Clements, C. C., Zoltowski, A. R., Yankowitz, L. D., Yerys, B. E., Schultz, R. T., & Herrington, J. D. (2018). Evaluation of the social motivation hypothesis of autism: A systematic review and meta-analysis. JAMA Psychiatry, 75(8), 797808. https://doi.org/10.1001/jamapsychiatry.2018.1100 CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). L. Erlbaum Associates.Google Scholar
Cohen, P., Cohen, J., Aiken, L. S., & West, S. G. (1999). The problem of units and the circumstances for POMP. Multivariate Behavioral Research, 34(3), 315346.CrossRefGoogle Scholar
Constantino, J. N., Charman, T., & Jones, E. (2021). Clinical and translational implications of an emerging developmental substructure for autism. Annual Review of Clinical Psychology, 17(1), 365389. https://doi.org/10.1146/annurev-clinpsy-081219-110503 CrossRefGoogle ScholarPubMed
Cronbach, L. J. (1951). Coefficient alpha and the internal structure of tests. Psychometrika, 16(3), 297334. https://doi.org/10.1007/BF02310555 CrossRefGoogle Scholar
Das, S., Glatard, T., MacIntyre, L. C., Madjar, C., Rogers, C., Rousseau, M. E., Rioux, P., MacFarlane, D., Mohades, Z., Gnanasekaran, R., Makowski, C., Kostopoulos, P., Adalat, R., Khalili-Mahani, N., Niso, G., Moreau, J. T., Evans, A. C. (2016). The MNI data-sharing and processing ecosystem. Neuroimage, 124(2), 11881195. https://doi.org/10.1016/j.neuroimage.2015.08.076 CrossRefGoogle ScholarPubMed
Elison, J. T. (2020). Editorial: Considering transient instantiators. Development and Psychopathology, 32(4), 11731174. https://doi.org/10.1017/S0954579420001807 CrossRefGoogle ScholarPubMed
Elsabbagh, M., & Johnson, M. H. (2016). Autism and the social brain: The first-year puzzle. Biological Psychiatry, 80(2), 9499. https://doi.org/10.1016/j.biopsych.2016.02.019 CrossRefGoogle ScholarPubMed
Emde, R. N., & Harmon, R. J. (1972). Endogenous and exogenous smiling systems in early infancy. Journal of the American Academy of Child Psychiatry, 11(2), 177200. https://doi.org/10.1016/s0002-7138(10)60071-4 CrossRefGoogle ScholarPubMed
Enders, C. K. (2017). Multiple imputation as a flexible tool for missing data handling in clinical research. Behaviour Research and Therapy, 98(1), 418. https://doi.org/10.1016/j.brat.2016.11.008 CrossRefGoogle ScholarPubMed
Estes, A., Munson, J., Rogers, S. J., Greenson, J., Winter, J., & Dawson, G. (2015). Long-term outcomes of early intervention in 6-year-old children with autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 54(7), 580587. https://doi.org/10.1016/j.jaac.2015.04.005 CrossRefGoogle ScholarPubMed
Estes, A., Zwaigenbaum, L., Gu, H., St John, T., Paterson, S., Elison, J. T., Hazlett, H., Botteron, K., Dager, S. R., Schultz, R. T., Kostopoulos, P., Evans, A., Dawson, G., Eliason, J., Alvarez, S., Piven, J., & IBIS Network (2015). Behavioral, cognitive, and adaptive development in infants with autism spectrum disorder in the first 2 years of life. Journal of Neurodevelopmental Disorders, 7(1), 24. https://doi.org/10.1186/s11689-015-9117-6 CrossRefGoogle ScholarPubMed
Fenson, L., Marchman, V. A., Thal, D. J., Dale, P. S., Reznick, J. S., & Bates, E. (2006). MacArthur-Bates communicative development inventories: User’s guide and technical manual (2nd ed.). Brookes Publishing Company.Google Scholar
Frazier, T. W., Ratliff, K. R., Gruber, C., Zhang, Y., Law, P. A., & Constantino, J. N. (2014). Confirmatory factor analytic structure and measurement invariance of quantitative autistic traits measured by the social responsiveness scale-2. Autism: The International Journal of Research and Practice, 18(1), 3144. https://doi.org/10.1177/1362361313500382 CrossRefGoogle ScholarPubMed
Fuller, E. A., & Kaiser, A. P. (2020). The effects of early intervention on social communication outcomes for children with autism spectrum disorder: A meta-analysis. Journal of Autism and Developmental Disorders, 50(5), 16831700. https://doi.org/10.1007/s10803-019-03927-z CrossRefGoogle ScholarPubMed
Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the revised infant behavior questionnaire. Infant Behavior and Development, 26(1), 6486. https://doi.org/10.1016/S0163-6383(02)00169-8 CrossRefGoogle Scholar
Guo, X., Duan, X., Suckling, J., Wang, J., Kang, X., Chen, H., Biswal, B. B., Cao, J., He, C., Xiao, J., Huang, X., Wang, R., Han, S., Fan, Y. S., Guo, J., Zhao, J., Wu, L., Chen, H. (2021). Mapping progressive gray matter alterations in early childhood autistic brain. Cerebral Cortex, 31(3), 15001510. https://doi.org/10.1093/cercor/bhaa304 CrossRefGoogle ScholarPubMed
Hay, D. F., Nash, A., & Pedersen, J. (1983). Interaction between six-month-old peers. Child Development, 54(3), 557562. https://doi.org/10.2307/1130042 CrossRefGoogle ScholarPubMed
Jaswal, V. K., & Akhtar, N. (2019). Being versus appearing socially uninterested: Challenging assumptions about social motivation in autism. Behavioral and Brain Sciences, 42, e82. https://doi.org/10.1017/S0140525X18001826 CrossRefGoogle Scholar
Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature, 504(7480), 427431. https://doi.org/10.1038/nature12715 CrossRefGoogle ScholarPubMed
Klein-Tasman, B. P., Li-Barber, K. T., & Magargee, E. T. (2010). Honing in on the social phenotype in Williams syndrome using multiple measures and multiple raters. Journal of Autism and Developmental Disorders, 41(3), 341351. https://doi.org/10.1007/s10803-010-1060-5 CrossRefGoogle Scholar
Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2000). Autism diagnostic observation scale. Western Psychological Services.Google Scholar
Markova, G. (2018). The games infants play: Social games during early mother-infant interactions and their relationship with oxytocin. Frontiers in Psychology, 9, 1041. https://doi.org/10.3389/fpsyg.2018.01041 CrossRefGoogle ScholarPubMed
Marrus, N., Grant, J. D., Harris-Olenak, B., Albright, J., Bolster, D., Haber, J. R., Jacob, T., Zhang, Y., Heath, A. C., Agrawal, A., Constantino, J. N., Elison, J. T., Glowinski, A. L. (2020). Genetic architecture of reciprocal social behavior in toddlers: Implications for heterogeneity in the early origins of autism spectrum disorder. Development and Psychopathology, 32(4), 11901205. https://doi.org/10.1017/S0954579420000723 CrossRefGoogle ScholarPubMed
Marrus, N., Hall, L. P., Paterson, S. J., Elison, J. T., Wolff, J. J., Swanson, M. R., Parish-Morris, J., Eggebrecht, A. T., Pruett, J. R. Jr, Hazlett, H. C., Zwaigenbaum, L., Dager, S., Estes, A. M., Schultz, R. T., Botteron, K. N., Piven, J., Constantino, J. N., & IBIS Network (2018). Language delay aggregates in toddler siblings of children with autism spectrum disorder. Journal of Neurodevelopmental Disorders, 10(1), 116. https://doi.org/10.1186/s11689-018-9247-8 CrossRefGoogle ScholarPubMed
Messinger, D. S., & Fogel, A. (1998). Give and take: The development of conventional infant gestures. Merrill-Palmer Quarterly, 44(4), 566590. https://www.jstor.org/stable/23093754 Google Scholar
Miller, M., Iosif, A. M., Hill, M., Young, G. S., Schwichtenberg, A. J., & Ozonoff, S. (2017). Response to name in infants developing autism spectrum disorder: A prospective study. The Journal of Pediatrics, 183, 141146. https://doi.org/10.1016/j.jpeds.2016.12.071 CrossRefGoogle ScholarPubMed
Mullen, E. (1995). Mullen scales of early learning. Guidance Service Publishing.Google Scholar
Neuhaus, E., Bernier, R. A., & Webb, S. J. (2021). Social motivation across multiple measures: Caregiver-report of children with autism spectrum disorder. Autism Research: Official Journal of the International Society for Autism Research, 14(2), 369379. https://doi.org/10.1002/aur.2386 CrossRefGoogle ScholarPubMed
Nunnally, J. C. (1978). Psychometric theory (2nd ed.). McGraw-Hill.Google Scholar
Ozonoff, S., Iosif, A. M., Baguio, F., Cook, I. C., Hill, M. M., Hutman, T., Rogers, S. J., Rozga, A., Sangha, S., Sigman, M., Steinfeld, M. B., Young, G. S. (2010). A prospective study of the emergence of early behavioral signs of autism. Journal of the American Academy of Child & Adolescent Psychiatry, 49(3), 256–266.e1-2. https://doi.org/10.1016/j.jaac.2009.11.009 Google ScholarPubMed
Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., Bryson, S., Carver, L. J., Constantino, J. N., Dobkins, K., Hutman, T., Iverson, J. M., Landa, R., Rogers, S. J., Sigman, M., Stone, W. L. (2011). Recurrence risk for autism spectrum disorders: A baby siblings research consortium study. Pediatrics, 128(3), e488e495. https://doi.org/10.1542/peds.2010-2825 CrossRefGoogle ScholarPubMed
Palomo, R., Belinchón, M., & Ozonoff, S. (2006). Autism and family home movies: A comprehensive review. Journal of Developmental & Behavioral Pediatrics, 27(2), S59S68. https://doi.org/10.1097/00004703-200604002-00003 CrossRefGoogle ScholarPubMed
Phillips, J. M., Uljarević, M., Schuck, R. K., Schapp, S., Solomon, E. M., Salzman, E., Allerhand, L., Libove, R. A., Frazier, T. W., Hardan, A. Y. (2019). Development of the Stanford Social Dimensions Scale: Initial validation in autism spectrum disorder and in neurotypicals. Molecular Autism, 10(1), 116. https://doi.org/10.1186/s13229-019-0298-9 CrossRefGoogle ScholarPubMed
Rosa Salva, O., Farroni, T., Regolin, L., Vallortigara, G., & Johnson, M. H. (2011). The evolution of social orienting: Evidence from chicks (Gallus gallus) and human newborns. PLoS One, 6(4), e18802. https://doi.org/10.1371/journal.pone.0018802 CrossRefGoogle ScholarPubMed
Ross, H. S., & Goldman, B. D. (1977). Infants’ sociability toward strangers. Child Development, 48(2), 638642.CrossRefGoogle Scholar
Rubin, D. B. (1996). Multiple imputation after 18+ years. Journal of the American Statistical Association, 91(434), 473489. https://doi.org/10.2307/2291635 CrossRefGoogle Scholar
Sacrey, L. A. R., Bennett, J. A., & Zwaigenbaum, L. (2015). Early infant development and intervention for autism spectrum disorder. Journal of Child Neurology, 30(14), 19211929. https://doi.org/10.1177/0883073815601500 CrossRefGoogle ScholarPubMed
Sacrey, L. A. R., Zwaigenbaum, L., Bryson, S., Brian, J., Smith, I. M., Roberts, W., Szatmari, P., Vaillancourt, T., Roncadin, C., Garon, N. (2021). Screening for behavioral signs of autism spectrum disorder in 9-month-old infant siblings. Journal of Autism and Developmental Disorders, 51(3), 839848. https://doi.org/10.1007/s10803-020-04371-0 CrossRefGoogle ScholarPubMed
Saint-Georges, C., Cassel, R. S., Cohen, D., Chetouani, M., Laznik, M. C., Maestro, S., & Muratori, F. (2010). What studies of family home movies can teach us about autistic infants: A literature review. Research in Autism Spectrum Disorders, 4(3), 355366. https://doi.org/10.1016/j.rasd.2009.10.017 CrossRefGoogle Scholar
Sato, W., & Uono, S. (2019). The atypical social brain network in autism: Advances in structural and functional MRI studies. Current Opinion in Neurology, 32(4), 617621. https://doi.org/10.1097/WCO.0000000000000713 CrossRefGoogle ScholarPubMed
Schaffer, H. R., & Emerson, P. E. (1964). The development of social attachments in infancy. Monographs of the Society for Research in Child Development, 29(3), 177.CrossRefGoogle ScholarPubMed
Shi, B., Wu, W., Dai, M., Zeng, J., Luo, J., Cai, L., Wan, B., & Jing, J. (2021). Cognitive, language, and behavioral outcomes in children with autism spectrum disorders exposed to early comprehensive treatment models: A meta-analysis and meta-regression. Frontiers in Psychiatry, 12, 691148. https://doi.org/10.3389/fpsyt.2021.691148 CrossRefGoogle ScholarPubMed
Simion, F., Regolin, L., & Bulf, H. (2008). A predisposition for biological motion in the newborn baby. Proceedings of the National Academy of Sciences, 105(2), 809813. https://doi.org/10.1073/pnas.0707021105 CrossRefGoogle ScholarPubMed
Sparrow, S. S., Balla, D. A., & Cicchetti, D. V. (2005). Vineland adaptive behavior scales (2nd ed.). American Guidance Service.Google Scholar
Stucky, B. D., Gottfredson, N. C., & Panter, A. T. (2012). Item-Level factor analysis. In Cooper, H. Camic, P. M. Long, D. L. Panter, A. T. Rindskopf, D. & Sher, K. J. (Eds.), APA handbook of research methods in psychology, Vol. 1. Foundations, planning, measures, and psychometrics (pp. 683–697). American Psychological Association. https://doi.org/10.1037/13619-036 CrossRefGoogle Scholar
Su, P. L., Rogers, S. J., Estes, A., & Yoder, P. (2021). The role of early social motivation in explaining variability in functional language in toddlers with autism spectrum disorder. Autism: The International Journal of Research and Practice, 25(1), 244257. https://doi.org/10.1177/1362361320953260 CrossRefGoogle ScholarPubMed
Sung, Y. J., Dawson, G., Munson, J., Estes, A., Schellenberg, G. D., & Wijsman, E. M. (2005). Genetic investigation of quantitative traits related to autism: Use of multivariate polygenic models with ascertainment adjustment. The American Journal of Human Genetics, 76(1), 6881. https://doi.org/10.1086/426951 CrossRefGoogle ScholarPubMed
Tremblay-Leveau, H., & Nadel, J. (1996). Exclusion in triads: Can it serve ‘meta-communicative’ knowledge in 11- and 23-month-old children? British Journal of Developmental Psychology, 14(2), 145158. https://doi.org/10.1111/j.2044-835X.1996.tb00698.x CrossRefGoogle Scholar
Uljarević, M., Frazier, T. W., Jo, B., Phillips, J. M., Billingham, W., Cooper, M. N., & Hardan, A. Y. (2021). Relationship between social motivation in children with autism spectrum disorder and their parents. Frontiers in Neuroscience, 15, 660330. https://doi.org/10.3389/fnins.2021.660330 CrossRefGoogle ScholarPubMed
Vernetti, A., Senju, A., Charman, T., Johnson, M. H., Gliga, T., & BASIS Team (2018). Simulating interaction: Using gaze-contingent eye-tracking to measure the reward value of social signals in toddlers with and without autism. Developmental Cognitive Neuroscience, 29(4), 2129. https://doi.org/10.1016/j.dcn.2017.08.004 CrossRefGoogle ScholarPubMed
Watson, L. R., Baranek, G. T., Crais, E. R., Reznick, J. S., Dykstra, J., & Perryman, T. (2007). The first year inventory: Retrospective parent responses to a questionnaire designed to identify one-year-olds at risk for autism. Journal of Autism and Developmental Disorders, 37(1), 4961. https://doi.org/10.1007/s10803-006-0334-4 CrossRefGoogle ScholarPubMed
Zou, G. Y. (2007). Toward using confidence intervals to compare correlations. Psychological Methods, 12(4), 399413. https://doi.org/10.1037/1082-989X.12.4.399 CrossRefGoogle ScholarPubMed
Zwaigenbaum, L., Bryson, S. E., Brian, J., Smith, I. M., Sacrey, L., Armstrong, V., Roberts, W., Szatmari, P., Garon, N., Vaillancourt, T., Roncadin, C. (2021). Assessment of autism symptoms from 6 to 18 months of age using the autism observation scale for infants in a prospective high-risk cohort. Child Development, 92(3), 11871198. https://doi.org/10.1111/cdev.13485 CrossRefGoogle Scholar
Supplementary material: File

Marrus et al. supplementary material

Marrus et al. supplementary material

Download Marrus et al. supplementary material(File)
File 1.4 MB