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Relationships between autistic traits, insufficient sleep, and real-world executive functions in children: a mediation analysis of a national epidemiological survey

Published online by Cambridge University Press:  26 November 2019

Tsung-Han Tsai ,
Yi-Lung Chen Open the ORCID record for Yi-Lung Chen [Opens in a new window]  and
Susan Shur-Fen Gau Open the ORCID record for Susan Shur-Fen Gau [Opens in a new window]
Tsung-Han Tsai
Affiliation:
School of Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan
Yi-Lung Chen
Affiliation:
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan
Susan Shur-Fen Gau*
Affiliation:
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan
*
Author for correspondence: Susan Shur-Fen Gau, E-mail: [email protected]
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Abstract

Background

Although the literature documents low executive functions and sleep deficits in individuals with autism spectrum disorder or subclinical autistic traits, no study has simultaneously examined their relationships in the general child population. This study aimed to examine whether autistic traits impacted real-world executive functions through insufficient sleep in a nationally representative sample of children.

Methods

This was a national survey of 6832 primary and secondary school students, aged 8–14 years old, with equal sex distribution (3479 boys, 50.8%). Parents reported their child's nocturnal sleep duration and the need for sleep to maintain their daytime function and the Social Responsiveness Scale and the Behavior Rating Inventory of Executive Function (BRIEF) for their children's autistic traits and real-world executive functions, respectively.

Results

We found that autistic traits exerted indirect effects on real-world executive functions through sleep deficits, independent of sex, and age. Moreover, such an indirect effect was observed only from restricted and repetitive behaviors to executive functions through sleep deficits, but not in the other components of autistic traits (i.e. social communication and interaction).

Conclusions

Our novel findings underscore the importance of sleep and autistic traits in executive functions and suggest potential mechanisms that may underlie the observed correlational structure among autistic behaviors, sleep deficits, and low executive function performance.

Keywords

Autism spectrum disorderautistic traitsexecutive functioninsufficient sleepmediation
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 4 , March 2021 , pp. 579 - 586
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Copyright
Copyright © Cambridge University Press 2019

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Footnotes

*

Tsung-Han Tsai and Yi-Lung Chen contributed equally to this work as the joint first authors.

References

Anderson, B., Storfer-Isser, A., Taylor, H. G., Rosen, C. L., & Redline, S. (2009). Associations of executive function with sleepiness and sleep duration in adolescents. Pediatrics, 123(4), e701–e707. doi:10.1542/peds.2008-1182.CrossRefGoogle ScholarPubMed
Astill, R. G., Van der Heijden, K. B., Van Ijzendoorn, M. H., & Van Someren, E. J. (2012). Sleep, cognition, and behavioral problems in school-age children: a century of research meta-analyzed. Psychological Bulletin, 138(6), 1109–1138. doi:10.1037/a0028204.CrossRefGoogle ScholarPubMed
Bajeux, E., Klemanski, D. H., Husky, M., Leray, E., Chee, C. C., Shojaei, T., … Kovess-Masfety, V. (2018). Factors associated with parent–child discrepancies in reports of mental health disorders in young children. Child Psychiatry & Human Development, 49(6), 1003–1010. doi:10.1007/s10578-018-0815-7.CrossRefGoogle ScholarPubMed
Baron, I. S. (2000). Behavior rating inventory of executive function. Child Neuropsychology, 6(3), 235–238. doi:10.1076/chin.6.3.235.3152.Google ScholarPubMed
Beebe, D. W. (2011). Cognitive, behavioral, and functional consequences of inadequate sleep in children and adolescents. Pediatric Clinics of North America, 58(3), 649–665. doi:10.1016/j.pcl.2011.03.002.CrossRefGoogle ScholarPubMed
Best, J. R., & Miller, P. H. (2010). A developmental perspective on executive function. Child Development, 81(6), 1641–1660. doi:10.1111/j.1467-8624.2010.01499.x.CrossRefGoogle ScholarPubMed
Chen, S. F., Chien, Y. L., Wu, C. T., Shang, C. Y., Wu, Y. Y., & Gau, S. S. (2016). Deficits in executive functions among youths with autism spectrum disorders: an age-stratified analysis. Psychological Medicine, 46(8), 1625–1638. doi:10.1017/S0033291715002238.CrossRefGoogle ScholarPubMed
Chen, Y.-L., Chen, W. J., Lin, K.-C., Shen, L.-J., & Gau, S. S.-F. (2019). Prevalence of DSM-5 mental disorders in a nationally representative sample of children in Taiwan: methodology and main findings. Epidemiology and Psychiatric Sciences, 1–9. doi:10.1017/S2045796018000793 (Epub ahead of print).Google Scholar
Chien, Y. L., Gau, S. S., Shang, C. Y., Chiu, Y. N., Tsai, W. C., & Wu, Y. Y. (2015). Visual memory and sustained attention impairment in youths with autism spectrum disorders. Psychological Medicine, 45(11), 2263–2273. doi:10.1017/S0033291714003201.CrossRefGoogle ScholarPubMed
Chou, M.-C., Chou, W.-J., Chiang, H.-L., Wu, Y.-Y., Lee, J.-C., Wong, C.-C., & Gau, S. S.-F. (2012). Sleep problems among Taiwanese children with autism, their siblings and typically developing children. Research in Autism Spectrum Disorders, 6(2), 665–672. doi:10.1016/j.rasd.2011.09.010.CrossRefGoogle Scholar
Cohen, S., Conduit, R., Lockley, S. W., Rajaratnam, S. M., & Cornish, K. M. (2014). The relationship between sleep and behavior in autism spectrum disorder (ASD): a review. Journal of Neurodevelopmental Disorders, 6(1), 44. doi:10.1186/1866-1955-6-44.CrossRefGoogle ScholarPubMed
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., … Reich, W. (2003). Validation of a BRIEF quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433. doi:10.1023/a:1025014929212.CrossRefGoogle ScholarPubMed
Cortesi, F., Giannotti, F., Ivanenko, A., & Johnson, K. (2010). Sleep in children with autistic spectrum disorder. Sleep Medicine, 11(7), 659–664. doi:10.1016/j.sleep.2010.01.010.CrossRefGoogle ScholarPubMed
Dai, M., Lin, L., Liang, J., Wang, Z., & Jing, J. (2018). Gender difference in the association between executive function and autistic traits in typically developing children. Journal of Autism and Developmental Disorders, 49(3), 1182–1192. doi:10.1007/s10803-018-3813-5.CrossRefGoogle Scholar
de Bruin, E. J., van Run, C., Staaks, J., & Meijer, A. M. (2017). Effects of sleep manipulation on cognitive functioning of adolescents: a systematic review. Sleep Medicine Reviews, 32, 45–57. doi:10.1016/j.smrv.2016.02.006.CrossRefGoogle ScholarPubMed
de Vries, M., & Geurts, H. (2015). Influence of autism traits and executive functioning on quality of life in children with an autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(9), 2734–2743. doi:10.1007/s10803-015-2438-1.CrossRefGoogle ScholarPubMed
Demetriou, E. A., Lampit, A., Quintana, D. S., Naismith, S. L., Song, Y. J. C., Pye, J. E., … Guastella, A. J. (2018). Autism spectrum disorders: a meta-analysis of executive function. Molecular Psychiatry, 23(5), 1198–1204. doi:10.1038/mp.2017.75.CrossRefGoogle ScholarPubMed
Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64, 135–168. doi:10.1146/annurev-psych-113011-143750.CrossRefGoogle ScholarPubMed
Frazier, T. W., Youngstrom, E. A., Speer, L., Embacher, R., Law, P., Constantino, J., …Eng, C. (2012). Validation of proposed DSM-5 criteria for autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 51(1), 28–40. e23. doi:10.1016/j.jaac.2011.09.021.CrossRefGoogle ScholarPubMed
Gau, S. F. and Soong, W. T. (2003). The transition of sleep-wake patterns in early adolescence. Sleep, 26(4), 449–454. doi:10.1093/sleep/26.4.449.CrossRefGoogle ScholarPubMed
Gau, S. S., & Merikangas, K. R. (2004). Similarities and differences in sleep-wake patterns among adults and their children. Sleep, 27(2), 299–304. doi:10.1093/sleep/27.2.299.CrossRefGoogle ScholarPubMed
Gau, S. S.-F., Liu, L.-T., Wu, Y.-Y., Chiu, Y.-N., & Tsai, W.-C. (2013). Psychometric properties of the Chinese version of the social responsiveness scale. Research in Autism Spectrum Disorders, 7(2), 349–360. doi:10.1016/j.rasd.2012.10.004.CrossRefGoogle Scholar
Hafeman, D. M. (2009). ‘Proportion explained’: a causal interpretation for standard measures of indirect effect? American Journal of Epidemiology, 170(11), 1443–1448. doi:10.1093/aje/kwp283.CrossRefGoogle Scholar
Happe, F., Booth, R., Charlton, R., & Hughes, C. (2006). Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: examining profiles across domains and ages. Brain and Cognition, 61(1), 25–39. doi:10.1016/j.bandc.2006.03.004.CrossRefGoogle ScholarPubMed
Harvey, A. G., Tang, N. K. Y., & Browning, L. (2005). Cognitive approaches to insomnia. Clinical Psychology Review, 25(5), 593–611. doi:10.1016/j.cpr.2005.04.005.CrossRefGoogle ScholarPubMed
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.Google Scholar
Hill, E. L. (2004). Evaluating the theory of executive dysfunction in autism. Developmental Review, 24(2), 189–233. doi:10.1016/j.dr.2004.01.001.CrossRefGoogle Scholar
Hollway, J. A., Aman, M. G., & Butter, E. (2013). Correlates and risk markers for sleep disturbance in participants of the autism treatment network. Journal of Autism and Developmental Disorders, 43(12), 2830–2843. doi:10.1007/s10803-013-1830-y.CrossRefGoogle ScholarPubMed
Hsiao, M. N., Tseng, W. L., Huang, H. Y., & Gau, S. S. (2013). Effects of autistic traits on social and school adjustment in children and adolescents: the moderating roles of age and gender. Research in Developmental Disabilities, 34(1), 254–265. doi:10.1016/j.ridd.2012.08.001.CrossRefGoogle ScholarPubMed
Humphreys, J. S., Gringras, P., Blair, P. S., Scott, N., Henderson, J., Fleming, P. J., & Emond, A. M. (2014). Sleep patterns in children with autistic spectrum disorders: a prospective cohort study. Archives of Disease in Childhood, 99(2), 114–118. doi:10.1136/archdischild-2013-304083.CrossRefGoogle ScholarPubMed
Hus, V., Bishop, S., Gotham, K., Huerta, M., & Lord, C. (2013). Factors influencing scores on the social responsiveness scale. Journal of Child Psychology and Psychiatry, 54(2), 216–224. doi:10.1111/j.1469-7610.2012.02589.x.CrossRefGoogle ScholarPubMed
Hyseni, F., Blanken, L. M. E., Muetzel, R., Verhulst, F. C., Tiemeier, H., & White, T. (2018). Autistic traits and neuropsychological performance in 6- to-10-year-old children: a population-based study. Child Neuropsychology, 25(3), 1–18. doi:10.1080/09297049.2018.1465543.Google ScholarPubMed
Hysing, M., Pallesen, S., Stormark, K. M., Lundervold, A. J., & Sivertsen, B. (2013). Sleep patterns and insomnia among adolescents: a population-based study. Journal of Sleep Research, 22(5), 549–556. doi:10.1111/jsr.12055.CrossRefGoogle ScholarPubMed
Ibañez, L. V., Kobak, K., Swanson, A., Wallace, L., Warren, Z., & Stone, W. L. (2018). Enhancing interactions during daily routines: a randomized controlled trial of a web-based tutorial for parents of young children with ASD. Autism Research, 11(4), 667–678. doi:10.1002/aur.1919.CrossRefGoogle ScholarPubMed
Johnson, M. H. (2012). Executive function and developmental disorders: the flip side of the coin. Trends in Cognitive Sciences, 16(9), 454–457. doi:10.1016/j.tics.2012.07.001.CrossRefGoogle ScholarPubMed
Kenny, L., Cribb, S. J., & Pellicano, E. (2018). Childhood executive function predicts later autistic features and adaptive behavior in young autistic people: a 12-year prospective study. Journal of Abnormal Child Psychology, 47(6), 1089–1099. doi:10.1007/s10802-018-0493-8.CrossRefGoogle Scholar
Kenworthy, L., Anthony, L. G., Naiman, D. Q., Cannon, L., Wills, M. C., Luong-Tran, C., … Wallace, G. L. (2014). Randomized controlled effectiveness trial of executive function intervention for children on the autism spectrum. Journal of Child Psychology and Psychiatry, 55(4), 374–383. doi:10.1111/jcpp.12161.CrossRefGoogle ScholarPubMed
Leung, R. C., Vogan, V. M., Powell, T. L., Anagnostou, E., & Taylor, M. J. (2016). The role of executive functions in social impairment in autism spectrum disorder. Child Neuropsychology, 22(3), 336–344. doi:10.1080/09297049.2015.1005066.CrossRefGoogle ScholarPubMed
Limoges, E., Bolduc, C., Berthiaume, C., Mottron, L., & Godbout, R. (2013). Relationship between poor sleep and daytime cognitive performance in young adults with autism. Research in Developmental Disabilities, 34(4), 1322–1335. doi:10.1016/j.ridd.2013.01.013.CrossRefGoogle ScholarPubMed
Liu, J., Wang, G., Ji, X., Cui, N., & Liu, X. (2018). Agreement between parent-reports and child self-reports of sleep problems in Chinese children. Sleep and Biological Rhythms, 16(3), 283–291. doi:10.1007/s41105-018-0152-z.CrossRefGoogle Scholar
Livingston, L. A., Colvert, E., Social Relationships Study, T., Bolton, P., & Happé, F. (2019). Good social skills despite poor theory of mind: exploring compensation in autism spectrum disorder. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 60(1), 102–110. doi:10.1111/jcpp.12886.CrossRefGoogle ScholarPubMed
Livingston, L. A., & Happe, F. (2017). Conceptualising compensation in neurodevelopmental disorders: reflections from autism spectrum disorder. Neuroscience and Biobehavioral Reviews, 80, 729–742. doi:10.1016/j.neubiorev.2017.06.005.CrossRefGoogle ScholarPubMed
Lowe, C. J., Safati, A., & Hall, P. A. (2017). The neurocognitive consequences of sleep restriction: a meta-analytic review. Neuroscience and Biobehavioral Reviews, 80, 586–604. doi:10.1016/j.neubiorev.2017.07.010.CrossRefGoogle ScholarPubMed
Mazurek, M. O., & Petroski, G. F. (2015). Sleep problems in children with autism spectrum disorder: examining the contributions of sensory over-responsivity and anxiety. Sleep Medicine, 16(2), 270–279. doi:10.1016/j.sleep.2014.11.006.CrossRefGoogle ScholarPubMed
Mazzone, L., Postorino, V., Siracusano, M., Riccioni, A., & Curatolo, P. (2018). The relationship between sleep problems, neurobiological alterations, core symptoms of autism spectrum disorder, and psychiatric comorbidities. Journal of Clinical Medicine, 7(5), pii: E102. doi:10.3390/jcm7050102.CrossRefGoogle ScholarPubMed
Mostert-Kerckhoffs, M. A., Staal, W. G., Houben, R. H., & de Jonge, M. V. (2015). Stop and change: inhibition and flexibility skills are related to repetitive behavior in children and young adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(10), 3148–3158. doi:10.1007/s10803-015-2473-y.CrossRefGoogle Scholar
Pellicano, E. (2012). The development of executive function in autism. Autism Research and Treatment, 2012, 146132–146132. doi:10.1155/2012/146132.CrossRefGoogle ScholarPubMed
Pugliese, C. E., Anthony, L., Strang, J. F., Dudley, K., Wallace, G. L., & Kenworthy, L. (2015). Increasing adaptive behavior skill deficits from childhood to adolescence in autism spectrum disorder: role of executive function. Journal of Autism and Developmental Disorders, 45(6), 1579–1587. doi:10.1007/s10803-014-2309-1.CrossRefGoogle ScholarPubMed
Rosenthal, M., Wallace, G. L., Lawson, R., Wills, M. C., Dixon, E., Yerys, B. E., & Kenworthy, L. (2013). Impairments in real-world executive function increase from childhood to adolescence in autism spectrum disorders. Neuropsychology, 27(1), 13–18. doi:10.1037/a0031299.CrossRefGoogle ScholarPubMed
Salmela, L., Kuula, L., Merikanto, I., Raikkonen, K., & Pesonen, A. K. (2018). Autistic traits and sleep in typically developing adolescents. Sleep Medicine, 54, 164–171. doi:10.1016/j.sleep.2018.09.028.CrossRefGoogle ScholarPubMed
Short, M. A., Blunden, S., Rigney, G., Matricciani, L., Coussens, S., Reynolds, C. M., & Galland, B. (2018). Cognition and objectively measured sleep duration in children: a systematic review and meta-analysis. Sleep Health, 4(3), 292–300. doi:10.1016/j.sleh.2018.02.004.CrossRefGoogle ScholarPubMed
Souders, M. C., Zavodny, S., Eriksen, W., Sinko, R., Connell, J., Kerns, C., … Pinto-Martin, J. (2017). Sleep in children with autism spectrum disorder. Current Psychiatry Reports, 19(6), 34. doi:10.1007/s11920-017-0782-x.CrossRefGoogle ScholarPubMed
Sulik, M. J., Blair, C., Mills-Koonce, R., Berry, D., Greenberg, M., & Family Life Project, I. (2015). Early parenting and the development of externalizing behavior problems: longitudinal mediation through children's executive function. Child Development, 86(5), 1588–1603. doi:10.1111/cdev.12386.CrossRefGoogle ScholarPubMed
Taveras, E. M., Rifas-Shiman, S. L., Bub, K. L., Gillman, M. W., & Oken, E. (2017). Prospective study of insufficient sleep and neurobehavioral functioning among school-age children. Academic Pediatrics, 17(6), 625–632. doi:10.1016/j.acap.2017.02.001.CrossRefGoogle ScholarPubMed
Verhoeff, M. E., Blanken, L. M. E., Kocevska, D., Mileva-Seitz, V. R., Jaddoe, V. W. V., White, T., … Tiemeier, H. (2018). The bidirectional association between sleep problems and autism spectrum disorder: a population-based cohort study. Molecular Autism, 9, 8. doi:10.1186/s13229-018-0194-8.CrossRefGoogle ScholarPubMed
Weismer, S. E., Kaushanskaya, M., Larson, C., Mathée, J., & Bolt, D. (2018). Executive function skills in school-age children with autism spectrum disorder: association with language abilities. Journal of Speech, Language, and Hearing Research, 61(11), 2641–2658. doi:10.1044/2018_JSLHR-L-RSAUT-18-0026.CrossRefGoogle Scholar
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