Preprint has been submitted for publication in journal
Preprint / Version 2

Autistic children use less efficient goal-directed whole body movements compared to neurotypical development

##article.authors##

  • Nicholas Fears University of Michigan https://orcid.org/0000-0001-7081-0015
  • Tylan Templin Southwest Research Institute
  • Gabriela Sherrod University of Alabama-Birmingham
  • Nicoleta Bugnariu University of the Pacific
  • Rita Patterson University of North Texas Health Science Center
  • Haylie Miller University of Michigan

DOI:

https://doi.org/10.51224/SRXIV.17

Keywords:

virtual reality, autism spectrum disorder, postural control, balance, movement, motor skills, kinematics

Abstract

Autistic children have differences in their movements which impact their functional performance. Virtual-reality enables researchers to study movement in safe, engaging environments. We used motion-capture to measure how 7-13-year-old autistic and neurotypical children make whole-body movements in a virtual-reality task. Although children in both groups were successful, we observed differences in their movements. Autistic children were less efficient moving to the target. Autistic children did not appear to use a movement strategy. While neurotypical children were more likely to overshoot near targets and undershoot far targets, autistic children did not modulate their strategy. Using kinematic data from tasks in virtual-reality, we can begin to understand the pattern of movement challenges experienced by autistic children.

Metrics

Metrics Loading ...

References

Adamovich, S. V., Archambault, P. S., Ghafouri, M., Levin, M. F., Poizner, H., & Feldman, A. G. (2001). Hand trajectory invariance in reaching movements involving the trunk. Experimental Brain Research, 138(3), 288-303. https://doi.org/10.1007/s002210100694

Adolph, K. E. (2008). Learning to Move. Current Directions in Psychological Science, 17, 213-218. doi:10.1111/j.1467-8721.2008.00577.x

Adolph, K. E., & Robinson, S. R. (2013). The road to walking: What learning to walk tells us about development. In P. D. Zelazo (Ed.), The Oxford Handbook of Developmental Psychology (Vol. 1, pp. 403-443): Oxford University Press. doi:10.1093/oxfordhb/9780199958450.013.0015

American Psychiatric Association. (2013). Autism Spectrum Disorder. In Diagnostic and Statistical Manual of Mental Disorders. (5 ed.). Arlington, VA: American Psychiatric Association. doi: 10.1176/appi.books.9780890425596

Ardalan, A., Assadi, A. H., Surgent, O. J., & Travers, B. G. (2019). Whole-body movement during videogame play distinguishes youth with autism from youth with typical development. Scientific Reports, 9(1), 20094. doi:10.1038/s41598-019-56362-6

Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67(1), 1-48. doi:10.18637/jss.v067.i01.

Bhat, A. N. (2020). Is motor impairment in Autism Spectrum Disorder (ASD) distinct from Developmental Coordination Disorder (DCD)? A report from the SPARK study. Physical Therapy 100(4), 633-644. doi:10.1093/ptj/pzz190

Bhat, A. N., Landa, R. J., & Galloway, J. C. (2011). Current perspectives on motor functioning in infants, children, and adults with autism spectrum disorders. Physical Therapy, 91(7), 1116-1129. doi:10.2522/ptj.20100294

Bojanek, E. K., Wang, Z., White, S. P., & Mosconi, M. W. (2020). Postural control processes during standing and step initiation in autism spectrum disorder. Journal of Neurodevelopmental Disorders, 12(1). doi:10.1186/s11689-019-9305-x

Cairney, J., Hay, J. A., Veldhuizen, S., Missiuna, C., & Faught, B. E. (2010). Developmental coordination disorder, sex, and activity deficit over time: a longitudinal analysis of participation trajectories in children with and without coordination difficulties. Developmental Medicine & Child Neurology, 52(3), e67-e72. https://doi.org/10.1111/j.1469-8749.2009.03520.x

Canning, C. G., Allen, N. E., Nackaerts, E., Paul, S. S., Nieuwboer, A., & Gilat, M. (2020). Virtual reality in research and rehabilitation of gait and balance in Parkinson disease. Nature Reviews Neurology. doi:10.1038/s41582-020-0370-2

Carment, L., Khoury, E., Dupin, L., Guedj, L., Bendjemaa, N., Cuenca, M., . . . Amado, I. (2020). Common vs. distinct visuomotor control deficits in Autism Spectrum Disorder and Schizophrenia. Autism Research. doi:10.1002/aur.2287

Chen, L. C., Su, W. C., Ho, T. L., Lu, L., Tsai, W. C., Chiu, Y. N., & Jeng, S. F. (2019). Postural control and interceptive skills in children with Autism Spectrum Disorder. Physical Therapy. doi:10.1093/ptj/pzz084

Chern, J. S., Lo, C. Y., Wu, C. Y., Chen, C. L., Yang, S., & Tang, F. T. (2010). Dynamic postural control during trunk bending and reaching in healthy adults and stroke patients. American journal of physical medicine & rehabilitation, 89(3), 186-197. doi: 10.1097/PHM.0b013e3181c56287

Cook, J. (2016). From movement kinematics to social cognition: the case of autism. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1693), 20150372. https://doi.org/10.1098/rstb.2015.0372

Davidovitch, M., Stein, N., Koren, G., & Friedman, B. C. (2018). Deviations from typical developmental trajectories detectable at 9 months of age in low risk children later diagnosed with Autism Spectrum Disorder. Journal of Autism and Developmental Disorders, 48(8), 2854-2869. doi:10.1007/s10803-018-3549-2

Doumas, M., McKenna, R., & Murphy, B. (2016). Postural control deficits in Autism Spectrum Disorder: The role of sensory integration. Journal of Autism and Developmental Disorders, 46(3), 853-861. doi:10.1007/s10803-015-2621-4

Dufek, J. S., Harry, J. R., Eggleston, J. D., & Hickman, R. A. (2018). Walking mechanics and movement pattern variability in monozygotic twins with autism Spectrum disorder. Journal of Developmental and Physical Disabilities, 30(6), 793-805. https://doi.org/10.1152/jn.00647.2015

Fisher, A., Engel, C., Geist, R., Lillie, K., Lutman, S., & Travers, B. G. (2018). Brief report: Postural balance and daily living skills in children and adolescents with autism. Journal of Autism and Developmental Disorders, 48(9), 3210-3215. doi:10.1007/s10803-018-3558-1

Fong, S. S., Ng, S. S., & Yiu, B. P. (2013). Slowed muscle force production and sensory organization deficits contribute to altered postural control strategies in children with developmental coordination disorder. Research in Developmental Disabilities, 34(9), 3040-3048. https://doi.org/10.1016/j.ridd.2013.05.035

Fournier, K. A., Hass, C. J., Naik, S. K., Lodha, N., & Cauraugh, J. H. (2010). Motor coordination in autism spectrum disorders: a synthesis and meta-analysis. Journal of Autism and Developmental Disorders, 40(10), 1227-1240. doi:10.1007/s10803-010-0981-3

Fox, J. & Weisberg, S. (2019). An {R} Companion to Applied Regression, Third Edition. Thousand Oaks CA: Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/

Fulceri, F., Grossi, E., Contaldo, A., Narzisi, A., Apicella, F., Parrini, I., . . . Muratori, F. (2019). Motor skills as moderators of core symptoms in Autism Spectrum Disorders: Preliminary data from an exploratory analysis With artificial neural networks. Frontiers in psychology, 9, 2683. doi:10.3389/fpsyg.2018.02683

Glazebrook, C. M., Elliott, D., & Lyons, J. (2006). A kinematic analysis of how young adults with and without autism plan and control goal-directed movements. Motor Control, 10, 244-264. doi:10.1123/mcj.10.3.244

Glazebrook, C. M., Elliott, D., & Szatmari, P. (2008). How do individuals with autism plan their movements?. Journal of autism and developmental disorders, 38(1), 114-126. https://doi.org/10.1007/s10803-007-0369-1

Gonsalves, L., Campbell, A., Jensen, L., & Straker, L. (2015). Children with Developmental Coordination Disorder play active virtual reality games differently than children with typical development. Physical Therapy, 95(3), 360-368. doi: 10.2522/ptj.20140116

Grace, N., Enticott, P. G., Johnson, B. P., & Rinehart, N. J. (2017). Do handwriting difficulties correlate with core symptomology, motor proficiency and attentional behaviours? Journal of Autism and Developmental Disorders, 47(4), 1006-1017. doi:10.1007/s10803-016-3019-7

Green, D., Charman, T., Pickles, A., Chandler, S., Loucas, T., Simonoff, E., & Baird, G. (2009). Impairment in movement skills of children with autistic spectrum disorders. Developmental Medicine & Child Neurology, 51(4), 311-316. doi:10.1111/j.1469-8749.2008.03242.x

Greffou, S., Bertone, A., Hahler, E. M., Hanssens, J. M., Mottron, L., & Faubert, J. (2012). Postural hypo-reactivityin autism is contengent on development and visual environment: A fully immersive virtual reality study. Journal of Autism and Developmental Disorders. 42, 961-970. doi:10.1007/s10803-011-1326-6.

Hendrix, C. G., Prins, M. R., & Dekkers, H. (2014). Developmental coordination disorder and overweight and obesity in children: a systematic review. Obesity Reviews, 15(5), 408-423. https://doi.org/10.1111/obr.12137

Hilton, C. L., Zhang, Y., Whilte, M. R., Klohr, C. L., & Constantino, J. (2012). Motor impairment in sibling pairs concordant and discordant for autism spectrum disorders. Autism, 16(4), 430-441. doi:10.1177/1362361311423018

Izadi-Najafabadi, S., Ryan, N., Ghafooripoor, G., Gill, K., & Zwicker, J. G. (2019). Participation of children with developmental coordination disorder. Research in developmental disabilities, 84, 75-84. https://doi.org/10.1016/j.ridd.2018.05.011

Jansiewicz, E. M., Goldberg, M. C., Newschaffer, C. J., Denckla, M. B., Landa, R., & Mostofsky, S. H. (2006). Motor signs distinguish children with high functioning autism and Asperger's syndrome from controls. Journal of Autism and Developmental Disorders, 36(5), 613-621. doi:10.1007/s10803-006-0109-y

Jasmin, E., Couture, M., McKinley, P., Reid, G., Fombonne, E., & Gisel, E. (2009). Sensori-motor and daily living skills of preschool children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 231-241. doi:10.1007/s10803-008-0617-z

LeBarton, E. S., & Iverson, J. M. (2016). Associations between gross motor and communicative development in at-risk infants. Infant Behavior and Development, 44, 59-67. doi:10.1016/j.infbeh.2016.05.003

Levac, D., Pierrynowski, M. R., Canestraro, M., Gurr, L., Leonard, L., & Neeley, C. (2010). Exploring children's movement characteristics during virtual reality video game play. Human Movement Science, 29(6), 1023-1038. doi:10.1016/j.humov.2010.06.006

Li, W., Lam-Damji, S., Chau, T., & Fehlings, D. (2009). The development of a home-based virtual reality therapy system to promote upper extremity movement for children with hemiplegic cerebral palsy. Technology and Disability, 21(3), 107-113. doi:10.3233/tad-2009-0277

Licari, M. K., Alvares, G. A., Varcin, K., Evans, K. L., Cleary, D., Reid, S. L., . . . Whitehouse, A. J. O. (2019). Prevalence of motor difficulties in Autism Spectrum Disorder: Analysis of a population-based cohort. Autism Research. doi:10.1002/aur.2230

Lim, Y. H., Partridge, K., Girdler, S., & Morris, S. L. (2017). Standing postural control in individuals with Autism Spectrum Disorder: Systematic review and meta-analysis. Journal of Autism and Developmental Disorders, 47(7), 2238-2253. doi:10.1007/s10803-017-3144-y

Liu, T., & Breslin, C. M. (2013). Fine and gross motor performance of the MABC-2 by children with autism spectrum disorder and typically developing children. Research in Autism Spectrum Disorders, 7(10), 1244-1249. doi:10.1016/j.rasd.2013.07.002

Lloyd, M., MacDonald, M., & Lord, C. (2013). Motor skills of toddlers with autism spectrum disorders. Autism, 17(2), 133-146. doi:10.1177/1362361311402230

Longhi, M., Merlo, A., Prati, P., Giacobbi, M., & Mazzoli, D. (2016). Instrumental indices for upper limb function assessment in stroke patients: a validation study. Journal of neuroengineering and rehabilitation, 13(1), 1-11. https://doi.org/10.1186/s12984-016-0163-4

Lord, C., Rutter, M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. L. (2012). Autism Diagnostic Observation Schedule, Second Edition (ADOS-2) Manual (Part I): Modules 1–4. . In. Torrance, CA: Western Psychological Services.

Maki, B. E., & McIlroy, W. E. (1996). Postural control in the older adult. Clinics in geriatric medicine, 12(4), 635-658. https://doi.org/10.1016/S0749-0690(18)30193-9

Malihi, M., Nguyen, J., Cardy, R. E., Eldon, S., Petta, C., & Kushki, A. (2020). Short report: Evaluating the safety and usability of head-mounted virtual reality compared to monitor-displayed video for children with autism spectrum disorder. Autism, 1362361320934214. doi:10.1177/1362361320934214

Miller, H. L., Bugnariu, N., Patterson, R. M., Wijayasinghe, I., & Popa, D. O. (2017). Development of a novel visuomotor integration paradigm by integrating a virtual environment with mobile eye-tracking and motion-capture systems. 2017 International Conference on Virtual Rehabilitation (ICVR). doi:10.1109/ICVR.2017.8007481

Miller, H. L., & Bugnariu, N. L. (2016). Level of Immersion in Virtual Environments Impacts the Ability to Assess and Teach Social Skills in Autism Spectrum Disorder. Cyberpsychology, Behavior, and Social Networking, 19, 246-256. doi:10.1089/cyber.2014.0682

Miller, H. L., Caçola, P., Sherrod, G., Patterson, R. M., & Bugnariu, N. L. (2019). Children with Autism Spectrum Disorder, Developmental Coordination Disorder, and typical development differ in characteristics of dynamic postural control: a preliminary study. Gait & Posture, 67, 9-11. doi:10.1016/j.gaitpost.2018.08.038

Miller, H. L., Sherrod, G. M., Mauk, J. E., Fears, N. E., Hynan, L. S., & Tamplain, P. M. (2021). Shared features or co-occurrence? Evaluating symptoms of Developmental Coordination Disorder in children and adolescents with Autism Spectrum Disorder. Journal of Autism and Developmental Disorders. doi:10.1007/s10803-020-04766-z

Mosconi, M. W., Mohanty, S., Greene, R. K., Cook, E. H., Vaillancourt, D. E., & Sweeney, J. A. (2015). Feedforward and feedback motor control abnormalities implicate cerebellar dysfunctions in Autism Spectrum Disorder. Journal of Neuroscience, 35(5), 2015-2025. doi:10.1523/jneurosci.2731-14.2015

Mostofsky, S. H., Dubey, P., Jerath, V. K., Jansiewicz, E. M., Goldberg, M. C., & Denckla, M. B. (2006). Developmental dyspraxia is not limited to imitation in children with autism spectrum disorders. Journal of the International Neuropsychological Society, 12(03). doi:10.1017/s1355617706060437

Neufeld, J., Hagström, A., Van't Westeinde, A., Lundin, K., Cauvet, É., Willfors, C., ... & Bölte, S. (2020). Global and local visual processing in autism–a co‐twin‐control study. Journal of Child Psychology and Psychiatry, 61(4), 470-479. https://doi.org/10.1111/jcpp.13120

Parma, V., & de Marchena, A. B. (2016). Motor signatures in autism spectrum disorder: the importance of variability. Journal of Neurophysiology. https://doi.org/10.1152/jn.00647.2015

Perin, C., Valagussa, G., Mazzucchelli, M., Gariboldi, V., Cerri, C. G., Meroni, R., ... & Piscitelli, D. (2020). Physiological profile assessment of posture in children and adolescents with autism spectrum disorder and typically developing peers. Brain sciences, 10(10), 681. https://doi.org/10.3390/brainsci10100681.

Prasertsakul, T., Kaimuk, P., Chinjenpradit, W., Limroongreungrat, W., & Charoensuk, W. (2018). The effect of virtual reality-based balance training on motor learning and postural control in healthy adults: a randomized preliminary study. Biomedical Engineering Online, 17(1), 124. doi:10.1186/s12938-018-0550-0

Purpura, G., Fulceri, F., Puglisi, V., Masoni, P., & Contaldo, A. (2020). Motor coordination impairment in children with autism spectrum disorder: a pilot study using Movement assessment Battery for children-2 checklist. Minerva Pediatrica, 72(1), 22-29. doi: 10.23736/S0026-4946.16.04633-8.

R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

Ravi, D. K., Kumar, N., & Singhi, P. (2017). Effectiveness of virtual reality rehabilitation for children and adolescents with cerebral palsy: an updated evidence-based systematic review. Physiotherapy, 103(3), 245-258. doi:10.1016/j.physio.2016.08.004

Rodgers, R. A., Travers, B. G., & Mason, A. H. (2019). Bimanual Reach to Grasp Movements in Youth With and Without Autism Spectrum Disorder. Frontiers in psychology, 9. doi:10.3389/fpsyg.2018.02720

Rutter, M., Bailey, A., & Lord, C. (2003). The social communication questionnaire: Manual. Los Angeles, CA: Western Psychological Services.

Rutter, M., Le Couteur, A., & Lord, C. (2003). Autism diagnostic interview-revised. Los Angeles, CA: Western Psychological Services

Schneiberg, S., McKinley, P., Gisel, E., Sveistrup, H., & Levin, M. F. (2010). Reliability of kinematic measures of functional reaching in children with cerebral palsy. Developmental Medicine & Child Neurology, 52(7), e167-e173. https://doi.org/10.1111/j.1469-8749.2010.03635.x

Stylianou, A. P., McVey, M. A., Lyons, K. E., Pahwa, R., & Luchies, C. W. (2011). Postural sway in patients with mild to moderate Parkinson's disease. International Journal of Neuroscience, 121(11), 614-621. https://doi.org/10.3109/00207454.2011.602807

Sun, R., Hsieh, K. L., & Sosnoff, J. J. (2019). Fall risk prediction in multiple sclerosis using postural sway measures: a machine learning approach. Scientific Reports, 9(1), 1-7. https://doi.org/10.1038/s41598-019-52697-2

Sveistrup, H., Schneiberg, S., McKinley, P. A., McFadyen, B. J., & Levin, M. F. (2008). Head, arm and trunk coordination during reaching in children. Experimental Brain Research, 188(2), 237-247. https://doi.org/10.1007/s00221-008-1357-1

Swanenburg, J., de Bruin, E. D., Uebelhart, D., & Mulder, T. (2010). Falls prediction in elderly people: a 1-year prospective study. Gait & posture, 31(3), 317-321. https://doi.org/10.1016/j.gaitpost.2009.11.013

Tamplain, P., & Miller, H. L. (2021). What can we do to promote mental health among individuals with developmental coordination disorder?. Current Developmental Disorders Reports, 8(1), 24-31. https://doi.org/10.1007/s40474-020-00209-7

Travers, B. G., Bigler, E. D., Duffield, T. C., Prigge, M. D. B., Froehlich, A. L., Lange, N., . . . Lainhart, J. E. (2017). Longitudinal development of manual motor ability in autism spectrum disorder from childhood to mid-adulthood relates to adaptive daily living skills. Developmental Science, 20, 1-15. doi:10.1111/desc.12401

Tunçgenç, B., Pacheco, C., Rochowiak, R., Nicholas, R., Rengarajan, S., Zou, E., . . . Mostofsky, S. H. (2020). Computerised Assessment of Motor Imitation (CAMI) as a scalable method for distinguishing children with autism. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging. doi:10.1016/j.bpsc.2020.09.001

Van Waelvelde, H., Oostra, A., Dewitte, G., Van Den Broeck, C., & Jongmans, M. J. (2010). Stability of motor problems in young children with or at risk of autism spectrum disorders, ADHD, and or developmental coordination disorder. Developmental Medicine and Child Neurology, 52(8), e174-178. doi:10.1111/j.1469-8749.2009.03606.x

Wang, Z., Hallac, R. R., Conroy, K. C., White, S. P., Kane, A. A., Collinsworth, A. L., . . . Mosconi, M. W. (2016). Postural orientation and equilibrium processes associated with increased postural sway in autism spectrum disorder (ASD). Journal of Neurodevelopmental Disorders, 8, 43. doi:10.1186/s11689-016-9178-1

Wang, Z., Magnon, G. C., White, S. P., Greene, R. K., Vaillancourt, D. E., & Mosconi, M. W. (2015). Individuals with autism spectrum disorder show abnormalities during initial and subsequent phases of precision gripping. Journal of Neurophysiology, 113(7), 1989-2001. doi:10.1152/jn.00661.2014

Wang, Z., Wang, Y., Sweeney, J. A., Gong, Q., Lui, S., & Mosconi, M. W. (2019). Resting-state brain network dysfunctions associated with visuomotor impairments in autism spectrum disorder. Frontiers in integrative neuroscience, 13, 17. https://doi.org/10.3389/fnint.2019.00017

Wechsler, D. (2011). WASI-II: Wechsler abbreviated scale of intelligence. Pearson.

Zablotsky, B., Pringle, B. A., Colpe, L. J., Kogan, M. D., Rice, C., & Blumberg, S. J. (2015). Service and treatment use among children diagnosed with Autism Spectrum Disorders. Journal of Developmental & Behavioral Pediatrics, 36(2), 98-105. doi:10.1097/DBP.0000000000000127

Zheng, R., Naiman, I. D., Skultety, J., Passmore, S. R., Lyons, J., & Glazebrook, C. M. (2019). The impact of different movement types on motor planning and execution in individuals with autism spectrum disorder. Motor control, 23(3), 398-417. https://doi.org/10.1123/mc.2017-0084

Zwicker, J. G., Suto, M., Harris, S. R., Vlasakova, N., & Missiuna, C. (2018). Developmental coordination disorder is more than a motor problem: Children describe the impact of daily struggles on their quality of life. British journal of occupational therapy, 81(2), 65-73. https://doi.org/10.1177%2F0308022617735046

Downloads

Posted

2021-10-07 — Updated on 2022-03-06

Versions