Movement smoothness during dynamic postural control to a static target differs between autistic and neurotypical children
Keywords:Autism Spectrum Disorder, motor skills, movement, postural control, balance, virtual reality, kinematics
Autistic children and adults have known differences in motor performance, including postural instability and atypical gross motor control. Few studies have specifically tested dynamic postural control. This is the first study to quantify movement smoothness and its relationship to task performance during lateral dynamic postural control tasks in autism. We sought to test the hypothesis that autistic children would have less smooth movements to lateral static targets compared to neurotypical children, and that this difference would relate to specific movement strategies. We used camera-based motion-capture to measure spatiotemporal characteristics of lateral movement of a marker placed on the C7 vertebrae, and of markers comprising trunk and pelvis segments during a dynamic postural control task administered in an immersive virtual environment. We tested a sample of 15 autistic children and 11 age-matched neurotypical children. We quantified movement smoothness using dimensionless jerk cost. Autistic children exhibited more medial-lateral pelvic position range of motion compared to neurotypical children, and used a stepping strategy more often compared to neurotypical children. Autistic children also had higher jerk cost than neurotypical children for motion of the C7 marker. All participants had higher jerk cost for far targets than for near targets. Autistic children had longer trial durations than neurotypical children, and younger children had longer trial durations than older children across diagnostic groups. The stepping strategy observed more often in the autistic group likely contributed to jerk cost and reduced movement smoothness. This strategy is indicative of either an attempt to prevent an impending loss of balance, or an attempt to compensate for and recover from a loss of balance once it is detected. Implications of results are discussed, specifically with respect to anticipatory, feed-forward control of movement.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., Text Revision). Washington, DC: American Psychiatric Publishing.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.
Balasubramanian, S., Melendez-Calderon, A., & Burdet, E. 2012. A robust and sensitive metric for quantifying movement smoothness. IEEE Transactions on Bio-Medical Engineering 59(8):2126–36. https://doi.org/10.1109/TBME.2011.2179545
Brenner, L. A., Turner, K. C., & Müller, R. A. 2007. Eye movement and visual search: Are there elementary abnormalities in autism? Journal of Autism and Developmental Disorders 37(7):1289–1309. https://doi.org/10.1007/s10803-006-0277-9
Bugnariu, N., Young, C., Rockenbach, K., Patterson, R. M. ,Garver, C., Ranatunga, I., Beltran, M., Torres-Arenas, N., & Popa, D. O. 2013. Human-robot interaction as a tool to evaluate and quantify imitative motor behavior in children with Autism Spectrum Disorders. Pp. 57–62 in 2013 International Conference on Virtual Rehabilitation, ICVR 2013. IEEE Computer Society. https://doi.org/10.1109/ICVR.2013.6662088
Caçola, P., Miller, H. L., & Williamson, P. O. (2017). Behavioral comparisons in Autism Spectrum Disorder and Developmental Coordination Disorder: A systematic literature review. Research in Autism Spectrum Disorders, 38, 6–18. https://doi.org/10.1016/j.rasd.2017.03.004
Cai, L. L., Fong, A. J., Otoshi, C. K., Liang, Y., Burdick, J. W., Roy, R. R., & Edgerton, V. R. (2006). Implications of assist-as-needed robotic step training after a complete spinal cord injury on intrinsic strategies of motor learning. Journal of Neuroscience, 26(41), 10564–10568. https://doi.org/10.1523/JNEUROSCI.2266-06.2006
Cirstea, M. C., & Levin, M. F. 2000. Compensatory strategies for reaching in stroke. Brain 123(5):940–53. https://doi.org/10.1093/brain/123.5.940
Cook, J. 2016. From movement kinematics to social cognition: The case of autism. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371(1693). https://doi.org/10.1098/rstb.2015.0372
Cook, J. L., Blakemore, S. J., & Press, C. 2013. Atypical basic movement kinematics in Autism Spectrum Conditions. Brain 136(9):2816–24. https://doi.org/10.1093/brain/awt208
Dewey, D., Cantell, M., & Crawford, S. J. 2007. Motor and gestural performance in children with Autism Spectrum Disorders, Developmental Coordination Disorder, and/or Attention Deficit Hyperactivity Disorder. Journal of the International Neuropsychological Society : JINS 13(2):246–56. https://doi.org/10.1017/S1355617707070270
Dinstein, I., Heeger, D. J., & Behrmann, M. 2015. Neural variability: Friend or foe? Trends in Cognitive Sciences, Vol. 19, pp. 322–328. https://doi.org/10.1016/j.tics.2015.04.005
Dixon, P. C., Stirling, L., Xu, X., Chang, C. C., Dennerlein, J. T., & Schiffman, J. M. (2018). Aging may negatively impact movement smoothness during stair negotiation. Human Movement Science, 60, 78–86. https://doi.org/10.1016/j.humov.2018.05.008
Dowd, A. M., McGinley, J. L., Taffe, J. R., & Rinehart, N. J. 2012. Do planning and visual integration difficulties underpin motor dysfunction in autism? A kinematic study of young children with autism. Journal of Autism and Developmental Disorders 42(8):1539–48. https://doi.org/10.1007/s10803-011-1385-8
Dziuk, M., Gidle, A., Larson, J. C., Apostu, A., Mahone, E. M., Denckla, M. B., & Mostofsky, S. H. 2007. Dyspraxia in autism: association with motor, social, and communicative deficits. Developmental Medicine and Child Neurology 49(10):734–39. https://doi.org/10.1111/j.1469-8749.2007.00734.x
Fetters, L., & Todd, J. 1987. Quantitative assessment of infant reaching movements. Journal of Motor Behavior 19(2):147–66. https://doi.org/10.1080/00222895.1987.10735405
Flash, T., & Hogan, N. 1985. The coordination of arm movements: An experimentally confirmed mathematical model. Journal of Neuroscience 5(7):1688–1703. https://doi.org/10.1523/JNEUROSCI.05-07-01688.1985
Fournier, K. A., Kimberg, C. I., Radonovich, K. J., Tillman, M. J., Chow, J. W., Lewis, M. H., Bodfish, J. W., & Hass, C. J. 2010. Decreased static and dynamic postural control in children with Autism Spectrum Disorders. Gait and Posture 32(1):6–9. https://doi.org/10.1016/j.gaitpost.2010.02.007
Fulceri, F., Grossi, E., Contaldo, A., Narzisi, A., Apicella, F., Parrini, I., Tancredi, R., Calderoni, S., & 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, 09 January 2019. https://doi.org/10.3389/fpsyg.2018.02683
Glazebrook, C. M., Elliott, D., & Szatmari, P. 2008. How do individuals with autism plan their movements? Journal of Autism and Developmental Disorders 38(1):114–26. https:/doi.org/ 10.1007/s10803-007-0369-1
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 and Child Neurology, 51(4), 311–316. https://doi.org/10.1111/j.1469-8749.2008.03242.x
Gulde, P., & Hermsdörfer, J. 2018. Smoothness metrics in complex movement tasks. Frontiers in Neurology, 9(SEP). https://doi.org/10.3389/fneur.2018.00615
Hallett, M., Lebiedowska, M. K., Thomas, S. L., Stanhope, S. J., Denckla, M. B., & Rumsey, L. 1993. Locomotion of autistic adults. Archives of Neurology 50(12):1304–8. https://doi.org/ 10.1001/archneur.1993.00540120019007
Harbourne, R. T., & Stergiou, N. (2009). Movement variability and the use of nonlinear tools: Principles to guide physical therapist practice. Physical Therapy, 89(3), 267–282. https://doi.org/10.2522/ptj.20080130
Heathcock, J. C., Tanner, K., Robson, D., Young, R., & Lane, A. E. (2015). Retrospective analysis of motor development in infants at high and low risk for autism spectrum disorder. American Journal of Occupational Therapy, 69(5), 6905185070. https://doi.org/10.5014/ajot.2015.017525
Hedgecock, J. B., Dannemiller, L. A., Shui, A. M., Rapport, M. J., & Katz, T. (2018). Associations of gross motor delay, behavior, and quality of life in young children with Autism Spectrum Disorder. Physical Therapy, 98. https://doi.org/10.1093/ptj/pzy006
Hogan, N., & Sternad, D. (2009). Sensitivity of smoothness measures to movement duration, amplitude, and arrests. Journal of Motor Behavior, 41(6), 529–534. https://doi.org/10.3200/35-09-004-RC
Jansiewicz, E. M., Goldberg, M. C., Newschaffer, C., Denckla, M., 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):613–21. https://doi.org/10.1007/s10803-006-0109-y
Kawato, M., & Wolpert, D. (1998). Internal models for motor control. Novartis Foundation Symposium, (218), 291–307.
Kern, J. K., Geier, D. A., Adams, J. B., Troutman, M. R., Davis, G., King, P. G.,…& Geier, M. R. (2011). Autism severity and muscle strength: A correlation analysis. Research in Autism Spectrum Disorders, 5(3), 1011-5. https://doi.org/10.1016/j.rasd.2010.11.002
Ketcham, C. J., Seidler, R. D., Van Gemmert, A. W. A., & Stelmach, G. E. 2002. Age-related kinematic differences as influenced by task difficulty, target size, and movement amplitude. Journals of Gerontology - Series B Psychological Sciences and Social Sciences 57(1). https://doi.org/10.1093/geronb/57.1.P54
Leary, M. R., & and Hill, D. A. 1996. Moving on: Autism and movement disturbance. Mental Retardation 34(1):39–53.
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. https://doi.org/10.1007/s10803-017-3144-y
Liu, D., & Todorov, E., Evidence for the flexible sensorimotor strategies predicted by optimal feedback control. Journal of Neuroscience, 27(35), 9354-9368. https://doi.org/10.1523/JNEUROSCI.1110-06.2007
Lord, C., Rutter, M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. 2012. Autism Diagnostic Observation Schedule, Second Edition (ADOS-2) Manual (Part I): Modules 1–4. Western Psychological Services, Torrance, CA.
Luna, B., Minshew, N. J., Garver, K. E., Lazar, N. A., Thulborn, K. R., Eddy, W. F., & Sweeney, J. A. 2002. Neocortical system abnormalities in autism: An fMRI study of spatial working memory. Neurology 59(6):834–40. https://doi.org/10.1212/WNL.59.6.834
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. International Conference on Virtual Rehabilitation, ICVR 2017-June. https://doi.org/10.1109/ICVR.2017.8007481
Miller, H. L., Sherrod, G., Mauk, J., Fears, N., & Caçola, P. (2021). Shared features or co-occurrence? Evaluating symptoms of Developmental Coordination Disorder in children and adolescents with Autism Spectrum Disorder. Journal of Autism & Developmental Disorders, ePub ahead of print. https://doi.org/10.1007/s10803-020-04766-z.
Miller, H. L., Caçola, P. M., Sherrod, G. M., 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 and Posture 67:9–11. https://doi.org/10.1016/j.gaitpost.2018.08.038
Miller, M., Chukoskie, L., Zinni, M., Townsend, J., & Trauner, D. 2014. Dyspraxia, motor function and visual-motor integration in autism. Behavior & Brain Research, 269, 95-102. https://doi.org/10.1016/j.bbr.2014.04.011
Ming, X., Brimacombe, M., & Wagner, G. C. 2007. Prevalence of motor impairment in Autism Spectrum Disorders. Brain & Development 29(9):565–70. https://doi.org/10.1016/j.braindev.2007.03.002
Minshew, N. J., Sung, K., Jones, B. J., & Furman, J. 2004. Underdevelopment of the postural control system in autism. Neurology 63(Ns 33355):2056–61. https://doi.org/10.1212/01.WNL.0000145771.98657.62
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. https://doi.org/10.1523/JNEUROSCI.2731-14.2015
Mostofsky, S. H., Burgess, M. P., & Gidley Larson, J. C. 2007. Increased motor cortex white matter volume predicts motor impairment in autism. Brain : A Journal of Neurology 130(Pt 8):2117–22. https://doi.org/10.1093/brain/awm129
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(3):314–26. https:/doi.org/ 10.1017/S1355617706060437
Nobile, M., Perego, P., Piccinini, L., Mani, E., Rossi, A., Bellina, M., & Molteni, M. 2011. Further evidence of complex motor dysfunction in drug naïve children with autism using automatic motion analysis of gait. Autism, 15(3):263-283. https://doi.org/10.1177%2F1362361309356929
Platz, T., Denzler, P., Kaden, B. & Mauritz, K. H. 1994. Motor learning after recovery from hemiparesis. Neuropsychologia 32(10):1209–23. https://doi.org/10.1016/0028-3932(94)90103-1
Provost, B., Heimerl, S. & Lopez, B. R. 2007. Levels of gross and fine motor development in young children with Autism Spectrum Disorder. Physical and Occupational Therapy in Pediatrics 27(3):21–36. https://doi.org/10.1080/J006v27n03_03
Rohrer, B., Fasoli, S., Krebs, H. I., Hughes, R., Volpe, B., Frontera, W. R., Stein, J., & Hogan, N. 2002. Movement smoothness changes during stroke recovery. Journal of Neuroscience 22(18):8297–8304. https://doi.org/10.1523/JNEUROSCI.22-18-08297.2002
Rutter, M., Bailey, A., & Lord, C. 2003. Social Communication Questionnaire. Western Psychological Services, Torrence, CA.
Salmond, L. H., Davidson, A. D., & Charles, S. K. 2017. Proximal-distal differences in movement smoothness reflect differences in biomechanics. Journal of Neurophysiology, 117(3):1239-1257. https://doi.org/10.1152/jn.00712.2015
Schmitz, C., Martineau, J., Barthelemey, C., & Assaiante, C.2003. Motor control and children with autism: a deficit of anticipatory function? Neuroscience Letters, 348(1), 17-20. https://doi.org/10.1016/S0304-3940(03)00644-X
Sharer E, Crocetti D, Muschelli J, et al. Neural correlates of visuomotor learning in autism. Journal of Child Neurology, 30(14):1877-1886. https://doi.org/10.1177%2F0883073815600869
Takarae, Y., Minshew, N. J., Luna, B., & Sweeney, J. A.. 2007. Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiatry Research 156(2):117–27. https://doi.org/10.1016/j.pscychresns.2007.03.008
Teulings, H. L., Contreras-Vidal, J. L., Stelmach, G. E., & Adler, C. H. 1997. Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Experimental Neurology 146(1):159–70. https://doi.org/10.1006/exnr.1997.6507
Todorov, E. & Jordan, M. I. 1998. Smoothness maximization along a predefined path accurately predicts the speed profiles of complex arm movements. Journal of Neurophysiology 80(2):696–714. https://doi.org/10.1152/jn.1922.214.171.1246
Todorov, E., & Jordan, M. I. 2002. Optimal feedback control as a theory of motor coordination. Nature Neuroscience, 5(11), 1226-1235.Stergiou, N., Harbourne, R. T., & Cavanaugh, J. T. 2006. Optimal movement variability. Journal of Neurologic Physical Therapy, 30(3), 120–129. https://doi.org/10.1038/nn963
Torres, E. B., & Denisova, K. (2016). Motor noise is rich signal in autism research and pharmacological treatments. OPEN, Nature Publishing Group. https://doi.org/10.1038/srep37422
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(4), e12401. https://doi.org/10.1111/desc.12401
Vernazza-Martin, S., N. Martin, A. Vernazza, A. Lepellec-Muller, M. Rufo, J. Massion, and C. Assaiante. 2005. Goal directed locomotion and balance control in autistic children. Journal of Autism and Developmental Disorders 35(1):91–102. http://doi.org/10.1007/s10803-004-1037-3
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. https://doi.org/10.1152/jn.00661.2014
Whyatt, C., & Craig, C. (2013). Sensory-motor problems in autism. Frontiers in Integrative Neuroscience, 7 (2013), p. 51 https://doi.org/10.3389/fnint.2013.00051
Williams, J. H. G., Whiten, A., & Singh, T. 2004. A systematic review of action imitation in Autistic Spectrum Disorder. Journal of Autism and Developmental Disorders 34(3):285–99. https://doi.org/10.1023/B:JADD.0000029551.56735.3a
- 2021-11-05 (2)
- 2021-11-05 (1)
Copyright (c) 2021 Haylie Miller, Ty Templin, Nicholas Fears, Gabriela Sherrod, Rita Patterson, Nicoleta Bugnariu
This work is licensed under a Creative Commons Attribution 4.0 International License.