Motor Memory Deficits Contribute to Motor Impairments in Autism Spectrum Disorder

  • Kristina A. Neely
  • Suman Mohanty
  • Lauren M. Schmitt
  • Zheng Wang
  • John A. Sweeney
  • Matthew W. Mosconi
Original Paper


Sensorimotor abnormalities are common in individuals with autism spectrum disorder (ASD); however, the processes underlying these deficits remain unclear. This study examined force production with and without visual feedback to determine if individuals with ASD can utilize internal representations to guide sustained force. Individuals with ASD showed a faster rate of force decay in the absence of visual feedback. Comparison of force output and tests of social and verbal abilities demonstrated a link between motor memory impairment and social and verbal deficits in individuals with ASD. This finding suggests that deficits in storage or retrieval of motor memories contribute to sensorimotor deficits and implicates frontoparietal networks involved in short-term consolidation of action dynamics used to optimize ongoing motor output.


Autism spectrum disorder Motor Visual feedback Precision grip Working memory 



This study was supported by NIMH 092696 and 67631, NICHD Autism Center of Excellence 055751, NINDS 082008, NINDS 078874, NCATS TR000126, and Autism Speaks 4853.

Authors’ Contributions

KN carried out data analyses, data interpretation, and drafting the manuscript. SM helped with statistical analyses, interpreting the data, and drafting the manuscript. LS helped with data collection, data analysis, and interpretation. ZW helped with data analysis and interpretation. JS helped with data analysis and manuscript preparation. MM provided input on conception and design of the study, assisted in data analysis and interpretation, and helped revise the manuscript for important intellectual content. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in the study.


  1. Annett, M. (1970). A classification of hand preference by association analysis. British Journal of Psychology, 61(3), 303–321.CrossRefPubMedGoogle Scholar
  2. Association, A. P. (1994). American Psychiatric Association: Diagnostic and statistical manual of mental disorders (4th ed.). Arlington, VA: Association, A. P.Google Scholar
  3. Baddeley, A. (1986). Modularity, mass-action and memory. Quarterly Journal of Experimental Psychology A, 38(4), 527–533.CrossRefGoogle Scholar
  4. Berument, S. K., Rutter, M., Lord, C., Pickles, A., & Bailey, A. (1999). Autism screening questionnaire: diagnostic validity. British Journal of Psychiatry, 175, 444–451.CrossRefPubMedGoogle Scholar
  5. Diedrichsen, J., Hashambhoy, Y., Rane, T., & Shadmehr, R. (2005a). Neural correlates of reach errors. Journal of Neuroscience, 25(43), 9919–9931. doi: 10.1523/JNEUROSCI.1874-05.2005.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Diedrichsen, J., Verstynen, T., Lehman, S. L., & Ivry, R. B. (2005b). Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. Journal of Neurophysiology, 93(2), 801–812. doi: 10.1152/jn.00662.2004.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. Dziuk, M. A., Gidley 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), 734–739. doi: 10.1111/j.1469-8749.2007.00734.x.CrossRefPubMedGoogle Scholar
  9. Elison, J. T., Wolff, J. J., Reznick, J. S., Botteron, K. N., Estes, A. M., Gu, H., et al. (2014). Repetitive behavior in 12-month-olds later classified with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 53(11), 1216–1224. doi: 10.1016/j.jaac.2014.08.004.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. Fuentes, C. T., Mostofsky, S. H., & Bastian, A. J. (2009). Children with autism show specific handwriting impairments. Neurology, 73(19), 1532–1537. doi: 10.1212/WNL.0b013e3181c0d48c.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Glazebrook, C., Gonzalez, D., Hansen, S., & Elliott, D. (2009). The role of vision for online control of manual aiming movements in persons with autism spectrum disorders. Autism, 13(4), 411–433. doi: 10.1177/1362361309105659.CrossRefPubMedGoogle Scholar
  13. Gordon, A. M., Westling, G., Cole, K. J., & Johansson, R. S. (1993). Memory representations underlying motor commands used during manipulation of common and novel objects. Journal of Neurophysiology, 69(6), 1789–1796.PubMedGoogle Scholar
  14. Grafton, S. T., Schmitt, P., Van Horn, J., & Diedrichsen, J. (2008). Neural substrates of visuomotor learning based on improved feedback control and prediction. Neuroimage, 39(3), 1383–1395. doi: 10.1016/j.neuroimage.2007.09.062.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Graham, S. A., Abbott, A. E., Nair, A., Lincoln, A. J., Muller, R. A., & Goble, D. J. (2015). The influence of task difficulty and participant age on balance control in ASD. Journal of Autism and Developmental Disorders, 45(5), 1419–1427. doi: 10.1007/s10803-014-2303-7.CrossRefPubMedGoogle Scholar
  16. Green, D., Baird, G., Barnett, A. L., Henderson, L., Huber, J., & Henderson, S. E. (2002). The severity and nature of motor impairment in Asperger’s syndrome: A comparison with specific developmental disorder of motor function. Journal of Child Psychology and Psychiatry, 43(5), 655–668.CrossRefPubMedGoogle Scholar
  17. Haswell, C. C., Izawa, J., Dowell, L. R., Mostofsky, S. H., & Shadmehr, R. (2009). Representation of internal models of action in the autistic brain. Nature Neuroscience, 12(8), 970–972. doi: 10.1038/nn.2356.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Herbert, M. R., Ziegler, D. A., Deutsch, C. K., O’Brien, L. M., Lange, N., Bakardjiev, A., & Caviness, V. S, Jr. (2003). Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain, 126(Pt 5), 1182–1192.CrossRefPubMedGoogle Scholar
  19. Izawa, J., Pekny, S. E., Marko, M. K., Haswell, C. C., Shadmehr, R., & Mostofsky, S. H. (2012). Motor learning relies on integrated sensory inputs in ADHD, but over-selectively on proprioception in autism spectrum conditions. Autism Research, 5(2), 124–136. doi: 10.1002/aur.1222.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Johansson, R. S., & Cole, K. J. (1992). Sensory-motor coordination during grasping and manipulative actions. Current Opinion in Neurobiology, 2(6), 815–823.CrossRefPubMedGoogle Scholar
  21. Johansson, R. S., & Westling, G. (1984). Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Experimental Brain Research, 56(3), 550–564.CrossRefPubMedGoogle Scholar
  22. Johnson, B. P., Rinehart, N. J., Papadopoulos, N., Tonge, B., Millist, L., White, O., & Fielding, J. (2012). A closer look at visually guided saccades in autism and Asperger’s disorder. Frontiers in Integrative Neuroscience, 6, 99. doi: 10.3389/fnint.2012.00099.CrossRefPubMedPubMedCentralGoogle Scholar
  23. LeBarton, E. S., & Iverson, J. M. (2013). Fine motor skill predicts expressive language in infant siblings of children with autism. Developmental Science, 16(6), 815–827. doi: 10.1111/desc.12069.PubMedGoogle Scholar
  24. Leonard, H. C., Bedford, R., Charman, T., Elsabbagh, M., Johnson, M. H., Hill, E. L., et al. (2014). Motor development in children at risk of autism: A follow-up study of infant siblings. Autism, 18(3), 281–291. doi: 10.1177/1362361312470037.CrossRefPubMedGoogle Scholar
  25. Lord, C., Risi, S., Lambrecht, L., Cook, E. H, Jr, Leventhal, B. L., DiLavore, P. C., & Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRefPubMedGoogle Scholar
  26. Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24(5), 659–685.CrossRefPubMedGoogle Scholar
  27. Luna, B., Doll, S. K., Hegedus, S. J., Minshew, N. J., & Sweeney, J. A. (2007). Maturation of executive function in autism. Biological Psychiatry, 61(4), 474–481. doi: 10.1016/j.biopsych.2006.02.030.CrossRefPubMedGoogle Scholar
  28. 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), 834–840.CrossRefPubMedGoogle Scholar
  29. Mari, M., Castiello, U., Marks, D., Marraffa, C., & Prior, M. (2003). The reach-to-grasp movement in children with autism spectrum disorder. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 358(1430), 393–403. doi: 10.1098/rstb.2002.1205.CrossRefGoogle Scholar
  30. Marsden, C. D., Rothwell, J. C., & Day, B. L. (1983). Long-latency automatic responses to muscle stretch in man: Origin and function. Advances in Neurology, 39, 509–539.PubMedGoogle Scholar
  31. Massaro, D. W., & Loftus, G. R. (1996). Sensory and perceptual storage. In E. L. Bjork & R. A. Bjork (Eds.), Memory (pp. 68–96). San Diego, CA: Academic Press.Google Scholar
  32. Minshew, N. J., Luna, B., & Sweeney, J. A. (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology, 52(5), 917–922.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Minshew, N. J., Sung, K., Jones, B. L., & Furman, J. M. (2004). Underdevelopment of the postural control system in autism. Neurology, 63(11), 2056–2061.CrossRefPubMedGoogle Scholar
  34. Molloy, C. A., Dietrich, K. N., & Bhattacharya, A. (2003). Postural stability in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 33(6), 643–652.CrossRefPubMedGoogle Scholar
  35. Mosconi, M. W., Kay, M., D'Cruz, A. M., Guter, S., Kapur, K., Macmillan, C., et al. (2010). Neurobehavioral abnormalities in first-degree relatives of individuals with autism. Archives of General Psychiatry, 67(8), 830–840. doi: 10.1001/archgenpsychiatry.2010.87.CrossRefGoogle Scholar
  36. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mostofsky, S. H., & Ewen, J. B. (2011). Altered connectivity and action model formation in autism is autism. Neuroscientist, 17(4), 437–448. doi: 10.1177/1073858410392381.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Nebel, M. B., Eloyan, A., Nettles, C. A., Sweeney, K. L., Ament, K., Ward, R. E., & Mostofsky, S. H. (2016). Intrinsic visual-motor synchrony correlates with social deficits in autism. Biological Psychiatry, 79(8), 633–641. doi: 10.1016/j.biopsych.2015.08.029.CrossRefPubMedGoogle Scholar
  39. Nickel, L. R., Thatcher, A. R., Keller, F., Wozniak, R. H., & Iverson, J. M. (2013). Posture development in infants at heightened vs. low risk for autism spectrum disorders. Infancy, 18(5), 639–661. doi: 10.1111/infa.12025.CrossRefPubMedGoogle Scholar
  40. Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113.CrossRefPubMedGoogle Scholar
  41. Ozonoff, S., Young, G. S., Belding, A., Hill, M., Hill, A., Hutman, T., et al. (2014). The broader autism phenotype in infancy: When does it emerge? Journal of the American Academy of Child and Adolescent Psychiatry, 53(4), 398–407. e2. doi: 10.1016/j.jaac.2013.12.020.
  42. Papadopoulos, N., McGinley, J., Tonge, B., Bradshaw, J., Saunders, K., Murphy, A., & Rinehart, N. (2012). Motor proficiency and emotional/behavioural disturbance in autism and Asperger’s disorder: Another piece of the neurological puzzle? Autism, 16(6), 627–640. doi: 10.1177/1362361311418692.CrossRefPubMedGoogle Scholar
  43. Reilly, J. L., Lencer, R., Bishop, J. R., Keedy, S., & Sweeney, J. A. (2008). Pharmacological treatment effects on eye movement control. Brain and Cognition, 68(3), 415–435. doi: 10.1016/j.bandc.2008.08.026.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rosenhall, U., Johansson, E., & Gillberg, C. (1988). Oculomotor findings in autistic children. Journal of Laryngology and Otology, 102(5), 435–439.CrossRefPubMedGoogle Scholar
  45. Schmitt, L. M., Cook, E. H., Sweeney, J. A., & Mosconi, M. W. (2014). Saccadic eye movement abnormalities in autism spectrum disorder indicate dysfunctions in cerebellum and brainstem. Mol Autism, 5(1), 47. doi: 10.1186/2040-2392-5-47.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sweeney, J. A., Mintun, M. A., Kwee, S., Wiseman, M. B., Brown, D. L., Rosenberg, D. R., & Carl, J. R. (1996). Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. Journal of Neurophysiology, 75(1), 454–468.PubMedGoogle Scholar
  47. Takagi, M., Zee, D. S., & Tamargo, R. J. (1998). Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. Journal of Neurophysiology, 80(4), 1911–1931.PubMedGoogle Scholar
  48. Takagi, M., Zee, D. S., & Tamargo, R. J. (2000). Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: Smooth pursuit. Journal of Neurophysiology, 83(4), 2047–2062.PubMedGoogle Scholar
  49. 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), 117–127. doi: 10.1016/j.pscychresns.2007.03.008.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Travers, B. G., Powell, P. S., Klinger, L. G., & Klinger, M. R. (2013). Motor difficulties in autism spectrum disorder: Linking symptom severity and postural stability. Journal of Autism and Developmental Disorders, 43(7), 1568–1583. doi: 10.1007/s10803-012-1702-x.CrossRefPubMedGoogle Scholar
  51. Tseng, Y. W., Diedrichsen, J., Krakauer, J. W., Shadmehr, R., & Bastian, A. J. (2007). Sensory prediction errors drive cerebellum-dependent adaptation of reaching. Journal of Neurophysiology, 98(1), 54–62. doi: 10.1152/jn.00266.2007.CrossRefPubMedGoogle Scholar
  52. Vaillancourt, D. E., Slifkin, A. B., & Newell, K. M. (2001). Visual control of isometric force in Parkinson's disease. Neuropsychologia, 39(13), 1410–1418.Google Scholar
  53. Vaillancourt, D. E., Thulborn, K. R., & Corcos, D. M. (2003). Neural basis for the processes that underlie visually guided and internally guided force control in humans. Journal of Neurophysiology, 90(5), 3330–3340. doi: 10.1152/jn.00394.2003.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wechsler, D. (1999). Wechsler abbreviated scale of intelligence. San Antonio, TX: Psychological Corporation.Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Kristina A. Neely
    • 1
  • Suman Mohanty
    • 2
  • Lauren M. Schmitt
    • 2
  • Zheng Wang
    • 2
  • John A. Sweeney
    • 2
  • Matthew W. Mosconi
    • 2
    • 3
  1. 1.Department of KinesiologyPennsylvania State UniversityState CollegeUSA
  2. 2.Center for Autism and Developmental Disabilities, Department of PsychiatryUniversity of Texas SouthwesternDallasUSA
  3. 3.Schiefelbusch Institute for Life Span Studies, Clinical Child Psychology ProgramUniversity of KansasLawrenceUSA

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