Skip to main content
SpringerLink
Log in

Three-Dimensional Kinematic Analysis of Prehension Movements in Young Children with Autism Spectrum Disorder: New Insights on Motor Impairment

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

The study was aimed at better clarifying whether action execution impairment in autism depends mainly on disruptions either in feedforward mechanisms or in feedback-based control processes supporting motor execution. To this purpose, we analyzed prehension movement kinematics in 4- and 5-year-old children with autism and in peers with typical development. Statistical analysis showed that the kinematics of the grasp component was spared in autism, whereas early kinematics of the reach component was atypical. We discussed this evidence as suggesting impairment in the feedforward processes involved in action execution, whereas impairment in feedback-based control processes remained unclear. We proposed that certain motor abilities are available in autism, and children may use them differently as a function of motor context complexity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington, DC: American Psychiatric Association.

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: American Psychiatric Association.

    Google Scholar 

  • Arbib, M. A. (1981). Perceptual structures and distributed motor control. In V. B. Brooks (Ed.), Motor control. Handbook of physiology (pp. 1449–1480). Baltimore: Williams & Wilkins.

    Google Scholar 

  • Barbieri, F., Buonocore, A., Bernardis, P., Dalla Volta, R., & Gentilucci, M. (2007). On the relations between affordance and representation of the agent’s effector. Experimental Brain Research, 180(3), 421–433.

    Article  PubMed  Google Scholar 

  • Bhat, A. N., Galloway, J. C., & Landa, R. J. (2012). Relation between early motor delay and later communication delay in infants at risk for autism. Infant Behavior and Development, 35(4), 838–846.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bootsma, R. J., Marteniuk, R. G., MacKenzie, C. L., & Zaal, F. T. (1994). The speed-accuracy trade-off in manual prehension: Effects of movement amplitude, object size and object width on kinematic characteristics. Experimental Brain Research, 98(3), 535–541.

    Article  PubMed  Google Scholar 

  • Brian, J. A., Bryson, S. E., & Zwaigenbaum, L. (2015). Autism spectrum disorder in infancy: Developmental considerations in treatment targets. Current Opinion in Neurology, 28(2), 117–123.

    Article  PubMed  Google Scholar 

  • Briggs, G. G., & Nebes, R. D. (1975). Patterns of hand preference in a student population. Cortex, 11(3), 230–238.

    Article  PubMed  Google Scholar 

  • Campione, G. C., & Gentilucci, M. (2010). Covert imitation of transitive actions activates effector-independent motor representations affecting “motor” knowledge of target-object properties. Behavioural Brain Research, 207, 343–352.

    Article  PubMed  Google Scholar 

  • Campione, G. C., & Gentilucci, M. (2011). Is the observation of the human kinematics sufficient to activate imitation of transitive actions? Behavioural Brain Research, 225(1), 201–208.

    Article  PubMed  Google Scholar 

  • Cianchetti, C., & Sannio Fancello, G. (2003). Test di Valutazione del Linguaggio. Trento: Edizioni Erickson.

    Google Scholar 

  • Cook, J. L., Blakemore, S. J., & Press, C. (2013). Atypical basic movement kinematics in autism spectrum conditions. Brain, 136, 2816–2824.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cook, J. L., Saygin, A. P., Swain, R., & Blakemore, S. J. (2009). Reduced sensitivity to minimum-jerk biological motion in autism spectrum conditions. Neuropsychologia, 47, 3275–3278.

    Article  PubMed  PubMed Central  Google Scholar 

  • Desmurget, M., & Grafton, S. (2000). Forward modeling allows feedback control for fast reaching movements. Trends in Cognitive Sciences, 4(11), 423–431.

    Article  PubMed  Google Scholar 

  • Esposito, G., Venuti, P., Maestro, S., & Muratori, F. (2009). An exploration of symmetry in early autism spectrum disorders: An analysis of lying. Brain and Development, 31(2), 131–138.

    Article  PubMed  Google Scholar 

  • Fabbri-Destro, M., Cattaneo, L., Boria, S., & Rizzolatti, G. (2009). Planning actions in autism. Experimental Brain Research, 192(3), 521–525.

    Article  PubMed  Google Scholar 

  • Fabbri-Destro, M., Gizzonio, V., & Avanzini, P. (2013). Autism, motor dysfunctions and mirror mechanism. Clinical Neuropsychiatry, 10, 177–187.

    Google Scholar 

  • Ferri, F., Campione, G. C., Dalla Volta, R., Gianelli, C., & Gentilucci, M. (2010). To you or to me: When the self is advantaged. Experimental Brain Research, 203, 637–646.

    Article  PubMed  Google Scholar 

  • Fitts, P. M. (1954). The information capacity of the human motor system in controlling the amplitude of movement. Journal of Experimental Psychology, 47(6), 381–391.

    Article  PubMed  Google Scholar 

  • Flanagan, J., Landa, R., Bhat, A., & Bauman, M. (2012). Head lag in infants at risk for autism: A preliminary study. American Journal of Occupational Therapy, 66, 1–9.

    Article  Google Scholar 

  • Flindall, J. W., & Gonzalez, C. L. R. (2013). On the evolution of handedness: Evidence for feeding biases. PLoS ONE, 8(11), e15855.

    Article  Google Scholar 

  • Flindall, J. W., & Gonzalez, C. L. R. (2015). Children’s bilateral advantage for grasp-to-eat actions becomes unimanual by age 10 years. Journal of Experimental Child Psychology, 133, 57–71.

    Article  PubMed  Google Scholar 

  • Forti, S., Valli, A., Perego, P., Nobile, M., Crippa, A., & Molteni, M. (2011). Motor planning and control in autism. A kinematic analysis of preschool children. Research in Autism Spectrum Disorders, 5, 834–842.

    Article  Google Scholar 

  • 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, 10, 1227–1240.

    Article  Google Scholar 

  • Gentilucci, M., & Campione, G. C. (2012). From action to speech. In Y. Coello & A. Bartolo (Eds.), Language and action in cognitive neuroscience (pp. 59–80). New York: Psychology Press.

    Google Scholar 

  • Gentilucci, M., Castiello, U., Corradini, M. L., Scarpa, M., Umiltà, C., & Rizzolatti, G. (1991). Influence of different types of grasping on the transport component of prehension movements. Neuropsychologia, 29, 361–378.

    Article  PubMed  Google Scholar 

  • Gernsbacher, M., Sauer, E., Geye, H., Schweigert, E., & Goldsmith, H. (2008). Infant and toddler oral- and manual-motor skills predict later speech fluency in autism. Journal of Child Psychology and Psychiatry, 49(1), 43–50.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerson, S. A., & Woodward, A. L. (2014). Learning from their own actions: The unique effect of producing actions on infants’ action understanding. Child Development, 85(1), 264–277.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gianelli, C., Dalla Volta, R., Barbieri, F., & Gentilucci, M. (2008). Automatic grasp imitation following action observation affects estimation of intrinsic object properties. Brain Research, 1218, 166–180.

    Article  PubMed  Google Scholar 

  • Gidley Larson, J. C., & Mostofky, S. H. (2006). Motor deficits in autism. In R. Tuchman & I. Rapin (Eds.), Autism: A neurological disorder of early brain development (pp. 231–247). London: Mac Keith Press for the International Review of Child Neurology Series.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Glover, S. (2004). Separate visual representations in the planning and control of action. Behavioral and Brain Sciences, 27, 3–24.

    PubMed  Google Scholar 

  • Henderson, S., & Sugden, D. (1992). The movement assessment battery for children. New York: Psychological Corporation.

    Google Scholar 

  • Hughes, C. (1996). Planning problems in autism at the level of motor control. Journal of Autism and Developmental Disorders, 26, 99–107.

    Article  PubMed  Google Scholar 

  • Iverson, J. M., & Goldin-Meadow, S. (2005). Gesture paves the way for language development. Psychological Science, 16, 367–371.

    Article  PubMed  Google Scholar 

  • Jeannerod, M. (1981). Intersegmental coordination during reaching at natural visual objects. In J. Long & A. Baddeley (Eds.), Attention and performance IX (pp. 153–168). Hillsdale, NJ: Lawrence Erlbaum Associates.

    Google Scholar 

  • Jeannerod, M. (1984). The timing of natural prehension movements. Journal of Motor Behavior, 16, 235–254.

    Article  PubMed  Google Scholar 

  • Jeannerod, M. (1988). The neural and behavioural organization of goal-directed movements. Oxford: Clarendon Press.

    Google Scholar 

  • Johnson-Frey, S., McCharty, M., & Keen, R. (2004). Reaching beyond spatial perception: Effects of intended future actions on visually-guided prehension. Visual Cognition, 11(2/3), 371–399.

    Article  Google Scholar 

  • Kuhtz-Buschbeck, J. P., Boczek-Funcke, A., Illert, M., Joehnk, K., & Stolze, H. (1999). Prehension movements and motor development in children. Experimental Brain Research, 128(1–2), 65–68.

    Article  PubMed  Google Scholar 

  • Kuhtz-Buschbeck, J. P., Stolze, H., Boczek-Funcke, A., Jöhnk, K., Heinrichs, H., & Illert, M. (1998a). Kinematic analysis of prehension movements in children. Behavioural Brain Research, 93(1–2), 131–141.

    Article  PubMed  Google Scholar 

  • Kuhtz-Buschbeck, J. P., Stolze, H., Jöhnk, K., Boczek-Funcke, A., & Illert, M. (1998b). Development of prehension movements in children: A kinematic study. Experimental Brain Research, 122(4), 424–432.

    Article  PubMed  Google Scholar 

  • Landa, R., & Garrett-Mayer, E. (2006). Development in infants with autism spectrum disorders: A prospective study. Journal of Child Psychology and Psychiatry, 47(6), 629–638.

    Article  PubMed  Google Scholar 

  • Leary, M. R., & Hill, D. A. (1996). Moving on: Autism and movement disturbance. Mental Retardation, 34, 39–53.

    PubMed  Google Scholar 

  • Libertus, K., Sheperd, K. A., Ross, S. W., & Landa, R. J. (2014). Limited fine motor and grasping skills in 6-month-old infants at high risk for autism. Child Development, 85(6), 2218–2231.

    PubMed  PubMed Central  Google Scholar 

  • Lloyd, M., Macdonald, M., & Lord, C. (2013). Motor skills of toddlers with autism spectrum disorders. Autism, 15(3), 1–18.

    Google Scholar 

  • Lord, C., Rutter, M., Dilavore, P. C., & Risi, S. (2002). Autism diagnostic observation schedule. Los Angeles: Western Psychological Services.

    Google Scholar 

  • MacNeil, L. K., & Mostofsky, S. H. (2012). Specificity of dyspraxia in children with autism. Neuropsychology, 26, 165–171.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 B: Biological Sciences, 358, 393–403.

    Article  Google Scholar 

  • Marteniuk, R. G., Leavitt, J. L., MacKenzie, C. L., & Athenes, S. (1990). Functional relationships between grasp and transport components in a prehension task. Human Movement Science, 9, 149–176.

    Article  Google Scholar 

  • Marteniuk, R. G., MacKenzie, C. L., Jeannerod, M., Athenes, S., & Dugas, C. (1987). Constraints on human arm movements trajectories. Canadian Journal of Psychology, 41, 365–378.

    Article  PubMed  Google Scholar 

  • Meyer, D. E., Abrams, R. A., Kornblum, S., Wright, C. E., & Smith, J. E. (1988). Optimality in human motor performance: Ideal control of rapid aimed movements. Psychological Review, 95(3), 340–370.

    Article  PubMed  Google Scholar 

  • Ming, X., Brimacombe, M., & Wagner, G. C. (2007). Prevalence of motor impairments in autism spectrum disorders. Brain and Development, 29, 565–570.

    Article  PubMed  Google Scholar 

  • 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 International Neuropsychological Society, 12, 314–326.

    Article  Google Scholar 

  • Nakano, T., Kato, N., & Kitazawa, S. (2012). Superior haptic-to-visual shape matching in autism spectrum disorders. Neuropsychologia, 50, 696–703.

    Article  PubMed  Google Scholar 

  • Nazarali, N., Glazebrook, C. M., & Elliott, D. (2009). Movement planning and reprogramming in individuals with autism. Journal of Autism and Developmental Disorders, 39, 1401–1411.

    Article  PubMed  Google Scholar 

  • Ozonoff, S., Young, G., Goldring, S., Greiss-Hess, L., Herrera, A., Steele, J., et al. (2008). Gross motor development, movement abnormalities, and early identification of autism. Journal of Autism and Developmental Disorders, 38(4), 644–656.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronconi, L., Gori, S., Giora, E., Ruffino, M., Molteni, M., & Facoetti, A. (2013). Deeper attentional masking by lateral objects in children with autism. Brain and Cognition, 82(2), 213–218.

    Article  PubMed  Google Scholar 

  • Ronconi, L., Gori, S., Ruffino, M., Franceschini, S., Urbani, B., Molteni, M., et al. (2012). Decreased coherent motion discrimination in autism spectrum disorder: The role of attentional zoom-out deficit. PLoS ONE, 7(11), e49019.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sacrey, L. A., Bennet, J. A., & Zwaigenbaum, L. (2015). Early infant development and intervention for autism spectrum disorder. Journal of Child Neurology, 30(14), 1921–1929.

    Article  PubMed  Google Scholar 

  • Sacrey, L. A., Germani, T., Bryson, S. E., & Zwaigenbaum, L. (2014). Reaching and grasping in autism spectrum disorder: A review of recent literature. Frontiers in Neurology, 23(5), 1–12.

    Google Scholar 

  • Sauer LeBarton, E., & Iverson, J. (2013). Fine motor skill predicts expressive language in infant siblings of children with autism. Developmental Science, 16(6), 815–827.

    Google Scholar 

  • Schmitz, C., Martineau, J., Barthelemy, C., & Assaiante, C. (2003). Motor control and children with autism: Deficit of anticipatory function? Neuroscience Letters, 348, 17–22.

    Article  PubMed  Google Scholar 

  • Stoit, A. M., van Schie, H. T., Slaat-Willemse, D. I., & Buitelaar, J. K. (2013). Grasping motor impairments in autism: Not action planning but movement execution is deficient. Journal of Autism and Developmental Disorders, 43(12), 2793–2806.

    Article  PubMed  Google Scholar 

  • Teitelbaum, P., Teitelbaum, O., Nye, J., Fryman, J., & Maurer, R. G. (1998). Movement analysis in infancy may be useful for early diagnosis of autism. Proceedings of the National Academy of Sciences of the United States of America, 95, 13982–13987.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wechsler, D. (2002). Wechsler preschool and primary scale of intelligence-third edition (WPPSI-III). San Antonio, TX: Harcourt Assessment.

    Google Scholar 

  • Zoia, S., Pezzetta, E., Blason, L., Scabar, A., Carrozzi, M., Bulgheroni, M., et al. (2006). A comparison of the reach-to-grasp movement between children and adults: A kinematic study. Developmental Neuropsychology, 30(2), 719–738.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Lara Nichesola for her help in recruiting patients with ASD, and Ilaria Negri for her help in collecting data. This study was supported by Italian Ministry of Health, Research Grant: RC 2013-2014 (3.11-2.6). Finally, we are also grateful to the families of the children who took part in the study.

Author Contributions

GCC conceived of the study and its design; participated in coordination and kinematic measurement; performed the statistical analysis, interpretation of the data, and drafted the manuscript; CP performed the kinematic measurement, participated in interpretation of the data, and helped to draft the manuscript; LV participated in the design of the study; MM participated in the coordination of the study and interpretation of the data.

Author information

Authors and Affiliations

  1. Child Psychopathology Unit, Scientific Institute, IRCCS Eugenio Medea, Via Don Luigi Monza 20, 23842, Bosisio Parini, Lecco, Italy

    Giovanna Cristina Campione, Laura Villa & Massimo Molteni

  2. Bioingineering Lab, Scientific Institute, IRCCS Eugenio Medea, Via Don Luigi Monza 20, 23842, Bosisio Parini, Lecco, Italy

    Caterina Piazza

  3. Department of Electronics Information and Bioengineering (DEIB), Politecnico di Milano, Via Ponzio 34, 20133, Milan, Italy

    Caterina Piazza

Authors
  1. Giovanna Cristina Campione
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caterina Piazza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Villa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Massimo Molteni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giovanna Cristina Campione.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Campione, G.C., Piazza, C., Villa, L. et al. Three-Dimensional Kinematic Analysis of Prehension Movements in Young Children with Autism Spectrum Disorder: New Insights on Motor Impairment. J Autism Dev Disord 46, 1985–1999 (2016). https://doi.org/10.1007/s10803-016-2732-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-016-2732-6

Keywords

Search

Navigation