Grasping motor impairments in Autism: Not action planning but movement execution is deficient

Journal of Autism and Developmental Disorders

Volumn 43, Issue 12, 2013, Pages 2793-2806

  Stoit, Astrid M B ^a   Van Schie, Hein T ^b   Slaats Willemse, Dorine I E ^b   Buitelaar, Jan K ^b,c  

^a Karakter Child and Adolescent Psychiatry   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c RADBOUD UNIVERSITY   (Netherlands)

Author keywords

Action chaining; Action planning; Autism; Feedforward model; Motor deficit; Movement execution

Indexed keywords

ARTICLE; AUTISM; CHILD; CLINICAL ARTICLE; FEMALE; HUMAN; MALE; MOTOR CONTROL; MOTOR DYSFUNCTION; MOVEMENT (PHYSIOLOGY); PRIORITY JOURNAL; REACTION TIME; SCHOOL CHILD; STIMULUS RESPONSE;

ADOLESCENT; AUTISTIC DISORDER; CHILD; CUES; FEMALE; HAND STRENGTH; HUMANS; MALE; MOVEMENT; REACTION TIME;

EID: 84888050413     PISSN: 01623257     EISSN: 15733432     Source Type: Journal    
DOI: 10.1007/s10803-013-1825-8     Document Type: Article

References (106)

1. Achenbach, T. M. (1991). Manual for the child behavior checklist/4-18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.
2. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders, fourth edition, text revision. Washington, DC: American Psychiatric Association.
3. Bachevalier, J.; & Loveland, K. A. (2006). The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neuroscience and Biobehavioral Reviews, 30(1), 97-117.
4. Baranek, G. T. (1999). Autism during infancy: A retrospective video analysis of sensory-motor and social behaviors at 9-12 months of age. Journal of Autism and Developmental Disorders, 29, 213-224.
5. Barnea-Goraly, N.; Lotspeich, L. J.; & Reiss, A. L. (2010). Similar white matter aberrations in children with autism and their unaffected siblings: A diffusion tensor imaging study using tract-based spatial statistics. Archives of General Psychiatry, 67(10), 1052-1060.
6. Belmonte, M. K.; Allen, G.; Beckel-Mitchener, A.; Boulanger, L. M.; Carper, R. A.; & Webb, S. J. (2004). Autism and abnormal development of brain connectivity. Journal of Neuroscience, 24(42), 9228-9231.
7. Bernier, R.; Dawson, G.; Webb, S.; & Murias, M. (2007). EEG mu rhythm and imitation impairments in individuals with autism spectrum disorder. Brain and Cognition, 64(3), 228-237.
8. Bhat, A.; Galloway, J.; & Landa, R. (2012). Relation between early motor delay and later communication delay in infants at risk for autism. Infant Behavior and Development, 35(4), 838-846.
9. Bird, G.; Leighton, J.; Press, C.; & Heyes, C. (2007). Intact automatic imitation of human and robot actions in autism spectrum disorders. Proceedings of the Royal Society B: Biological Sciences, 274(1628), 3027-3031.
10. Boria, S.; Fabbri-Destro, M.; Cattaneo, L.; Sparaci, L.; Sinigaglia, C.; Santelli, E.; et al. (2009). Intention understanding in autism. PLoS ONE, 4(5), e5596.
11. Brisson, J.; Warreyn, P.; Serres, J.; Foussier, S.; & Adrien-Louis, J. (2012). Motor anticipation failure in infants with autism: A retrospective analysis of feeding situations. Autism, 16(4), 420-429.
12. Brock, J.; Brown, C. C.; Boucher, J.; & Rippon, G. (2002). The temporal binding deficit hypothesis of autism. Development and Psychopathology, 14(2), 209-224.
13. Buccino, G.; Vogt, S.; Ritzl, A.; Fink, G. R.; Zilles, K.; Freund, H. J.; et al. (2004). Neural circuits underlying imitation learning of hand actions: An event-related fMRI study. Neuron, 42, 323-334.
14. Cattaneo, L.; Fabbri-Destro, M.; Boria, S.; Pieraccini, C.; Monti, A.; Cossu, G.; et al. (2007). Impairment of actions chains in autism and its possible role in intention understanding. Proceedings of the National Academy of Sciences of the United States of America, 104, 17825-17830.
15. Chartrand, T. L.; & van Baaren, R. (2009). Human mimicry. Advances in Experimental Social Psychology, 41, 219-274.
16. Constantino, J. N.; & Gruber, C. P. (2005). The Social Responsiveness Scale (SRS) manual. Los Angeles: Western Psychological Services.
17. Courchesne, E.; Pierce, K.; Schumann, C. M.; Redcay, E.; Buckwalter, J. A.; Kennedy, D. P.; et al. (2007). Mapping early brain development in autism. Neuron, 56(2), 399-413.
18. Danev, S. G.; de Winter, C. R.; & Wartna, G. F. (1971). On the relation between reaction and motion time in a choice reaction task. Acta Psychologica, 35(3), 188-197.
19. Dapretto, M.; Davies, M. S.; Pfeifer, J. H.; Scott, A. A.; Sigman, M.; Bookheimer, S. Y.; et al. (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9(1), 28-30.
20. De Sonneville, L. (1999). Amsterdam Neuro-psychological Tasks: A computer-aided assessment program. In B. P. L. M. den Brinker, P. J. Beek, A. N. Brand, S. J. Maarse, & L. J. M. Mulder (Eds.), Cognitive ergonomics, clinical assessment and computer-assisted learning (pp. 187-203). Lisse: Swets.
21. Dinstein, I.; Thomas, C.; Humphreys, K.; Minshew, N.; Behrmann, M.; & Heeger, D. J. (2010). Normal movement selectivity in autism. Neuron, 66(3), 461-469.
22. Dziuk, M. A.; Larson, J. C. G.; 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, 734-739.
23. Fabbri-Destro, M.; Cattaneo, L.; Boria, S.; & Rizzolatti, G. (2009). Planning actions in autism. Experimental Brain Research, 192, 521-525.
24. Fan, Y.-T.; Decety, J.; Yang, C.-Y.; Liu, J.-L.; & Cheng, Y. (2010). Unbroken mirror neurons in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 51(9), 981-988.
25. Fogassi, L.; Ferrari, P. F.; Gesierich, B.; Rozzi, S.; Chersi, F.; & Rizzolatti, G. (2005). Parietal lobe: From action organization to intention understanding. Science, 308, 662-667.
26. 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(2), 834-842.
27. Freitag, C. M.; Konrad, C.; Häberlen, M.; Kleser, C.; von Gontard, A.; Reith, W.; et al. (2008). Perception of biological motion in autism spectrum disorders. Neuropsychologia, 46(5), 1480-1494.
28. Gazzola, V.; & Keysers, C. (2009). The observation and execution of actions share motor and somatosensory voxels in all tested subjects: Single-subject analyses of unsmoothed fMRI data. Cerebral Cortex, 19(6), 1239-1255.
29. Geschwind, D. H.; & Levitt, P. (2007). Autism spectrum disorders: Developmental disconnection syndromes. Current Opinion in Neurobiology, 17(1), 103-111.
30. Ghaziuddin, M.; & Butler, E. (1998). Clumsiness in autism and Asperger syndrome: A further report. Journal of Intellectual Disability Research, 42, 43-48.
31. 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.
32. Glazebrook, C. M.; Elliott, D.; & Szatmari, P. (2008). How do individuals with autism plan their movements? Journal of Autism and Developmental Disorders, 38, 114-126.
33. Gowen, E.; Stanley, J.; & Miall, R. C. (2008). Movement interference in autism-spectrum disorder. Neuropsychologia, 46(4), 1060-1068.
34. Grafton, S. T.; & Hamilton, A. F. D. (2007). Evidence for a distributed hierarchy of action representation in the brain. Human Movement Science, 26, 590-616.
35. Green, D.; Charman, T.; Pickles, A.; Chandler, S.; Loucas, T.; Simonoff, E.; et al. (2009). Impairment in movement skills of children with autistic spectrum disorders. Developmental Medicine and Child Neurology, 51, 311-316.
36. Greimel, E.; Schulte-Ruether, M.; Kircher, T.; Kamp-Becker, I.; Remschmidt, H.; Fink, G. R.; et al. (2010). Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. Neuroimage, 49(1), 1055-1065.
37. Hadjikhani, N.; Joseph, R. M.; Snyder, J.; & Tager-Flusberg, H. (2006). Anatomical differences in the mirror neuron system and social cognition network in autism. Cerebral Cortex, 16, 1276-1282.
38. Hamilton, A. F. C. (2008). Emulation and mimicry for social interaction: A theoretical approach to imitation in autism. Quarterly Journal of Experimental Psychology, 61(1), 101-115.
39. Hamilton, A. F. C. (2009). Research review: Goals, intentions and mental states: Challenges for theories of autism. Journal of Child Psychology and Psychiatry, 50(8), 881-892.
40. Hamilton, A. F. D.; Brindley, R. M.; & Frith, U. (2007). Imitation and action understanding in autistic spectrum disorders: How valid is the hypothesis of a deficit in the mirror neuron system? Neuropsychologia, 45(8), 1859-1868.
41. Happe, F.; & Frith, U. (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5-25.
42. 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.
43. Hill, E. L. (2004). Executive dysfunction in autism. Trends in Cognitive Sciences, 8(1), 26-32.
44. Hobson, R. P.; & Hobson, J. A. (2008). Dissociable aspects of imitation: A study in autism. Journal of Experimental Child Psychology, 101(3), 170-185.
45. Hobson, R. P.; & Lee, A. (1999). Imitation and identification in autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 40(4), 649-659.
46. Hughes, C. (1996). Brief report: Planning problems in autism at the level of motor control. Journal of Autism and Developmental Disorders, 26, 99-107.
47. Hughes, C.; & Russell, J. (1993). Autistic children's difficulty with mental disengagement from an object: Its implications for theories of autism. Developmental Psychology, 29, 498-510.
48. Iacoboni, M. (2005). Neural mechanisms of imitation. Current Opinion in Neurobiology, 15, 632-637.
49. Iacoboni, M.; & Dapretto, M. (2006). The mirror neuron system and the consequences of its dysfunction. Nature Reviews Neuroscience, 7(12), 942-951.
50. Kaufman, A. S.; Kaufman, J. C.; Balgopal, R.; & McLean, J. E. (1996). Comparison of three WISC-III short forms: Weighing psychometric, clinical, and practical factors. Journal of Clinical Child Psychology, 25(1), 97-105.
51. Kenworthy, L.; Yerys, B. E.; Anthony, L. G.; & Wallace, G. L. (2008). Understanding executive control in autism spectrum disorders in the lab and in the real world. Neuropsychology Review, 18(4), 320-338.
52. Leary, M. R.; & Hill, D. A. (1996). Moving on: Autism and movement disturbance. Mental Retardation, 34, 39-53.
53. Leighton, J.; Bird, G.; Charman, T.; & Heyes, C. (2008). Weak imitative performance is not due to a functional 'mirroring' deficit in adults with Autism Spectrum Disorders. Neuropsychologia, 46(4), 1041-1049.
54. Leonard, J. A. (1959). Tactual choice reactions. Quarterly Journal of Experimental Psychology, 11(2), 76-83.
55. Liberman, A. M.; & Mattingly, I. G. (1985). The motor theory of speech-perception revised. Cognition, 21, 1-36.
56. Lord, C.; Rutter, M.; Dilavore, P.; & Riso, S. (2001). Autism diagnostic observation schedule (ADOS) manual. Los Angeles, CA: Western Psychological Services.
57. Luteijn, E. F.; Minderaa, R.; & Jackson, S. (2002). Vragenlijst voor Inventarisatie van Sociaal gedrag bij Kinderen (VISK), handleiding. Lisse: Swets.
58. 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 Series B-Biological Sciences, 358, 393-403.
59. Martineau, J.; Cochin, S.; Magne, R.; & Barthelemy, C. (2008). Impaired cortical activation in autistic children: Is the mirror neuron system involved? International Journal of Psychophysiology, 68(1), 35-40.
60. McIntosh, D. N.; Reichmann-Decker, A.; Winkielman, P.; & Wilbarger, J. L. (2006). When the social mirror breaks: Deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. Developmental Science, 9, 295-302.
61. Miall, R. C. (2003). Connecting mirror neurons and forward models. NeuroReport, 14(17), 2135-2137.
62. Ming, X.; Brimacombe, M.; & Wagner, G. C. (2007). Prevalence of motor impairment in autism spectrum disorders. Brain and Development, 29(9), 565-570.
63. Minshew, N. J.; & Williams, D. L. (2007). The new neurobiology of autism - Cortex, connectivity, and neuronal organization. Archives of Neurology, 64(7), 945-950.
64. Mostofsky, S. H.; & Ewen, J. B. (2011). Altered connectivity and action model formation in autism is autism. Neuroscientist, 17(4), 437-448.
65. Mundy, P. (2003). Annotation: The neural basis of social impairments in autism: The role of the dorsal medial-frontal cortex and anterior cingulate system. Journal of Child Psychology and Psychiatry and Allied Disciplines, 44(6), 793-809.
66. Nazarali, N.; Glazebrook, C. M.; & Elliott, D. (2009). Movement planning and reprogramming in individuals with autism. Journal of Autism and Developmental Disorders, 39(10), 1401-1411.
67. Nishitani, N.; Avikainen, S.; & Hari, R. (2004). Abnormal imitation-related cortical activation sequences in Asperger's syndrome. Annals of Neurology, 55, 558-562.
68. Oberman, L. M.; Hubbard, E. M.; McCleery, J. P.; Altschuler, E. L.; Ramachandran, V. S.; & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cognitive Brain Research, 24, 190-198.
69. Oberman, L. M.; Ramachandran, V. S.; & Pineda, J. A. (2008). Modulation of mu suppression in children with autism spectrum disorders in response to familiar or unfamiliar stimuli: The mirror neuron hypothesis. Neuropsychologia, 46(5), 1558-1565.
70. Ozonoff, S.; & Strayer, D. L. (2001). Further evidence of intact working memory in autism. Journal of Autism and Developmental Disorders, 31(3), 257-263.
71. Pardo, C. A.; & Eberhart, C. G. (2007). The neurobiology of autism. Brain Pathology, 17(4), 434-447.
72. Paulus, M.; Hunnius, S.; Vissers, M.; & Bekkering, H. (2011). Bridging the gap between the other and me: The functional role of motor resonance and action effects in infants' imitation. Developmental Science, 14, 901-910.
73. Pennington, B. F.; & Ozonoff, S. (1996). Executive functions and developmental psychopathology. Journal of Child Psychology and Psychiatry, 37(1), 51-87.
74. Perkins, T.; Stokes, M.; McGillivray, J.; & Bittar, R. (2010). Mirror neuron dysfunction in autism spectrum disorders. Journal of Clinical Neuroscience, 17(10), 1239-1243.
75. Polleux, F.; & Lauder, J. M. (2004). Toward a developmental neurobiology of autism. Mental Retardation and Developmental Disabilities Research Reviews, 10(4), 303-317.
76. Raymaekers, R.; Wiersema, J. R.; & Roeyers, H. (2009). EEG study of the mirror neuron system in children with high functioning autism. Brain Research, 1304, 113-121.
77. Rinehart, N. J.; Bellgrove, M. A.; Tonge, B. J.; Brereton, A. V.; Howells-Rankin, D.; & Bradshaw, J. L. (2006a). An examination of movement kinematics in young people with high-functioning autism and Asperger's disorder: Further evidence for a motor planning deficit. Journal of Autism and Developmental Disorders, 36, 757-767.
78. Rinehart, N. J.; Bradshaw, J. L.; Brereton, A. V.; & Tonge, B. J. (2001). Movement preparation in high-functioning autism and Asperger disorder: A serial choice reaction time task involving motor reprogramming. Journal of Autism and Developmental Disorders, 31, 79-88.
79. Rinehart, N. J.; Tonge, B. J.; Bradshaw, J. L.; Iansek, R.; Enticott, P. G.; & Johnson, K. A. (2006b). Movement-related potentials in high-functioning autism and Asperger's disorder. Developmental Medicine and Child Neurology, 48(4), 272-277.
80. Rizzolatti, G.; & Fabbri-Destro, M. (2010). Mirror neurons: From discovery to autism. Experimental Brain Research, 200, 223-237.
81. Rizzolatti, G.; Fabbri-Destro, M.; & Cattaneo, L. (2009). Mirror neurons and their clinical relevance. Nature Clinical Practice Neurology, 5, 24-34.
82. Rizzolatti, G.; Fogassi, L.; & Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience, 2, 661-670.
83. Robbins, T. W.; James, M.; Owen, A.; Sahakian, B.; McInnes, L.; & Rabbitt, P. (1994). Cambridge neuropsychological test automated battery (CANTAB): A factor analytic study of a large sample of normal elderly volunteers. Dementia and Geriatric Cognitive Disorders, 5(5), 266-281.
84. Rogers, S.; & Williams, J. (2006). Imitation in autism: Findings and controversies. In S. J. Rogers & J. H. G. Williams (Eds.), Imitation and the social mind: Autism and typical development (pp. 277-309). New York: The Guilford Press.
85. Rosenbaum, D. A.; & Jorgensen, M. J. (1992). Planning macroscopic aspects of manual control. Human Movement Science, 11, 61-69.
86. Rutherford, M. D.; & Rogers, S. J. (2003). Cognitive underpinnings of pretend play in autism. Journal of Autism and Developmental Disorders, 33(3), 289-302.
87. Rutter, M.; Le Couteur, A.; & Lord, C. (2003). Autism diagnostic interview-revised. Los Angeles, CA: Western Psychological Services.
88. Schmitz, C.; Martineau, J.; Barthelemy, C.; & Assaiante, C. (2003). Motor control and children with autism: Deficit of anticipatory function? Neuroscience Letters, 348, 17-20.
89. Schurink, J.; Hartman, E.; Scherder, E. J. A.; Houwen, S.; & Visscher, C. (2012). Relationship between motor and executive functioning in school-age children with pervasive developmental disorder not otherwise specified. Research in Autism Spectrum Disorders, 6(2), 726-732.
90. Sebanz, N.; Bekkering, H.; & Knoblich, G. (2006). Joint action: Bodies and minds moving together. Trends in Cognitive Sciences, 10, 70-76.
91. Sebanz, N.; Knoblich, G.; Stumpf, L.; & Prinz, W. (2005). Far from action-blind: Representation of others' actions in individuals with autism. Cognitive Neuropsychology, 22(3-4), 433-454.
92. Smith, I. M.; & Bryson, S. E. (1994). Imitation and action in autism: A critical review. Psychological Bulletin, 116, 259-273.
93. Southgate, V.; & Hamilton, A. F. C. (2008). Unbroken mirrors: Challenging a theory of autism. Trends in Cognitive Sciences, 12(6), 225-229.
94. Stoit, A. M. B.; van Schie, H. T.; Riem, M.; Meulenbroek, R. G. J.; Newman-Norlund, R. D.; Slaats-Willemse, D. I. E.; et al. (2011). Internal model deficits impair joint action in children and adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders, 5(4), 1526-1537.
95. Szatmari, P.; Tuff, L.; Finlayson, A. J.; & Bartolucci, G. (1990). Aspergers syndrome and autism: Neurocognitive aspects. Journal of the American Academy of Child and Adolescent Psychiatry, 29, 130-136.
96. Theoret, H.; Halligan, E.; Kobayashi, M.; Fregni, F.; Tager-Flusberg, H.; & Pascual-Leone, A. (2005). Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Current Biology, 15, R84-R85.
97. van der Helden, J.; van Schie, H. T.; & Rombouts, C. (2010). Observational learning of new movement sequences is reflected in fronto-parietal coherence. PLoS ONE, 5(12), e14482.
98. van Elk, M.; van Schie, H. T.; & Bekkering, H. (2009a). Action semantic knowledge about objects is supported by functional motor activation. Journal of Experimental Psychology-Human Perception and Performance, 35, 1118-1128.
99. van Elk, M.; van Schie, H. T.; & Bekkering, H. (2009b). Short-term action intentions overrule long-term semantic knowledge. Cognition, 111, 72-83.
100. van Elk, M.; van Schie, H. T.; Lindemann, O.; & Bekkering, H. (2007). Using conceptual knowledge in action and language. In P. Haggard, Y. Rossetti, & M. Kawato (Eds.), Attention and performance XXII: Sensorimotor foundations of higher cognition (pp. 575-599). Oxford: Oxford University Press.
101. van Schie, H. T.; & Bekkering, H. (2007). Neural mechanisms underlying immediate and final action goals in object use reflected by slow wave brain potentials. Brain Research, 1148, 183-197.
102. Wechsler, D. (1991). The Wechsler intelligence scale for children - (3rd ed.). San Antonio, TX: The Psychological Corporation.
103. Wechsler, D. (1997). Wechsler adult intelligence scale (3rd ed.). San Antonio, TX: The Psychological Corporation.
104. Williams, J. H. G.; Waiter, G. D.; Gilchrist, A.; Perrett, D. I.; Murray, A. D.; & Whiten, A. (2006). Neural mechanisms of imitation and 'mirror neuron' functioning in autistic spectrum disorder. Neuropsychologia, 44(4), 610-621.
105. 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), 285-299.
106. Wolpert, D. M.; & Flanagan, J. R. (2001). Motor prediction. Current Biology, 11, R729-R732.