Motor learning relies on integrated sensory inputs in ADHD, but over-selectively on proprioception in autism spectrum conditions

Autism Research

Volumn 5, Issue 2, 2012, Pages 124-136

  Izawa, Jun ^a,b   Pekny, Sarah E ^a   Marko, Mollie K ^a   Haswell, Courtney C ^a,d   Shadmehr, Reza ^a   Mostofsky, Stewart H ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ADVANCED TELECOMMUNICATIONS RESEARCH INSTITUTE INTERNATIONAL   (Japan)

^c KENNEDY KRIEGER INSTITUTE   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

Generalization; Internal model; Motor learning

Indexed keywords

ADAPTATION; ARTICLE; ATTENTION DEFICIT DISORDER; AUTISM; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FORCE; HUMAN; LEARNING; MALE; MEMORY; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); PRIORITY JOURNAL; PROPRIOCEPTION; SCHOOL CHILD; SENSORY STIMULATION; STIMULUS GENERALIZATION; VELOCITY; CASE CONTROL STUDY; IMITATION; PATHOPHYSIOLOGY; PERCEPTION; PSYCHOLOGICAL ASPECT; PSYCHOLOGICAL MODEL; PSYCHOPHYSIOLOGY; SENSORY FEEDBACK;

ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CASE-CONTROL STUDIES; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; FEEDBACK, SENSORY; FEMALE; GENERALIZATION (PSYCHOLOGY); HUMANS; IMITATIVE BEHAVIOR; MALE; MODELS, PSYCHOLOGICAL; MOTOR SKILLS; PROPRIOCEPTION; PSYCHOPHYSIOLOGY; SOCIAL PERCEPTION;

EID: 84865347695     PISSN: 19393792     EISSN: 19393806     Source Type: Journal    
DOI: 10.1002/aur.1222     Document Type: Article

References (67)

1. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders, 4th ed. Washington, DC: American Psychiatric Association.
2. Bauman, M.L. (1991). Microscopic neuroanatomic abnormalities in autism. Pediatrics, 87, 791-796.
3. 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, 9228-9231.
4. Casanova, M.F., van Kooten, I.A., Switala, A.E., van Engeland, H., Heinsen, H., et al. (2006). Minicolumnar abnormalities in autism. Acta Neuropathologica, 112, 287-303.
5. Cattaneo, L., Fabbri-Destro, M., Boria, S., Pieraccini, C., Monti, A., 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.
6. Cole, W.R., Mostofsky, S.H., Larson, J.C., Denckla, M.B., & Mahone, E.M. (2008). Age-related changes in motor subtle signs among girls and boys with ADHD. Neurology, 71, 1514- 1520.
7. Conners, C.K. (1997). Conners' rating scales-revised. North Tonawanda. New York: Multi-Health Systems.
8. Constantino, J. (2005). Social responsiveness scale. Los Angeles, CA: Western Psychological Services.
9. Courchesne, E., Saitoh, O., Yeung-Courchesne, R., Press, G.A., Lincoln, A.J., et al. (1994). Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: Identification of hypoplastic and hyperplastic subgroups with MR imaging. AJR. American Journal of Roentgenology, 162, 123- 130.
10. Criscimagna-Hemminger, S.E., & Shadmehr, R. (2008). Consolidation patterns of human motor memory. Journal of Neuroscience, 28, 9610-9618.
11. Darainy, M., Mattar, A.A., & Ostry, D.J. (2009). Effects of human arm impedance on dynamics learning and generalization. Journal of Neurophysiology, 101, 3158-3168.
12. Denckla, M.B. (1985). Revised neurological examination for subtle signs. Psychopharmacology Bulletin, 21, 773-800.
13. Dewey, D., Cantell, M., & Crawford, S.G. (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, 13, 246-256.
14. Donchin, O., Francis, J.T., & Shadmehr, R. (2003). Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: Theory and experiments in human motor control. Journal of Neuroscience, 23, 9032-9045.
15. Dowell, L.R., Mahone, E.M., & Mostofsky, S.H. (2009). Associations of postural knowledge and basic motor skill with dyspraxia in autism: Implication for abnormalities in distributed connectivity and motor learning. Neuropsychology, 23, 563- 570.
16. DuPaul, G.J., Power, T.J., Anastopoulos, A.D., & Reid, R. (1998). ADHD rating scale-IV. New York: Guilford Press.
17. 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, 734-739.
18. Frith, U. (2001). Mind blindness and the brain in autism. Neuron, 32, 969-979.
19. Galea, J.M., Vazquez, A., Pasricha, N., Orban de Xivry, J.J., & Celnik, P. (2010). Dissociating the roles of the cerebellum and motor cortex during adaptive learning: The motor cortex retains what the cerebellum learns. Cereb Cortex, 21, 1761-1770.
20. Geurts, H.M., Grasman, R.P., Verte, S., Oosterlaan, J., Roeyers, H., et al. (2008). Intra-individual variability in ADHD, autism spectrum disorders and Tourette's syndrome. Neuropsychologia, 46, 3030-3041.
21. Gidley Larson, J.C., Bastian, A.J., Donchin, O., Shadmehr, R., & Mostofsky, S.H. (2008). Acquisition of internal models of motor tasks in children with autism. Brain, 131, 2894-2903.
22. Harris, C.M., & Wolpert, D.M. (1998). Signal-dependent noise determines motor planning. Nature, 394, 780-784.
23. \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, 970-972.
24. Herbert, M.R., Ziegler, D.A., Makris, N., Filipek, P.A., Kemper, T.L., et al. (2004). Localization of white matter volume increase in autism and developmental language disorder. Annals of Neurology, 55, 530-540.
25. Hwang, E.J., & Shadmehr, R. (2005). Internal models of limb dynamics and the encoding of limb state. Journal of Neural Engineering, 2, S266-S278.
26. Hwang, E.J., Smith, M.A., & Shadmehr, R. (2006). Adaptation and generalization in acceleration-dependent force fields. Experimental Brain Research, 169, 496-506.
27. Izawa, J., & Shadmehr, R. (2011). Learning from sensory and reward prediction errors during motor adaptation. PLoS Computational Biology, 7, e1002012.
28. Izawa, J., Rane, T., Donchin, O., & Shadmehr, R. (2008). Motor adaptation as a process of reoptimization. Journal of Neuroscience, 28, 2883-2891.
29. 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, 613-621.
30. Kates, W.R., Mostofsky, S.H., Zimmerman, A.W., Mazzocco, M.M., Landa, R., et al. (1998). Neuroanatomical and neurocognitive differences in a pair of monozygous twins discordant for strictly defined autism. Annals of Neurology, 43, 782-791.
31. Keisler, A., & Shadmehr, R. (2010). A shared resource between declarative memory and motor memory. Journal of Neuroscience, 30, 14817-14823.
32. Klin, A., Jones, W., Schultz, R., & Volkmar, F. (2003). The enactive mind, or from actions to cognition: Lessons from autism. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358, 345-360.
33. Kording, K.P., Tenenbaum, J.B., & Shadmehr, R. (2007). The dynamics of memory as a consequence of optimal adaptation to a changing body. Nature Neuroscience, 10, 779-786.
34. Krakauer, J.W., Mazzoni, P., Ghazizadeh, A., Ravindran, R., & Shadmehr, R. (2006). Generalization of motor learning depends on the history of prior action. PLoS Biology, 4, e316.
35. Lang, C.E., & Bastian, A.J. (1999). Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. Journal of Neurophysiology, 82, 2108-2119.
36. Leth-Steensen, C., Elbaz, Z.K., & Douglas, V.I. (2000). Mean response times, variability, and skew in the responding of ADHD children: A response time distributional approach. Acta Psychologica, 104, 167-190.
37. Lord, C., Risi, S., Lambrecht, L., Cook, E.H. Jr, Leventhal, B.L., et al. (2000). The autism diagnostic observation schedulegeneric: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205-223.
38. Lord, C., Rutter, M., DiLavore, P., & Risi, S. (1999). Autism diagnostic observation scale-WPS edition. Los Angeles, CA: Western Psychological Services.
39. 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, 659-685.
40. Macneil, L.K., Xavier, P., Garvey, M.A., Gilbert, D.L., Ranta, M.E., et al. (2011). Quantifying excessive mirror overflow in children with attention-deficit/hyperactivity disorder. Neurology, 76, 622-628.
41. Malfait, N., Gribble, P.L., & Ostry, D.J. (2005). Generalization of motor learning based on multiple field exposures and local adaptation. Journal of Neurophysiology, 93, 3327-3338.
42. Malfait, N., Shiller, D.M., & Ostry, D.J. (2002). Transfer of motor learning across arm configurations. Journal of Neuroscience, 22, 9656-9660.
43. Mattar, A.A., & Gribble, P.L. (2005). Motor learning by observing. Neuron, 46, 153-160.
44. Mattar, A.A., & Ostry, D.J. (2010). Generalization of dynamics learning across changes in movement amplitude. Journal of Neurophysiology, 104, 426-438.
45. Miall, R.C. (2003). Connecting mirror neurons and forward models. Neuroreport, 14, 2135-2137.
46. Mostofsky, S.H., Burgess, M.P., & Gidley Larson, J.C. (2007). Increased motor cortex white matter volume predicts motor impairment in autism. Brain, 130, 2117-2122.
47. 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, 314-326.
48. Mostofsky, S.H., Newschaffer, C.J., & Denckla, M.B. (2003). Overflow movements predict impaired response inhibition in children with ADHD. Perceptual and Motor Skills, 97, 1315- 1331.
49. Mottron, L. (2004). Matching strategies in cognitive research with individuals with high-functioning autism: Current practices, instrument biases, and recommendations. Journal of Autism and Developmental Disorders, 34, 19-27.
50. Ochipa, C., Rapcsak, S.Z., Maher, L.M., Rothi, L.J., Bowers, D., & Heilman, K.M. (1997). Selective deficit of praxis imagery in ideomotor apraxia. Neurology, 49, 474-480.
51. Poggio, T., & Bizzi, E. (2004). Generalization in vision and motor control. Nature, 431, 768-774.
52. Ratcliff, R. (1993). Methods for dealing with reaction time outliers. Psychological Bulletin, 114, 510-532.
53. Reich, W. (2000). Diagnostic interview for children and adolescents (DICA). Journal of the American Academy of Child and Adolescent Psychiatry, 39, 59-66.
54. Reich, W., Welner, Z., & Herjanic, B. (1997). The diagnostic interview for children and adolescents-IV. North Tonawanda: Multi-Health Systems.
55. Rizzolatti, G., Fogassi, L., & Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews. Neuroscience, 2, 661-670.
56. Rizzolatti, G., Fogassi, L., & Gallese, V. (2002). Motor and cognitive functions of the ventral premotor cortex. Current Opinion in Neurobiology, 12, 149-154.
57. Rogers, S.J., Bennetto, L., McEvoy, R., & Pennington, B.F. (1996). Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Development, 67, 2060-2073.
58. Scheidt, R.A., Reinkensmeyer, D.J., Conditt, M.A., Rymer, W.Z., & Mussa-Ivaldi, F.A. (2000). Persistence of motor adaptation during constrained, multi-joint, arm movements. Journal of Neurophysiology, 84, 853-862.
59. Shadmehr, R. (2004). Generalization as a behavioral window to the neural mechanisms of learning internal models. Human Movement Science, 23, 543-568.
60. Shadmehr, R., & Krakauer, J.W. (2008). A computational neuroanatomy for motor control. Experimental Brain Research, 185, 359-381.
61. Shadmehr, R., & Moussavi, Z.M. (2000). Spatial generalization from learning dynamics of reaching movements. Journal of Neuroscience, 20, 7807-7815.
62. Smith, M.A., Ghazizadeh, A., & Shadmehr, R. (2006). Interacting adaptive processes with different timescales underlie shortterm motor learning. PLoS Biology, 4, e179.
63. Synofzik, M., Lindner, A., & Thier, P. (2008). The cerebellum updates predictions about the visual consequences of one's behavior. Current Biology, 18, 814-818.
64. Tanaka, H., Sejnowski, T.J., & Krakauer, J.W. (2009). Adaptation to visuomotor rotation through interaction between posterior parietal and motor cortical areas. Journal of Neurophysiology, 102, 2921-2932.
65. Thoroughman, K.A., & Shadmehr, R. (2000). Learning of action through adaptive combination of motor primitives. Nature, 407, 742-747.
66. Vaurio, R.G., Simmonds, D.J., & Mostofsky, S.H. (2009). Increased intra-individual reaction time variability in attention-deficit/hyperactivity disorder across response inhibition tasks with different cognitive demands. Neuropsychologia, 47, 2389-2396.
67. Wechsler, D. (2003). Wechsler intelligence scale for childrenfourth edition. San Antonio, TX: Psychological Corporation.