Brain activation associated with motor skill practice in children with developmental coordination disorder: An fMRI study

International Journal of Developmental Neuroscience

Volumn 29, Issue 2, 2011, Pages 145-152

  Zwicker, Jill G ^a,c   Missiuna, Cheryl ^b   Harris, Susan R ^a   Boyd, Lara A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Developmental coordination disorder, DCD; FMRI; Motor skill acquisition

Indexed keywords

ACCURACY; ARTICLE; BEHAVIOR; BRAIN MAPPING; BRAIN REGION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL COORDINATION DISORDER; ELECTROENCEPHALOGRAM; FEMALE; FRONTAL GYRUS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; LINGUAL GYRUS; MALE; MOTOR PERFORMANCE; PARIETAL CORTEX; PRIORITY JOURNAL; SCHOOL CHILD;

BEHAVIOR; BRAIN; BRAIN MAPPING; CHILD; FEMALE; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MOTOR SKILLS; MOTOR SKILLS DISORDERS;

EID: 79951576231     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2010.12.002     Document Type: Article

References (73)

1. Allen G., McColl R., Barnard H., Ringe W.K., Fleckenstein J., Cullum C.M. Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. Neuroimage 2005, 28:39-48.
2. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2000, American Psychiatric Association, Washington, DC, Author. 4th edition - text revision ed.
3. Anguera J.A., Reuter-Lorenz P.A., Willingham D.T., Seidler R.D. Contributions of spatial working memory to visuomotor learning. Journal of Cognitive Neuroscience 2010, 22:1917-1930.
4. Boyd L.A., Vidoni E.D., Siengsukon C.F., Wessel B.D. Manipulating time-to-plan alters patterns of brain activation during the Fitts' task. Experimental Brain Research 2009, 194:527-539.
5. Boyd L.A., Winstein C.J. Cerebellar stroke impairs temporal but not spatial accuracy during implicit motor learning. Neurorehabilitation and Neural Repair 2004, 18:134-143.
6. Cantin N., Polatajko H.J., Thach W.T., Jaglal S. Developmental coordination disorder: exploration of a cerebellar hypothesis. Human Movement Science 2007, 26:491-509.
7. Clements-Stephens A.M., Rimrodt S.L., Cutting L.E. Developmental sex differences in basic visuospatial processing: differences in strategy use?. Neuroscience Letters 2009, 16:155-160.
8. Clower D.M., West R.A., Lynch J.C., Strick P.L. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. Journal of Neuroscience 2001, 21:6283-6291.
9. Cohen J. Statistical Power Analysis for the Behavioral Sciences 1988, Erlbaum, Hillsdale, NJ. 2nd ed.
10. Conners C.K. Conners' Rating Scales - Revised (CRS-R) Technical Manual 2001, Multi-Health Systems, Toronto, ON.
11. Courtney S.M., Petit L., Maisog J.M., Ungerleider L.G., Haxby J.V. An area specialized for spatial working memory in human frontal cortex. Science 1998, 279:1347-1351.
12. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, an International Journal 1996, 29:162-173.
13. Dewey D., Kaplan B.J., Crawford S.G., Wilson B.N. Developmental coordination disorder: associated problems in attention, learning, and psychosocial adjustment. Human Movement Science 2002, 21:905-918.
14. Dickstein S.G., Bannon K., Castellanos F.X., Milham M.P. The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. Journal of Child Psychology and Psychiatry, and Allied Disciplines 2006, 47:1051-1062.
15. Diedrichsen J., Hashambhoy Y., Rane T., Shadmehr R. Neural correlates of reach errors. Journal of Neuroscience 2005, 25:9919-9931.
16. Doyon J., Owen A.M., Petrides M., Sziklas V., Evans A.C. Functional anatomy of visuomotor skill learning in human subjects examined with positron emission tomography. European Journal of Neuroscience 1996, 8:637-648.
17. Doyon J., Penhune V., Ungerleider L.G. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 2003, 41:252-262.
18. Doyon J., Song A.W., Karni A., Lalonde F., Adams M.M., Ungerleider L.G. Experience-dependent changes in cerebellar contributions to motor sequence learning. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:1017-1022.
19. Estil L.B., Ingvaldsen R.P., Whiting H.T. Spatial and temporal constraints on performance in children with movement co-ordination problems. Experimental Brain Research 2002, 147:153-161.
20. Fassbender C., Murphy K., Foxe J.J., Wylie G.R., Javitt D.C., Robertson I.H., et al. A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. Brain Research. Cognitive Brain Research 2004, 20:132-143.
21. Fitts P.M. The information capacity of the human motor system in controlling the amplitude of movement. Journal of Experimental Psychology 1954, 47:381-391.
22. Geuze R.H. Postural control in children with developmental coordination disorder. Neural Plasticity 2005, 12:183-196.
23. Ghez C., Thach W. The cerebellum. Principles of Neural Science 2000, 832-852. McGraw-Hill, New York. 4th edition. E.R. Kandel, J.H. Schwartz, T.M. Jessel (Eds.).
24. Grafton S.T., Schmitt P., Van Horn J., Diedrichsen J. Neural substrates of visuomotor learning based on improved feedback control and prediction. Neuroimage 2008, 39:1383-1395.
25. Gramsbergen A. Clumsiness and disturbed cerebellar development: insights from animal experiments. Neural Plasticity 2003, 10:129-140.
26. Graydon F.X., Friston K.J., Thomas C.G., Brooks V.B., Menon R.S. Learning-related fMRI activation associated with a rotational visuo-motor transformation. Brain Research. Cognitive Brain Research 2005, 22:373-383.
27. Habas C., Kamdar N., Nguyen D., Prater K., Beckmann C.F., Menon V., et al. Distinct cerebellar contributions to intrinsic connectivity networks. Journal of Neuroscience 2009, 29:8586-8594.
28. Halsband U., Lange R.K. Motor learning in man: a review of functional and clinical studies. Journal of Physiology 2006, 99:414-424.
29. Henderson S.E., Sugden D.A. Movement Assessment Battery for Children 1992, Harcourt Assessment, London.
30. Henderson S.E., Sugden D.A. Movement Assessment Battery for Children (MABC-2) 2007, Harcourt Assessment, London. 2nd ed.
31. Hwang E.J., Shadmehr R. Internal models of limb dynamics and the encoding of limb state. Journal of Neural Engineering 2005, 2:S266-S278.
32. Ivry R.B. Cerebellar involvement in clumsiness and other developmental disorders. Neural Plasticity 2003, 10:141-153.
33. Jenkins I.H., Brooks D.J., Nixon P.D., Frackowiak R.S., Passingham R.E. Motor sequence learning: a study with positron emission tomography. Journal of Neuroscience 1994, 14:3775-3790.
34. Johnston L.M., Burns Y.R., Brauer S.G., Richardson C.A. Differences in postural control and movement performance during goal directed reaching in children with developmental coordination disorder. Human Movement Science 2002, 21:583-601.
35. Jueptner M., Frith C.D., Brooks D.J., Frackowiak R.S., Passingham R.E. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. Journal of Neurophysiology 1997, 77:1325-1337.
36. Jueptner M., Stephan K.M., Frith C.D., Brooks D.J., Frackowiak R.S., Passingham R.E. Anatomy of motor learning. I. Frontal cortex and attention to action. Journal of Neurophysiology 1997, 77(3):1313-1324.
37. Kagerer F.A., Bo J., Contreras-Vidal J.L., Clark J.E. Visuomotor adaptation in children with developmental coordination disorder. Motor Control 2004, 8:450-460.
38. Kagerer F.A., Contreras-Vidal J.L., Bo J., Clark J.E. Abrupt, but not gradual visuomotor distortion facilitates adaptation in children with developmental coordination disorder. Human Movement Science 2006, 25:622-633.
39. Kashiwagi M., Iwaki S., Narumi Y., Tamai H., Suzuki S. Parietal dysfunction in developmental coordination disorder: a functional MRI study. Neuroreport 2009, 20:1319-1324.
40. Kaufman A.S., Kaufman N.L. K-BIT-2: Kaufman Brief Intelligence Test 2004, NCS Pearson, Minneapolis, MN. 2nd ed.
41. Lang C.E., Bastian A.J. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. Journal of Neurophysiology 1999, 82:2108-2119.
42. Lundy-Ekman L., Ivry R., Keele S., Woollacott M. Timing and force control deficits in clumsy children. Journal of Cognitive Neuroscience 1991, 3:367-376.
43. Marchiori G.E., Wall A.E., Bedingfield E.W. Kinematic analysis of skill acquisition in physically awkward boys. Adapted Physical Activity Quarterly 1987, 4:305-315.
44. Miall R.C., Imamizu H., Miyauchi S. Activation of the cerebellum in co-ordinated eye and hand tracking movements: an fMRI study. Experimental Brain Research 2000, 135:22-33.
45. Miall R.C., Jenkinson E.W. Functional imaging of changes in cerebellar activity related to learning during a novel eye-hand tracking task. Experimental Brain Research 2005, 166:170-183.
46. Miall R.C., Reckess G.Z., Imamizu H. The cerebellum coordinates eye and hand tracking movements. Nature Neuroscience 2001, 4:638-644.
47. Milham M.P., Banich M.T., Claus E.D., Cohen N.J. Practice-related effects demonstrate complementary roles of anterior cingulate and prefrontal cortices in attentional control. Neuroimage 2003, 18:483-493.
48. Missiuna C., Moll S., Law M., King S., King G. Mysteries and mazes: parents' experiences of children with developmental coordination disorder. Canadian Journal of Occupational Therapy 2006, 73:7-17.
49. Orban P., Peigneux P., Lungu O., Albouy G., Breton E., Laberenne F., et al. The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 2010, 49:694-702.
50. Pascual-Leone A., Grafman J., Clark K., Stewart M., Massaquoi S., Lou J.S., et al. Procedural learning in Parkinson's disease and cerebellar degeneration. Annals of Neurology 1993, 34:594-602.
51. Pavlides C., Miyashita E., Asanuma H. Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. Journal of Neurophysiology 1993, 70:733-741.
52. Piek J.P., Skinner R.A. Timing and force control during a sequential tapping task in children with and without motor coordination problems. Journal of the International Neuropsychological Society 1999, 5:320-329.
53. Polatajko H.J., Cantin N. Developmental coordination disorder (dyspraxia): an overview of the state of the art. Seminars in Pediatric Neurology 2005, 12(4):250-258.
54. Querne L., Berquin P., Vernier-Hauvette M.P., Fall S., Deltour L., Meyer M.E., et al. Dysfunction of the attentional brain network in children with developmental coordination disorder: a fMRI study. Brain Research 2008, 1244:89-102.
55. Reuter-Lorenz P.A., Jonides J., Smith E.E., Hartley A., Miller A., Marshuetz C., et al. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. Journal of Cognitive Neuroscience 2000, 12:174-187.
56. Revie G., Larkin D. Task specific intervention for children with developmental coordination disorder: a systems view. Adapted Physical Activity Quarterly 1993, 10:29-41.
57. Sakai K., Hikosaka O., Miyauchi S., Takino R., Sasaki Y., Putz B. Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. Journal of Neuroscience 1998, 18:1827-1840.
58. Schmahmann J.D., Doyon J., McDonald D., Holmes C., Lavoie K., Hurwitz A.S., et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage 1999, 10:233-260.
59. Seidler R.D., Purushotham A., Kim S.G., Ugurbil K., Willingham D., Ashe J. Cerebellum activation associated with performance change but not motor learning. Science 2002, 296:2043-2046.
60. Silk T., Vance A., Rinehart N., Egan G., O'Boyle M., Bradshaw J.L., et al. Fronto-parietal activation in attention-deficit hyperactivity disorder, combined type: functional magnetic resonance imaging study. British Journal of Psychiatry: Journal of Mental Science 2005, 187:282-283.
61. Stoodley C.J., Schmahmann J.D. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 2009, 44:489-501.
62. Talairach J., Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain 1988, Thieme, New York, NY.
63. Thomas J.R., Salazar W., Landers D.M. What is missing in p less than .05? Effect size. Research Quarterly for Exercise and Sport 1991, 62:344-348.
64. Thoroughman K.A., Shadmehr R. Electromyographic correlates of learning an internal model of reaching movements. Journal of Neuroscience 1999, 19:8573-8588.
65. Toni I., Krams M., Turner R., Passingham R.E. The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 1998, 8:50-61.
66. Vidoni E.D., Acerra N.E., Dao E., Meehan S.K., Boyd L.A. Role of the primary somatosensory cortex in motor learning: an rTMS study. Neurobiology of Learning and Memory 2010, 93:532-539.
67. Vidoni E.D., Boyd L.A. Preserved motor learning after stroke is related to the degree of proprioceptive deficit. Behavioral and Brain Functions 2009, 5:36.
68. Williams J., Thomas P.R., Maruff P., Butson M., Wilson P.H. Motor, visual and egocentric transformations in children with developmental coordination disorder. Child: Care, Health and Development 2006, 32:633-647.
69. Wilson, B.N., Kaplan, B.J., Crawford, S.G., Roberts, G., 2007. Developmental coordination questionnaire 2007 (DCDQ'07). Available from: (accessed 6.03.07). http://www.dcdq.ca/.
70. Wilson P.H., Maruff P., Butson M., Williams J., Lum J., Thomas P.R. Internal representation of movement in children with developmental coordination disorder: a mental rotation task. Developmental Medicine and Child Neurology 2004, 46:754-759.
71. Wilson P.H., Maruff P., Ives S., Currie J. Abnormalities of motor and praxis imagery in children with DCD. Human Movement Science 2001, 20:135-159.
72. Zwicker J.G., Missiuna C., Boyd L.A. Neural correlates of developmental coordination disorder: a review of hypotheses. Journal of Child Neurology 2009, 24:1273-1281.
73. Zwicker J.G., Missiuna C., Harris S.R., Boyd L.A. Brain activation of children with developmental coordination disorder is different than peers. Pediatrics 2010, 126:e678-686.