Individuals with autism spectrum disorder show abnormalities during initial and subsequent phases of precision gripping

Journal of Neurophysiology

Volumn 113, Issue 7, 2015, Pages 1989-2001

  Wang, Zheng ^a   Magnon, Grant C ^a   White, Stormi P ^a   Greene, Rachel K ^a   Vaillancourt, David E ^b,c   Mosconi, Matthew W ^a,d  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c University of Florida   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Autism spectrum disorder; Cerebellum; Feedback motor control; Feedforward motor control; Precision grip; Visuomotor deficit

Indexed keywords

ADOLESCENT; ARTICLE; AUTISM; CHILD; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROL STRATEGY; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; GRIP STRENGTH; HUMAN; INDEX FINGER; LOCOMOTION; MALE; MOTOR ACTIVITY; MOTOR CONTROL; MOTOR DYSFUNCTION; MUSCLE RELAXATION; NEUROFEEDBACK; PRECISION GRIP; PRIORITY JOURNAL; SCHOOL CHILD; TASK PERFORMANCE; THUMB; VISUAL FEEDBACK; VISUOMOTOR COORDINATION; AUTISM SPECTRUM DISORDER; HAND STRENGTH; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PRESCHOOL CHILD; PROCEDURES; PSYCHOMOTOR PERFORMANCE; TIME FACTOR;

ADOLESCENT; AUTISM SPECTRUM DISORDER; CHILD; CHILD, PRESCHOOL; FEMALE; HAND STRENGTH; HUMANS; MALE; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; TIME FACTORS;

EID: 84926343332     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00661.2014     Document Type: Article

References (79)

1. Allen G, Courchesne E. Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: an fMRI study of autism. Am J Psychiatry 160: 262–273, 2003.
2. Bailey A, Luthert P, Dean A, Harding B, Janota I, Montgomery M, Rutter M, Lantos P. A clinicopathological study of autism. Brain 121: 889–905, 1998.
3. Baranek GT. Autism during infancy: a retrospective video analysis of sensory- motor and social behaviors at 9–12 months of age. J Autism Dev Disord 29: 213–224, 1999.
4. Bastian AJ. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16: 645–649, 2006.
5. Bauman ML, Kemper TL. Neuroanatomic observations of the brain in autism: a review and future directions. Int J Dev Neurosci 23: 183–187, 2005.
6. Berument SK, Rutter M, Lord C, Pickles A, Bailey A. Autism screening questionnaire: diagnostic validity. Br J Psychiatry 175: 444–451, 1999.
7. Bryson SE, Zwaigenbaum L, Brian J, Roberts W, Szatmari P, Rombough V, McDermott C. A prospective case series of high-risk infants who developed autism. J Autism Dev Disord 37: 12–24, 2007.
8. Carper RA, Courchesne E. Localized enlargement of the frontal cortex in early autism. Biol Psychiatry 57: 126–133, 2005.
9. Catani M, Jones DK, Daly E, Embiricos N, Deeley Q, Pugliese L, Curran S, Robertson D, Murphy DG. Altered cerebellar feedback projections in Asperger syndrome. Neuroimage 41: 1184–1191, 2008.
10. Cook JL, Blakemore SJ, Press C. Atypical basic movement kinematics in autism spectrum conditions. Brain 136: 2816–2824, 2013.
11. Coombes SA, Corcos DM, Sprute L, Vaillancourt DE. Selective regions of the visuomotor system are related to gain-induced changes in force error. J Neurophysiol 103: 2114–2123, 2010.
12. Courchesne E, Yeung-Courchesne R, Press GA, Hesselink JR, Jernigan TL. Hypoplasia of cerebellar vermal lobules VI and VII in autism. N Engl J Med 318: 1349–1354, 1988.
13. David FJ, Baranek GT, Giuliani CA, Mercer VS, Poe MD, Thorpe DE. A pilot study: coordination of precision grip in children and adolescents with high functioning autism. Pediatr Phys Ther 21: 205–211, 2009.
14. David FJ, Baranek GT, Wiesen C, Miao AF, Thorpe DE. Coordination of precision grip in 2–6 years-old children with autism spectrum disorders compared to children developing typically and children with developmental disabilities. Front Integr Neurosci 6: 122, 2012.
15. Day BL, Thompson PD, Harding AE, Marsden CD. Influence of vision on upper limb reaching movements in patients with cerebellar ataxia. Brain 121: 357–372, 1998.
16. Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST. Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2: 563–567, 1999.
17. Deutsch KM, Newell KM. Age differences in noise and variability of isometric force production. J Exp Child Psychol 80: 392–408, 2001.
18. Deutsch KM, Newell KM. Deterministic and stochastic processes in children’s isometric force variability. Dev Psychobiol 43: 335–345, 2003.
19. Dziuk MA, Gidley Larson JC, Apostu A, Mahone EM, Denckla MB, Mostofsky SH. Dyspraxia in autism: association with motor, social and communicative deficits. Dev Med Child Neurol 49: 734–739, 2007.
20. Eidenmüller S, Randerath J, Goldenberg G, Li Y, Hermsdorfer J. The impact of unilateral brain damage on anticipatory grip force scaling when lifting everyday objects. Neuropsychologia 61: 222–234, 2014.
21. Fellows SJ, Ernst J, Schwarz M, Töpper R, Noth J. Precision grip deficits in cerebellar disorders in man. Clin Neurophysiol 112: 1793–1802, 2001.
22. Fishbach A, Roy SA, Bastianen C, Miller LE, Houk JC. Kinematic properties of on-line error corrections in the monkey. Exp Brain Res 164: 442–457, 2005.
23. Fournier KA, Hass CJ, Naik SK, Lodha N, Cauraugh JH. Motor coordination in autism spectrum disorders: a synthesis and meta-analysis. J Autism Dev Disord 40: 1227–1240, 2010a.
24. Fournier KA, Kimberg CI, Radonovich KJ, Tillman MD, Chow JW, Lewis MH, Bodfish JW, Hass CJ. Decreased static and dynamic postural control in children with autism spectrum disorders. Gait Posture 32: 6–9, 2010b.
25. Fuentes CT, Mostofsky SH, Bastian AJ. Children with autism show specific handwriting impairments. Neurology 73: 1532–1537, 2009.
26. Gallese V, Rochat MJ, Berchio C. The mirror mechanism and its potential role in autism spectrum disorder. Dev Med Child Neurol 55: 15–22, 2013.
27. Gepner B, Mestre DR. Brief report: postural reactivity to fast visual motion differentiates autistic from children with Asperger syndrome. J Autism Dev Disord 32: 231–238, 2002.
28. Glazebrook CM, Elliott D, Szatmari P. How do individuals with autism plan their movements? J Autism Dev Disord 38: 114–126, 2007.
29. Glazebrook CM, Gonzalez D, Hansen S, Elliott D. The role of vision for online control of manual aiming movements in persons with autism spectrum disorders. Autism 13: 411–433, 2009.
30. Gordon AM, Duff SV. Fingertip forces during object manipulation in children with hemiplegic cerebral palsy. I. Anticipatory scaling. Dev Med Child Neurol 41: 166–175, 1999.
31. Grafton ST, Tunik E. Human basal ganglia and the dynamic control of force during online corrections. J Neurosci 31: 1600–1605, 2011.
32. Groen WB, Buitelaar JK, van der Gaag RJ, Zwiers MP. Pervasive microstructural abnormalities in autism: a DTI study. J Psychiatry Neurosci 6: 32–40, 2011.
33. Hallett M, Lebiedowska MK, Thomas SL, Stanhope SJ, Benckla MB, Rumsey J. Locomotion of autistic adults. Arch Neurol 50: 1304–1308, 1993.
34. Hardan AY, Kilpatrick M, Keshavan MS, Minshew NJ. Motor performance and anatomic magnetic resonance imaging (MRI) of the basal ganglia in autism. J Child Neurol 18: 317–324, 2003.
35. Haswell CC, Izawa J, Dowell LR, Mostofsky SH, Shadmehr R. Representation of internal models of action in the autistic brain. Nat Neurosci 12: 970–972, 2009.
36. Hermsdörfer J, Hagl E, Nowak DA. Deficits of anticipatory grip force control after damage to peripheral and central sensorimotor systems. Hum Mov Sci 23: 643–662, 2004.
37. Hermsdörfer J, Hagl E, Nowak DA, Marquardt C. Grip force control during object manipulation in cerebral stroke. Clin Neurophysiol 114: 915–929, 2003.
38. Izawa J, Pekny SE, Marko MK, Haswell CC, Shadmehr R, Mostofsky SH. Motor learning relies on integrated sensory inputs in ADHD, but overselectively on proprioception in autism spectrum conditions. Autism Res 5: 124–136, 2012.
39. Johnson BP, Rinehart NJ, White O, Millist L, Fielding J. Saccade adaptation in autism and Asperger’s disorder. Neuroscience 243: 76–87, 2013.
40. Kawato M. Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9: 718–727, 1999.
41. Kern JK, Geier DA, Adams JB, Troutman MR, Davis G, King PG, Young JL, Geier MR. Autism severity and muscle strength: a correlation analysis. Res Autism Spectr Disord 5: 1011–1015, 2011.
42. LeBarton ES, Iverson JM. Fine motor skill predicts expressive language in infant siblings of children with autism. Dev Sci 16: 815–827, 2013.
43. Lord C, Rutter M, DiLavore PC, Risi S, Gotham K, Bishop SL. Autism Diagnostic Observation Schedule (2nd ed.) (ADOS-2). Torrance, CA: Western Psychological Services, 2012.
44. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24: 659–685, 1994.
45. Mai N, Bolsinger P, Avarello M, Diener HC, Dichgans J. Control of isometric finger force in patients with cerebellar disease. Brain 111: 973– 998, 1988.
46. Mari M, Castiello U, Marks D, Marraffa C, Prior M. The reach-to-grasp movement in children with autism spectrum disorder. Philos Trans R Soc Lond B Biol Sci 358: 393–403, 2003.
47. Miall RC. The cerebellum, predictive control and motor coordination. In: Sensory Guidance of Movement (1st ed.), edited by Glickstein M, Bock R. New York: Wiley, 1998, p. 272–290.
48. Minshew NJ, Sung K, Jones BL, Furman JM. Underdevelopment of the postural control system in autism. Neurology 63: 2056–2061, 2007.
49. Mosconi MW, Kay M, D’Cruz AM, Guter S, Kapur K, Macmillan C, Stanford LD, Sweeney JA. Neurobehavioral abnormalities in first-degree relatives of individuals with autism. Arch Gen Psychiatry 67: 830–841, 2010.
50. Mosconi MW, Luna B, Kay-Stacey M, Nowinski CV, Rubin LH, Scudder C, Minshew NJ, Sweeney JA. Saccade adaptation abnormalities implicate dysfunction of cerebellar-dependent learning mechanisms in autism spectrum disorders (ASD). PloS One 8: e63709, 2013.
51. Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, Pekar JJ. Decreased connectivity and cerebellar activity in autism during motor task performance. Brain 132: 2413–2425, 2009.
52. Müller F, Dichgans BJ. Dyscoordination of pinch and lift forces during grasping in patients with cerebellar lesions. Exp Brain Res 101: 485–492, 1994.
53. Neely KA, Planetta PJ, Prodoehl J, Corcos DM, Comella CL, Goetz CG, Shannon KL, Vaillancourt DE. Force control deficits in individuals with Parkinson’s disease, multiple systems atrophy, and progressive supranuclear palsy. PLoS One 8: e58403, 2013.
54. Novak KE, Miller LE, Houk JC. Kinematic properties of rapid hand movements in a knob turning task. Exp Brain Res 132: 419–433, 2000.
55. Nowak DA, Hermsdörfer J, Marquardt C, Fuchs HH. Grip and load force coupling during discrete vertical arm movements with a grasped object in cerebellar atrophy. Exp Brain Res 145: 28–39, 2002.
56. Nowak DA, Hemsdörfer J, Rost K, Timmann D, Topka H. Predictive and reactive finger force control during catching in cerebellar degeneration. Cerebellum 3: 227–235, 2004.
57. Potter NL, Kent RD, Lindstrom MJ, Lazarus JA. Power and precision grip force control in three-to-five-year-old children: velocity control precedes amplitude control in development. Exp Brain Res 172: 246–260, 2006.
58. Prablanc C, Martin O. Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67: 455–469, 1992.
59. Provost B, Lopez BR, Heimerl S. A comparison of motor delays in young children: autism spectrum disorder, developmental delay, and developmental concerns. J Autism Dev Disord 37: 321–328, 2006.
60. Quaney BM, Perera S, Maletsky R, Luchies CW, Nudo RJ. Impaired grip force modulation in the ipsilesional hand after unilateral middle cerebral artery stroke. Neurorehabil Neural Repair 19: 338–349, 2005.
61. Reilly JL, Lencer R, Bishop JR, Keedy S, Sweeney JA. Pharmacological treatment effects on eye movement control. Brain Cogn 68: 415–435, 2008.
62. Rutter M, DiLavore PC, Risi S, Gotham K, Bishop S. Autism Diagnostic Observation Schedule: ADOS-2. Torrance, CA: Western Psychological Services, 2012.
63. Schmitt LM, Cook EH, Sweeney JA, Mosconi MW. Saccadic eye movement abnormalities in autism spectrum disorder indicate dysfunctions in both cerebellum and brainstem. Mol Autism 5: 47, 2014.
64. Serrien JD, Wiesendanger M. Grip-load force coordination in cerebellar patients. Exp Brain Res 128: 76–80, 1999.
65. Shah A, Frith U. Why do autistic individuals show superior performance on the block design task? J Child Psychol Psychiatry 34: 1351–1364, 1993.
66. Spraker MB, Corcos DM, Kurani AS, Prodoehl J, Swinnen SP, Vaillancourt DE. Specific cerebellar regions are related to force amplitude and rate of force development. Neuroimage 59: 1647–1656, 2012.
67. Stanfield AC, McLntosh AM, Spencer MD, Philip R, Gaur S, Lawrie SM. Towards a neuroanatomy of autism: a systematic review and meta-analysis of structural magnetic resonance imaging studies. Eur Psychiatry 23: 289– 299, 2008.
68. Stein JF, Glickstein M. Role of the cerebellum in visual guidance of movement. Physiol Rev 72: 967–1017, 1992.
69. Stoodley C, Schmahmann J. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44: 489–501, 2009.
70. Sutera S, Pandey J, Esser EL, Rosenthal MA, Wilson LB, Barton M, Green J, Hodgson S, Robins DL, Dumont-Mathieu T. Predictors of optimal outcome in toddlers diagnosed with autism spectrum disorders. J Autism Dev Disord 37: 98–107, 2007.
71. Takarae Y, Minshew NJ, Luna B, Krisky CM, Sweene JA. Pursuit eye movement deficits in autism. Brain 127: 2584–2594, 2004.
72. Vaillancourt DE, Larsson L, Newell KM. Effects of aging on force variability, single motor unit discharge patterns, and the structure of 10, 20, and 40 Hz EMG activity. Neurobiol Aging 24: 25–35, 2003.
73. Vaillancourt DE, Mayka MA, Corcos DM. Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex. J Neurophysiol 95: 922–931, 2006.
74. Valvano J, Newell KM. Practice of a precision isometric grip-force task by children with spastic cerebral palsy. Dev Med Child Neurol 40: 464–473, 1998.
75. Vernazza-Martin S, Martin N, Vernazza A, Lepellec-Muller A, Rufo M, Massion J, Assaiante C. Goal directed locomotion and balance control in autistic children. J Autism Dev Disord 35: 91–102, 2005.
76. Vilis T, Hore J. Central neural mechanisms contributing to cerebellar tremor produced by limb perturbation. J Neurophysiol 43: 279–291, 1980.
77. Wang SS, Kloth AD, Badura A. The cerebellum, sensitive periods, and autism. Neuron 83: 518–532, 2014.
78. Whitney ER, Kemper TL, Bauman ML, Rosene DL, Blatt GJ. Cerebellar Purkinje cells are reduced in a subpopulation of autistic brains: a stereological experiment using calbindin-D28k. Cerebellum 7: 406–416, 2008.
79. Wisleder D, Dounskaia N. The role of different submovement types during pointing to a target. Exp Brain Res 176: 132–149, 2007.