Disruption of functional organization within the primary motor cortex in children with autism

Human Brain Mapping

Volumn 35, Issue 2, 2014, Pages 567-580

  Nebel, Mary Beth ^a,b   Joel, Suresh E ^a,b   Muschelli, John ^a,c   Barber, Anita D ^a,b   Caffo, Brian S ^c   Pekar, James J ^a,b   Mostofsky, Stewart H ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

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

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Autistic disorder; Clustering; Functional connectivity; Motor cortex; Resting state

Indexed keywords

ADULT; ARTICLE; AUTISM; BRAIN FUNCTION; BRAIN FUNCTIONAL CONNECTIVITY; BRAIN MAPPING; BRAIN REGION; CHILD; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL MORPHOLOGY; HUMAN; MALE; MOTOR CONTROL; MOTOR DYSFUNCTION; NERVE CELL NETWORK; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; SCHOOL CHILD;

AUTISTIC DISORDER; CLUSTERING; FUNCTIONAL CONNECTIVITY; MOTOR CORTEX; RESTING STATE;

ADULT; AUTISTIC DISORDER; BRAIN MAPPING; CHILD; DEVELOPMENTAL DISABILITIES; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR CORTEX; OXYGEN; YOUNG ADULT;

EID: 84892470282     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22188     Document Type: Article

References (90)

1. Alkadhi H, Crelier GR, Boendermaker SH, Golay X, Hepp-Reymond MC, Kollias SS (2002): Reproducibility of primary motor cortex somatotopy under controlled conditions. AJNR Am J Neuroradiol 23:1524-1532.
2. American Psychiatric Association (1994): Diagnostic and Statistical Manual of Mental Disorders, 4th ed. Washington, DC: American Psychiatric Association.
3. Barber AD, Srinivasan P, Joel SE, Caffo BS, Pekar JJ, Mostofsky SH (2012): Motor "dexterity"?: Evidence that left hemisphere lateralization of motor circuit connectivity is associated with better motor performance in children. Cereb Cortex 22:51-59.
4. Barnes KA, Cohen AL, Power JD, Nelson SM, Dosenbach YB, Miezin FM, Petersen SE, Schlaggar BL (2010): Identifying basal ganglia divisions in individuals using resting-state functional connectivity MRI. Front Syst Neurosci 4:18.
5. Barnes KA, Nelson SM, Cohen AL, Power JD, Coalson RS, Miezin FM, Vogel AC, Dubis JW, Church JA, Petersen SE, Schlagger BL (2012): Parcellation in left lateral parietal cortex is similar in adults and children. Cereb Cortex 22:1148-1158.
6. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005): Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001-1013.
7. Behzadi Y, Restom K, Liau J, Liu TT (2007): A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90-101.
8. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ (2004): Autism and abnormal development of brain connectivity. J Neurosci 24:9228-9231.
9. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995): Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
10. Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002): Minicolumnar pathology in autism. Neurology 58:428-432.
11. Casanova MF, van Kooten IA, Switala AE, van Engeland H, Heinsen H, Steinbusch HW, Hof PR, Trippe J, Stone J, Schmitz C (2006): Minicolumnar abnormalities in autism. Acta Neuropathol 112:287-303.
12. Casanova MF, El-Baz A, Mott M, Mannheim G, Hassan H, Fahmi R, Giedd J, Rumsey JM, Switala AE, Farag A (2009): Reduced gyral window and corpus callosum size in autism: Possible macroscopic correlates of a minicolumnopathy. J Autism Dev Disord 39:751-764.
13. Cheney PD, Fetz EE (1985): Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: Evidence for functional groups of CM cells. J Neurophysiol 53:786-804.
14. Cohen AL, Fair DA, Dosenbach NU, Miezin FM, Dierker D, Van Essen DC, Schlaggar BL, Petersen SE (2008): Defining functional areas in individual human brains using resting functional connectivity MRI. Neuroimage 41:45-57.
15. Cole LL (2008): Autism in school-age chidren. A complex collage of development, behavior and communication. Adv Nurse Pract 16:38-47; quiz 47-48.
16. Courchesne E (2004): Brain development in autism: Early overgrowth followed by premature arrest of growth. Ment Retard Dev Disabil Res Rev 10:106-111.
17. Craddock RC, James GA, Holtzheimer PEIII, Hu XP, Mayberg HS (2012): A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum Brain Mapp 33:1914-1928.
18. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006): Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848-13853.
19. De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM (2006): fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29:1359-1367.
20. Dice L (1945): Measures of the amount of ecologic association between species. Ecology 26:297-302.
21. Doron KW, Gazzaniga MS (2008): Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 44:1023-1029.
22. Dowell LR, Mahone EM, Mostofsky SH (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.
23. Dubois J, Hertz-Pannier L, Cachia A, Mangin JF, Le Bihan D, Dehaene-Lambertz G (2009): Structural asymmetries in the infant language and sensori-motor networks. Cereb Cortex 19:414-423.
24. Dziuk MA, Gidley Larson JC, Apostu A, Mahone EM, Denckla MB, Mostofsky SH (2007): Dyspraxia in autism: Association with motor, social, and communicative deficits. Dev Med Child Neurol 49:734-739.
25. Esposito G, Venuti P (2008): Analysis of toddlers' gait after six months of independent walking to identify autism: A preliminary study. Percept Mot Skills 106:259-269.
26. Fair DA, Dosenbach NU, Church JA, Cohen AL, Brahmbhatt S, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2007): Development of distinct control networks through segregation and integration. Proc Natl Acad Sci USA 104:13507-13512.
27. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, Schlaggar BL, Petersen SE (2009): Functional brain networks develop from a "local to distributed" organization. PLoS Comput Biol 5:e1000381.
28. Fournier KA, Kimberg CI, Radonovich KJ, Tillman MD, Chow JW, Lewis MH, Bodfish JW, Hass CJ (2010): Decreased static and dynamic postural control in children with autism spectrum disorders. Gait Posture 32:6-9.
29. Fuentes CT, Mostofsky SH, Bastian AJ (2009): Children with autism show specific handwriting impairments. Neurology 73:1532-1537.
30. Garvey MA, Barker CA, Bartko JJ, Denckla MB, Wassermann EM, Castellanos FX, Dell ML, Ziemann U (2005): The ipsilateral silent period in boys with attention-deficit/hyperactivity disorder. Clin Neurophysiol 116:1889-1896.
31. Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, Klingberg T, Larsson J, Zilles K, Roland PE (1996): Two different areas within the primary motor cortex of man. Nature 382:805-807.
32. Gidley-Larson JC, Mostofsky SH (2006): Motor deficits in autism. In: Tuchman R, Rapin I, editors. Autism: A Neurobiological Disorder of Early Brain Development. International review of child neurology series. London: MacKeith Press: 231-247.
33. Grabski K, Lamalle L, Vilain C, Schwartz JL, Vallee N, Tropres I, Baciu M, Le Bas JF, Sato M (2011): Functional MRI assessment of orofacial articulators: Neural correlates of lip, jaw, larynx, and tongue movements. Hum Brain Mapp 33:2306-2321.
34. Grafton ST, Woods RP, Mazziotta JC, Phelps ME (1991): Somatotopic mapping of the primary motor cortex in humans: Activation studies with cerebral blood flow and positron emission tomography. J Neurophysiol 66:735-743.
35. Haswell CC, Izawa J, Dowell LR, Mostofsky SH, Shadmehr R (2009): Representation of internal models of action in the autistic brain. Nat Neurosci 12:970-972.
36. Herbert MR, Ziegler DA, Makris N, Filipek PA, Kemper TL, Normandin JJ, Sanders HA, Kennedy DN, Caviness VSJr (2004): Localization of white matter volume increase in autism and developmental language disorder. Ann Neurol 55:530-540.
37. Houzel JC, Milleret C (1999): Visual inter-hemispheric processing: Constraints and potentialities set by axonal morphology. J Physiol 93:271-284.
38. Hughes C (1996): Brief report: Planning problems in autism at the level of motor control. J Autism Dev Disord 26:99-107.
39. Iverson JM, Fagan MK (2004): Infant vocal-motor coordination: Precursor to the gesture-speech system? Child Dev 75:1053-1066.
40. Jansiewicz EM, Goldberg MC, Newschaffer CJ, Denckla MB, Landa R, Mostofsky SH (2006): Motor signs distinguish children with high functioning autism and Asperger's syndrome from controls. J Autism Dev Disord 36:613-621.
41. Jones V, Prior M (1985): Motor imitation abilities and neurological signs in autistic children. J Autism Dev Disord 15:37-46.
42. Kawashima R, Itoh H, Ono S, Satoh K, Furumoto S, Gotoh R, Koyama M, Yoshioka S, Takahashi T, Yanagisawa T (1995): Activity in the human primary motor cortex related to arm and finger movements. Neuroreport 6:238-240.
43. Kelly C, Uddin LQ, Shehzad Z, Margulies DS, Castellanos FX, Milham MP, Petrides M (2010): Broca's region: Linking human brain functional connectivity data and non-human primate tracing anatomy studies. Eur J Neurosci 32:383-398.
44. Kelly C, Toro R, Di Martino A, Cox CL, Bellec P, Castellanos FX, Milham MP (2012): A convergent functional architecture of the insula emerges across imaging modalities. Neuroimage 61:1129-1142.
45. Kim JH, Lee JM, Jo HJ, Kim SH, Lee JH, Kim ST, Seo SW, Cox RW, Na DL, Kim SI, Saad ZS (2010): Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity-based parcellation method. Neuroimage 49:2375-2386.
46. Landa R, Garrett-Mayer E (2006): Development in infants with autism spectrum disorders: A prospective study. J Child Psychol Psychiatry 47:629-638.
47. Landman BA, Huang AJ, Gifford A, Vikram DS, Lim IA, Farrell JA, Bogovic JA, Hua J, Chen M, Jarso S, Smith SA, Joel SE, Mori S, Pekar JJ, Barker PB, Prince JL, van Zijl PC (2011): Multi-parametric neuroimaging reproducibility: A 3-T resource study. Neuroimage 54:2854-2866.
48. Libertus K, Needham A (2011): Reaching experience increases face preference in 3-month-old infants. Dev Sci 14:1355-1364.
49. 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. J Autism Dev Disord 24:659-685.
50. Lord C, Risi S, Lambrecht L, Cook EHJr, Leventhal BL, DiLavore PC, Pickles A, Rutter M (2000): The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30:205-223.
51. Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE (2006): Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis. Neuroimage 31:1453-1474.
52. McKiernan BJ, Marcario JK, Karrer JH, Cheney PD (2000): Correlations between corticomotoneuronal (CM) cell postspike effects and cell-target muscle covariation. J Neurophysiol 83:99-115.
53. Meier JD, Aflalo TN, Kastner S, Graziano MS (2008): Complex organization of human primary motor cortex: A high-resolution fMRI study. J Neurophysiol 100:1800-1812.
54. Meister IG, Foltys H, Gallea C, Hallett M (2010): How the brain handles temporally uncoupled bimanual movements. Cereb Cortex 20:2996-3004.
55. Minshew NJ, Sung K, Jones BL, Furman JM (2004): Underdevelopment of the postural control system in autism. Neurology 63:2056-2061.
56. Mostofsky SH, Goldberg MC, Landa RJ, Denckla MB (2000): Evidence for a deficit in procedural learning in children and adolescents with autism: Implications for cerebellar contribution. J Int Neuropsychol Soc 6:752-759.
57. Mostofsky SH, Dubey P, Jerath VK, Jansiewicz EM, Goldberg MC, Denckla MB (2006): Developmental dyspraxia is not limited to imitation in children with autism spectrum disorders. J Int Neuropsychol Soc 12:314-326.
58. Mostofsky SH, Burgess MP, Gidley Larson JC (2007): Increased motor cortex white matter volume predicts motor impairment in autism. Brain 130 (Part 8):2117-2122.
59. Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, Pekar JJ (2009): Decreased connectivity and cerebellar activity in autism during motor task performance. Brain 132 (Part 9):2413-2425.
60. Mottron L (2004): Matching strategies in cognitive research with individuals with high-functioning autism: Current practices, instrument biases, and recommendations. J Autism Dev Disord 34:19-27.
61. Muller RA, Cauich C, Rubio MA, Mizuno A, Courchesne E (2004): Abnormal activity patterns in premotor cortex during sequence learning in autistic patients. Biol Psychiatry 56:323-332.
62. Nelson SM, Cohen AL, Power JD, Wig GS, Miezin FM, Wheeler ME, Velanova K, Donaldson DI, Phillips JS, Schlaggar BL, Petersen SE (2010): A parcellation scheme for human left lateral parietal cortex. Neuron 67:156-170.
63. Newton JM, Dong Y, Hidler J, Plummer-D'Amato P, Marehbian J, Albistegui-Dubois RM, Woods RP, Dobkin BH (2008): Reliable assessment of lower limb motor representations with fMRI: Use of a novel MR compatible device for real-time monitoring of ankle, knee and hip torques. Neuroimage 43:136-146.
64. Noterdaeme M, Mildenberger K, Minow F, Amorosa H (2002): Evaluation of neuromotor deficits in children with autism and children with a specific speech and language disorder. Eur Child Adolesc Psychiatry 11:219-225.
65. Oberman LM, Hubbard EM, McCleery JP, Altschuler EL, Ramachandran VS, Pineda JA (2005): EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Brain Res Cogn Brain Res 24:190-198.
66. Oishi K, Faria A, Jiang H, Li X, Akhter K, Zhang J, Hsu JT, Miller MI, van Zijl PC, Albert M, Lyketsos CG, Woods R, Toga AW, Pike GB, Rosa-Neto P, Evans A, Mazziotta J, Mori S (2009): Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: Application to normal elderly and Alzheimer's disease participants. Neuroimage 46:486-499.
67. Oldfield RC (1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9:97-113.
68. Penfield W, Boldrey E (1937): Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389-443.
69. Penfield W, Rasmussen TB (1950): The Cerebral Cortex of Man: A Clinical Study of Localization of Function. New York: Macmillan.
70. Plow EB, Arora P, Pline MA, Binenstock MT, Carey JR (2010): Within-limb somatotopy in primary motor cortex-Revealed using fMRI. Cortex 46:310-321.
71. Rasmussen TB (1977): Wilder Penfield: His legacy to neurology. Surgical treatment of epilepsy. Can Med Assoc J 116:1369-1370.
72. Rathelot JA, Strick PL (2009): Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci USA 106:918-923.
73. Rinehart NJ, Bradshaw JL, Brereton AV, Tonge BJ (2001): Movement preparation in high-functioning autism and Asperger disorder: A serial choice reaction time task involving motor reprogramming. J Autism Dev Disord 31:79-88.
74. Rogers SJ, Bennetto L, McEvoy R, Pennington BF (1996): Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Dev 67:2060-2073.
75. Schmahmann JD, Pandya DN (2007): The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16:362-377.
76. Schroeder CE, Lakatos P (2009): The gamma oscillation: Master or slave? Brain Topogr 22:24-26.
77. Strick PL, Preston JB (1982): Two representations of the hand in area 4 of a primate. I. motor output organization. J Neurophysiol 48:139-149.
78. Sutera S, Pandey J, Esser EL, Rosenthal MA, Wilson LB, Barton M, Green J, Hodgson S, Robins DL, Dumont-Mathieu T, Fein D (2007): Predictors of optimal outcome in toddlers diagnosed with autism spectrum disorders. J Autism Dev Disord 37:98-107.
79. Teitelbaum P, Teitelbaum O, Nye J, Fryman J, Maurer RG (1998): Movement analysis in infancy may be useful for early diagnosis of autism. Proc Natl Acad Sci USA 95:13982-13987.
80. Teitelbaum O, Benton T, Shah PK, Prince A, Kelly JL, Teitelbaum P (2004): Eshkol-Wachman movement notation in diagnosis: The early detection of Asperger's syndrome. Proc Natl Acad Sci USA 101:11909-11914.
81. Ullman MT (2004): Contributions of memory circuits to language: The declarative/procedural model. Cognition 92:231-270.
82. van den Heuvel MP, Hulshoff Pol HE (2010): Specific somatotopic organization of functional connections of the primary motor network during resting state. Hum Brain Mapp 31:631-644.
83. van den Heuvel M, Mandl R, Hulshoff Pol H (2008): Normalized cut group clustering of resting-state FMRI data. PLoS One 3:e2001.
84. Wahl M, Lauterbach-Soon B, Hattingen E, Jung P, Singer O, Volz S, Klein JC, Steinmetz H, Ziemann U (2007): Human motor corpus callosum: Topography, somatotopy, and link between microstructure and function. J Neurosci 27:12132-12138.
85. Wechsler D (2003): Wechsler Intelligence Scale for Children, 4th ed. San Antonio, TX: The Psychological Corporation.
86. Welner Z, Reich W, Herjanic B, Jung KG, Amado H (1987): Reliability, validity, and parent-child agreement studies of the diagnostic interview for children and adolescents (DICA). J Am Acad Child Adolesc Psychiatry 26:649-653.
87. Williams JH, Whiten A, Suddendorf T, Perrett DI (2001): Imitation, mirror neurons and autism. Neurosci Biobehav Rev 25:287-295.
88. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997): Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120 (Part 1):141-157.
89. Zelnik-Manor L, Perona P (2004): Self-tuning spectral clustering. In: Saul L, Weiss Y, Bottou L, editors. Advances in Neural Information Processing Systems, 17th ed. Cambridge, MA: MIT Press. pp1601-1608.
90. Zwaigenbaum L, Bryson S, Lord C, Rogers S, Carter A, Carver L, Chawarska K, Constantino J, Dawson G, Dobkins K, Fein D, Iverson J, Klin A, Landa R, Messinger D, Ozonoff S, Sigman M, Stone W, Tager-Flusberg H, Yirmiya N (2009): Clinical assessment and management of toddlers with suspected autism spectrum disorder: Insights from studies of high-risk infants. Pediatrics 123:1383-1391.