Dynamic functional reorganization of the motor execution network after stroke

Brain

Volumn 133, Issue 4, 2010, Pages 1224-1238

  Wang, Liang ^a   Yu, Chunshui ^b,c   Chen, Hai ^c   Qin, Wen ^c   He, Yong ^a   Fan, Fengmei ^a   Zhang, Yujin ^a   Wang, Moli ^c   Li, Kuncheng ^c   Zang, Yufeng ^a   Woodward, Todd S ^d   Zhu, Chaozhe ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Connectivity; Functional magnetic resonance imaging; Network; Small world; Stroke

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN INFARCTION; BRAIN REGION; CEREBELLUM; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CLINICAL FEATURE; CONVALESCENCE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL STATUS; HUMAN; MALE; MOTOR PERFORMANCE; NEUROLOGIC EXAMINATION; PRIORITY JOURNAL; REST; STROKE;

ADULT; AGED; AGED, 80 AND OVER; FEMALE; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MOTOR CORTEX; MOTOR SKILLS; NERVE NET; NEURONAL PLASTICITY; STROKE; TIME FACTORS;

EID: 77950799117     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq043     Document Type: Article

References (103)

1. Achard S, Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol 2007; 3: e17. (Pubitemid 46318379)
2. Ago T, Kitazono T, Ooboshi H, Takada J, Yoshiura T, Mihara F, et al. Deterioration of pre-existing hemiparesis brought about by subsequent ipsilateral lacunar infarction. J Neurol Neurosurg Psychiatry 2003; 74: 1152-1153 (Pubitemid 36936405)
3. Allen G, Buxton RB, Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement. Science 1997; 275: 1940-1943 (Pubitemid 27148817)
4. Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O. Modeling the impact of lesions in the human brain. PLoS Comput Biol 2009; 5: e1000408.
5. Barrat A, Barthelemy M, Pastor-Satorras R, Vespignani A. The architecture of complex weighted networks. Proc Natl Acad Sci USA 2004; 101: 3747-3752 (Pubitemid 38381049)
6. Bartolomei F, Bosma I, Klein M, Baayen JC, Reijneveld JC, Postma TJ, et al. Disturbed functional connectivity in brain tumour patients: evaluation by graph analysis of synchronization matrices. Clin Neurophysiol 2006a; 117: 2039-2049 (Pubitemid 44262515)
7. Bartolomei F, Bosma I, Klein M, Baayen JC, Reijneveld JC, Postma TJ, et al. How do brain tumors alter functional connectivity? A magnetoencephalography study. Ann Neurol 2006b; 59: 128-138 (Pubitemid 43042879)
8. Bassett DS, Bullmore E. Small-world brain networks. Neuroscientist 2006; 12: 512-523 (Pubitemid 44657966)
9. Bassett DS, Bullmore ET. Human brain networks in health and disease. Curr Opin Neurol 2009; 22: 340-347
10. Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang DU. Complex networks: structure and dynamics. Phys Rep 2006; 424: 175-308. (Pubitemid 43135890)
11. Bracha V, Zhao L, Irwin KB, Bloedel JR. The human cerebellum and associative learning: dissociation between the acquisition, retention and extinction of conditioned eyeblinks. Brain Res 2000; 860: 87-94. (Pubitemid 30155840)
12. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009; 10: 186-198
13. Calautti C, Baron JC. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke 2003; 34: 1553-1566 (Pubitemid 36693533)
14. Calautti C, Leroy F, Guincestre JY, Baron JC. Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 2001; 32: 2534-2542 (Pubitemid 33055302)
15. Calautti C, Leroy F, Guincestre JY, Baron JC. Displacement of primary sensorimotor cortex activation after subcortical stroke: a longitudinal PET study with clinical correlation. Neuroimage 2003; 19: 1650-1654 (Pubitemid 37025861)
16. Calautti C, Naccarato M, Jones PS, Sharma N, Day DD, Carpenter AT, et al. The relationship between motor deficit and hemisphere activation balance after stroke: a 3T fMRI study. Neuroimage 2007; 34: 322-331 (Pubitemid 44773795)
17. Carmichael ST. Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 2006; 59: 735-742
18. Carmichael ST. Themes and strategies for studying the biology of stroke recovery in the poststroke epoch. Stroke 2008; 39: 1380-1388
19. Carmichael ST, Chesselet M-F. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J Neurosci 2002; 22: 6062-6070
20. Carmichael ST, Wei L, Rovainen CM, Woolsey TA. New patterns of intracortical projections after focal cortical stroke. Neurobiol Dis 2001; 8: 910-922 (Pubitemid 33055605)
21. Chollet F, DiPiero V, Wise RJ, Brooks DJ, Dolan RJ, Frackowiak RS. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 1991; 29: 63-71.
22. Church JA, Fair DA, Dosenbach NU, Cohen AL, Miezin FM, Petersen SE, et al. Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity. Brain 2009; 132: 225-238
23. Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV, et al. Extensive cortical rewiring after brain injury. J Neurosci 2005; 25: 10167-10179 (Pubitemid 41636213)
24. De Vico Fallani F, Astolfi L, Cincotti F, Mattia D, Marciani MG, Salinari S, et al. Cortical functional connectivity networks in normal and spinal cord injured patients: evaluation by graph analysis. Hum Brain Mapp 2007; 28: 1334-1346 (Pubitemid 350234185)
25. Delvaux V, Alagona G, Gerard P, De Pasqua V, Pennisi G, de Noordhout AM. Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation. Clin Neurophysiol 2003; 114: 1217-1225 (Pubitemid 36776819)
26. Dijkhuizen RM, Ren J, Mandeville JB, Wu O, Ozdag FM, Moskowitz MA, et al. Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc Natl Acad Sci USA 2001; 98: 12766-12771 (Pubitemid 33020019)
27. Dong Y, Winstein CJ, Albistegui-DuBois R, Dobkin BH. Evolution of FMRI activation in the perilesional primary motor cortex and cerebellum with rehabilitation training-related motor gains after stroke: a pilot study. Neurorehabil Neural Repair 2007; 21: 412-428 (Pubitemid 47246438)
28. Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, et al. Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 2007; 104: 11073-11078
29. Duncan PW, Min Lai S, Keighley J. Defining post-stroke recovery: implications for design and interpretation of drug trials. Neuropharmacology 2000; 39: 835-841 (Pubitemid 30103686)
30. Fair DA, Cohen AL, Dosenbach NU, Church JA, Miezin FM, Barch DM, et al. The maturing architecture of the brain's default network. Proc Natl Acad Sci USA 2008; 105: 4028-4032
31. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, et al. Functional brain networks develop from a "local to distributed" organization. PLoS Comput Biol 2009; 5: e1000381.
32. Feydy A, Carlier R, Roby-Brami A, Bussel B, Cazalis F, Pierot L, et al. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 2002; 33: 1610-1617 (Pubitemid 34619967)
33. Fink GR, Frackowiak RS, Pietrzyk U, Passingham RE. Multiple nonprimary motor areas in the human cortex. J Neurophysiol 1997; 77: 2164-2174 (Pubitemid 27175001)
34. Fox MD, Corbetta M, Snyder AZ, Vincent JL, Raichle ME. Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc Natl Acad Sci USA 2006; 103: 10046-10051 (Pubitemid 43993620)
35. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 2005; 102: 9673-9678 (Pubitemid 40981739)
36. Freeman LC. A set of measures of centrality based on betweenness. Sociometry 1977; 40: 35-41.
37. Friston K. Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 1994; 2: 56-78. (Pubitemid 124000442)
38. Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Functional connectivity: the principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab 1993; 13: 5-14. (Pubitemid 23016598)
39. Friston KJ, Harrison L, Penny W. Dynamic causal modelling. Neuroimage 2003; 19: 1273-1302 (Pubitemid 37025831)
40. Gerloff C, Bushara K, Sailer A, Wassermann EM, Chen R, Matsuoka T, et al. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 2006; 129: 791-808. (Pubitemid 43278240)
41. Gibbons RD, Hedeker D, Waternaux C, Davis JM. Random regression models: a comprehensive approach to the analysis of longitudinal psychiatric data. Psychopharmacol Bull 1988; 24: 438-443 (Pubitemid 19031632)
42. Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Kust J, Karbe H, et al. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 2008; 63: 236-246 (Pubitemid 351355302)
43. Hanakawa T, Dimyan MA, Hallett M. Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex 2008; 18: 2775-2788
44. Harrison L, Penny WD, Friston K. Multivariate autoregressive modeling of fMRI time series. Neuroimage 2003; 19: 1477-1491 (Pubitemid 37025846)
45. He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M. Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 2007; 53: 905-918 (Pubitemid 46367552)
46. He Y, Chen Z, Evans A. Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J Neurosci 2008; 28: 4756-4766
47. Honey CJ, Sporns O. Dynamical consequences of lesions in cortical networks. Hum Brain Mapp 2008; 29: 802-809 (Pubitemid 351813081)
48. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, et al. Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 2009; 106: 2035-2040
49. Horwitz B, Rumsey JM, Donohue BC. Functional connectivity of the angular gyrus in normal reading and dyslexia. Proc Natl Acad Sci USA 1998; 95: 8939-8944 (Pubitemid 28350593)
50. Jaillard A, Martin CD, Garambois K, Lebas JF, Hommel M. Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. Brain 2005; 128: 1122-1138 (Pubitemid 40675467)
51. Jiang T, He Y, Zang Y, Weng X. Modulation of functional connectivity during the resting state and the motor task. Hum Brain Mapp 2004; 22: 63-71. (Pubitemid 38586101)
52. Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM. The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA 2002; 99: 14518-14523 (Pubitemid 35257703)
53. Kaiser M, Hilgetag CC. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2006; 2: e95.
54. Kaiser M, Hilgetag CC, van Ooyen A. A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions. Cereb Cortex 2009; 19: 3001-3010
55. Latora V, Marchiori M. Efficient behavior of small-world networks. Phys Rev Lett 2001; 87: 198701.
56. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 2000; 20: 4615-4626
57. Lotze M, Markert J, Sauseng P, Hoppe J, Plewnia C, Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci 2006; 26: 6096-6102 (Pubitemid 44318375)
58. Maslov S, Sneppen K. Specificity and stability in topology of protein networks. Science 2002; 296: 910-913 (Pubitemid 34464896)
59. McIntosh AR, Bookstein FL, Haxby JV, Grady CL. Spatial pattern analysis of functional brain images using partial least squares. Neuroimage 1996; 3: 143-157
60. McIntosh AR, Gonzalez-Lima F. Structural equation modeling and its application to network analysis in functional brain imaging. Hum Brain Mapp 1994; 2: 2-22. (Pubitemid 124000439)
61. McKeown MJ, Sejnowski TJ. Independent component analysis of fMRI data: examining the assumptions. Hum Brain Mapp 1998; 6: 368-372 (Pubitemid 28460594)
62. Meunier D, Achard S, Morcom A, Bullmore E. Age-related changes in modular organization of human brain functional networks. Neuroimage 2009; 44: 715-723
63. Micheloyannis S, Pachou E, Stam CJ, Breakspear M, Bitsios P, Vourkas M, et al. Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr Res 2006; 87: 60-66 (Pubitemid 44428137)
64. Mima T, Toma K, Koshy B, Hallett M. Coherence between cortical and muscular activities after subcortical stroke. Stroke 2001; 32: 2597-2601 (Pubitemid 33055313)
65. Murata Y, Sakatani K, Hoshino T, Fujiwara N, Kano T, Nakamura S, et al. Effects of cerebral ischemia on evoked cerebral blood oxygenation responses and BOLD contrast functional MRI in stroke patients. Stroke 2006; 37: 2514-2520 (Pubitemid 44454671)
66. Nair DG, Hutchinson S, Fregni F, Alexander M, Pascual-Leone A, Schlaug G. Imaging correlates of motor recovery from cerebral infarction and their physiological significance in well-recovered patients. Neuroimage 2007; 34: 253-263 (Pubitemid 44802814)
67. Nakamura T, Hillary FG, Biswal BB. Resting network plasticity following brain injury. PLoS One 2009; 4: e8220.
68. Nathan PW, Smith MC. Effects of two unilateral cordotomies on the motility of the lower limbs. Brain 1973; 96: 471-494
69. Nelles G, Spiekramann G, Jueptner M, Leonhardt G, Muller S, Gerhard H, et al. Evolution of functional reorganization in hemiplegic stroke: a serial positron emission tomographic activation study. Ann Neurol 1999; 46: 901-909 (Pubitemid 29379594)
70. Newman MEJ. The structure and function of complex networks. SIAM Rev 2003; 45: 167-256.
71. Onnela JP, Saramaki J, Kertesz J, Kaski K. Intensity and coherence of motifs in weighted complex networks. Phys Rev E Stat Nonlin Soft Matter Phys 2005; 71: 065103. (Pubitemid 41663802)
72. Pineiro R, Pendlebury S, Johansen-Berg H, Matthews PM. Functional MRI detects posterior shifts in primary sensorimotor cortex activation after stroke: evidence of local adaptive reorganization? Stroke 2001; 32: 1134-1139 (Pubitemid 32825797)
73. Ponten SC, Bartolomei F, Stam CJ. Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 2007; 118: 918-927 (Pubitemid 46349824)
74. Roebroeck A, Formisano E, Goebel R. Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 2005; 25: 230-242 (Pubitemid 40289151)
75. Rubinov M, Knock SA, Stam CJ, Micheloyannis S, Harris AW, Williams LM, et al. Small-world properties of nonlinear brain activity in schizophrenia. Hum Brain Mapp 2009; 30: 403-416
76. Salvador R, Suckling J, Coleman MR, Pickard JD, Menon D, Bullmore E. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex 2005; 15: 1332-1342 (Pubitemid 41191541)
77. Saur D, Lange R, Baumgaertner A, Schraknepper V, Willmes K, Rijntjes M, et al. Dynamics of language reorganization after stroke. Brain 2006; 129: 1371-1384 (Pubitemid 43999371)
78. Schaechter JD, Moore CI, Connell BD, Rosen BR, Dijkhuizen RM. Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. Brain 2006; 129: 2722-2733 (Pubitemid 44522105)
79. Shibasaki H, Sadato N, Lyshkow H, Yonekura Y, Honda M, Nagamine T, et al. Both primary motor cortex and supplementary motor area play an important role in complex finger movement. Brain 1993; 116: 1387-1398 (Pubitemid 24038858)
80. Small SL, Hlustik P, Noll DC, Genovese C, Solodkin A. Cerebellar hemispheric activation ipsilateral to the paretic hand correlates with functional recovery after stroke. Brain 2002; 125: 1544-1557 (Pubitemid 34755169)
81. Sporns O, Zwi JD. The small world of the cerebral cortex. Neuroinformatics 2004; 2: 145-162 (Pubitemid 41214095)
82. Stam CJ, de Haan W, Daffertshofer A, Jones BF, Manshanden I, van Cappellen van Walsum AM, et al. Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain 2009; 132: 213-224
83. Stam CJ, Reijneveld JC. Graph theoretical analysis of complex networks in the brain. Nonlinear Biomed Phys 2007; 1: 3.
84. Stam CJ, van Dijk BW. Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets. Physica D Nonlinear Phen 2002; 163: 236-251
85. Strens LH, Asselman P, Pogosyan A, Loukas C, Thompson AJ, Brown P. Corticocortical coupling in chronic stroke: its relevance to recovery. Neurology 2004; 63: 475-484 (Pubitemid 39031377)
86. Stroemer RP, Kent TA, Hulsebosch CE. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 1995; 26: 2135-2144
87. Sun FT, Miller LM, D'Esposito M. Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data. Neuroimage 2004; 21: 647-658 (Pubitemid 38229927)
88. Supekar K, Musen M, Menon V. Development of large-scale functional brain networks in children. PLoS Biol 2009; 7: e1000157.
89. Thomas B, Eyssen M, Peeters R, Molenaers G, Van Hecke P, De Cock P, et al. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 2005; 128: 2562-2577 (Pubitemid 41552942)
90. Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, et al. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage 2004; 23: 827-839 (Pubitemid 39446517)
91. Tononi G, Edelman GM, Sporns O. Complexity and coherency: integrating information in the brain. Trends Cogn Sci 1998; 2: 474-484 (Pubitemid 28557110)
92. van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE. Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 2009; 30: 3127-3141
93. Wang C, Stebbins GT, Nyenhuis DL, deToledo-Morrell L, Freels S, Gencheva E, et al. Longitudinal changes in white matter following ischemic stroke: a three-year follow-up study. Neurobiol Aging 2006; 27: 1827-1833 (Pubitemid 44572581)
94. Wang L, Zhu C, He Y, Zang Y, Cao Q, Zhang H, et al. Altered smallworld brain functional networks in children with attention-deficit/ hyperactivity disorder. Hum Brain Mapp 2009; 30: 638-649
95. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 2003; 126: 2476-2496 (Pubitemid 37314437)
96. Watts DJ, Strogatz SH. Collective dynamics of 'small-world' networks. Nature 1998; 393: 440-442
97. Weiller C, Chollet F, Friston KJ, Wise RJ, Frackowiak RS. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol 1992; 31: 463-472
98. Wieloch T, Nikolich K. Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 2006; 16: 258-264 (Pubitemid 43949227)
99. Wiese H, Stude P, Sarge R, Nebel K, Diener HC, Keidel M. Reorganization of motor execution rather than preparation in poststroke hemiparesis. Stroke 2005; 36: 1474-1479 (Pubitemid 40967515)
100. Woodward TS, Cairo TA, Ruff CC, Takane Y, Hunter MA, Ngan ET. Functional connectivity reveals load dependent neural systems underlying encoding and maintenance in verbal working memory. Neuroscience 2006; 139: 317-325
101. Wu T, Zang Y, Wang L, Long X, Hallett M, Chen Y, et al. Aging influence on functional connectivity of the motor network in the resting state. Neurosci Lett 2007; 422: 164-168 (Pubitemid 47077595)
102. Zheng X, Rajapakse JC. Learning functional structure from fMR images. Neuroimage 2006; 31: 1601-1613 (Pubitemid 44192496)
103. Zhou D, Thompson WK, Siegle G. MATLAB toolbox for functional connectivity. Neuroimage 2009; 47: 1590-1607