Disrupted structural and functional connectivity networks in ischemic stroke patients

Neuroscience

Volumn 364, Issue , 2017, Pages 212-225

  Zhang, Jingna ^a   Zhang, Ye ^a   Wang, Li ^a   Sang, Linqiong ^a   Yang, Jun ^a   Yan, Rubing ^a   Li, Pengyue ^a   Wang, Jian ^a   Qiu, Mingguo ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

decoupling; functional connectivity network; ischemic stroke; structural connectivity network; topological properties

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN ISCHEMIA; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FUGL MEYER ASSESSMENT; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR PARIETAL LOBULE; MALE; MOTOR DYSFUNCTION; NERVE CELL NETWORK; NEUROPSYCHOLOGICAL TEST; POSTERIOR CINGULATE; PRIORITY JOURNAL; PRODUCTIVITY; RESTING STATE NETWORK; STROKE PATIENT; CEREBROVASCULAR ACCIDENT; DIAGNOSTIC IMAGING; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY;

AGED; BRAIN ISCHEMIA; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; STROKE;

EID: 85030866851     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2017.09.009     Document Type: Article

References (76)

1. Achard, S., Salvador, R., Whitcher, B., Suckling, J., Bullmore, E., A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26:1 (2006), 63–72.
2. Achard, S., Bullmore, E., Efficiency and cost of economical brain functional networks. PLoS Comput Biol, 3(2), 2007, e17.
3. Baldassarre, A., Ramsey, L., Hacker, C.L., Callejas, A., Astafiev, S.V., Metcalf, N.V., Zinn, K., Rengachary, J., Snyder, A.Z., Carter, A.R., Shulman, G.L., Corbetta, M., Large-scale changes in network interactions as a physiological signature of spatial neglect. Brain 137:Pt 12 (2014), 3267–3283, 10.1093/brain/awu297.
4. Bonilha, L., Rorden, C., Fridriksson, J., Assessing the clinical effect of residual cortical disconnection after ischemic strokes. Stroke 45:4 (2014), 988–993, 10.1161/STROKEAHA.113.004137.
5. Bonilha, L., Gleichgerrcht, E., Nesland, T., Rorden, C., Fridriksson, J., Success of anomia treatment in aphasia is associated with preserved architecture of global and left temporal lobe structural networks. Neurorehabil Neural Repair 30:3 (2016), 266–279, 10.1177/1545968315593808.
6. Bullmore, E., Sporns, O., Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10 (2009), 186–198, 10.1038/nrn2575.
7. Carter, A.R., Shulman, G.L., Corbetta, M., Why use a connectivity-based approach to study stroke and recovery of function?. Neuroimage 62:4 (2012), 2271–2280, 10.1016/j.neuroimage.2012.02.070.
8. Carter, A.R., Astafiev, S.V., Lang, C.E., Connor, L.T., Rengachary, J., Strube, M.J., Pope, D.L.W., Shulman, G.L., Corbetta, M., Resting inter-hemispheric fMRI connectivity predicts performance after stroke. Ann Neurol 67:3 (2010), 365–375, 10.1002/ana.21905.
9. Catani, M., Howard, R.J., Pajevic, S., Jones, D.K., Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:1 (2002), 77–94.
10. Chen, J.L., Schlaug, G., Resting state interhemispheric motor connectivity and white matter integrity correlate with motor impairment in chronic stroke. Front Neurol, 4, 2013, 178, 10.3389/fneur.2013.00178.
11. Chiang, S., Stern, J.M., Engel, J. Jr., Haneef, Z., Structural-functional coupling changes in temporal lobe epilepsy. Brain Res 1616 (2015), 45–57, 10.1016/j.brainres.2015.04.052.
12. Crofts, J.J., Higham, D.J., Bosnell, R., Jbabdi, S., Matthews, P.M., Behrens, T.E., Johansen-Berg, H., Network analysis detects changes in the contralesional hemisphere following stroke. Neuroimage 54:1 (2011), 161–169, 10.1016/j.neuroimage.2010.08.032.
13. Dacosta-Aguayo, R., Graña, M., Savio, A., Fernández-Andújar, M., Millán, M., et al. Prognostic value of changes in resting-state functional connectivity patterns in cognitive recovery after stroke: a 3T fMRI pilot study. Hum Brain Mapp 35 (2014), 3819–3831, 10.1002/hbm.22439.
14. Dacosta-Aguayo, R., Graña, M., Iturria-Medina, Y., Fernández-Andújar, M., et al. Impairment of functional integration of the default mode network correlates with cognitive outcome at three months after stroke. Hum Brain Mapp 36 (2015), 577–590, 10.1002/hbm.22648.
15. Damoiseaux, J.S., Greicius, M.D., Greater than the sum of its parts: review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct Funct 213 (2009), 525–533, 10.1007/s00429-009-0208-6.
16. Dang, C., Liu, G., Xing, S., Xie, C., Peng, K., Li, C., Li, J., Zhang, J., Chen, L., Pei, Z., Zeng, J., Longitudinal cortical volume changes correlate with motor recovery in patients after acute local subcortical infarction. Stroke 44 (2013), 2795–2801, 10.1161/STROKEAHA.113.000971.
17. De Vico Fallani, F., Astolfi, L., Cincotti, F., Mattia, D., la Rocca, D., Maksuti, E., Salinari, S., Babiloni, F., Vegso, B., Kozmann, G., Nagy, Z., Evaluation of the brain network organization from EEG signals: a preliminary evidence in stroke patient. Anat Rec (Hoboken) 292:12 (2009), 2023–2031, 10.1002/ar.20965.
18. Dijkhuizen, R.M., van der Marel, K., Otte, W.M., Hoff, E.I., van der Zijden, J.P., van der Toorn, A., van Meer, M.P., Functional MRI and diffusion tensor imaging of brain reorganization after experimental stroke. Transl Stroke Res 3:1 (2012), 36–43, 10.1007/s12975-011-0143-8.
19. Freeman, L.C., Set of measures of centrality based on betweenness. Sociometry 40 (1977), 35–41.
20. Gong, G., He, Y., Concha, L., Lebel, C., Gross, D.W., Evans, A.C., Beaulieu, C., Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb Cortex 19 (2009), 524–536.
21. Grefkes, C., Nowak, D.A., Eickhoff, S.B., Dafotakis, M., Küst, J., Karbe, H., Fink, G.R., Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 63:2 (2008), 236–246.
22. Grefkes, C., Fink, G.R., Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain 134:Pt 5 (2011), 1264–1276, 10.1093/brain/awr033.
23. Greicius, M.D., Srivastava, G., Reiss, A.L., Menon, V., Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101:13 (2004), 4637–4642.
24. Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C.J., Wedeen, V.J., Sporns, O., Mapping the structural core of human cerebral cortex. PLoS Biol, 6, 2008, e159, 10.1371/journal.pbio.0060159.
25. Hagmann, P., Sporns, O., Madan, N., Cammoun, L., Pienaar, R., Wedeen, V.J., Meuli, R., Thiran, J.P., Grant, P.E., White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci USA 107 (2010), 19067–19072, 10.1073/pnas.1009073107.
26. Hermundstad, A., Brown, K., Bassett, D., Aminoff, E., Frithsen, A., Johnson, A., Tip- per, C., Miller, M., Grafton, S., Carlson, J., Structurally-constrained relationships between cognitive states in the human brain. PLoS Comput Biol, 10, 2014, e1003591, 10.1371/journal.pcbi.1003591.
27. Honey, C.J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J.P., Meuli, R., Hagmann, P., Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106:6 (2009), 2035–2040, 10.1073/pnas.0811168106.
28. Honey, C.J., Thivierge, J.P., Sporns, O., Can structure predict function in the human brain?. Neuroimage 52:3 (2010), 766–776, 10.1016/j.neuroimage.2010.01.071.
29. Huang, X., Du, X., Song, H., Zhang, Q., Jia, J., Xiao, T., Wu, J., Cognitive impairments associated with corpus callosum infarction: a ten cases study. Int J Clin Exp Med 8:11 (2015), 21991–21998.
30. Humphries, M.D., Gurney, K., Prescott, T.J., The brainstem reticular formation is a small-world, not scale-free, network. Proc Biol Sci 273:1585 (2006), 503–511.
31. Johansen-Berg, H., Rushworth, M.F., Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 32 (2009), 75–94, 10.1146/annurev.neuro.051508.
32. Koch, P., Schulz, R., Hummel, F.C., Structural connectivity analyses in motor recovery research after stroke. Ann Clin Transl Neurol 3:3 (2016), 233–244, 10.1002/acn3.278.
33. Koch, M.A., Norris, D.G., Hund-Georgiadis, M., An investigation of functional and anatomical connectivity using magnetic resonance imaging. Neuroimage 16:1 (2002), 241–250.
34. Latora, V., Marchio, M., Efficient behavior of small-world networks. Phys Rev Lett, 87(19), 2001, 198701.
35. Li, Y., Wu, P., Liang, F., Huang, W., The Microstructural status of the corpus callosum is associated with the degree of motor function and neurological deficit in stroke patients. PLoS ONE, 10(4), 2015, e0122615, 10.1371/journal.pone.0122615.
36. Liu, J., Qin, W., Zhang, J., Zhang, X., Yu, C., Enhanced interhemispheric functional connectivity compensates for anatomical connection damages in subcortical stroke. Stroke 46 (2015), 1045–1051, 10.1161/STROKEAHA.114.007044.
37. Liu, J., Qin, W., Wang, H., Zhang, J., Xue, R., Zhang, X., Yu, C., Altered spontaneous activity in the default-mode network and cognitive decline in chronic subcortical stroke. J Neurol Sci 347:1–2 (2014), 193–198, 10.1016/j.jns.2014.08.049.
38. Long, Z., Duan, X., Xie, B., Du, H., Li, R., Xu, Q., Wei, L., Zhang, S.X., Wu, Y., Gao, Q., Chen, H., Alteredbrainstructuralconnectivityinpost-traumaticstressdisorder: a diffusion tensor imaging tractography study. J Affect Disord 150 (2013), 798–806.
39. Lo, C.Y., Wang, P.N., Chou, K.H., Wang, J., He, Y., Lin, C.P., Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer's disease. J Neurosci 30:50 (2010), 16876–16885, 10.1523/JNEUROSCI.4136-10.2010.
40. Meyer, S., Kessner, S.S., Cheng, B., Bönstrup, M., Schulz, R., Hummel, F.C., De Bruyn, N., Peeters, A., Van Pesch, V., Duprez, T., Sunaert, S., Schrooten, M., Feys, H., Gerloff, C., Thomalla, G., Thijs, V., Verheyden, G., Voxel-based lesion-symptom mapping of stroke lesions underlying somatosensory deficits. Neuroimage Clin 10 (2015), 257–266, 10.1016/j.nicl.2015.12.005.
41. Mikell, C.B., Banks, G.P., Frey, H.P., Youngerman, B.E., Nelp, T.B., Karas, P.J., Chan, A.K., Voss, H.U., Connolly, E.S., Frontal networks associated with command following after hemorrhagic stroke. Stroke 46:1 (2016), 49–57, 10.1161/STROKEAHA.114.007645.
42. Newman, M.E.J., The structure and function of complex networks. SIAM Rev 45 (2003), 167–256.
43. Oldfield, R., The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:1 (1971), 97–113.
44. Park, C.H., Chang, W.H., Ohn, S.H., Kim, S.T., Bang, O.Y., Pascual-Leone, A., Kim, Y.H., Longitudinal changes of resting-state functional connectivity during motor recovery after stroke. Stroke 42:5 (2011), 1357–1362, 10.1161/STROKEAHA.110.596155.
45. Park, H.J., Friston, K., Structural and functional brain networks: from connections to cognition. Science, 342(6158), 2013, 1238411, 10.1126/science.1238411.
46. Puh, U., Vovk, A., Sevšek, F., Šuput, D., Increased cognitive load during simple and complex motor tasks in acute stage after stroke. Int J Psychophysiol 63:2 (2007), 173–180.
47. Rehme, A.K., Grefkes, C., Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol 591:1 (2013), 17–31, 10.1113/jphysiol.2012.243469.
48. Rushworth, M.F., Johansen-Berg, H., Göbel, S., Devlin, J., The left parietal and premotor cortices: motor attention and selection. NeuroImage 20 (2003), S89–S100.
49. Salvador, R., Suckling, J., Coleman, M.R., Pickard, J.D., Menon, D., Bullmore, E., Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex 15:9 (2005), 1332–1342.
50. Sang, L., Zhang, J., Wang, L., Zhang, J., Zhang, Y., Li, P., Wang, J., Qiu, M., Alteration of brain functional networks in early-stage Parkinson's disease: a resting-state fMRI study. PLoS ONE, 10(10), 2015, e0141815, 10.1371/journal.pone.0141815.
51. Shi, L., Wang, D., Chu, W.C., Liu, S., Xiong, Y., Wang, Y., Wang, Y., Wong, L.K., Mok, V.C., Abnormal organization of white matter network in patients with no dementia after ischemic stroke. PLoS ONE, 8(12), 2013, e81388, 10.1371/journal.pone.0081388.
52. Skudlarski, P., Jagannathan, K., Calhoun, V., Hampson, M., Skudlarska, B., Pearlson, G., Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. NeuroImage 43:3 (2008), 554–561, 10.1016/j.neuroimage.2008.07.063.
53. Stewart, J.C., Dewanjee, P., Shariff, U., Cramer, S.C., Dorsal premotor activity and connectivity relate to action selection performance after stroke. Hum Brain Mapp 37:5 (2016), 1816–1830, 10.1002/hbm.23138.
54. Sporns, O., Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23:2 (2013), 162–171, 10.1016/j.conb.2012.11.015.
55. Sporns, O., The human connectome: a complex network. Ann N Y Acad Sci 1224 (2011), 109–125, 10.1111/j.1749-6632.2010.05888.x.
56. Tuladhar, A.M., Snaphaan, L., Shumskaya, E., Rijpkema, M., Fernández, G., Norris, D., de Leeuw, F.E., Default mode network connectivity in stroke patients. PLoS ONE, 8(6), 2013, e66556, 10.1371/journal.pone.0066556.
57. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., Joliot, M., Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:1 (2002), 273–289.
58. Van den Heuvel, M., Mandl, R., Luigjes, J., Hulshoff Pol, H., Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28:43 (2008), 10844–10851, 10.1523/JNEUROSCI.2964-08.2008.
59. Van den Heuvel, M.P., Mandl, R.C., Kahn, R.S., Hulshoff Pol, H.E., Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30:10 (2009), 3127–3141, 10.1002/hbm.20737.
60. Van Meer, M.P., van der Marel, K., Otte, W.M., Berkelbach van der Sprenkel, J.W., Dijkhuizen, R.M., Correspondence between altered functional and structural connectivity in the contralesional sensorimotor cortex after unilateral stroke in rats: a combined resting-state functional MRI and manganese-enhanced MRI study. J Cereb Blood Flow Metab 30:10 (2010), 1707–1711, 10.1038/jcbfm.2010.124.
61. Wang, L., Yu, C., Chen, H., Qin, W., He, Y., Fan, F., Zhang, Y., Wang, M., Li, K., Zang, Y., Woodward, T.S., Zhu, C., Dynamic functional reorganization of the motor execution network after stroke. Brain 133:Pt 4 (2010), 1224–1238, 10.1093/brain/awq043.
62. Watts, D.J., Strogatz, S.H., Collective dynamics of ‘small-world’ networks. Nature 393:6684 (1998), 440–442.
63. Wu, P., Zeng, F., Li, Y.X., Yu, B.L., Qiu, L.H., Qin, W., Li, J., Zhou, Y.M., Liang, F.R., Changes of resting cerebral activities in subacute ischemic stroke patients. Neural Regen Res 10:5 (2015), 760–765, 10.4103/1673-5374.156977.
64. Xu, H., Qin, W., Chen, H., Jiang, L., Li, K., Yu, C., Contribution of the resting-state functional connectivity of the contralesional primary sensorimotor cortex to motor recovery after subcortical stroke. PLoS ONE, 9(1), 2014, e84729, 10.1371/journal.pone.0084729.
65. Yang, M., Li, J., Li, Y., Li, R., Pang, Y., Yao, D., Liao, W., Chen, H., Altered intrinsic regional activity and interregional functional connectivity in post-stroke aphasia. Sci Rep, 6, 2016, 24803, 10.1038/srep 24803.
66. Yang, M., Li, J., Yao, D., Chen, H., Disrupted intrinsic local synchronization in poststroke aphasia. Medicine (Baltimore), 95(11), 2016, e3101, 10.1097/MD.0000000000003101.
67. Yang, M., Li, Y., Li, J., Yao, D., Liao, W., Chen, H., Beyond the arcuate fasciculus: damage to ventral and dorsal language pathways in aphasia. Brain Topogr, 2016 (Epub ahead of print).
68. Yin, D., Song, F., Xu, D., Peterson, B.S., Sun, L., Men, W., Yan, X., Fan, M., Patterns in cortical connectivity for determining outcomes in hand function after subcortical stroke. PLoS ONE, 7(12), 2012, e52727, 10.1371/journal.pone.0052727.
69. Yin, D., Song, F., Xu, D., Sun, L., Men, W., Zang, L., Yan, X., Fan, M., Altered topological properties of the cortical motor-related network in patients with subcortical stroke revealed by graph theoretical analysis. Hum Brain Mapp 35:7 (2014), 3343–3359, 10.1002/hbm.22406.
70. Zalesky, A., Fornito, A., Cocchi, L., Gollo, L.L., van den Heuvel, M.P., Breakspear, M., Connectome sensitivity or specificity: which is more important?. Neuroimage, 2016, 10.1016/j.neuroimage.2016.06.035 pii: S1053-8119(16)30284-1.
71. Zhang, J., Wang, J., Wu, Q., Kuang, W., Huang, X., He, Y., Gong, Q., Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biol Psychiatry 70:4 (2011), 334–342, 10.1016/j.biopsych.2011.05.018.
72. Zhang, Y., Liu, H., Wang, L., Yang, J., Yan, R., Zhang, J., Sang, L., Li, P., Wang, J., Qiu, M., Relationship between functional connectivity and motor function assessment in stroke patients with hemiplegia: a resting-state functional MRI study. Neuroradiology 58:5 (2016), 503–511, 10.1007/s00234-016-1646-5.
73. Zhang, Z., Liao, W., Chen, H., Mantini, D., Ding, J.R., Xu, Q., Wang, Z., Yuan, C., Chen, G., Jiao, Q., Lu, G., Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 134 (2011), 2912–2928, 10.1093/brain/awr223.
74. Zhu, J., Jin, Y., Wang, K., Zhou, Y., Feng, Y., Yu, M., Jin, X., Frequency-dependent changes in the regional amplitude and synchronization of resting-state functional MRI in stroke. PLoS ONE, 10(4), 2015, e0123850, 10.1371/journal.pone.0123850.
75. Zhu, J., Wang, C., Liu, F., Qin, W., Li, J., Zhuo, C., Alterations of functional and structural networks in schizophrenia patients with auditory verbal hallucinations. Front Hum Neurosci, 10, 2016, 114, 10.3389/fnhum.2016.00114.
76. Zhu, Y., Bai, L., Liang, P., Kang, S., Gao, H., Yang, H., Disrupted brain connectivity networks in acute ischemic stroke patients. Brain Imaging Behav 11:2 (2017), 444–453, 10.1007/s11682-016-9525-6.