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Neuroradiology

, Volume 55, Issue 7, pp 913–925 | Cite as

Cortical reorganization after motor imagery training in chronic stroke patients with severe motor impairment: a longitudinal fMRI study

  • Limin Sun
  • Dazhi Yin
  • Yulian Zhu
  • Mingxia Fan
  • Lili Zang
  • Yi Wu
  • Jie Jia
  • Yulong Bai
  • Bing Zhu
  • Yongshan Hu
Functional Neuroradiology

Abstract

Introduction

Despite its clinical efficacy, few studies have examined the neural mechanisms of motor imagery training (MIT) in stroke. Our objective was to find the cortical reorganization patterns after MIT in chronic stroke patients.

Methods

Twenty stroke patients with severe motor deficits were randomly assigned to the MIT or conventional rehabilitation therapy (CRT) group, but two lost in the follow-up. All 18 patients received CRT 5 days/week for 4 weeks. Nine subjects in the MIT group received 30-min MIT 5 days/week for 4 weeks. Before and after the interventions, the upper limb section of the Fugl–Meyer Scale (FM-UL) was blindly evaluated, and functional magnetic resonance imaging was administered while the patients executed a passive fist clutch task.

Results

Two cortical reorganization patterns were found. One pattern consisted of the growth in activation in the contralateral sensorimotor cortex (cSMC) for most patients (six in the MIT group, five in the CRT group), and the other consisted of focusing of the activation in the cSMC with increasing of the laterality index of the SMC for a small portion of patients (three in the MIT group, one in the CRT group). When we applied correlation analyses to the variables of relative ΔcSMC and ΔFM-UL in the 11 patients who experienced the first pattern, a positive relationship was detected.

Conclusions

Our results indicate that different cortical reorganization patterns (increases in or focusing of recruitment to the cSMC region) exist in chronic stroke patients after interventions, and patients may choose efficient patterns to improve their motor function.

Keywords

Cortical reorganization Functional magnetic resonance imaging Motor imagery Rehabilitation Stroke 

Notes

Acknowledgments

This research was supported by the National Natural Science Foundation of China (grant no. 81272169) and 12th Five-Year Plan supporting project of Ministry of Science and Technology of the People’s Republic of China (grant no. 2013BAI10B03). We thank Professor Yongshan Hu and Mingxia Fan for guidance. We also thank Dazhi Yin and Lili Zang for the fMRI processes and analyses they provided. We acknowledge the generous support of the Shanghai Key Laboratory of Magnetic Resonance, East China Normal University.

Conflict of interest

We declare that we have no conflict of interest.

References

  1. 1.
    Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J (1992) Measurement of motor recovery after stroke. Outcome assessment and sample size requirements. Stroke 23(8):1084–1089PubMedCrossRefGoogle Scholar
  2. 2.
    Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, Hailpern SM, Ho M, Howard V, Kissela B, Kittner S, Lloyd-Jones D, McDermott M, Meigs J, Moy C, Nichol G, O’Donnell C, Roger V, Sorlie P, Steinberger J, Thom T, Wilson M, Hong Y (2008) Heart disease and stroke statistics–2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 117(4):e25–e146. doi: 10.1161/CIRCULATIONAHA.107.187998 PubMedCrossRefGoogle Scholar
  3. 3.
    Colebatch JG, Gandevia SC (1989) The distribution of muscular weakness in upper motor neuron lesions affecting the arm. Brain 112(Pt 3):749–763PubMedCrossRefGoogle Scholar
  4. 4.
    Braun SM, Beurskens AJ, Borm PJ, Schack T, Wade DT (2006) The effects of mental practice in stroke rehabilitation: a systematic review. Arch Phys Med Rehabil 87(6):842–852. doi: 10.1016/j.apmr.2006.02.034 PubMedCrossRefGoogle Scholar
  5. 5.
    Sharma N, Pomeroy VM, Baron JC (2006) Motor imagery: a backdoor to the motor system after stroke? Stroke 37(7):1941–1952. doi: 10.1161/01.STR.0000226902.43357.fc PubMedCrossRefGoogle Scholar
  6. 6.
    Malouin F, Richards CL, Durand A, Doyon J (2008) Clinical assessment of motor imagery after stroke. Neurorehabil Neural Repair 22(4):330–340. doi: 10.1177/1545968307313499 PubMedGoogle Scholar
  7. 7.
    Page SJ, Levine P, Leonard A (2007) Mental practice in chronic stroke: results of a randomized, placebo-controlled trial. Stroke 38(4):1293–1297. doi: 10.1161/01.STR.0000260205.67348.2b PubMedCrossRefGoogle Scholar
  8. 8.
    Page SJ, Levine P, Leonard AC (2005) Effects of mental practice on affected limb use and function in chronic stroke. Arch Phys Med Rehabil 86(3):399–402. doi: 10.1016/j.apmr.2004.10.002 PubMedCrossRefGoogle Scholar
  9. 9.
    Page SJ, Levine P, Sisto S, Johnston MV (2001) A randomized efficacy and feasibility study of imagery in acute stroke. Clin Rehabil 15(3):233–240PubMedCrossRefGoogle Scholar
  10. 10.
    Sharma N, Simmons LH, Jones PS, Day DJ, Carpenter TA, Pomeroy VM, Warburton EA, Baron JC (2009) Motor imagery after subcortical stroke: a functional magnetic resonance imaging study. Stroke 40(4):1315–1324. doi: 10.1161/STROKEAHA.108.525766 PubMedCrossRefGoogle Scholar
  11. 11.
    Page SJ, Szaflarski JP, Eliassen JC, Pan H, Cramer SC (2009) Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil Neural Repair 23(4):382–388. doi: 10.1177/1545968308326427 PubMedGoogle Scholar
  12. 12.
    Butler AJ, Page SJ (2006) Mental practice with motor imagery: evidence for motor recovery and cortical reorganization after stroke. Arch Phys Med Rehabil 87(12 Suppl 2):S2–S11. doi: 10.1016/j.apmr.2006.08.326 PubMedCrossRefGoogle Scholar
  13. 13.
    Cramer SC, Bastings EP (2000) Mapping clinically relevant plasticity after stroke. Neuropharmacology 39(5):842–851PubMedCrossRefGoogle Scholar
  14. 14.
    Calautti C, Naccarato M, Jones PS, Sharma N, Day DD, Carpenter AT, Bullmore ET, Warburton EA, Baron JC (2007) The relationship between motor deficit and hemisphere activation balance after stroke: a 3T fMRI study. NeuroImage 34(1):322–331. doi: 10.1016/j.neuroimage.2006.08.026 PubMedCrossRefGoogle Scholar
  15. 15.
    Ward NS, Cohen LG (2004) Mechanisms underlying recovery of motor function after stroke. Arch Neurol 61(12):1844–1848. doi: 10.1001/archneur.61.12.1844 PubMedCrossRefGoogle Scholar
  16. 16.
    Gerloff C, Bushara K, Sailer A, Wassermann EM, Chen R, Matsuoka T, Waldvogel D, Wittenberg GF, Ishii K, Cohen LG, Hallett M (2006) Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 129(Pt 3):791–808. doi: 10.1093/brain/awh713 PubMedCrossRefGoogle Scholar
  17. 17.
    Seitz RJ, Huang Y, Knorr U, Tellmann L, Herzog H, Freund HJ (1995) Large-scale plasticity of the human motor cortex. Neuroreport 6(5):742–744PubMedCrossRefGoogle Scholar
  18. 18.
    Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL (2000) Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 31(3):656–661PubMedCrossRefGoogle Scholar
  19. 19.
    Calautti C, Leroy F, Guincestre JY, Baron JC (2001) Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 32(11):2534–2542PubMedCrossRefGoogle Scholar
  20. 20.
    Johansen-Berg H, Dawes H, Guy C, Smith SM, Wade DT, Matthews PM (2002) Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain 125(Pt 12):2731–2742PubMedCrossRefGoogle Scholar
  21. 21.
    Brunnstrom S (1966) Motor testing procedures in hemiplegia: based on sequential recovery stages. Phys Ther 46(4):357–375PubMedGoogle Scholar
  22. 22.
    Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedCrossRefGoogle Scholar
  23. 23.
    Bohannon RW, Smith MB (1987) Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 67(2):206–207PubMedGoogle Scholar
  24. 24.
    Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7(1):13–31PubMedGoogle Scholar
  25. 25.
    Liu KP, Chan CC, Lee TM, Hui-Chan CW (2004) Mental imagery for promoting relearning for people after stroke: a randomized controlled trial. Arch Phys Med Rehabil 85(9):1403–1408PubMedCrossRefGoogle Scholar
  26. 26.
    Duncan PW, Propst M, Nelson SG (1983) Reliability of the Fugl–Meyer assessment of sensorimotor recovery following cerebrovascular accident. Phys Ther 63(10):1606–1610PubMedGoogle Scholar
  27. 27.
    Di Fabio RP, Badke MB (1990) Relationship of sensory organization to balance function in patients with hemiplegia. Phys Ther 70(9):542–548PubMedGoogle Scholar
  28. 28.
    Friston KJ (1998) Imaging neuroscience: principles or maps? Proc Natl Acad Sci U S A 95(3):796–802PubMedCrossRefGoogle Scholar
  29. 29.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289. doi: 10.1006/nimg.2001.0978 PubMedCrossRefGoogle Scholar
  30. 30.
    Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR (1997) A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28(12):2518–2527PubMedCrossRefGoogle Scholar
  31. 31.
    Hewett TE, Ford KR, Levine P, Page SJ (2007) Reaching kinematics to measure motor changes after mental practice in stroke. Top Stroke Rehabil 14(4):23–29. doi: 10.1310/tsr1404-23 PubMedCrossRefGoogle Scholar
  32. 32.
    Lee CC, Jack CR Jr, Riederer SJ (1998) Mapping of the central sulcus with functional MR: active versus passive activation tasks. AJNR Am J Neuroradiol 19(5):847–852PubMedGoogle Scholar
  33. 33.
    Weiller C, Juptner M, Fellows S, Rijntjes M, Leonhardt G, Kiebel S, Muller S, Diener HC, Thilmann AF (1996) Brain representation of active and passive movements. NeuroImage 4(2):105–110. doi: 10.1006/nimg.1996.0034 PubMedCrossRefGoogle Scholar
  34. 34.
    Puce A, Constable RT, Luby ML, McCarthy G, Nobre AC, Spencer DD, Gore JC, Allison T (1995) Functional magnetic resonance imaging of sensory and motor cortex: comparison with electrophysiological localization. J Neurosurg 83(2):262–270. doi: 10.3171/jns.1995.83.2.0262 PubMedCrossRefGoogle Scholar
  35. 35.
    Yetkin FZ, Mueller WM, Hammeke TA, Morris GL 3rd, Haughton VM (1995) Functional magnetic resonance imaging mapping of the sensorimotor cortex with tactile stimulation. Neurosurgery 36(5):921–925PubMedCrossRefGoogle Scholar
  36. 36.
    Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, Cassol E, Chollet F (2004) A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. NeuroImage 23(3):827–839. doi: 10.1016/j.neuroimage.2004.07.058 PubMedCrossRefGoogle Scholar
  37. 37.
    Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H, Freund HJ (1998) Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol 55(8):1081–1088PubMedCrossRefGoogle Scholar
  38. 38.
    Mima T, Sadato N, Yazawa S, Hanakawa T, Fukuyama H, Yonekura Y, Shibasaki H (1999) Brain structures related to active and passive finger movements in man. Brain 122(Pt 10):1989–1997PubMedCrossRefGoogle Scholar
  39. 39.
    Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77(4–5):677–682PubMedCrossRefGoogle Scholar
  40. 40.
    Loubinoux I, Dechaumont-Palacin S, Castel-Lacanal E, De Boissezon X, Marque P, Pariente J, Albucher JF, Berry I, Chollet F (2007) Prognostic value of FMRI in recovery of hand function in subcortical stroke patients. Cereb Cortex 17(12):2980–2987. doi: 10.1093/cercor/bhm023 PubMedCrossRefGoogle Scholar
  41. 41.
    Rehme AK, Eickhoff SB, Wang LE, Fink GR, Grefkes C (2011) Dynamic causal modeling of cortical activity from the acute to the chronic stage after stroke. NeuroImage 55(3):1147–1158. doi: 10.1016/j.neuroimage.2011.01.014 PubMedCrossRefGoogle Scholar
  42. 42.
    Dong Y, Winstein CJ, Albistegui-DuBois R, Dobkin BH (2007) 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 21(5):412–428. doi: 10.1177/1545968306298598 PubMedCrossRefGoogle Scholar
  43. 43.
    Ward NS, Brown MM, Thompson AJ, Frackowiak RS (2003) Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 126(Pt 11):2476–2496. doi: 10.1093/brain/awg245 PubMedCrossRefGoogle Scholar
  44. 44.
    Jang SH, Kim YH, Cho SH, Lee JH, Park JW, Kwon YH (2003) Cortical reorganization induced by task-oriented training in chronic hemiplegic stroke patients. Neuroreport 14(1):137–141. doi: 10.1097/01.wnr.0000051544.96524.f2 PubMedCrossRefGoogle Scholar
  45. 45.
    Binkofski F, Seitz RJ (2004) Modulation of the BOLD-response in early recovery from sensorimotor stroke. Neurology 63(7):1223–1229PubMedCrossRefGoogle Scholar
  46. 46.
    Askim T, Indredavik B, Vangberg T, Haberg A (2009) Motor network changes associated with successful motor skill relearning after acute ischemic stroke: a longitudinal functional magnetic resonance imaging study. Neurorehabil Neural Repair 23(3):295–304. doi: 10.1177/1545968308322840 PubMedGoogle Scholar
  47. 47.
    Carey LM, Abbott DF, Egan GF, O’Keefe GJ, Jackson GD, Bernhardt J, Donnan GA (2006) Evolution of brain activation with good and poor motor recovery after stroke. Neurorehabil Neural Repair 20(1):24–41. doi: 10.1177/1545968305283053 PubMedCrossRefGoogle Scholar
  48. 48.
    Calautti C, Leroy F, Guincestre JY, Baron JC (2003) Displacement of primary sensorimotor cortex activation after subcortical stroke: a longitudinal PET study with clinical correlation. NeuroImage 19(4):1650–1654PubMedCrossRefGoogle Scholar
  49. 49.
    Rehme AK, Fink GR, von Cramon DY, Grefkes C (2011) The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI. Cereb Cortex 21(4):756–768. doi: 10.1093/cercor/bhq140 PubMedCrossRefGoogle Scholar
  50. 50.
    Hamzei F, Liepert J, Dettmers C, Weiller C, Rijntjes M (2006) Two different reorganization patterns after rehabilitative therapy: an exploratory study with fMRI and TMS. NeuroImage 31(2):710–720. doi: 10.1016/j.neuroimage.2005.12.035 PubMedCrossRefGoogle Scholar
  51. 51.
    Hamzei F, Dettmers C, Rijntjes M, Weiller C (2008) The effect of cortico-spinal tract damage on primary sensorimotor cortex activation after rehabilitation therapy. Exp Brain Res 190(3):329–336. doi: 10.1007/s00221-008-1474-x PubMedCrossRefGoogle Scholar
  52. 52.
    Feydy A, Carlier R, Roby-Brami A, Bussel B, Cazalis F, Pierot L, Burnod Y, Maier MA (2002) Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 33(6):1610–1617PubMedCrossRefGoogle Scholar
  53. 53.
    Nelles G, Jentzen W, Jueptner M, Muller S, Diener HC (2001) Arm training induced brain plasticity in stroke studied with serial positron emission tomography. NeuroImage 13(6 Pt 1):1146–1154. doi: 10.1006/nimg.2001.0757 PubMedCrossRefGoogle Scholar
  54. 54.
    Lindberg P, Schmitz C, Forssberg H, Engardt M, Borg J (2004) Effects of passive-active movement training on upper limb motor function and cortical activation in chronic patients with stroke: a pilot study. J Rehabil Med 36(3):117–123PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Limin Sun
    • 1
  • Dazhi Yin
    • 2
  • Yulian Zhu
    • 1
  • Mingxia Fan
    • 2
  • Lili Zang
    • 2
  • Yi Wu
    • 1
  • Jie Jia
    • 1
  • Yulong Bai
    • 1
  • Bing Zhu
    • 1
  • Yongshan Hu
    • 1
  1. 1.Department of Rehabilitation, Huashan HospitalFudan UniversityShanghaiChina
  2. 2.Shanghai Key Laboratory of Magnetic ResonanceEast China Normal UniversityShanghaiChina

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