Annals of Clinical and Experimental NeurologyAnnals of Clinical and Experimental NeurologyАнналы клинической и экспериментальной неврологии2075-54732409-2533Eco-Vector29610.17816/psaic296ReviewsОбзорыUnknownThe use of structural and functional neuroimaging for the evaluation of motor rehabilitation in patients with ischemic strokeВозможности функциональной и структурной нейровизуализации в изучении восстановления двигательных функций после ишемического инсультаhttps://orcid.org/0000-0001-9929-2725DobryninaLarisa A.ДобрынинаЛариса Анатольевна
Russian Federation

D. Sci. (Med.), Head, 3rd Neurology department

д.м.н., г.н.с., рук. 3-го неврологического отделения

dobrla@mail.ruResearch Center of NeurologyФГБНУ «Научный центр неврологии»1309201153536103022017Copyright ©; 2011, Dobrynina L.A.Copyright ©; 2011, Dobrynina L.A.2011Dobrynina L.A.Dobrynina L.A.https://creativecommons.org/licenses/by/4.0https://annaly-nevrologii.com/pathID/article/view/296

We briefly review the methods of structural and functional neuroimaging use for the evaluation of motor rehabilitation after ischemic stroke. The results of studies for functional adaptive changes in stroke patients with different severity of corticospinal tract damage, various approaches to evaluation of rehabilitation prognosis and development of rehabilitation strategies designed to reduce impairment are discussed.

В настоящем обзоре представлены краткие сведения о возможностях основных структурных и функциональных нейровизуализационных методов в изучении восстановления двигательных функций после ишемического инсульта; обобщены результаты исследований, посвященные функциональным адаптивным изменениям у больных с мозговыми инфарктами и разной степенью вовлечения кортикоспинального тракта; освещены подходы к оценке прогноза восстановления и разработке реабилитационных стратегий, направленных на уменьшение степени неврологического дефекта.

fMRItranscranial magnetic stimulationplasticityischemic strokerehabilitationфункциональная МРТтранскраниальная магнитная стимуляцияпластичностьишемический инсультвосстановлениеAndres F.G., Mima T., Schulman A.E. et al. Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. Brain 1999; 122: 855–870.Arthurs O., Boniface S. How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci. 2002; 25: 27–31.Barker A.T., Jalinos R., Freeston I.L. Non invasive stimulation of human motor cortex. Lancet 1985; 1: 1106–1107.Baron J.C., Cohen L.G., Cramer S.C. et al. Neuroimaging in stroke recovery: a position paper from the First International Workshop on Neuroimaging and Stroke Recovery. Cerebrovasc. Dis. 2004; 18: 260–267.Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B. 1996; 111: 209–219.Binkofski F., Seitz R.J., Arnold S. et al. Thalamic metabolism and cortocospinal tract integrity determine motor recovery in stroke. Ann. Neurol. 1996; 39: 460–470.Bonaiuti D., Grimaldi M. Neuroimaging: a new challenge in neurorehabilitation of stroke patients. Eura. Medicophys. 2007; 43 (2): 215–219.Brown J.A., Lutsep H., Cramer S.C., Weinand M.Motor cortex stimulation for enhancement of recovery after stroke: case report. Neurol. Res. 2003; 25: 815–818.Butefisch C.M., Kleiser R., Korber B. et al. Recruitment of contralesional motor cortex in stroke patients with recovery of hand function. Neurology 2005; 64: 1067–1069.Butefisch C.M., Kleiser R., Seitz R.J. Post-lesional cerebral reorganization: evidence from functional neuroimaging and transcranial magnetic stimulation. J. Physiol Paris 2006; 99: 437–454.Butefisch C.M., Netz J., Wessling M., Homberg V. Remote changes in cortical excitability after stroke. Brain 2003; 126: 470–481.Calautti C., Baron J.C. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke 2003; 34: 1553–1566.Calautti C., Leroy F., Guincestre J.Y., Baron J.C. Displacement of primary sensorimotor cortex activation after subcortical stroke: a longitudinal PET study with clinical correlation. Neuroimage 2003 (b); 19: 1650–1654.Calautti C., Leroy F., Guincestre J.Y., Baron J.C. Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 2001; 32: 2534–2542.Carey L.M., Abbot D.F., Egan G.F. et al. Evolution of brain activation with good and poor motor recovery after stroke. Neurorehabil. Neural. Repair 2006; 20: 24–41.Carey L.M., Abbot D.F., Egan G.F. et al. Motor impairment and recovery in the upper limb after stroke: behavioral and neuroanatomical correlates. Stroke 2005; 36: 625–629.Carusone L.M., Srinivasan J., Gitelman D.R. Restoring Neurological function: putting the neurosciences to work in neuroreabilitation. The Academy of Medical Sciences 2004.Catano A., Houa M., Caroyer J.M. et al. Magnetic transcranial stimulation in non-haemorrhagic sylvian strokes: interest of facilitation for early functional prognosis. Electroenceph. Clin. Neurophysiol. 1995; 97 (6): 349–354.Chen R. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp. Brain Res. 2004; 154: 1–10.Сhеn R., Сohеn L.G., Hаllett M. Nеrvous systеm геorgаnizаtiоn following injuгy. Neuroscience 2002; 11: 761–773.Cholet F., DiPiero V., Wise R.J. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann. Neurol. 1991; 29: 63–71.Cicinelli P., Traversa R., Rossini P.M. Post-stroke reorganization of brain motor output to the hand: a 2–4 month follow-up with focal magnetic transcranial stimulation. Electroencephalogr Clin Neurophysiol 1997; 105 (6): 438–450.Classen J., Gerloff C., Honda M., Hallett M. Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. J. Neurophysiol. 1998; 79: 1567–1573.Conturo T.E., Lori N.F., Cull T.S. et al. Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. USA 1999; 96: 10422–10427.Cramer S.C., Moore C.I., Finklestein S.P., Rosen B.R. A pilot study of somatotopic mapping after cortical infarct. Stroke 2000; 31: 668–671.Cramer S.C., Nelles G., Benson R.R. et al. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 1997; 28: 2518–2527.Cramer S.C., Nelles G., Schaechter J.D. et al. A functional MRI study of three motor tasks in the evaluation of stroke recovery. Neurorehabil. Neural Repair 2001; 15: 1–8.Del Gratta C., Pizzella V., Tecchio F. et al. Magnetoencephalography: a noninvasive brain imaging method with 1 ms resolution. Rep. Prog. Phys. 2001; 64: 1759–1814.Delvaux V., Alagona G., Gérard P. et al. Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation. Clin. Neurophysiol. 2003; 114 (7): 1217–1225.Dhamala M., Pagnoni G., Wiesenfeld K. et al. Neural correlates of the complexity of rhythmic finger tapping. Neuroimage 2003; 20: 918–926.Dobkin B.H. Strategies for stroke rehabilitation. Lancet Neurol .2004; 3: 528–536.Dum R.P., Strick P.L. Spinal cord terminations of the medial wall motor areas in macaque monkeys. J. Neurosci. 1996; 16: 6513–6525.Dunсan P.W., Goldstеin L.B., Маtсhаr D. et al. Меasurement of motor recovery аftеr stгoke: outcome asses sment and samplе sizе requirmеnts. Stroke l992; 23: l084–1089.Ferbert A., Priori A., Rothwell J.C. et al. Interhemispheric inhibition of the human motor cortex. J. Physiol. 1992; 453: 525–546.Feydy A., Carlier R., Roby-Brami A. et al. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 2002; 33: 1610–1617.Gerloff C., Bushara K., Sailer A. 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.Gould H.J., Cusick C.G., Pons T.P., Kaas J.H. The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys. J. Comp. Neurol. 1986; 247: 297–325.Heald A., Bates D., Cartlidge N.E. et al. Longitudinal study of central motor conduction time following stroke. 2. Central motor conduction measured within 72 h after stroke as a predictor of functional outcome at 12 months. Brain 1993; 116 (6): 1371–1385.Hebb D.O. The organization of behavior: A neurophysiological theory. New York: Wiley, 1949.Hummel F., Gerloff C. Larger interregional synchrony is associated with greater behavioral success in a complex sensory integration task in humans. Cereb. Cortex 2005; 15: 670–678.Hummel F., Kirsammer R., Gerloff C. Ipsilateral cortical activation during finger sequences of increasing complexity: representation of movement difficulty or memory load? Clin. Neurophysiol. 2003; 114: 605–613.Hutchinson S., Kobayashi M., Horkan C.M. et al. Age-related differences in movement representation. Neuroimage 2002; 17: 1720–1728.Jaillard A., Martin C.D., Garambois K. et al. Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. Brain 2005; 128 (5): 11122–11138.Jang S.H., Ahn S.H., Ha J.S. et al. Peri-infarct reorganization in a patient with corona radiate infarct: a combined study of functional MRI and diffusion tensor image tractography. Restor. Neurol. Neurosci. 2006; 24: 65–68.Jang S.H., Cho S.H., Kim Y.H. et al. Cortical activation changes associated with motor recovery in patients with precentral knob infarct. Neuroreport 2004; 1: 15: 395–399.Jang S.H., Cho S.H., Kim Y.H. et al. Diffusion anisotrophy in the early stages of stroke can predict motor outcome. Restor. Neurol. Neurosci. 2005; 23: 11–17.Karni A., Meyer G., Jezzard P. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 1995; 377: 155–158.Khedr E.M., Ahmed M.A., Fathy N., Rothwell J.C. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology 2005; 65 (3): 466–468.Kim Y.H., You S.H., Kwon Y.H. et al. Longitudinal fMRI study for locomotor recovery in patients with stroke. Neurology 2006; 67: 330–333.Kleim J.A., Chan S., Pringle E. et al. BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat. Neurosci. 2006; 9 (6): 735–737.Kobayashi M., Ng J., Theoret H., Pascual-Leone A. Modulation of intracortical neuronal circuits in human hand motor area by digit stimulation. Exp. Brain Res. 2003; 149: 1–8.Kocak M., Ulmer J.L., Ugurel M.S. et al. Motor Homunculus: Passive mapping in healthy volunteers by using functional MR Imaging—initial results. Radiology 2009; 251: 485–492.Konishi J., Yamada K., Kizu O. et al. MR tractography for the evaluation of functional recovery from lenticulostriate infarcts. Neurology 2005; 64: 108–113.Kujirai T., Caramia M.D., Rothwell J.C. et al. Corticocortical inhibition in human motor cortex. J. Physiol. 1993; 471: 501–519.Kunimatsu A., Aoki S., Masutani Y. et al. Three-dimensional white matter tractography by diffusion tensor imaging in ischaemic stroke involving the corticospinal tract. Neuroradiology 2003; 45: 532–535.Kunimatsu A., Aoki S., Masutani Y. et al. The optimal trackability threshold of fractional anisotropy for diffusion tensor tractography of the corticospinal tract. Magnetic resonance in medical sciences 2004; 1 (3): 11–17.Lawrence D.G., Kuypers H.G. Pyramidal and non-pyramidal pathways in monkeys: anatomical and functional correlation. Science 1965; 148: 973–975.Lawrence D.G., Kuypers H.G. The functional organization of the motor system in the monkey, I: the effect of bilateral pyramidal lesions. Brain 1968; 91: 1–14.Lee H., Gunraj C., Chen R. The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex. J. Physiol. 2007; 580: 1021–1032.Lee J.S., Han M-K., Kim S.H. et al. Fiber tracking by diffusion tensor imaging in corticospinal tract stroke: Topographical correlation with clinical symptoms. NeuroImage 2005; 26: 771–776.Leuner B., Falduto J., Shors T.J. Associative memory formation increases the observation of dendritic spines in the hippocampus. J. Neurosci. 2003; 23: 659–665.Liepert J., Hamzei F., Weiller C. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve 2000; 23: 1761–1763.Liepert J., Restemeyer C., Kucinski T. et al.Motor strokes: the lesion location determines motor excitability changes. Stroke 2005; 36 (12): 2648–2653.Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008; 453 (12): 869–878.Lotze M., Markert J., Sauseng P. et al. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J. Neurosci. 2006; 26: 6096–6102.Macaluso E.B., Cherubini А., Sabatini U. Bimanual passive movement: functional activation and inter-regional coupling. Frontiers in Integrative Neuroscience 2007; 1: article 5.Manganotti P., Gerloff C., Toro C. et al. Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr. Clin. Neurophysiol. 1998; 109: 50–62.Matthews P.M., Honey G.D., Bullmore E.T. Applications of fMRI in translational medicine and clinical practice. Nat. Rev. Neurosci. 2006; 7: 732–744.Merzenich M.M., Jenkins W.M. Reorganization of cortical representations of the hand following alterations of skin inputs induced by nerve injury, skin island transfers, and experience. J. Hand Ther. 1993; 6: 89–104.Mima T., Matsuoka T., Hallett M. Information flow from the sensorimotor cortex to muscle in humans. Clin. Neurophysiol. 2001a; 112: 122–126.Mori S., van Zijl P.C. Fiber tracking: principles and strategies—a technical review. NMR Biomed. 2002; 15: 468–480.Nardone R., Tezzon F. Inhibitory and excitatory circuits of cerebral cortex after ischaemic stroke: prognostic value of the transcranial magnetic stimulation. Electromyogr. Clin. Neurophysiol. 2002; 42 (3): 131–136.Nelles G., Jentzen W., Jueptner M. et al. Arm training induced brain plasticity in stroke studied with serial PET. Neuroimage 2001; 13 (6; 1): 1146–1154.Newton J., Sunderland A., Butterworth S.E. et al. A pilot study of event related functional magnetic resonance imaging of monitored wrist movements in patients with partial recovery. Stroke 2002; 33: 2881–2887.Newton J.M., Ward N.S., Parker G.J. et al. Non-invasive mapping corticofugal fibres from multiple motor areas – relevance to stroke recovery. Brain 2006; 129: 1844–1858.Nudo R.J., Wise B.M., SiFuentes F., Milliken G.W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 1996; 272: 1791–1794.Nudo R.J. Functional and structural plasticity in motor cortex: implications for stroke recovery. Phys. Med. Rehabil. Clin. N. Am. 2003; 14: S57–76.Nudo R.J. Remodeling of cortical motor representations after stroke: implications for recovery from brain damage. Mol. Psychiatry 1997; 2 (3): 188–191.Pennisi G., Rapisarda G., Bella R. et al. Absence of response to early transcranial magnetic stimulation in ischemic stroke patients. Prognostic value for hand motor recovery. Stroke 1999; 30: 2666–2670.Pineiro R., Pendlebury S., Johansen-Berg H., Matthews P.M. Functional MRI detects posterior shifts in primary sensorimotor cortex activation after stroke: evidence of local adaptive reorganization? Stroke 2001; 32: 1134–1139.Plewnia C., Lotze M., Gerloff C. Disinhibition of the contralateral motor cortex by low-frequency rTMS. Neuroreport 2003; 14: 609–612.Rogers B.P., Morgan V.L., Newton A.T., Gore J.C. Assessing functional connectivity in the human brain by fMRI. Magn. Reson Imaging 2007; 25 (10): 1347–1357.Rossini P.M. Tracking post-stroke recovery with magnetoencephalography. Ann. Neurol. 2001; 49: 136.Rossini P.M., Caltagirone C., Castriota-Scanderberg A. et al. Hand motor cortical area reorganization in stroke: a study with f MRI, MEG and TMS maps. NeuroReport 1998; 9: 2141–2146.Rossini P.M., Altamura C., Ferreri F. et al. Neuroimaging experimental studies on brain plasticity in recovery from stroke. Eura medicophys 2007; 43: 241–254.Rossini P.M., Altamura C., Ferretti A. et al. Does cerebrovascular disease affect the coupling between neuronal activity and local haemodinamics? Brain 2004 (b); 127: 99–110.Rossini P.M., Calautti C., Pauri F., Baron J.C. Post-stroke plastic reorganization in the adult brain. Lancet Neurol. 2003; 2: 493–502.Rossini P.M., Caramia M., Zarola F. Central motor tract propagation in man: studies with non-invasive, unifocal scalp stimulation. Brain Res. 1987; 415: 211–225.Rossini P.M., Dal Forno G. Integrated technology for evaluation of brain function and neural plasticity. Phys. Med. Rehabil. Clin. N. Am. 2004; 15: 263–306.Rother J., Knab R., Hamzei F. et al. Negative dip BOLD fMRI is caused by blood flow – oxygen consumption uncoupling in humans. Neuroimage 2002; 15: 98–102.Rouiller E.M., Moret V., Tanne J., Boussaoud D. Evidence for direct connections between the hand region of the supplementary motor area and cervical motoneurons in the macaque monkey. Eur. J. Neurosci. 1996; 8: 1055–1059.Sadato N., Campbell G., Ibanez V. et al. Complexity affects regional cerebral blood flow change during sequential finger movements. J. Neurosci. 1996; 16: 2691–2700.Seitz R.J., Hoflich P., Binkofski F. et al. Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch. Neurol. 1998; 55: 1081–1088.Shimizu T., Hosaki A., Hino T. et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 2002; 125: 1896–1907.Stefan K., Kunesch E., Benecke R., et al. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J. Physiol. 2002; 543: 699–708.Stefanovic B., Warnking J.M., Pike G.B. Hemodynamic and metabolic responses to neuronal inhibition. Neuroimage 2004; 22: 771–778.Stinear C.M., Barber P.A., Smale PR et al. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 2007 Jan.; 130 (1): 170–180.Strick P.L. Anatomical organization of multiple motor areas in te frontal lobe: implications for recovery of function. Adv. Neurol. 1988; 47: 293–312.Takeuchi N., Chuma T., Matsuo Y. et al. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 2005; 36 (12): 2681–2686.Talelli P., Rothwell J. Does brain stimulation after stroke have a future? Curr. Opin. Neurol. 2006; 19: 543–550.Tecchio F., Rossini P.M., Pizella V. et al. A neuromagnetic normative data set for hemispheric sensory hand cortical representations and thear interhemispheric differences. Brain Res. Brain Res. Protoc. 1998; 2: 306–314.Tecchio F., Pasqualetti P., Zappasodi F. Prognostic value of magnetoencephalography parameters in acute monohemispheric stroke. J. Neurol. In press 2007.Tecchio F., Rossini P.M., Pizzella V. Spatial properties and interhemispheric differences of the sensory hand cortical representation: a neuromagnetic study. Brain Res. 1997; 767: 100–108.Thomalla G., Glauche V., Koch M.A. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage 2004; 22: 1767–1774.Traversa R., Cicinelli P., Bassi A. et al. Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke 1997; 28 (1): 110–117.Turton A., Wroe S., Trepte N. et al. Contralateral and ipsilateral EMG responses to transcranial magnetic stimulation during recovery of arm and hand function after stroke. Electroencephalogr. Clin. Neurophysiol 1996; 101 (4): 316–328.107. Wang X.Q., Merzenich M.M., Sameshima K., Jenkins W.M. Remodeling of hand representation in adult cortex determined by timing of tactile stimulation. Nature 1995; 378: 71–75.Ward N.S. Future perspectives in functional neuroimaging in stroke recovery. Eura. medicophys. 2007; 43: 285–294.Ward N.S., Brown M.M., Thompson A.J., Frackowiak R.S. Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain 2003; 126: 1430–1448.Ward N.S., Frackowiak R.S. The functional anatomy of cerebral reorganization after focal brain injury. J.Physiol. Paris 2006 (b); 99: 425–436.Ward N.S., Newton J.M., Swayne O.B. et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 2006; 129 (Pt3): 809–819.Weder B., Knorr U., Herzog H. et al. Tactile exploration of shape after subcortical ischaemic infarction stadied with PET. Brain 1994; 11: 593–605.Weiller C., Chollet F., Friston K.J. et al. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann. Neurol. 1992; 31: 463–472.Weiller C., Ramsay S.C., Wise R.J. et al. Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann. Neurol. 1993; 33: 181–189.