Inter-hemispheric coupling changes associate with motor improvements after robotic stroke rehabilitation

Restorative Neurology and Neuroscience

Volumn 30, Issue 6, 2012, Pages 497-510

  Pellegrino, G ^a   Tomasevic, L ^b   Tombini, M ^a   Assenza, G ^a   Bravi, M ^c   Sterzi, S ^c   Giacobbe, V ^c   Zollo, L ^c   Guglielmelli, E ^c   Cavallo, G ^c   Vernieri, F ^a   Tecchio, F ^b  

^a Department of Neurology Campus Bio Medico University ^*  (Italy)

^b FATEBENEFRATELLI HOSPITAL   (Italy)

^c UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

Chronic stroke; Functional Source Separation (FSS); interhemispheric coherence; primary somatosensory hand area (S1); resting state EEG; robotic rehabilitation

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN FUNCTION; BRAIN PLASTIC REORGANIZATION; CEREBROVASCULAR ACCIDENT; CHRONIC DISEASE; CLINICAL ARTICLE; ELECTROENCEPHALOGRAPHY; FEMALE; FUGL MEYER ASSESSMENT SCALE; FUNCTIONAL SOURCE SEPARATION METHOD; HUMAN; MALE; MIDDLE CEREBRAL ARTERY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; NERVE CELL PLASTICITY; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; PROCEDURES; RATING SCALE; ROBOTICS; STROKE PATIENT; TASK PERFORMANCE; VISUAL FEEDBACK;

EID: 84872228103     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-2012-120227     Document Type: Article

References (60)

1. Allison, T., McCarthy, G., Wood, C.C. & Jones, S.J. (1991). Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. Brain, 114, 2465-2503.
2. Alonso, J.M., Usrey,W.M.&Reid, R.C. (1996). Precisely correlated firing in cells of the lateral geniculate nucleus. Nature, 383, 815-819.
3. Altamura, C., Torquati, K., Zappasodi, F., Ferretti, A., Pizzella, V., Tibuzzi, F., Vernieri, F., Pasqualetti, P., Landi, D., Del Gratta, C., Romani, G.-L., Maria Rossini, P. & Tecchio, F. (2007). fMRI-vs-MEG evaluation of post-stroke interhemispheric asymmetries in primary sensorimotor hand areas. Exp Neurol, 204, 631-639.
4. Barbati, G., Porcaro, C., Zappasodi, F., Rossini, P.M. & Tecchio, F. (2004). Optimization of an independent component analysis approach for artifact identification and removal in magnetoencephalographic signals. Clin Neurophysiol, 115, 1220-1232.
5. Barbati, G., Sigismondi, R., Zappasodi, F., Porcaro, C., Graziadio, S., Valente, G., Balsi, M., Rossini, P.M. & Tecchio, F. (2006). Functional source separation from magnetoencephalographic signals. Hum Brain Mapp, 27, 925-34.
6. Brochard, S., Robertson, J., Medee, B. & Remy-Neris, O. (2010). What's new in new technologies for upper extremity rehabilitation? Curr Opin Neurol, 23, 683-687.
7. 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. (2010). Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol, 67, 365-375.
8. Conchou, F., Loubinoux, I., Castel-Lacanal, E., Le Tinnier, A., Gerdelat-Mas, A., Faure-Marie, N., Gros, H., Thalamas, C., Calvas, F., Berry, I., Chollet, F.&Simonetta Moreau, M. (2009). Neural substrates of low-frequency repetitive transcranial magnetic stimulation duringmovement in healthy subjects and acute stroke patients.APET study. Hum Brain Mapp, 30, 2542-2557.
9. Cramer, S.C. (2008). Repairing the human brain after stroke. II. Restorative therapies. Ann Neurol, 63, 549-560.
10. Cramer, S.C., Sur,M., Dobkin, B.H., O'Brien, C., Sanger, T.D., Trojanowski, J.Q., Rumsey, J.M., Hicks, R., Cameron, J., Chen, D., Chen,W.G., Cohen, L.G., deCharms, C., Duffy, C.J., Eden, G.F., Fetz, E.E., Filart, R., Freund, M., Grant, S.J., Haber, S., Kalivas, P.W., Kolb, B., Kramer, A.F., Lynch, M., Mayberg, H.S., McQuillen, P.S., Nitkin, R., Pascual-Leone, A., Reuter-Lorenz, P., Schiff, N., Sharma, A., Shekim, L., Stryker, M., Sullivan, E.V. & Vinogradov, S. (2011). Harnessing neuroplasticity for clinical applications. Brain, 134, 1591-1609.
11. 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. (2009). Evaluation of the brain network organization from EEG signals: A preliminary evidence in stroke patient. Anat Rec (Hoboken), 292, 2023-2031.
12. Deco, G.&Corbetta, M. (2011). The dynamical balance of the brain at rest. Neuroscientist, 17, 107-123.
13. Dimyan, M.A. & Cohen, L.G. (2011). Neuroplasticity in the context of motor rehabilitation after stroke. Nat Rev Neurol, 7, 76-85.
14. Engel, A.K.&Fries, P. (2010). Beta-band oscillations-signalling the status quo? Curr Opin Neurobiol, 20, 156-165.
15. Floel, A., Nagorsen, U., Werhahn, K.J., Ravindran, S., Birbaumer, N., Knecht, S. & Cohen, L.G. (2004). Influence of somatosensory input on motor function in patients with chronic stroke. Ann Neurol, 56, 206-212.
16. Forss, N., Hietanen, M., Salonen, O. & Hari, R. (1999). Modified activation of somatosensory cortical network in patients with right-hemisphere stroke. Brain, 122, 1889-1899.
17. Gerloff, C., Bushara, K., Sailer, A., Wassermann, E.M., Chen, R., Matsuoka,T.,Waldvogel, D.,Wittenberg, G.F., Ishii, K., Cohen, L.G.&Hallett, M. (2006). Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain, 129, 791-808.
18. Grefkes, C., Nowak, D.A., Eickhoff, S.B., Dafotakis, M., Kust, J., Karbe, H. & Fink, G.R. (2008). Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol, 63, 236-246.
19. Grefkes, C., Nowak, D.A., Wang, L.E., Dafotakis, M., Eickhoff, S.B. & Fink, G.R. (2010). Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage, 50, 233-242.
20. Grefkes, C. & Fink, G.R. (2011). Reorganization of cerebral networks after stroke: New insights from neuroimaging with connectivity approaches. Brain, 134, 1264-1276.
21. Krebs, H.I., Volpe, B.T., Williams, D., Celestino, J., Charles, S.K., Lynch, D. & Hogan, N. (2007). Robot-aided neurorehabilitation: A robot for wrist rehabilitation. IEEE Trans Neural Syst Rehabil Eng, 15, 327-335.
22. Kwakkel, G., Kollen, B.J. & Krebs, H.I. (2008). Effects of robotassisted therapy on upper limb recovery after stroke: A systematic review. Neurorehabil Neural Repair, 22, 111-121.
23. Landi, D. & Rossini, P.M. (2010). Cerebral restorative plasticity from normal ageing to brain diseases: A "never ending story". Restor Neurol Neurosci, 28, 349-366.
24. Laufer, Y. & Elboim-Gabyzon, M. (2011). Does sensory transcutaneous electrical stimulation enhance motor recovery following a stroke? A systematic review. Neurorehabil Neural Repair, 25, 799-809.
25. Lee, H., Gunraj, C. & Chen, R. (2007). The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex. J Physiol, 580, 1021-1032.
26. Lo, A.C., Guarino, P.D., Richards, L.G., Haselkorn, J.K., Wittenberg, G.F., Federman, D.G., Ringer, R.J.,Wagner, T.H., Krebs, H.I., Volpe, B.T., Bever, C.T., Bravata, D.M., Duncan, P.W., Corn, B.H., Maffucci, A.D., Nadeau, S.E., Conroy, S.S., Powell, J.M., Huang, G.D. & Peduzzi, P. (2010). Robot-assisted therapy for long-term upper-limb impairment after stroke. N Engl J Med, 362, 1772-1783.
27. Mansur, C.G., Fregni, F., Boggio, P.S., Riberto, M., Gallucci-Neto, J., Santos, C.M., Wagner, T., Rigonatti, S.P., Marcolin, M.A. & Pascual-Leone, A. (2005). A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology, 64, 1802-1804.
28. Murase, N., Duque, J., Mazzocchio, R. & Cohen, L.G. (2004). Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol, 55, 400-409.
29. Muthukumaraswamy, S.D. & Singh, K.D. (2008). Spatiotemporal frequency tuning of BOLD and gamma band MEG responses compared in primary visual cortex. Neuroimage, 40, 1552-1560.
30. Nowak, D.A., Grefkes, C., Dafotakis, M., Eickhoff, S., Kust, J., Karbe, H. & Fink, G.R. (2008). Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol, 65, 741-747.
31. Nudo, R.J., Wise, B.M., SiFuentes, F. & Milliken, G.W. (1996). Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science, 272, 1791-1794.
32. Oliveri, M., Rossini, P.M., Traversa, R., Cicinelli, P., Filippi, M.M., Pasqualetti, P., Tomaiuolo, F. & Caltagirone, C. (1999). Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. Brain, 122, 1731-1739.
33. Pascual-Marqui, R.D. (2002). Methods Find Exp Clin Pharmacol. Methods and Findings in Experimental and Clinical Pharmacology, 24(Suppl D), 5-12.
34. Porcaro, C., Barbati, G., Zappasodi, F., Rossini, P.M. & Tecchio, F. (2008). Hand sensory-motor cortical network assessed by functional source separation. Hum Brain Mapp, 29, 70-81.
35. Porcaro, C., Coppola, G., Di Lorenzo, G., Zappasodi, F., Siracusano, A., Pierelli, F., Rossini, P.M., Tecchio, F. & Seri, S. (2009). Hand somatosensory subcortical and cortical sources assessed by functional source separation: An EEG study. Hum Brain Mapp, 30, 660-674.
36. Roger, V.L., Go, A.S., Lloyd-Jones, D.M., Adams, R.J., Berry, J.D., Brown, T.M., Carnethon, M.R., Dai, S., de Simone, G., Ford, E.S., Fox, C.S., Fullerton, H.J., Gillespie, C., Greenlund, K.J., Hailpern, S.M., Heit, J.A., Ho, P.M., Howard, V.J., Kissela, B.M., Kittner, S.J., Lackland, D.T., Lichtman, J.H., Lisabeth, L.D., Makuc, D.M., Marcus, G.M., Marelli, A., Matchar, D.B., McDermott, M.M., Meigs, J.B., Moy, C.S., Mozaffarian, D., Mussolino, M.E., Nichol, G., Paynter, N.P., Rosamond, W.D., Sorlie, P.D., Stafford, R.S., Turan, T.N., Turner, M.B., Wong, N.D. & Wylie-Rosett, J. (2011). American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2011 update: A report from the American Heart Association. Circulation, 123(4), e18-e209.
37. Epub 2010 Dec 15. Rossini, P.M., Tecchio, F., Pizzella, V., Lupoi, D., Cassetta, E., Pasqualetti, P., Romani, G.L. & Orlacchio, A. (1998). On the reorganization of sensory hand areas after mono-hemispheric lesion: A functional (MEG)/anatomical (MRI) integrative study. Brain Res, 782, 153-166.
38. Rossini, P.M., Tecchio, F., Pizzella, V., Lupoi, D., Cassetta, E., Pasqualetti, P. & Paqualetti, P. (2001). Interhemispheric differences of sensory hand areas after monohemispheric stroke: MEG/MRI integrative study. Neuroimage, 14, 474-485.
39. Rossini, P.M., Calautti, C., Pauri, F. & Baron, J.-C. (2003). Poststroke plastic reorganisation in the adult brain. Lancet Neurol, 2, 493-502.
40. Rossini, P.M., Altamura, C., Ferretti, A., Vernieri, F., Zappasodi, F., Caulo, M., Pizzella,V., Del Gratta, C., Romani, G.L.&Tecchio, F. (2004). Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? Brain, 127, 99-110.
41. Shimizu, T., Hosaki, A., Hino, T., Sato, M., Komori, T., Hirai, S. & Rossini, P.M. (2002). Motor cortical disinhibition in the unaf fected hemisphere after unilateral cortical stroke. Brain, 125, 1896-1907.
42. Siegel, M., Donner, T.H.&Engel, A.K. (2012). Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci, 13, 121-134.
43. Sivan, M., O'Connor, R.J., Makower, S., Levesley, M. & Bhakta, B. (2011). Systematic review of outcome measures used in the evaluation of robot-assisted upper limb exercise in stroke. J Rehabil Med, 43, 181-189.
44. Strens, L.H.A., Asselman, P., Pogosyan, A., Loukas, C., Thompson, A.J. & Brown, P. (2004). Corticocortical coupling in chronic stroke: Its relevance to recovery. Neurology, 63, 475-484.
45. Szurhaj, W. & Derambure, P. (2006). Intracerebral study of gamma oscillations in the human sensorimotor cortex. Prog Brain Res, 159, 297-310.
46. Takeuchi, N., Tada, T., Toshima, M.&Ikoma, K. (2010). Correlation of motor function with transcallosal and intracortical inhibition after stroke. J Rehabil Med, 42, 962-966.
47. Tecchio, F., Zappasodi, F., Tombini, M., Oliviero, A., Pasqualetti, P., Vernieri, F., Ercolani, M., Pizzella, V. & Rossini, P.M. (2006). Brain plasticity in recovery from stroke: An MEG assessment. Neuroimage, 32, 1326-1334.
48. Tecchio, F., Graziadio, S., Barbati, G., Sigismondi, R., Zappasodi, F., Porcaro, C., Valente, G., Balsi, M. & Rossini, P.M. (2007). Somatosensory dynamic gamma-band synchrony: A neural code of sensorimotor dexterity. Neuroimage, 35, 185-193.
49. Tecchio, F., Porcaro, C., Barbati, G. & Zappasodi, F. (2007). Functional source separation and hand cortical representation for a brain-computer interface feature extraction. J Physiol, 580, 703-721.
50. Tecchio, F., Zappasodi, F., Tombini, M., Caulo, M., Vernieri, F. & Rossini, P.M. (2007). Interhemispheric asymmetry of primary hand representation and recovery after stroke: A MEG study. Neuroimage, 36, 1057-1064.
51. Tecchio, F., Zappasodi, F., Porcaro, C., Barbati, G., Assenza, G., Salustri, C. & Rossini, P.M. (2008). High-gamma band activity of primary hand cortical areas: A sensorimotor feedback efficiency index. Neuroimage, 40, 256-264.
52. Tombini, M., Zappasodi, F., Zollo, L., Pellegrino, G., Cavallo, G., Tecchio, F., Guglielmelli, E. & Rossini, P.M. (2009). Brain activity preceding a 2D manual catching task. Neuroimage, 47, 1735-1746.
53. Traversa, R., Cicinelli, P., Pasqualetti, P., Filippi, M.&Rossini, P.M. (1998). Follow-up of interhemispheric differences of motor evoked potentials from the 'affected' and 'unaffected' hemispheres in human stroke. Brain Res, 803, 1-8.
54. van Meer, M.P., van der Marel, K., Wang, K., Otte, W.M., El Bouazati, S., Roeling, T.A., Viergever, M.A., Berkelbach van der Sprenkel, J.W. & Dijkhuizen, R.M. (2010). Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci, 30, 3964-3972.
55. Volpe, B.T., Huerta, P.T., Zipse, J.L., Rykman, A., Edwards, D., Dipietro, L., Hogan, N. & Krebs, H.I. (2009). Robotic devices as therapeutic and diagnostic tools for stroke recovery. Arch Neurol, 66, 1086-1090.
56. 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. (2010). Dynamic functional reorganization of the motor execution network after stroke. Brain, 133, 1224-1238.
57. Wheaton, L.A., Bohlhalter, S., Nolte, G., Shibasaki, H., Hattori, N., Fridman, E., Vorbach, S., Grafman, J. & Hallett, M. (2008). Cortico-cortical networks in patients with ideomotor apraxia as revealed by EEG coherence analysis. Neurosci Lett, 433, 87-92.
58. Wikstrom, H., Roine, R.O., Aronen, H.J., Salonen, O., Sinkkonen, J., Ilmoniemi, R.J. & Huttunen, J. (2000). Specific changes in somatosensory evoked magnetic fields during recovery from sensorimotor stroke. Ann Neurol, 47, 353-360.
59. Zollo, L., Gallotta, E., Guglielmelli, E. & Sterzi, S. (2011). Robotic technologies and rehabilitation: new tools for upper-limb therapy and assessment in chronic stroke. Eur J Phys Rehabil Med, 47, 223-236.
60. Zollo, L., Rossini, L., Bravi, M., Magrone, G., Sterzi, S. & Guglielmelli, E. (2011). Quantitative evaluation of upper-limb motor control in robot-aided rehabilitation. Med Biol Eng Comput, 49, 1131-1144.