Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface

Journal of Neurophysiology

Volumn 115, Issue 3, 2016, Pages 1410-1421

  Mrachacz Kersting, Natalie ^a   Jiang, Ning ^b   Thomas Stevenson, Andrew James ^a   Niazi, Imran Khan ^a   Kostic, Vladimir ^c   Pavlovic, Aleksandra ^c   Radovanovic, Sasa ^c   Djuric Jovicic, Milica ^d   Agosta, Federica ^e   Dremstrup, Kim ^a   Farina, Dario ^b  

^a AALBORG UNIVERSITY   (Denmark)

^b BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

^c UNIVERSITY OF BELGRADE   (Serbia)

^d Center of the School of Electrical Engineering in Belgrade   (Serbia)

^e VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Associativity; Brain computer interface; Hebb; Neuroplasticity; Stroke

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN COMPUTER INTERFACE; CEREBROVASCULAR ACCIDENT; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFUSION TENSOR IMAGING; DOUBLE BLIND PROCEDURE; ELECTRODE; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY PARAMETERS; FEMALE; FOOT AND HAND TAPPING FREQUENCY; HUMAN; IMAGE ANALYSIS; LONG TERM POTENTIATION; MALE; MIDDLE AGED; MIDDLE CEREBRAL ARTERY; MOTOR EVOKED POTENTIAL; MOTOR FUNCTION TEST; MOVEMENT RELATED CORTICAL POTENTIAL; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE STIMULATOR; NEUROPHYSIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PERONEUS NERVE; PRIORITY JOURNAL; PYRAMIDAL TRACT; QUANTITATIVE ANALYSIS; STROKE PATIENT; SYNAPSE; TIBIALIS ANTERIOR MUSCLE; TRANSCRANIAL MAGNETIC STIMULATION SYSTEM; WALKING SPEED; YOUNG ADULT; ASSOCIATION; CONVALESCENCE; FOOT; HAND; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; STROKE REHABILITATION;

ADULT; AGED; ASSOCIATION; BRAIN-COMPUTER INTERFACES; EVOKED POTENTIALS, MOTOR; FEMALE; FOOT; HAND; HUMANS; MALE; MIDDLE AGED; MUSCLE, SKELETAL; NEURONAL PLASTICITY; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; STROKE; STROKE REHABILITATION;

EID: 84971486925     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00918.2015     Document Type: Article

References (73)

1. Ang KK, Guan C, Chua KS, Ang BT, Kuah C, Wang C, Phua KS, Chin ZY, Zhang H. A clinical study of motor imagery-based brain-computer interface for upper limb robotic rehabilitation. Conf Proc IEEE Eng Med Biol Soc, 2009: 5981-5984, 2009.
2. Ang KK, Guan C, Chua KS, Ang BT, Kuah C, Wang C, Phua KS, Chin ZY, Zhang H. Clinical study of neurorehabilitation in stroke using EEGbased motor imagery brain-computer interface with robotic feedback. Conf Proc IEEE Eng Med Biol Soc, 2010: 5549-5552, 2010.
3. Ang KK, Guan C, Phua KS, Wang C, Zhou L, Tang KY, Ephraim Joseph GJ, Kuah CW, Chua KS. Brain-computer interface-based robotic end effector system for wrist and hand rehabilitation: results of a three-armed randomized controlled trial for chronic stroke. Front Neuroeng, 7: 30, 2014.
4. Avanzino L, Tacchino A, Abbruzzese G, Quartarone A, Ghilardi MF, Bonzano L, Ruggeri P, Bove M. Recovery of motor performance deterioration induced by a demanding finger motor task does not follow cortical excitability dynamics. Neuroscience, 174: 84-90, 2011.
5. Bawa P, Chalmers GR, Stewart H, Eisen AA. Responses of ankle extensor and flexor motoneurons to transcranial magnetic stimulation. J Neurophysiol 88: 124-132, 2002.
6. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther, 67: 2: 206-207, 1987.
7. Bonita R, Beaglehole R. Recovery of motor function after stroke. Stroke, 19: 1497-1500, 1988.
8. Broetz D, Braun C, Weber C, Soekadar SR, Caria A, Birbaumer N. Combination of brain-computer interface training and goal-directed physical therapy in chronic stroke: a case report. Neurorehabil Neural Repair, 24: 7: 674-679, 2010.
9. Brouwer B, Qiao J. Characteristics and variability of lower limb motoneuron responses to transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol, 97: 49-54, 1995.
10. Brown CE, Aminoltejari K, Erb H, Winship IR, Murphy TH. In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites. J Neurosci, 29: 1719-1734, 2009.
11. Buch E, Weber C, Cohen LG, Braun C, Dimyan MA, Ard T, Mellinger J, Caria A, Soekadar S, Fourkas A, Birbaumer N. Think to move: a neuromagnetic brain-computer interface (BCI) system for chronic stroke. Stroke, 39: 910-917, 2008.
12. Burridge JH, Taylor PN, Hagan SA, Wood DE, Swain ID. The effects of common peroneal stimulation on the effort and speed of walking: a randomized controlled trial with chronic hemiplegic patients. Clin Rehabil, 11: 201-210, 1997.
13. Chen Y, Chen L, Liu R, Wang Y, Chen XY, Wolpaw JR. Locomotor impact of beneficial or nonbeneficial H-reflex conditioning after spinal cord injury. J Neurophysiol, 111: 1249-1258, 2014.
14. Cincotti F, Pichiorri F, Arico P, Aloise F, Leotta F, de Vico Fallani F, Millan Jdel R, Molinari M, Mattia D. EEG-based brain-computer interface to support post-stroke motor rehabilitation of the upper limb. Conf Proc IEEE Eng Med Biol Soc, 2012: 4112-4115, 2012.
15. Daly JJ, Cheng R, Rogers J, Litinas K, Hrovat K, Dohring M. Feasibility of a new application of noninvasive brain computer interface (BCI): a case study of training for recovery of volitional motor control after stroke. J Neurol Phys Ther, 33: 203-211, 2009.
16. Dawes H, Enzinger C, Johansen-Berg H, Bogdanovic M, Guy C, Collett J, Izadi H, Stagg C, Wade D, Matthews P. Walking performance and its recovery in chronic stroke in relation to extent of lesion overlap with the descending motor tract. Exp Brain Res, 186: 325-333, 2008.
17. Djuric-Jovicic MD, Jovicic NS, Popovic DB. Kinematics of gait: new method for angle estimation based on accelerometers. Sensors (Basel), 11: 10571-10585, 2011.
18. Everaert DG, Thompson AK, Su LC, Stein RB. Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair, 24: 168-177, 2010.
19. Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med, 7: 13-31, 1975.
20. Grey MJ, Mazzaro N, Nielsen JB, Sinkjaer T. Ankle extensor proprioceptors contribute to the enhancement of the soleus EMG during the stance phase of human walking. Can J Physiol Pharmacol, 82: 610-616, 2004.
21. Hamilton M. Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol, 6: 278-296, 1967.
22. Hebb DO. The Organization of Behavior: a Neuropsychological Theory. Mahwah, NJ: Erlbaum, 1949.
23. Hendricks HT, Pasman JW, Merx JL, van Limbeek J, Zwarts MJ. Analysis of recovery processes after stroke by means of transcranial magnetic stimulation. J Clin Neurophysiol 20: 188-195, 2003a.
24. Hendricks HT, Pasman JW, van Limbeek J, Zwarts MJ. Motor evoked potentials of the lower extremity in predicting motor recovery and ambulation after stroke: a cohort study. Arch Phys Med Rehabil 84: 1373-1379, 2003b.
25. Heremans E, Helsen WF, De Poel HJ, Alaerts K, Meyns P, Feys P. Facilitation of motor imagery through movement-related cueing. Brain Res 1278: 50-58, 2009.
26. Jiang N, Gizzi L, Mrachacz-Kersting N, Dremstrup K, Farina D. A brain-computer interface for single-trial detection of gait initiation from movement related cortical potentials. Clin Neurophysiol, 126: 154-159, 2014.
27. Kasashima-Shindo Y, Fujiwara T, Ushiba J, Matsushika Y, Kamatani D, Oto M, Ono T, Nishimoto A, Shindo K, Kawakami M, Tsuji T, Liu M. Brain-computer interface training combined with transcranial direct current stimulation in patients with chronic severe hemiparesis: proof of concept study. J Rehabil Med, 47: 318-324, 2015.
28. Khaslavskaia S, Sinkjaer T. Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res, 162: 497-502, 2005.
29. Knash M, Kido A, Gorassini M, Chan KM, Stein R. Electrical stimulation of the human common peroneal nerve elicits lasting facilitation of cortical motor-evoked potentials. Exp Brain Res, 153: 366-377, 2003.
30. Kornhuber HH, Deecke L. Changes in the brain potential in voluntary movements and passive movements in man: readiness potential and reafferent potential. Pflügers Arch, 284: 1-17, 1965.
31. Kuhtz-Buschbeck JP, Mahnkopf C, Holzknecht C, Siebner H, Ulmer S, Jansen O. Effector-independent representations of simple and complex imagined finger movements: a combined fMRI and TMS study. Eur J Neurosci, 18: 3375-3387, 2003.
32. Kumpulainen S, Mrachacz-Kersting N, Peltonen J, Voigt M, Avela J. The optimal interstimulus interval and repeatability of paired associative stimulation when the soleus muscle is targeted. Exp Brain Res, 221: 241-249, 2012.
33. Leifert-Fiebach G, Welfringer A, Babinsky R, Brandt T. Motor imagery training in patients with chronic neglect: A pilot study. NeuroRehabilitation 32: 43-58, 2013.
34. Li M, Liu Y, Wu Y, Liu S, Jia J, Zhang L. Neurophysiological substrates of stroke patients with motor imagery-based brain-computer interface training. Int J Neurosci, 124: 403-415, 2014.
35. Lyden PD, Lu M, Levine SR, Brott TG, Broderick J, NINDS rtPA Stroke Study Group. A modified National Institutes of Health Stroke Scale for use in stroke clinical trials: preliminary reliability and validity. Stroke, 32: 1310-1317, 2001.
36. Lyons GM, Sinkjaer T, Burridge JH, Wilcox DJ. A review of portable FES-based neural orthoses for the correction of drop foot. IEEE Trans Neural Syst Rehabil Eng, 10: 260-279, 2002.
37. Mazzaro N, Grey M, do Nascimento O, Sinkjaer T. Afferent-mediated modulation of the soleus muscle activity during the stance phase of human walking. Exp Brain Res, 173: 713-723, 2006.
38. McFarland DJ, McCane LM, David SV, Wolpaw JR. Spatial filter selection for EEG-based communication. Electroencephalogr Clin Neurophysiol, 103: 386-394, 1997.
39. Mrachacz-Kersting N, Fong M, Murphy BA, Sinkjaer T. Changes in excitability of the cortical projections to the human tibialis anterior after paired associative stimulation. J Neurophysiol, 97: 1951-1958, 2007.
40. Mrachacz-Kersting N, Kristensen SR, Niazi IK, Farina D. Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity. J Physiol 590: 1669-1682, 2012a.
41. Mrachacz-Kersting N, Niazi IK, Jiang N, Pavlovic AM, Radovanovic S, Kostiç VS, Popovic DB, Dremstrup K, Farina D. A novel brain-computer interface for chronic stroke patients. In: Biosystems and Biorobotics: International Conference on Neurorehabilitation, Berlin: Springer, 2012b, p. 837-841.
42. Mukaino M, Ono T, Shindo K, Fujiwara T, Ota T, Kimura A, Liu M, Ushiba J. Efficacy of brain-computer interface-driven neuromuscular electrical stimulation for chronic paresis after stroke. J Rehabil Med, 46: 378-382, 2014.
43. Murphy TH, Corbett D. Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci, 10: 861-872, 2009.
44. Niazi IK, Jiang N, Tiberghien O, Feldbæk-Nielsen J, Dremstrup K, Farina D. Detection of movement intention from single-trial movement-related cortical potentials. J Neural Eng, 8: 066009, 2011.
45. Niazi IK, Mrachacz-Kersting N, Jiang N, Dremstrup K, Farina D. Peripheral electrical stimulation triggered by self-paced detection of motor intention enhances motor evoked potentials. IEEE Trans Neural Syst Rehabil Eng 20: 595-604, 2012.
46. Nielsen JB. How we walk: central control of muscle activity during human walking. Neuroscientist, 9: 195-204, 2003.
47. Nielsen JB. Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans. J Appl Physiol, 96: 1961-1967, 2004.
48. Nielsen JB, Sinkjaer T. Afferent feedback in the control of human gait. J Electromyogr Kinesiol, 12: 213-217, 2002.
49. Ono T, Shindo K, Kawashima K, Ota N, Ito M, Ota T, Mukaino M, Fujiwara T, Kimura A, Liu M, Ushiba J. Brain-computer interface with somatosensory feedback improves functional recovery from severe hemiplegia due to chronic stroke. Front Neuroeng, 7: 19, 2014.
50. Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74: 1037-1045, 1995.
51. Pavlides C, Miyashita E, Asanuma H. Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. J Neurophysiol, 70: 733-741, 1993.
52. Perez MA, Lungholt BK, Nyborg K, Nielsen JB. Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res, 159: 197-205, 2004.
53. Peters M. Neuropsychological identification of motor problems: can we learn something from the feet and legs that hands and arms will not tell us? Neuropsychol Rev, 1: 165-183, 1990.
54. Petersen NT, Pyndt HS, Nielsen JB. Investigating human motor control by transcranial magnetic stimulation. Exp Brain Res, 152: 1-16, 2003.
55. Pichiorri F, Morone G, Petti M, Toppi J, Pisotta I, Molinari M, Paolucci S, Inghilleri M, Astolfi L, Cincotti F, Mattia D. Brain-computer interface boosts motor imagery practice during stroke recovery. Ann Neurol, 77: 851-865, 2015.
56. Piron L, Piccione F, Tonin P, Dam M. Clinical correlation between motor evoked potentials and gait recovery in poststroke patients. Arch Phys Med Rehabil, 86: 1874-1878, 2005.
57. Platz T, Kim IH, Pintschovius H, Winter T, Kieselbach A, Villringer K, Kurth R, Mauritz KH. Multimodal EEG analysis in man suggests impairment- specific changes in movement-related electric brain activity after stroke. Brain, 123: 2475-2490, 2000.
58. Ramos-Murguialday A, Broetz D, Rea M, Laer L, Yilmaz O, Brasil FL, Liberati G, Curado MR, Garcia-Cossio E, Vyziotis A, Cho W, Agostini M, Soares E, Soekadar S, Caria A, Cohen LG, Birbaumer N. Brainmachine interface in chronic stroke rehabilitation: a controlled study. Ann Neurol, 74: 100-108, 2013.
59. Salinet AS, Robinson TG, Panerai RB. Reproducibility of cerebral and peripheral haemodynamic responses to active, passive and motor imagery paradigms in older healthy volunteers: a fTCD study. J Neurosci Methods 206: 143-150, 2012.
60. Silvoni S, Ramos-Murguialday A, Cavinato M, Volpato C, Cisotto G, Turolla A, Piccione F, Birbaumer N. Brain-computer interface in stroke: a review of progress. Clin EEG Neurosci, 42: 245-252, 2011.
61. Sinkjaer T, Andersen JB, Ladouceur M, Christensen LO, Nielsen JB. Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol, 523: 817-827, 2000.
62. Song J, Young BM, Nigogosyan Z, Walton LM, Nair VA, Grogan SW, Tyler ME, Farrar-Edwards D, Caldera KE, Sattin JA, Williams JC, Prabhakaran V. Characterizing relationships of DTI, fMRI, and motor recovery in stroke rehabilitation utilizing brain-computer interface technology. Front Neuroeng, 7: 31, 2014.
63. Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol, 543: 699-708, 2002.
64. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain, 130: 170-180, 2007.
65. Teo WP, Chew E. Is motor-imagery brain-computer interface feasible in stroke rehabilitation? PM R, 6: 723-728, 2014.
66. Thompson AK, Stein RB. Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res, 159: 491-500, 2004.
67. Thompson AK, Wolpaw JR. Restoring walking after spinal cord injury: operant conditioning of spinal reflexes can help. Neuroscientist, 21: 203-215, 2015.
68. Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, Cassol E, Chollet F. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage, 23: 827-839, 2004.
69. Walter WG, Cooper R, Aldridge VJ, McCallum WC, Winter AL. Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature, 203: 380-384, 1964.
70. Wolpaw JR. Spinal cord plasticity in acquisition and maintenance of motor skills. Acta Physiol, 189: 155-169, 2007.
71. Xu R, Jiang N, Mrachacz-Kersting N, Lin C, Asin Prieto G, Moreno JC, Pons JL, Dremstrup K, Farina D. A closed-loop braincomputer interface triggering an active ankle-foot orthosis for inducing cortical neural plasticity. IEEE Trans Biomed Eng, 61: 2092-2101, 2014.
72. Yilmaz O, Cho W, Braun C, Birbaumer N, Ramos-Murguialday A. Movement related cortical potentials in severe chronic stroke. Conf Proc IEEE Eng Med Biol Soc, 2013: 2216 -2219, 2013.
73. Young BM, Nigogosyan Z, Walton LM, Song J, Nair VA, Grogan SW, Tyler ME, Edwards DF, Caldera K, Sattin JA, Williams JC, Prabhakaran V. Changes in functional brain organization and behavioral correlations after rehabilitative therapy using a brain-computer interface. Front Neuroeng, 7: 26, 2014.