Increased reward in ankle robotics training enhances motor control and cortical efficiency in stroke

Journal of Rehabilitation Research and Development

Volumn 51, Issue 2, 2014, Pages 213-227

  Goodman, Ronald N ^a   Rietschel, Jeremy C ^a   Roy, Anindo ^a,b   Jung, Brian C ^a,b   Diaz, Jason ^a   Macko, Richard F ^a,b   Forrester, Larry W ^a,b  

^a BALTIMORE VA MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Ankle robotics; Anklebot; Chronic hemiparetic stroke; Cognitive motor learning; EEG; EEG coherence; EEG spectral power; Gait; Plasticity; Reward

Indexed keywords

ELECTROENCEPHALOGRAPHY; HUMAN REHABILITATION EQUIPMENT; PLASTICITY; RESEARCH;

ANKLEBOT; CHRONIC HEMIPARETIC STROKE; EEG COHERENCES; GAIT; MOTOR LEARNING; REWARD; SPECTRAL POWER;

ROBOTICS;

ADULT; AGED; ANKLE; ARTICLE; BRAIN CORTEX; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; CLINICAL TRIAL; ELECTRODE; ELECTROENCEPHALOGRAPHY; FEMALE; GAIT; GAIT ORTHOSIS; GAME; HUMAN; IMPEDANCE; INTERVENTION STUDY; JOINT MOBILITY; LEARNING CURVE; MALE; MIDDLE AGED; MOTOR CONTROL; MOTOR PERFORMANCE; MUSCLE LENGTH; MUSCLE TRAINING; NERVE CELL PLASTICITY; PARESIS; PILOT STUDY; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; REHABILITATION MEDICINE; REWARD; ROBOTICS; TASK PERFORMANCE; CONTROLLED STUDY; CONVALESCENCE; FOLLOW UP; GAIT DISORDERS, NEUROLOGIC; KINESIOTHERAPY; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; STROKE; TREATMENT OUTCOME; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANKLE; EXERCISE THERAPY; FEMALE; FOLLOW-UP STUDIES; GAIT DISORDERS, NEUROLOGIC; HUMANS; MALE; MIDDLE AGED; MOTOR ACTIVITY; RECOVERY OF FUNCTION; ROBOTICS; STROKE; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84900869921     PISSN: 07487711     EISSN: 19381352     Source Type: Journal    
DOI: 10.1682/JRRD.2013.02.0050     Document Type: Article

References (67)

1. American Heart Association [Internet]. Heart and stroke statistics 2010. Dallas (TX): AHA; 2014. Available from: http://www.heart.org/HEARTORG/General/Heart-and-Stroke- Association%20Statistics_UCM_319064_SubHomePage.jsp
2. Medicare.gov [Internet]. Health database. Baltimore (MD): Centers for Medicare and Medicaid Services; 2012. Available from: https://data.medicare.gov/
3. Hachinski V, Iadecola C, Petersen RC, Breteler MM, Nyenhuis DL, Black SE, Powers WJ, DeCarli C, Merino JG, Kalaria RN, Vinters HV, Holtzman DM, Rosenberg GA, Wallin A, Dichgans M, Marler JR, Leblanc GG. National Institute of Neurological Disorders and Stroke-Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke. 2006;37(9):2220-41. [PMID:16917086] http://dx.doi.org/10.1161/01.STR.0000237236.88823.47
4. Jørgensen HS, Nakayama H, Raaschou HO, Olsen TS. Recovery of walking function in stroke patients: The Copenhagen Stroke Study. Arch Phys Med Rehabil. 1995; 76(1):27-32. [PMID:7811170] http://dx.doi.org/10.1016/S0003-9993(95)80038-7
5. Forster A, Young J. Incidence and consequences of falls due to stroke: A systematic inquiry. BMJ. 1995;311(6997): 83-86. [PMID:7613406] http://dx.doi.org/10.1136/bmj.311.6997.83
6. Dennis MS, Lo KM, McDowall M, West T. Fractures after stroke: frequency, types, and associations. Stroke. 2002; 33(3):728-34. [PMID:11872896] http://dx.doi.org/10.1161/hs0302.103621
7. Kanis J, Oden A, Johnell O. Acute and long-term increase in fracture risk after hospitalization for stroke. Stroke. 2001;32(3):702-6. [PMID:11239190] http://dx.doi.org/10.1161/01.STR.32.3.702
8. Krakauer JW. Motor learning: Its relevance to stroke recovery and neurorehabilitation. Curr Opin Neurol. 2006;19(1): 84-90. [PMID:16415682] http://dx.doi.org/10.1097/01.wco.0000200544.29915.cc
9. Macko RF, Ivey FM, Forrester LW, Hanley D, Sorkin JD, Katzel LI, Silver KH, Goldberg AP. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke: a randomized, controlled trial. Stroke. 2005;36(10):2206-11. [PMID:16151035] http://dx.doi.org/10.1161/01.STR.0000181076.91805.89
10. Forrester LW, Roy A, Krebs HI, Macko RF. Ankle training with a robotic device improves hemiparetic gait after a stroke. Neurorehabil Neural Repair. 2011;25(4):369-77. [PMID:21115945] http://dx.doi.org/10.1177/1545968310388291
11. Roy A, Forrester LW, Macko RF. Short-term ankle motor performance with ankle robotics training in chronic hemiparetic stroke. J Rehabil Res Dev. 2011;48(4):417-29. [PMID:21674391] http://dx.doi.org/10.1682/JRRD.2010.04.0078
12. Roy A, Forrester LW, Macko RF, Krebs HI. Changes in passive ankle stiffness and its effects on gait function in people with chronic stroke. J Rehabil Res Dev. 2013;50(4): 555-72. [PMID:23934875] http://dx.doi.org/10.1682/JRRD.2011.10.0206
13. Barbeau H, Visintin M. Optimal outcomes obtained with body-weight support combined with treadmill training in stroke subjects. Arch Phys Med Rehabil. 2003;84(10): 1458-65. [PMID:14586912] http://dx.doi.org/10.1016/S0003-9993(03)00361-7
14. Krebs HI, Hogan N, Aisen ML, Volpe BT. Robot-aided neurorehabilitation. IEEE Trans Rehabil Eng. 1998;6(1): 75-87. [PMID:9535526] http://dx.doi.org/10.1109/86.662623
15. Mehrholz J, Werner C, Kugler J, Pohl M. Electromechanical- assisted training for walking after stroke. Cochrane Database Syst Rev. 2007;(4):CD006185. [PMID:17943893]
16. Moseley AM, Stark A, Cameron ID, Pollock A. Treadmill training and body weight support for walking after stroke. Cochrane Database Syst Rev. 2003;(3):CD002840. [PMID:12917932]
17. Duncan PW, Sullivan KJ, Behrman AL, Azen SP, Wu SS, Nadeau SE, Dobkin BH, Rose DK, Tilson JK, Cen S, Hayden SK; LEAPS Investigative Team. Body-weightsupported treadmill rehabilitation after stroke. N Engl J Med. 2011;364(21):2026-36. [PMID:21612471] http://dx.doi.org/10.1056/NEJMoa1010790
18. Luft AR, Macko RF, Forrester LW, Villagra F, Ivey F, Sorkin JD, Whitall J, McCombe-Waller S, Katzel L, Goldberg AP, Hanley DF. Treadmill exercise activates subcortical neural networks and improves walking after stroke: A randomized controlled trial. Stroke. 2008;39(12):3341-50. [PMID:18757284] http://dx.doi.org/10.1161/STROKEAHA.108.527531
19. Luft AR, Forrester L, Macko RF, McCombe-Waller S, Whitall J, Villagra F, Hanley DF. Brain activation of lower extremity movement in chronically impaired stroke survivors. Neuroimage. 2005;26(1):184-94. [PMID:15862218] http://dx.doi.org/10.1016/j.neuroimage.2005.01.027
20. Huang VS, Krakauer JW. Robotic neurorehabilitation: A computational motor learning perspective. J Neuroeng Rehabil. 2009;6:5. [PMID:19243614] http://dx.doi.org/10.1186/1743-0003-6-5
21. Rijntjes M. Mechanisms of recovery in stroke patients with hemiparesis or aphasia: New insights, old questions and the meaning of therapies. Curr Opin Neurol. 2006;19(1):76-83. [PMID:16415681] http://dx.doi.org/10.1097/01.wco.0000203886.28068.38
22. Nashner LM, McCollum G. The organization of human postural movements: A formal basis and experimental synthesis. Behav Brain Sci. 1985;8(1):135-50. http://dx.doi.org/10.1017/S0140525X00020008
23. Winter DA. Human balance and posture control during standing and walking. Gait Posture. 1995;3(4):193-214. http://dx.doi.org/10.1016/0966-6362(96)82849-9
24. Rohrer B, Fasoli S, Krebs HI, Hughes R, Volpe B, Frontera WR, Stein J, Hogan N. Movement smoothness changes during stroke recovery. J Neurosci. 2002;22(18):8297-8304. [PMID:12223584]
25. Rohrer B. Evolution of movement smoothness and submovement patterns in persons with stroke [dissertation]. [Cambridge, MA]: Massachusetts Institute of Technology; 2002.
26. Goodman RN, Rietschel JC, Roy A, Jung BC, Diaz J, Macko RF, Forrester LW. Oral presentation: The efficacy and mechanisms of robot-assisted therapies in neurorehabilitation. 10th Annual World Conference of the Society for Brain Mapping and Therapeutics; 2013 May; Baltimore, MD.
27. Bromberg-Martin ES, Matsumoto M, Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron. 2010;68(5):815-34. [PMID:21144997] http://dx.doi.org/10.1016/j.neuron.2010.11.022
28. Pleger B, Ruff CC, Blankenburg F, Klöppel S, Driver J, Dolan RJ. Influence of dopaminergically mediated reward on somatosensory decision-making. PLoS Biol. 2009;7 (7): e1000164. [PMID:19636360] http://dx.doi.org/10.1371/journal.pbio.1000164
29. Hosp JA, Pekanovic A, Rioult-Pedotti MS, Luft AR. Dopaminergic projections from midbrain to primary motor cortex mediate motor skill learning. J Neurosci. 2011;31(7): 2481-87. [PMID:21325515] http://dx.doi.org/10.1523/JNEUROSCI.5411-10.2011
30. Kringelbach ML, Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology. Prog Neurobiol. 2004;72(5): 341-72. [PMID:15157726] http://dx.doi.org/10.1016/j.pneurobio.2004.03.006
31. LeDoux JE. The synaptic self: How our brains become who we are. New York (NY): Viking; 2002.
32. Schultheiss OC, Wirth MM, Waugh CE, Stanton SJ, Meier EA, Reuter-Lorenz P. Exploring the motivational brain: Effects of implicit power motivation on brain activation in response to facial expressions of emotion. Soc Cogn Affect Neurosci. 2008;3(4):333-43. [PMID:19015083] http://dx.doi.org/10.1093/scan/nsn030
33. Small DM, Gitelman D, Simmons K, Bloise SM, Parrish T, Mesulam MM. Monetary incentives enhance processing in brain regions mediating top-down control of attention. Cereb Cortex. 2005;15(12):1855-65. [PMID:15746002] http://dx.doi.org/10.1093/cercor/bhi063
34. Engelmann JB, Pessoa L. Motivation sharpens exogenous spatial attention. Emotion. 2007;7(3):668-74. [PMID:17683222] http://dx.doi.org/10.1037/1528-3542.7.3.668
35. Pessoa L. How do emotion and motivation direct executive control? Trends Cogn Sci. 2009;13(4):160-66. [PMID:19285913] http://dx.doi.org/10.1016/j.tics.2009.01.006
36. Scudder MR, Drollette ES, Pontifex MB, Hillman CH. Neuroelectric indices of goal maintenance following a single bout of physical activity. Biol Psychol. 2012;89(2): 528-31. [PMID:22200656] http://dx.doi.org/10.1016/j.biopsycho.2011.12.009
37. Schmidt RA, Wrisberg CA. Motor learning and performance: A situation-based learning approach. Champaign (IL): Human Kinetics; 2008.
38. Vallerand RJ. Intrinsic and extrinsic motivation in sport and physical activity: A review and a look to the future. In: Tenebaum G, Eklund RC, editors. Handbook of sport psychology. 3rd ed. Hoboken (NJ): Wiley; 2007.
39. Ghashghaei HT, Hilgetag CC, Barbas H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage. 2007;34(3):905-23. [PMID:17126037] http://dx.doi.org/10.1016/j.neuroimage.2006.09.046
40. Tran AH, Tamura R, Uwano T, Kobayashi T, Katsuki M, Ono T. Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place. Proc Natl Acad Sci USA. 2005;102(6):2117-22. [PMID:15684065] http://dx.doi.org/10.1073/pnas.0409726102
41. Siegert RJ, Taylor WJ. Theoretical aspects of goal-setting and motivation in rehabilitation. Disabil Rehabil. 2004; 26(1):1-8. [PMID:14660192] http://dx.doi.org/10.1080/09638280410001644932
42. Salomons TV, Johnstone T, Backonja MM, Davidson RJ. Perceived controllability modulates the neural response to pain. J Neurosci. 2004;24(32):7199-7203. [PMID:15306654] http://dx.doi.org/10.1523/JNEUROSCI.1315-04.2004
43. Lutz A, Greischar LL, Rawlings NB, Ricard M, Davidson RJ. Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. Proc Natl Acad Sci USA. 2004;101(46):16369-73. [PMID:15534199] http://dx.doi.org/10.1073/pnas.0407401101
44. Lutz A, Lachaux JP, Martinerie J, Varela FJ. Guiding the study of brain dynamics by using first-person data: Synchrony patterns correlate with ongoing conscious states during a simple visual task. Proc Natl Acad Sci USA. 2002; 99(3):1586-91. [PMID:11805299] http://dx.doi.org/10.1073/pnas.032658199
45. Hatfield BD, Haufler AJ, Hung TM, Spalding TW. Electroencephalographic studies of skilled psychomotor performance. J Clin Neurophysiol. 2004;21(3):144-56. [PMID:15375345] http://dx.doi.org/10.1097/00004691-200405000-00003
46. Hatfield BD, Kerick SE. The psychology of superior sport performance. In: Tenebaum G, Eklund RC, editors. Handbook of sport psychology. 3rd ed. Hoboken (NJ): Wiley; 2007. p. 84-109.
47. Del Percio C, Infarinato F, Iacoboni M, Marzano N, Soricelli A, Aschieri P, Eusebi F, Babiloni C. Movement-related desynchronization of alpha rhythms is lower in athletes than non-athletes: A high-resolution EEG study. Clin Neurophysiol. 2010;121(4):482-91. [PMID:20097129] http://dx.doi.org/10.1016/j.clinph.2009.12.004
48. Perry J. Gait analysis: Normal and pathological function. Thorofare (NJ): SLACK; 1992.
49. Jasper HH. The ten-twenty electrode system of the international system federation. Electroencephalogr Clin Neurophysiol. 1958;10:371-75.
50. Onton J, Westerfield M, Townsend J, Makeig S. Imaging human EEG dynamics using independent component analysis. Neurosci Biobehav Rev. 2006;30(6):808-22. [PMID:16904745] http://dx.doi.org/10.1016/j.neubiorev.2006.06.007
51. Rohrer B, Fasoli S, Krebs HI, Volpe B, Frontera WR, Stein J, Hogan N. Submovements grow larger, fewer, and more blended during stroke recovery. Mot Control. 2004;8(4): 472-83. [PMID:15585902]
52. Coan JA, Allen JJ. Handbook of emotion elicitation and assessment. Oxford (England): Oxford University Press; 2007.
53. Rolls ET. The brain and emotion. Oxford (England): Oxford University Press; 1999.
54. Rolls ET. Emotion explained. Oxford (England): Oxford University Press; 2005.
55. Schultz W. Behavioral theories and the neurophysiology of reward. Annu Rev Psychol. 2006;57:87-115. [PMID:16318590] http://dx.doi.org/10.1146/annurev.psych.56.091103.070229
56. Fregni F, Pascual-Leone A. Hand motor recovery after stroke: Tuning the orchestra to improve hand motor function. Cogn Behav Neurol. 2006;19(1):21-33. [PMID:16633016] http://dx.doi.org/10.1097/00146965-200603000-00003
57. Serrien DJ, Strens LH, Cassidy MJ, Thompson AJ, Brown P. Functional significance of the ipsilateral hemisphere during movement of the affected hand after stroke. Exp Neurol. 2004;190(2):425-32. [PMID:15530881] http://dx.doi.org/10.1016/j.expneurol.2004.08.004
58. Fitts PM, Posner MI. Human performance. Belmont (CA): Brooks/Cole Publishing Co; 1967.
59. Mishra J, Zinni M, Bavelier D, Hillyard SA. Neural basis of superior performance of action videogame players in an attention-demanding task. J Neurosci. 2011;31(3):992-98. [PMID:21248123] http://dx.doi.org/10.1523/JNEUROSCI.4834-10.2011
60. Mirelman A, Bonato P, Deutsch JE. Effects of training with a robot-virtual reality system compared with a robot alone on the gait of individuals after stroke. Stroke. 2009;40(1): 169-74. [PMID:18988916] http://dx.doi.org/10.1161/STROKEAHA.108.516328
61. Onla-or S, Winstein CJ. Determining the optimal challenge point for motor skill learning in adults with moderately severe Parkinson's disease. Neurorehabil Neural Repair. 2008;22(4):385-95. [PMID:18326891] http://dx.doi.org/10.1177/1545968307313508
62. Guadagnoli MA, Lee TD. Challenge point: A framework for conceptualizing the effects of various practice conditions in motor learning. J Mot Behav. 2004;36(2):212-24. [PMID:15130871] http://dx.doi.org/10.3200/JMBR.36.2.212-224
63. Mattia D, Spanedda F, Babiloni F, Romigi A, Marciani MG. Quantitative EEG patterns following unilateral stroke: A study in chronic stage. Int J Neurosci. 2003;113(4):465-82. [PMID:12856476] http://dx.doi.org/10.1080/00207450390162227
64. Nolfe G, Cobianchi A, Mossuto-Agatiello L, Giaquinto S. The role of P300 in the recovery of post-stroke global aphasia. Eur J Neurol. 2006;13(4):377-84. [PMID:16643316] http://dx.doi.org/10.1111/j.1468-1331.2006.01237.x
65. Mima T, Toma K, Koshy B, Hallett M. Coherence between cortical and muscular activities after subcortical stroke. Stroke. 2001;32(11):2597-2601. [PMID:11692023] http://dx.doi.org/10.1161/hs1101.098764
66. Strens LH, Asselman P, Pogosyan A, Loukas C, Thompson AJ, Brown P. Corticocortical coupling in chronic stroke: Its relevance to recovery. Neurology. 2004;63(3):475-84. [PMID:15304578] http://dx.doi.org/10.1212/01.WNL.0000133010.69694.F8
67. 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). 2009;292(12):2023-31. [PMID:19943355] http://dx.doi.org/10.1002/ar.20965