The Effect of Action Observation Combined with Motor Imagery Training on Upper Extremity Function and Corticospinal Excitability in Stroke Patients: A Randomized Controlled Trial
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Procedure
2.3. Intervention
2.3.1. AO in Parallel with MI
2.3.2. AO
2.4. Outcome Measures
2.4.1. Motor Evoked Potential (MEP) Amplitude
2.4.2. Fugl-Meyer Assessment Upper Extremity (FMA UE)
2.4.3. Wolf Motor Function Test (WMFT)
2.4.4. Motor Activity Log (MAL)
2.5. Statistical Analysis
2.6. Ethical Approval
3. Results
3.1. Participants’ Characteristics
3.2. Upper Extremity Function Evaluation
3.3. Corticospinal Excitability
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Demartino, A.M.; Rodrigues, L.C.; Gomes, R.P.; Michaelsen, S.M. Hand function and type of grasp used by chronic stroke individuals in actual environment. Top. Stroke Rehabil. 2019, 26, 247–254. [Google Scholar] [CrossRef]
- Veldema, J.; Nowak, D.A.; Gharabaghi, A. Resting motor threshold in the course of hand motor recovery after stroke: A systematic review. J. Neuroeng. Rehabil. 2021, 18, 158. [Google Scholar] [CrossRef]
- Borges, L.R.; Fernandes, A.B.; Melo, L.P.; Guerra, R.O.; Campos, T.F. Action observation for upper limb rehabilitation after stroke. Cochrane Database Syst. Rev. 2018, 10, CD011887. [Google Scholar] [CrossRef]
- Maida, C.D.; Norrito, R.L.; Daidone, M.; Tuttolomondo, A.; Pinto, A. Neuroinflammatory Mechanisms in Ischemic Stroke: Focus on Cardioembolic Stroke, Background, and Therapeutic Approaches. Int. J. Mol. Sci. 2020, 21, 6454. [Google Scholar] [CrossRef]
- Rosso, C.; Lamy, J.C. Prediction of motor recovery after stroke: Being pragmatic or innovative? Curr. Opin. Neurol. 2020, 33, 482–487. [Google Scholar] [CrossRef]
- Maier, M.; Ballester, B.R.; Verschure, P. Principles of Neurorehabilitation After Stroke Based on Motor Learning and Brain Plasticity Mechanisms. Front. Syst. Neurosci. 2019, 13, 74. [Google Scholar] [CrossRef]
- Ranzani, R.; Lambercy, O.; Metzger, J.C.; Califfi, A.; Regazzi, S.; Dinacci, D.; Petrillo, C.; Rossi, P.; Conti, F.M.; Gassert, R. Neurocognitive robot-assisted rehabilitation of hand function: A randomized control trial on motor recovery in subacute stroke. J. Neuroeng. Rehabil. 2020, 17, 115. [Google Scholar] [CrossRef]
- Ozen, S.; Senlikci, H.B.; Guzel, S.; Yemisci, O.U. Computer Game Assisted Task Specific Exercises in the Treatment of Motor and Cognitive Function and Quality of Life in Stroke: A Randomized Control Study. J. Stroke Cerebrovasc. Dis. 2021, 30, 105991. [Google Scholar] [CrossRef]
- Lee, H.C.; Kuo, F.L.; Lin, Y.N.; Liou, T.H.; Lin, J.C.; Huang, S.W. Effects of Robot-Assisted Rehabilita tion on Hand Function of People With Stroke: A Randomized, Crossover-Controlled, Assessor-Blinded Study. Am. J. Occup. Ther. 2021, 75, 7501205020p1–7501205020p11. [Google Scholar] [CrossRef]
- Kim, J.; Yim, J. Effects of High-Frequency Repetitive Transcranial Magnetic Stimulation Combined with Task-Oriented Mirror Therapy Training on Hand Rehabilitation of Acute Stroke Patients. Med. Sci. Monit. 2018, 24, 743–750. [Google Scholar] [CrossRef] [Green Version]
- Davies, L.; Delcourt, C. Current approach to acute stroke management. Intern. Med. J. 2021, 51, 481–487. [Google Scholar] [CrossRef]
- Ryan, D.; Fullen, B.; Rio, E.; Segurado, R.; Stokes, D.; O’Sullivan, C. Effect of Action Observation Therapy in the Rehabilitation of Neurologic and Musculoskeletal Conditions: A Systematic Review. Arch. Rehabil. Res. Clin. Transl. 2021, 3, 100106. [Google Scholar] [CrossRef]
- Sarasso, E.; Agosta, F.; Piramide, N.; Gardoni, A.; Canu, E.; Leocadi, M.; Castelnovo, V.; Basaia, S.; Tettamanti, A.; Volonte, M.A.; et al. Action Observation and Motor Imagery Improve Dual Task in Parkinson’s Disease: A Clinical/fMRI Study. Mov. Disord. 2021, 36, 2569–2582. [Google Scholar] [CrossRef]
- Morioka, S.; Osumi, M.; Nishi, Y.; Ishigaki, T.; Ishibashi, R.; Sakauchi, T.; Takamura, Y.; Nobusako, S. Motor-imagery ability and function of hemiplegic upper limb in stroke patients. Ann. Clin. Transl. Neurol. 2019, 6, 596–604. [Google Scholar] [CrossRef]
- Tani, M.; Ono, Y.; Matsubara, M.; Ohmatsu, S.; Yukawa, Y.; Kohno, M.; Tominaga, T. Action observation facilitates motor cortical activity in patients with stroke and hemiplegia. Neurosci. Res. 2018, 133, 7–14. [Google Scholar] [CrossRef]
- Guerra, Z.F.; Lucchetti, A.L.G.; Lucchetti, G. Motor Imagery Training After Stroke: A Systematic Review and Meta-analysis of Randomized Controlled Trials. J. Neurol. Phys. Ther. 2017, 41, 205–214. [Google Scholar] [CrossRef]
- Friesen, C.L.; Bardouille, T.; Neyedli, H.F.; Boe, S.G. Combined Action Observation and Motor Imagery Neurofeedback for Modulation of Brain Activity. Front. Hum. Neurosci. 2016, 10, 692. [Google Scholar] [CrossRef]
- Sun, Y.; Wei, W.; Luo, Z.; Gan, H.; Hu, X. Improving motor imagery practice with synchronous action observation in stroke patients. Top. Stroke Rehabil. 2016, 23, 245–253. [Google Scholar] [CrossRef]
- Shih, T.Y.; Wu, C.Y.; Lin, K.C.; Cheng, C.H.; Hsieh, Y.W.; Chen, C.L.; Lai, C.J.; Chen, C.C. Effects of action observation therapy and mirror therapy after stroke on rehabilitation outcomes and neural mechanisms by MEG: Study protocol for a randomized controlled trial. Trials 2017, 18, 459. [Google Scholar] [CrossRef]
- Herranz-Gomez, A.; Gaudiosi, C.; Angulo-Diaz-Parreno, S.; Suso-Marti, L.; La Touche, R.; Cuenca-Martinez, F. Effectiveness of motor imagery and action observation on functional variables: An umbrella and mapping review with meta-meta-analysis. Neurosci. Biobehav. Rev. 2020, 118, 828–845. [Google Scholar] [CrossRef]
- Ono, Y.; Wada, K.; Kurata, M.; Seki, N. Enhancement of motor-imagery ability via combined action observation and motor-imagery training with proprioceptive neurofeedback. Neuropsychologia 2018, 114, 134–142. [Google Scholar] [CrossRef]
- Fuchshofer, K.; Merz, C.; Denecke, K.; Schuster-Amft, C. Intervention Platform for Action Observation and Motor Imagery Training After Stroke: Usability Test. Stud. Health Technol. Inform. 2022, 292, 71–74. [Google Scholar]
- Oostra, K.M.; Oomen, A.; Vanderstraeten, G.; Vingerhoets, G. Influence of motor imagery training on gait rehabilitation in sub-acute stroke: A randomized controlled trial. J. Rehabil. Med. 2015, 47, 204–209. [Google Scholar] [CrossRef] [PubMed]
- Aoyama, T.; Kaneko, F.; Kohno, Y. Motor imagery combined with action observation training optimized for individual motor skills further improves motor skills close to a plateau. Hum. Mov. Sci. 2020, 73, 102683. [Google Scholar] [CrossRef] [PubMed]
- Fu, J.; Zeng, M.; Shen, F.; Cui, Y.; Zhu, M.; Gu, X.; Sun, Y. Effects of action observation therapy on upper extremity function, daily activities and motion evoked potential in cerebral infarction patients. Medicine 2017, 96, e8080. [Google Scholar] [CrossRef] [PubMed]
- Stinear, C.M. Prediction of motor recovery after stroke: Advances in biomarkers. Lancet Neurol. 2017, 16, 826–836. [Google Scholar] [CrossRef]
- Grant, V.M.; Gibson, A.; Shields, N. Somatosensory stimulation to improve hand and upper limb function after stroke-a systematic review with meta-analyses. Top. Stroke Rehabil. 2018, 25, 150–160. [Google Scholar] [CrossRef]
- Rech, K.D.; Salazar, A.P.; Marchese, R.R.; Schifino, G.; Cimolin, V.; Pagnussat, A.S. Fugl-Meyer Assessment Scores Are Related With Kinematic Measures in People with Chronic Hemiparesis after Stroke. J. Stroke Cerebrovasc. Dis. 2020, 29, 104463. [Google Scholar] [CrossRef]
- Gladstone, D.J.; Danells, C.J.; Black, S.E. The fugl-meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil. Neural. Repair. 2002, 16, 232–240. [Google Scholar] [CrossRef]
- Hodics, T.M.; Nakatsuka, K.; Upreti, B.; Alex, A.; Smith, P.S.; Pezzullo, J.C. Wolf Motor Function Test for characterizing moderate to severe hemiparesis in stroke patients. Arch. Phys. Med. Rehabil. 2012, 93, 1963–1967. [Google Scholar] [CrossRef]
- Van de Winckel, A.; Gauthier, L. A Revised Motor Activity Log Following Rasch Validation (Rasch-Based MAL-18) and Consensus Methods in Chronic Stroke and Multiple Sclerosis. Neurorehabil. Neural. Repair. 2019, 33, 787–791. [Google Scholar] [CrossRef] [PubMed]
- Uswatte, G.; Taub, E.; Morris, D.; Light, K.; Thompson, P.A. The Motor Activity Log-28: Assessing daily use of the hemiparetic arm after stroke. Neurology 2006, 67, 1189–1194. [Google Scholar] [CrossRef] [PubMed]
- Fu, T.S.; Wu, C.Y.; Lin, K.C.; Hsieh, C.J.; Liu, J.S.; Wang, T.N.; Ou-Yang, P. Psychometric comparison of the shortened Fugl-Meyer Assessment and the streamlined Wolf Motor Function Test in stroke rehabilitation. Clin. Rehabil. 2012, 26, 1043–1047. [Google Scholar] [CrossRef]
- Ji, E.K.; Wang, H.H.; Jung, S.J.; Lee, K.B.; Kim, J.S.; Jo, L.; Hong, B.Y.; Lim, S.H. Graded motor imagery training as a home exercise program for upper limb motor function in patients with chronic stroke: A randomized controlled trial. Medicine 2021, 100, e24351. [Google Scholar] [CrossRef] [PubMed]
- Macuga, K.L.; Papailiou, A.P. Motor imagery of tool use: Relationship to actual use and adherence to Fitts’ law across tasks. Exp. Brain Res. 2012, 218, 169–179. [Google Scholar] [CrossRef]
- Taube, W.; Mouthon, M.; Leukel, C.; Hoogewoud, H.M.; Annoni, J.M.; Keller, M. Brain activity during observation and motor imagery of different balance tasks: An fMRI study. Cortex 2015, 64, 102–114. [Google Scholar] [CrossRef]
- Eaves, D.L.; Behmer, L.P., Jr.; Vogt, S. EEG and behavioural correlates of different forms of motor imagery during action observation in rhythmical actions. Brain Cogn. 2016, 106, 90–103. [Google Scholar] [CrossRef]
- Vogt, S.; Di Rienzo, F.; Collet, C.; Collins, A.; Guillot, A. Multiple roles of motor imagery during action observation. Front. Hum. Neurosci. 2013, 7, 807. [Google Scholar] [CrossRef]
- Emerson, J.R.; Binks, J.A.; Scott, M.W.; Kenny, R.P.W.; Eaves, D.L. Combined action observation and motor imagery therapy: A novel method for post-stroke motor rehabilitation. AIMS. Neurosci. 2018, 5, 236–252. [Google Scholar] [CrossRef]
Characteristics | Experimental Group (n = 22) | Control Group (n = 23) | X2/t | p |
---|---|---|---|---|
Age (year), mean ± SD | 62.68 ± 8.54 | 63.43 ± 9.57 | −0.276 | 0.784 |
Gender (male/female) | 12/10 | 12/11 | −0.156 | 0.877 |
Type of stroke (Hemorrhage/Infarction) | 9/13 | 11/12 | 0.457 | 0.650 |
Side of stroke (Right/Left) | 12/10 | 7/16 | −1.647 | 0.463 |
Time since onset of stroke months, mean ± SD | 4.82 ± 2.08 | 4.61 ± 1.69 | 0.370 | 0.713 |
Experimental Group | Control Group | Between Groups p-Values | |||||||
---|---|---|---|---|---|---|---|---|---|
Before Treatment | After Treatment | Mean Difference | p-Value | Before Treatment | After Treatment | Mean Difference | p-Value | ||
FMA UE | 15.50 (3.41) | 18.59 (3.86) | 3.09 (2.82) †† | 0.000 ** | 13.04 (5.02) | 14.22 (5.06) | 1.17 (1.07) | 0.000 ** | 0.002 † |
WMFT | 12.09 (4.40) | 14.41 (4.95) | 2.32 (1.70) | 0.000 ** | 11.52 (4.83) | 13.00 (5.03) | 1.00 (1.20) | 0.000 ** | 0.350 |
MAL QOM | 0.89 (0.40) | 1.62 (0.73) | 0.72 (0.54) | 0.000 ** | 1.07 (0.33) | 1.66 (0.76) | 0.59 (0.60) | 0.000 ** | 0.834 |
MAL AOU | 0.84 (0.32) | 2.02 (0.48) | 1.18 (0.45) † | 0.000 ** | 1.00 (0.37) | 1.60 (0.68) | 0.59 (0.57) | 0.000 ** | 0.022 † |
MEP amplitude | 84.29 (34.43) | 128.90 (49.82) | 44.60 (47.51) † | 0.000 ** | 101.66 (46.01) | 109.88 (46.86) | 8.21 (6.97) | 0.000 ** | 0.194 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Choi, J.-B.; Yang, S.-W.; Ma, S.-R. The Effect of Action Observation Combined with Motor Imagery Training on Upper Extremity Function and Corticospinal Excitability in Stroke Patients: A Randomized Controlled Trial. Int. J. Environ. Res. Public Health 2022, 19, 12048. https://doi.org/10.3390/ijerph191912048
Choi J-B, Yang S-W, Ma S-R. The Effect of Action Observation Combined with Motor Imagery Training on Upper Extremity Function and Corticospinal Excitability in Stroke Patients: A Randomized Controlled Trial. International Journal of Environmental Research and Public Health. 2022; 19(19):12048. https://doi.org/10.3390/ijerph191912048
Chicago/Turabian StyleChoi, Jong-Bae, Seo-Won Yang, and Sung-Ryong Ma. 2022. "The Effect of Action Observation Combined with Motor Imagery Training on Upper Extremity Function and Corticospinal Excitability in Stroke Patients: A Randomized Controlled Trial" International Journal of Environmental Research and Public Health 19, no. 19: 12048. https://doi.org/10.3390/ijerph191912048