Alternative Motor Task-Based Pattern Training With a Digital Mirror Therapy System Enhances Sensorimotor Signal Rhythms Post-stroke

Chao-Sheng Chang, Ying-Ying Lo, Chien-Liang Chen, Hsin-Min Lee, Wei-Chi Chiang, Ping-Chia Li, Chao-Sheng Chang, Ying-Ying Lo, Chien-Liang Chen, Hsin-Min Lee, Wei-Chi Chiang, Ping-Chia Li

Abstract

Mirror therapy (MT) facilitates motor learning and induces cortical reorganization and motor recovery from stroke. We applied the new digital mirror therapy (DMT) system to compare the cortical activation under the three visual feedback conditions: (1) no mirror visual feedback (NoMVF), (2) bilateral synchronized task-based mirror visual feedback training (BMVF), and (3) reciprocal task-based mirror visual feedback training (RMVF). During DMT, EEG recordings, including time-dependent event-related desynchronization (ERD) signal amplitude in both mu and beta bands, were obtained from the standard C3 (ispilesional hemisphere, IH), C4 (contralesional hemisphere, CH), and Cz scalp sites (supplementary motor area, SMA). The entire ERD curve was separated into three time-phases: P0 (-2 to 0 s), P1 (0 to 2 s), and P2 (2 to 4 s). Four-way and subsequent repeated-measures analyses of variance were used to examine the effects of group (stroke vs. control group), test condition (NoMVF, BMVF, and RMVF), time-phase (P0, P1, and P2), and brain area (IH, CH, SMA) on the ERD areas (%) in mu and beta bands. For the mu band, generally, ERD areas (%) were larger in the control than in the stroke group. The ERD areas (%) were largest under the RMVF condition, followed by BMVF and NoMVF conditions. Similar results were found in the beta bands. The main effects of group, time-phase, and test condition on the ERD areas (%) were significant for the three brain areas, except the main effect of group in the SMA (Cz) and CH (C4) brain area. The ERD areas (%) were larger in the control than in the stroke group. The ERD area (%) was significantly larger during P1 than during P0 and P2 (ps < 0.02), and during P2 than during P0 (ps < 0.01). The ERD area (%) under the RMVF condition was significantly larger than that under the BMVF condition and NoMVF condition (ps < 0.05). The present study suggests that cortical activation particularly in the SMA (Cz) of the brain increases in the RMVF condition in both healthy subjects and stroke patients. This result supports the hypothesis that stroke patients may benefit from RMVF training.

Keywords: mirror therapy system; occupational therapy; pattern training; sensorimotor training; stroke therapy.

Copyright © 2019 Chang, Lo, Chen, Lee, Chiang and Li.

Figures

Figure 1
Figure 1
Experimental set up: The DMT system consists of a host personal computer, camera, and therapy table with a movement area and a mirror area. The participant sits behind the table and places a paper cup for task-based training on the mirror area and their non-impaired hand (active hand) on the movement area. In the mirror area of the table, a slim, 27-inch liquid crystal display monitor was situated slightly above the table to reserve the underlying space for the impaired hand as the non-active hand.
Figure 2
Figure 2
Operation process of three test conditions that were used to test their impact on sensorimotor cortical activity. (A) The mirror area showed only a paper cup with a still image of the mirror area without the hand (NoMVF condition). (B) The mirror area showed synchronous, simultaneous mirrored images of the movements of the left hand with bilateral task-based mirror visual feedback (MVF; BMVF condition). (C) The mirrored images of the movements of the left hand were shown in a 2-s delay of the reciprocal action task-based MVF (RMVF condition).
Figure 3
Figure 3
Three-way repeated-measures analysis of variance was used to examine the effects of group, test condition, and time-phase on the event-related desynchronization (ERD) areas (%) in the mu band. (A) There is a statistically significant interaction effect between group and time-phase in the IH brain area (C3). (B) There is a significant interaction effect between the test condition and time-phase in the CH brain area (C4).
Figure 4
Figure 4
Mu band event-related desynchronization (ERD) areas (%) of the control and stroke group (n = 16 each) with error bars (standard deviations) for the three test conditions (NoMVF, BMVF, and delayed RMVF) for the IH (C3), SMA (Cz), and CH (C4) brain areas, respectively. The ERD areas (%) are shown as P0: white, P1: gray, and P2: black; a time-course change in cortical activation can be observed. *,†ERD areas (%) of this test condition are significantly higher than the areas of the previous test condition for the same brain area.
Figure 5
Figure 5
Overall event-related desynchronization (ERD) areas of the control and stroke group (n = 16 each) with error bars (standard deviations) for the three test conditions (NoMVF: white; BMVF: gray, and RMVF: black) for the IH (C3), SMA (Cz), and CH (C4) brain areas, respectively. (A) Overall ERD areas (%) of the mu band (B) Overall ERD areas (%) of the beta band. *,†Overall ERD areas (%) of this test condition are significantly higher than the previous one for the same brain area.
Figure 6
Figure 6
Three-way repeated-measures analysis of variance in the beta band revealed that both test condition and time-phase have main effects in all three brain areas, while group also had a main effect in the IH brain area (C3). Comparison of the mean value of event-related desynchronization (ERD) areas for each main effect are shown for (A) test condition, (B) time-phase, and (C) group. *,†ERD areas (%) of this test condition, time-phase, or group are significantly higher than the previous one in each comparison.

References

    1. Veerbeek JM, Kwakkel G, van Wegen EE, Ket JC, Heymans MW. Early prediction of outcome of activities of daily living after stroke: a systematic review. Stroke. (2011) 42:1482–88. 10.1161/STROKEAHA.110.604090
    1. Kim K, Kim YM, Kim EK. Correlation between the activities of daily living of stroke patients in a community setting and their quality of life. J Phys Ther Sci. (2014) 26:417–9. 10.1589/jpts.26.417
    1. Neuper C, Scherer R, Wriessnegger S, Pfurtscheller G. Motor imagery and action observation: modulation of sensorimotor brain rhythms during mental control of a brain-computer interface. Clin Neurophysiol. (2009) 120:239–47. 10.1016/j.clinph.2008.11.015
    1. Arya KN, Pandian S, Kumar D, Puri V. Task-based mirror therapy augmenting motor recovery in poststroke hemiparesis: a randomized controlled trial. J Stroke Cerebrovasc Dis. (2015) 24:1738–48. 10.1016/j.jstrokecerebrovasdis.2015.03.026
    1. Zhang Y, Cai J, Zhang Y, Ren T, Zhao M, Zhao Q. Improvement in stroke-induced motor dysfunction by music-supported therapy: a systematic review and meta-analysis. Sci Rep. (2016) 6:38521. 10.1038/srep38521
    1. Bae SH, Jeong WS, Kim KY. Effects of mirror therapy on subacute stroke patients' brain waves and upper extremity functions. J Phys Ther Sci. (2012) 24:1119–22. 10.1589/jpts.24.1119
    1. Cha YJ, Yoo EY, Jung MY, Park SH, Park JH, Lee J. Effects of mental practice with action observation training on occupational performance after stroke. J Stroke Cerebrovasc Dis. (2015) 24:1405–13. 10.1016/j.jstrokecerebrovasdis.2015.02.022
    1. Susanto EA, Tong RK, Ockenfeld C, Ho NS. Efficacy of robot-assisted fingers training in chronic stroke survivors: a pilot randomized-controlled trial. J Neuroeng Rehabil. (2015) 12:42. 10.1186/s12984-015-0033-5
    1. Kitahara K, Hayashi Y, Yano S, Kondo T. Target-directed motor imagery of the lower limb enhances event-related desynchronization. PLoS ONE. (2017) 12:e0184245. 10.1371/journal.pone.0184245
    1. Lu Z, Tong K-Y, Shin H, Li S, Zhou P. Advanced myoelectric control for robotic hand-assisted training: outcome from a stroke patient. Front Neurol. (2017) 8:107. 10.3389/fneur.2017.00107
    1. Zeng W, Guo Y, Wu G, Liu X, Fang Q. Mirror therapy for motor function of the upper extremity in patients with stroke: a meta-analysis. J Rehabil Med. (2018) 50:8–15. 10.2340/16501977-2287
    1. Ramachandran VS, Rogers-Ramachandran DJ. Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci. (1996) 263:377–86. 10.1098/rspb.1996.0058
    1. Cacchio A, De Blasis E, De Blasis V, Santilli V, Spacca G. Mirror therapy in complex regional pain syndrome type 1 of the upper limb in stroke patients. Neurorehab Neural Repair. (2009) 23:792–9. 10.1177/1545968309335977
    1. Wu C-Y, Huang P-C, Chen Y-T, Lin K-C, Yang H-W. Effects of mirror therapy on motor and sensory recovery in chronic stroke: a randomized controlled trial. Arch Phys Med Rehabil. (2013) 94:1023–30. 10.1016/j.apmr.2013.02.007
    1. Ono T, Shindo K, Kawashima K, Ota N, Ito M, Ota T, et al. . Brain-computer interface with somatosensory feedback improves functional recovery from severe hemiplegia due to chronic stroke. Front Neuroeng. (2014) 7:19. 10.3389/fneng.2014.00019
    1. Duann JR, Chiou JC. A comparison of independent event-related desynchronization responses in motor-related brain areas to movement execution, movement imagery, and movement observation. PLoS ONE. (2016) 11:e0162546. 10.1371/journal.pone.0162546
    1. Lee H-M, Li P-C, Fan S-C. Delayed mirror visual feedback presented using a novel mirror therapy system enhances cortical activation in healthy adults. J Neuroeng Rehabil. (2015) 12:56. 10.1186/s12984-015-0053-1
    1. Stepien M, Conradi J, Waterstraat G, Hohlefeld FU, Curio G, Nikulin VV. Event-related desynchronization of sensorimotor EEG rhythms in hemiparetic patients with acute stroke. Neurosci Lett. (2011) 488:17–21. 10.1016/j.neulet.2010.10.072
    1. Rossiter HE, Borrelli MR, Borchert RJ, Bradbury D, Ward NS. Cortical mechanisms of mirror therapy after stroke. Neurorehabil Neural Repair. (2015) 29:444–452. 10.1177/1545968314554622
    1. Fong KNK, Ting KH, Chan CCH, Li LSW. Mirror therapy with bilateral arm training for hemiplegic upper extremity motor functions in patients with chronic stroke. Hong Kong Med J. (2019) 25(Suppl. 3):30–4.
    1. Jeunet C, Glize B, Mcgonigal A, Batail JM, Micoulaud-Franchi JA. Using EEG-based brain computer interface and neurofeedback targeting sensorimotor rhythms to improve motor skills: Theoretical background, applications and prospects. Neurophysiologie Clinique. (2018) 49:125–36. 10.1016/j.neucli.2018.10.068
    1. Orgs G, Dombrowski JH, Heil M, Jansen-Osmann P. Expertise in dance modulates alpha/beta event-related desynchronization during action observation. Eur J Neurosci. (2008) 27:3380–4. 10.1111/j.1460-9568.2008.06271.x
    1. Pfurtscheller G, da Silva FL. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. (1999) 110:1842–57. 10.1016/S1388-2457(99)00141-8
    1. Perry A, Bentin S. Mirror activity in the human brain while observing hand movements: a comparison between EEG desynchronization in the mu-range and previous fMRI results. Brain Res. (2009) 1282:126–32. 10.1016/j.brainres.2009.05.059
    1. Formaggio E, Storti SF, Galazzo IB, Gandolfi M, Geroin C, Smania N, et al. . Modulation of event-related desynchronization in robot-assisted hand performance: brain oscillatory changes in active, passive and imagined movements. J Neuroeng Rehabil. (2013) 10:24. 10.1186/1743-0003-10-24
    1. Rossiter HE, Boudrias M-H, Ward NS. Do movement-related beta oscillations change after stroke? J Neurophysiol. (2014) 112:2053–8. 10.1152/jn.00345.2014
    1. Touzalin –Chretien P, Ehrler S, Dufour AJ. Dominance of vision over proprioception on motor programming: evidence from ERP. Cereb Cortex. (2009) 20:2007–16. 10.1093/cercor/bhp271
    1. Touzalin-Chretien P, Dufour AJ. Motor cortex activation induced by a mirror: evidence from lateralized readiness potentials. J Neurophysiol. (2008) 100:19–23. 10.1152/jn.90260.2008
    1. Bai O, Mari Z, Vorbach S, Hallett M. Asymmetric spatiotemporal patterns of event-related desynchronization preceding voluntary sequential finger movements: a high-resolution EEG study. Clin Neurophysiol. (2005) 116:1213–21. 10.1016/j.clinph.2005.01.006
    1. Jang SH, Kim Y-H, Cho S-H, Lee J-H, Park J-W, Kwon YN. Cortical reorganization induced by task-oriented training in chronic hemiplegic stroke patients. Neuroreport. (2003) 14:137–41. 10.1097/00001756-200301200-00025
    1. Paik YR, Kim SK, Lee JS, Jeon BJ. Simple and task-oriented mirror therapy for upper extremity function in stroke patients: a pilot study. Hong Kong J Occup Ther. (2014) 24:6–12. 10.1016/j.hkjot.2014.01.002

Source: PubMed

3
구독하다