Bilateral Sensorimotor Cortical Communication Modulated by Multiple Hand Training in Stroke Participants: A Single Training Session Pilot Study

Jian-Jia Huang, Yu-Cheng Pei, Yi-Yu Chen, Shen-Shiou Tseng, Jen-Wen Hung, Jian-Jia Huang, Yu-Cheng Pei, Yi-Yu Chen, Shen-Shiou Tseng, Jen-Wen Hung

Abstract

Bi-manual therapy (BT), mirror therapy (MT), and robot-assisted rehabilitation have been conducted in hand training in a wide range of stages in stroke patients; however, the mechanisms of action during training remain unclear. In the present study, participants performed hand tasks under different intervention conditions to study bilateral sensorimotor cortical communication, and EEG was recorded. A multifactorial design of the experiment was used with the factors of manipulating objects (O), robot-assisted bimanual training (RT), and MT. The sum of spectral coherence was applied to analyze the C3 and C4 signals to measure the level of bilateral corticocortical communication. We included stroke patients with onset <6 months (n = 6), between 6 months and 1 year (n = 14), and onset >1 year (n = 20), and their Brunnstrom recovery stage ranged from 2 to 4. The results showed that stroke duration might influence the effects of hand rehabilitation in bilateral cortical corticocortical communication with significant main effects under different conditions in the alpha and beta bands. Therefore, stroke duration may influence the effects of hand rehabilitation on interhemispheric coherence.

Keywords: EEG; bimanual training; coherence; mirror therapy; robot-assisted training; sensorimotor cortex; stroke.

Conflict of interest statement

Jian-Jia Huang is the designer of the Mirror Hand and the funder of Rehabotics Medical Technology, Taiwan. Other authors had no conflict of interest.

Figures

Figure 1
Figure 1
The exoskeleton hand device and the study design. (A) The exoskeleton hand device; (B) the diagram of 2 (with vs. without object manipulation) × 2 (with vs. without robot-assisted) × 2 (with vs. without mirror) factorially experimental design.
Figure 2
Figure 2
The experimental setup, analyzed electrodes, and the eight experimental conditions. (A) The experimental setup using the dry-electrode-based EEG recorder when the exoskeleton robot was applied on the participant. (B) The 10–20 EEG map, among which the coherence between C3 and C4 electrodes was analyzed, by assuming the right and left heads were controlled by the motor cortexes overlying the C3 and C4 electrodes, respectively. (C–J) The eight experimental conditions (using a factorial design of 2 object manipulation × 2 robot therapy × 2 mirror therapy conditions), including the unilateral hand movement without applying robot, mirror and object (C), conventional mirror therapy (D), robot-assisted bimanual training (E); robot-assisted mirror therapy (F); (G–J) were the trainings of (C–F) with object manipulation.
Figure 3
Figure 3
An example of MT × RT condition for coherence sum analysis. (A) The raw traces of channel C3 and C4 recoded from stroke patient under MT × RT condition; (B) the recorded traces were filtered (pass frequency band: 1–12-Hz); (C) coherence analysis using channel C3 as reference, the frequency band range in (C–a) was divided into three frequency bands and calculated the coherence sum.
Figure 4
Figure 4
Interhemispheric coherences in the three bands: the alpha, low beta, and high beta bands.

References

    1. Feys H.M., De Weerdt W.J., Selz B.E., Cox Steck G.A., Spichiger R., Vereeck L.E., Putman K.D., Van Hoydonck G.A. Effect of a therapeutic intervention for the hemiplegic upper limb in the acute phase after stroke: A single-blind, randomized, controlled multicenter trial. Stroke. 1998;29:785–792. doi: 10.1161/01.STR.29.4.785.
    1. Duncan P.W., Goldstein L.B., Horner R.D., Landsman P.B., Samsa G.P., Matchar D.B. Similar motor recovery of upper and lower extremities after stroke. Stroke. 1994;25:1181–1188. doi: 10.1161/01.STR.25.6.1181.
    1. Fu Q., Zhang W., Santello M. Anticipatory planning and control of grasp positions and forces for dexterous two-digit manipulation. J. Neurosci. 2010;30:9117–9126. doi: 10.1523/JNEUROSCI.4159-09.2010.
    1. Johnston J.A., Winges S.A., Santello M. Neural control of hand muscles during prehension. Prog. Mot. Control. 2009;629:577–596.
    1. Fischer H.C., Stubblefield K., Kline T., Luo X., Kenyon R.V., Kamper D.G. Hand rehabilitation following stroke: A pilot study of assisted finger extension training in a virtual environment. Top. Stroke Rehabil. 2007;14:1–12. doi: 10.1310/tsr1401-1.
    1. Bayona N.A., Bitensky J., Salter K., Teasell R. The role of task-specific training in rehabilitation therapies. Top. Stroke Rehabil. 2005;12:58–65. doi: 10.1310/BQM5-6YGB-MVJ5-WVCR.
    1. Gordon A.M., Schneider J.A., Chinnan A., Charles J.R. Efficacy of a hand–arm bimanual intensive therapy (HABIT) in children with hemiplegic cerebral palsy: A randomized control trial. Dev. Med. Child Neurol. 2007;49:830–838. doi: 10.1111/j.1469-8749.2007.00830.x.
    1. Yavuzer G., Selles R., Sezer N., Sütbeyaz S., Bussmann J.B., Köseoğlu F., Atay M.B., Stam H.J. Mirror therapy improves hand function in subacute stroke: A randomized controlled trial. Arch. Phys. Med. Rehabil. 2008;89:393–398. doi: 10.1016/j.apmr.2007.08.162.
    1. Kim D.H., Lee K.-D., Bulea T.C., Park H.-S. Increasing motor cortex activation during grasping via novel robotic mirror hand therapy: A pilot fNIRS study. J. Neuroeng. Rehabil. 2022;19:8. doi: 10.1186/s12984-022-00988-7.
    1. Chen Y.-M., Lai S.-S., Pei Y.-C., Hsieh C.-J., Chang W.-H. Development of a Novel Task-oriented Rehabilitation Program using a Bimanual Exoskeleton Robotic Hand. JoVE J. Vis. Exp. 2020;159:e61057. doi: 10.3791/61057.
    1. Susanto E.A., Tong R.K., Ockenfeld C., Ho N.S. Efficacy of robot-assisted fingers training in chronic stroke survivors: A pilot randomized-controlled trial. J. Neuroeng. Rehabil. 2015;12:42. doi: 10.1186/s12984-015-0033-5.
    1. Cauraugh J.H., Summers J.J. Neural plasticity and bilateral movements: A rehabilitation approach for chronic stroke. Prog. Neurobiol. 2005;75:309–320. doi: 10.1016/j.pneurobio.2005.04.001.
    1. Zult T., Goodall S., Thomas K., Hortobágyi T., Howatson G. Mirror illusion reduces motor cortical inhibition in the ipsilateral primary motor cortex during forceful unilateral muscle contractions. J. Neurophysiol. 2015;113:2262–2270. doi: 10.1152/jn.00686.2014.
    1. Zult T., Howatson G., Goodall S., Thomas K., Solnik S. Mirror training augments the cross-education of strength and affects inhibitory paths. Med. Sci. Sports Exerc. 2016;48:1001–1013. doi: 10.1249/MSS.0000000000000871.
    1. Jasper H., Penfield W. Electrocorticograms in man: Effect of voluntary movement upon the electrical activity of the precentral gyrus. Arch. Psychiatr. Nervenkrankh. 1949;183:163–174. doi: 10.1007/BF01062488.
    1. Rougeul A., Bouyer J., Dedet L., Debray O. Fast somato-parietal rhythms during combined focal attention and immobility in baboon and squirrel monkey. Electroencephalogr. Clin. Neurophysiol. 1979;46:310–319. doi: 10.1016/0013-4694(79)90205-0.
    1. Ray A.M., Figueiredo T.D., López-Larraz E., Birbaumer N., Ramos-Murguialday A. Brain oscillatory activity as a biomarker of motor recovery in chronic stroke. Hum. Brain Mapp. 2020;41:1296–1308. doi: 10.1002/hbm.24876.
    1. Platz T., Kim I., Pintschovius H., Winter T., Kieselbach A., Villringer K., Kurth R., Mauritz K.-H. Multimodal EEG analysis in man suggests impairment-specific changes in movement-related electric brain activity after stroke. Brain. 2000;123:2475–2490. doi: 10.1093/brain/123.12.2475.
    1. Grefkes C., Fink G.R. Connectivity-based approaches in stroke and recovery of function. Lancet Neurol. 2014;13:206–216. doi: 10.1016/S1474-4422(13)70264-3.
    1. Irlbacher K., Brocke J., Mechow J., Brandt S. Effects of GABAA and GABAB agonists on interhemispheric inhibition in man. Clin. Neurophysiol. 2007;118:308–316. doi: 10.1016/j.clinph.2006.09.023.
    1. Pellegrino G., Tomasevic L., Tombini M., Assenza G., Bravi M., Sterzi S., Giacobbe V., Zollo L., Guglielmelli E., Cavallo G. Inter-hemispheric coupling changes associate with motor improvements after robotic stroke rehabilitation. Restor. Neurol. Neurosci. 2012;30:497–510. doi: 10.3233/RNN-2012-120227.
    1. Naghdi S., Ansari N.N., Mansouri K., Hasson S. A neurophysiological and clinical study of Brunnstrom recovery stages in the upper limb following stroke. Brain Inj. 2010;24:1372–1378. doi: 10.3109/02699052.2010.506860.
    1. Cordella F., Di Luzio F.S., Bravi M., Santacaterina F., Bressi F., Zollo L. Hand motion analysis during robot-aided rehabilitation in chronic stroke. J. Biol. Regul. Homeost. Agents. 2020;34:45–52.
    1. Takahashi C.D., Der-Yeghiaian L., Le V., Cramer S.C. A robotic device for hand motor therapy after stroke; Proceedings of the 9th International Conference on Rehabilitation Robotics (ICORR 2005); Chicago, IL, USA. 28 June–1 July 2005; pp. 17–20.
    1. Homan R.W., Herman J., Purdy P. Cerebral location of international 10–20 system electrode placement. Electroencephalogr. Clin. Neurophysiol. 1987;66:376–382. doi: 10.1016/0013-4694(87)90206-9.
    1. Vecchio F., Lacidogna G., Miraglia F., Bramanti P., Ferreri F., Rossini P.M. Prestimulus Interhemispheric Coupling of Brain Rhythms Predicts Cognitive–Motor Performance in Healthy Humans. J. Cogn. Neurosci. 2014;26:1883–1890. doi: 10.1162/jocn_a_00615.
    1. Leiguarda R.C., Marsden C.D. Limb apraxias: Higher-order disorders of sensorimotor integration. Brain. 2000;123:860–879. doi: 10.1093/brain/123.5.860.
    1. Rapcsak S.Z., Ochipa C., Anderson K.C., Poizner H. Progressive ideomotor apraxia: Evidence for a selective impairment of the action production system. Brain Cogn. 1995;27:213–236. doi: 10.1006/brcg.1995.1018.
    1. Agnew Z.K., Wise R.J., Leech R. Dissociating object directed and non-object directed action in the human mirror system; Implications for theories of motor simulation. PLoS ONE. 2012;7:e32517. doi: 10.1371/journal.pone.0032517.
    1. Pfurtscheller G., Pregenzer M., Neuper C. Visualization of sensorimotor areas involved in preparation for hand movement based on classification of μ and central β rhythms in single EEG trials in man. Neurosci. Lett. 1994;181:43–46. doi: 10.1016/0304-3940(94)90556-8.
    1. Schnitzler A., Gross J., Timmermann L. Synchronised oscillations of the human sensorimotor cortex. Acta Neurobiol. Exp. 2000;60:271–288.
    1. Manganotti P., Gerloff C., Toro C., Katsuta H., Sadato N., Zhuang P., Leocani L., Hallett M. Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr. Clin. Neurophysiol. Electromyogr. Mot. Control. 1998;109:50–62. doi: 10.1016/S0924-980X(97)00074-X.
    1. Gerloff C., Andres F.G. Bimanual coordination and interhemispheric interaction. Acta Psychol. 2002;110:161–186. doi: 10.1016/S0001-6918(02)00032-X.
    1. Leocani L., Toro C., Manganotti P., Zhuang P., Hallett M. Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. Electroencephalogr. Clin. Neurophysiol. Evoked Potentials Sect. 1997;104:199–206. doi: 10.1016/S0168-5597(96)96051-7.
    1. Gerloff C., Richard J., Hadley J., Schulman A.E., Honda M., Hallett M. Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain A J. Neurol. 1998;121:1513–1531. doi: 10.1093/brain/121.8.1513.
    1. El Nahas N., Roushdy T.M., Shokri H.M., Moustafa R.R., Elsayed A.M., Amin R.M., Ashour A.A., Abd Eldayem E.H., Elhawary G.A., Elbokl A.M. Lateralized readiness potentials can identify hemisphere of recovery in stroke patients. Restor. Neurol. Neurosci. 2022;40:63–71. doi: 10.3233/RNN-211222.
    1. Philips G.R., Daly J.J., Príncipe J.C. Topographical measures of functional connectivity as biomarkers for post-stroke motor recovery. J. Neuroeng. Rehabil. 2017;14:67. doi: 10.1186/s12984-017-0277-3.
    1. Hao Z., Wang D., Zeng Y., Liu M. Repetitive transcranial magnetic stimulation for improving function after stroke. Cochrane Database Syst. Rev. 2013 doi: 10.1002/14651858.CD008862.pub2.
    1. Vahdat S., Darainy M., Thiel A., Ostry D.J. A single session of robot-controlled proprioceptive training modulates functional connectivity of sensory motor networks and improves reaching accuracy in chronic stroke. Neurorehabilit. Neural Repair. 2019;33:70–81. doi: 10.1177/1545968318818902.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe