Exploring Hemodynamic Responses Using Mirror Visual Feedback With Electromyogram-Triggered Stimulation and Functional Near-Infrared Spectroscopy

Yuji Inagaki, Kazunori Seki, Hitoshi Makino, Yuichirou Matsuo, Tamaki Miyamoto, Katsunori Ikoma, Yuji Inagaki, Kazunori Seki, Hitoshi Makino, Yuichirou Matsuo, Tamaki Miyamoto, Katsunori Ikoma

Abstract

In recent years, mirror visual feedback (MVF) therapy combined with electrical stimulation (ES) have been proposed for patients with hemiparesis. However, the neurophysiological effect remains unknown. We investigated the effects of MVF by itself and along with electromyogram-triggered ES (ETES) on hemodynamic responses using functional near-infrared spectroscopy (NIRS). Eighteen healthy subjects participated in this study. We measured changes in brain oxygenation using 48 NIRS channels. We investigated the effects of three main factors of visual feedback (observation of a mark, right hand, and hand movements via mirror) with or without ES on bilateral precentral gyrus (PrG), postcentral gyrus (PoG), supplementary motor area (SMA), supramarginal gyrus area (SMG), and angular gyrus (AG) to determine the contribution of each factor. The results showed that the left PoG was significantly more activated when performing mirrored tasks (MT) than when performing circle or Right-hand Tasks (RTs). In addition, the right PoG and right SMA in MT were significantly more activated than in MT + ES cases. Our findings suggested that observation of movements through the mirror caused activation of the postcentral gyrus rather than the PrG, and MVF along with ETES decreased cortical activation.

Keywords: electric stimulation; electromyogram; mirror visual feedback; near-infrared spectroscopy; postcentral gyrus.

Figures

Figure 1
Figure 1
Schematic illustration of the experimental setup. The arrow in each task represents where the subjects were asked to look. The shaded portion indicates the areas that cannot be observed by subjects.
Figure 2
Figure 2
Near-infrared spectroscopy (NIRS) channels setting. The red square indicates the optical sources and the blue square indicates the detector. The midline shows T3-Cz-T4 line.
Figure 3
Figure 3
Oxygenated hemoglobin (Oxy-Hb) concentration in the left postcentral gyrus (PoG). *p < 0.05, **p < 0.01.
Figure 4
Figure 4
Time course of mean activation changes in oxy-Hb in response to Circle Task (CT), Right-hand Task (RT), and Mirror Task (MT) in left PoG that shows significant differences between groups.
Figure 5
Figure 5
Oxy-Hb concentration in the right PoG. *p < 0.05, **p < 0.01.
Figure 6
Figure 6
Time course of mean activation changes in oxy-Hb in response to RT, Right-hand + electrical stimulation (ES) Task, MT, and Mirror + ES Task in Right PoG that shows significant differences between groups.
Figure 7
Figure 7
Oxy-Hb concentration in the right supplementary motor area (SMA). *p < 0.05.
Figure 8
Figure 8
Time course of mean activation changes in oxy-Hb in response to MT and Mirror + ES Task in right SMA that shows significant differences between groups.

References

    1. Altschuler E. L., Wisdom S. B., Stone L., Foster C., Galasko D., Llewellyn D. M., et al. . (1999). Rehabilitation of hemiparesis after stroke with a mirror. Lancet 353, 2035–2036. 10.1016/s0140-6736(99)00920-4
    1. Arya K. N. (2016). Underlying neural mechanisms of mirror therapy: implications for motor rehabilitation in stroke. Neurol. India 64, 38–44. 10.4103/0028-3886.173622
    1. Balconi M., Cortesi L. (2016). Brain activity (fNIRS) in control state differs from the execution and observation of object-related and object-unrelated actions. J. Mot. Behav. 48, 289–296. 10.1080/00222895.2015.1092936
    1. Chapman L. J., Chapman J. P. (1987). The measurement of handedness. Brain Cogn. 6, 175–183. 10.1016/0278-2626(87)90118-7
    1. Debnath R., Franz E. A. (2016). Perception of hand movement by mirror reflection evokes brain activation in the motor cortex contralateral to a non-moving hand. Cortex 81, 118–125. 10.1016/j.cortex.2016.04.015
    1. Fritzsch C., Wang J., Santos L. F., Mauritz K. H., Brunetti M., Dohle C. (2014). Different effects of the mirror illusion on motor and somatosensory processing. Restor. Neurol. Neurosci. 32, 269–280. 10.3233/RNN-130343
    1. Fujiwara N., Sakatani K., Katayama Y., Murata Y., Hoshino T., Fukaya C., et al. . (2004). Evoked-cerebral blood oxygenation changes in false-negative activations in BOLD contrast functional MRI of patients with brain tumors. Neuroimage 21, 1464–1471. 10.1016/j.neuroimage.2003.10.042
    1. Fukumura K., Sugawara K., Tanabe S., Ushiba J., Tomita Y. (2007). Influence of mirror therapy on human motor cortex. Int. J. Neurosci. 117, 1039–1048. 10.1080/00207450600936841
    1. Futami R., Seki K., Kawanishi T., Sugiyama T., Cikajlo I., Handa Y. (2005). “Application of local EMG-driven FES to incompletely paralyzed lower extremities,” in Proceedings of 10th Annual Conference of IFESS, 204–206. Available online at:
    1. Garry M. I., Loftus A., Summers J. J. (2005). Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Exp. Brain Res. 163, 118–122. 10.1007/s00221-005-2226-9
    1. Jang S. H., Jang W. H., Chang P. H., Lee S. H., Jin S. H., Kim Y. G., et al. . (2014). Cortical activation change induced by neuromuscular electrical stimulation during hand movements: a functional NIRS study. J. Neuroeng. Rehabil. 11:29. 10.1186/1743-0003-11-29
    1. Jasper H. H. (1958). The ten-twenty electrode system of the international federation. Electroencephalogr. Clin. Neurophysiol. 10, 371–375.
    1. Ji S. G., Cha H. G., Kim M. K., Lee C. R. (2014). The effect of mirror therapy integrating functional electrical stimulation on the gait of stroke patients. J. Phys. Ther. Sci. 26, 497–499. 10.1589/jpts.26.497
    1. Kim H., Lee G., Song C. (2014). Effect of functional electrical stimulation with mirror therapy on upper extremity motor function in poststroke patients. J. Stroke Cerebrovasc. Dis. 23, 655–661. 10.1016/j.jstrokecerebrovasdis.2013.06.017
    1. Kumru H., Albu S., Pelayo R., Rothwell J., Opisso E., Leon D., et al. . (2016). Motor cortex plasticity during unilateral finger movement with mirror visual feedback. Neural Plast. 2016:6087896. 10.1155/2016/6087896
    1. Lee D., Lee G., Jeong J. (2016). Mirror therapy with neuromuscular electrical stimulation for improving motor function of stroke survivors: a pilot randomized clinical study. Technol. Health Care 24, 503–511. 10.3233/thc-161144
    1. Lin K. C., Chen Y. T., Huang P. C., Wu C. Y., Huang W. L., Yang H. W., et al. . (2014). Effect of mirror therapy combined with somatosensory stimulation on motor recovery and daily function in stroke patients: a pilot study. J. Formos. Med. Assoc. 113, 422–428. 10.1016/j.jfma.2012.08.008
    1. McCabe C. S., Haigh R. C., Ring E. F., Halligan P. W., Wall P. D., Blake D. R. (2003). A controlled pilot study of the utility of mirror visual feedback in the treatment of complex regional pain syndrome (type 1). Rheumatology 42, 97–101. 10.1093/rheumatology/keg041
    1. McCormick P. W., Stewart M. S., Lewis G., Dujovny M., Ausman J. I. (1992). Intracerebral penetration of infrared light. J. Neurosurg. 76, 315–318. 10.3171/jns.1992.76.2.0315
    1. Michielsen M. E., Smits M., Ribbers G. M., Stam H. J., Geest J. N., Bussmann J. B., et al. . (2011). The neuronal correlates of mirror therapy: an fMRI study on mirror induced visual illusions in patients with stroke. J. Neurol. Neurosurg. Psychiatry 82, 393–398. 10.1136/jnnp.2009.194134
    1. Milde C., Rance M., Kirsch P., Trojan J., Fuchs X., Foell J., et al. . (2015). Do mirror glasses have the same effect on brain activity as a mirror box? Evidence from a functional magnetic resonance imaging study with healthy subjects. PLoS One 10:e0127694. 10.1371/journal.pone.0127694
    1. Moseley G. L. (2004). Graded motor imagery is effective for long-standing complex regional pain syndrome: a randomised controlled trial. Pain 108, 192–198. 10.1016/j.pain.2004.01.006
    1. Murata Y., Sakatani K., Katayama Y., Fukaya C. (2002). Increase in focal concentration of deoxyhaemoglobin during neuronal activity in cerebral ischaemic patients. J. Neurol. Neurosurg. Psychiatry 73, 182–184. 10.1136/jnnp.73.2.182
    1. Murkin J. M., Arango M. (2009). Near-infrared spectroscopy as an index of brain and tissue oxygenation. Br. J. Anaesth. 103, i3–i13. 10.1093/bja/aep299
    1. Nagapattinam S., Vinod B. K., Sai K. N., Ayyappan V. R. (2015). Effect of task specific mirror therapy with functional electrical stimulation on upper limb function for subacute hemiplegia. Int. J. Physiother. 2, 840–849. 10.15621/ijphy/2015/v2i5/78243
    1. Ramachandran V. S., Rogers-Ramachandran D. (1996). Synaesthesia in phantom limbs induced with mirrors. Proc. Biol. Sci. 263, 377–386. 10.1098/rspb.1996.0058
    1. Rjosk V., Lepsien J., Kaminski E., Hoff M., Sehm B., Steele C. J., et al. . (2017). Neural correlates of mirror visual feedback-induced performance improvements: a resting-state fMRI study. Front. Hum. Neurosci. 11:54. 10.3389/fnhum.2017.00054
    1. Sathian K., Greenspan A. I., Wolf S. L. (2000). Doing it with mirrors: a case study of a novel approach to neurorehabilitation. Neurorehabil. Neural. Repair. 14, 73–76. 10.1177/154596830001400109
    1. Schroeter M. L., Zysset S., von Cramon D. Y. (2004). Shortening intertrial intervals in event-related cognitive studies with near-infrared spectroscopy. Neuroimage 22, 341–346. 10.1016/j.neuroimage.2003.12.041
    1. Seiyama A., Seki J., Tanabe H. C., Sase I., Takatsuki A., Miyauchi S., et al. . (2004). Circulatory basis of fMRI signals: relationship between changes in the hemodynamic parameters and BOLD signal intensity. Neuroimage 21, 1204–1214. 10.1016/j.neuroimage.2003.12.002
    1. Tominaga W., Matsubayashi J., Furuya M., Matsuhashi M., Mima T., Fukuyama H., et al. . (2011). Asymmetric activation of the primary motor cortex during observation mirror reflection of a hand. PLoS One 6:e28226. 10.1371/journal.pone.0028226
    1. Toni I., Krams M., Turner R., Passingham R. E. (1998). The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8, 50–61. 10.1006/nimg.1998.0349
    1. Tuscan L., Herbert J. D., Forman E. M., Juarascio A. S., Izzetoglu M., Schultheis M. (2013). Exploring frontal asymmetry using functional near-infrared spectroscopy: a preliminary study of the effects of social anxiety during interaction and performance tasks. Brain Imaging Behav. 7, 140–153. 10.1007/s11682-012-9206-z
    1. Wang J., Fritzsh C., Bernarding J., Holtze S., Mauritz K. H., Brunetti M., et al. . (2013). A comparison of neural mechanisms in mirror therapy and movement observation therapy. J. Rehabil. Med. 45, 410–413. 10.2340/16501977-1127
    1. Yavuzer G., Selles R., Sezer N., Sutbeyaz S., Bussmann J. B., Koseoglu F., et al. . (2008). Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch. Phys. Med. Rehabil. 89, 393–398. 10.1016/j.apmr.2007.08.162
    1. Yun G. J., Chun M. H., Park J. Y., Kim B. R. (2011). The synergic effects of mirror therapy and neuromuscular electrical stimulation for hand function in stroke patients. Ann. Rehabil. Med. 35, 316–321. 10.5535/arm.2011.35.3.316

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