Cortical mapping of mirror visual feedback training for unilateral upper extremity: A functional near-infrared spectroscopy study

Zhongfei Bai, Kenneth N K Fong, Jiaqi Zhang, Zhishan Hu, Zhongfei Bai, Kenneth N K Fong, Jiaqi Zhang, Zhishan Hu

Abstract

Introduction: Mirror therapy has been shown to be effective in promoting hemiplegic arm recovery in patients with stroke or unilateral cerebral palsy. This study aimed to explore the cortical mapping associated with mirror therapy in a group of healthy adults by using functional near-infrared spectroscopy.

Methods: Fifteen right-handed healthy adults were recruited by means of convenience sampling. A 2 × 2 factorial design was used: movement complexity with two levels-task-based (T) and movement-based (M), and visual direction with two levels-mirror visual feedback task (MT) and covered mirror with normal visual feedback task (NoT) as the control, constituting four conditions, namely TMT, MMT, TNoT, and MNoT. The regions of interest were the sensorimotor cortex (SMC), the supplementary motor area (SMA), the superior parietal cortex (SPL), and the precuneus in both the contralateral and ipsilateral hemispheres.

Results: Our findings showed that in the ipsilateral hemisphere, MT induced a higher activation in the SMA and SPL than NoT. With regard to the activation of the ipsilateral SMC, only one channel was found showing superior effects of MT compared with NoT. In addition, MT can strengthen the functional connectivity between the SMC and SMA. In the contralateral hemisphere, both movement complexity and visual direction showed significant main effects in the SMC, while only movement complexity showed a significant main effect in the SMA and SPL. The precuneus of both sides was deactivated and showed no significant difference among the four conditions.

Conclusions: Our experiment implies that the modest activation of ipsilateral SMC during MT is likely to be associated with the enhanced activity of ipsilateral SMA and that the precuneus may not be an essential component of the MT-related neural network.

Keywords: deactivation; functional near-infrared spectroscopy; mirror therapy; mirror visual feedback; precuneus; sensorimotor cortex; supplementary motor area.

© 2019 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Experimental design. (a) Experimental setup. (b) Experimental design. MMT, movement‐based mirror therapy; MNoT, movement‐based with normal visual feedback; TMT, task‐based mirror therapy; TNoT, task‐based with normal visual feedback
Figure 2
Figure 2
Arrangement of fNIRS channels. (a) Two 3 × 3 and one 3 × 5 optode probe sets. (b) The locations of channels in the MNI standard brain template
Figure 3
Figure 3
Post hoc analysis and baseline‐corrected time course curves. The bar charts show the post hoc paired t test analysis, and the line charts show the baseline‐corrected time course curves between −5 and 40 s relative to the onset of tasks. *: Post hoc analysis which passed the Bonferroni correction at p ≤ .013 (0.05/4; 4 = number of comparisons); CH, channel; MMT, movement‐based mirror therapy; MNoT, movement‐based with normal visual feedback; PC, precuneus; ROI, region of interest‐based analysis; SMA, supplementary motor area; SMC, sensorimotor cortex; TMT, task‐based mirror therapy; TNoT, task‐based with normal visual feedback [Correction added on 20 December 2019, after first online publication: Figure 3 has been updated and p values in caption have been corrected.]
Figure 4
Figure 4
The differences of functional connectivity among conditions. a, b, e, and f show the significant functional connectivity of task‐based mirror therapy (TMT), movement‐based mirror therapy (MMT), task‐based with normal visual feedback (TNoT), and movement‐based with normal visual feedback (MNoT), respectively. c, d, g, h, i, and j show comparisons between conditions. “>” means functional connectivity whose left condition is stronger than right condition. PC, precuneus; SMA, supplementary motor area; SMC, sensorimotor cortex

References

    1. Aarabi, A. , Osharina, V. , & Wallois, F. (2017). Effect of confounding variables on hemodynamic response function estimation using averaging and deconvolution analysis: An event‐related NIRS study. NeuroImage, 155, 25–49. 10.1016/j.neuroimage.2017.04.048
    1. Arya, K. N. , Pandian, S. , Kumar, D. , & Puri, V. (2015). Task‐based mirror therapy augmenting motor recovery in poststroke hemiparesis: A randomized controlled rrial. Journal of Stroke and Cerebrovascular Diseases, 24, 1738–1748.
    1. Bai, Z. , Zhang, J. , Zhang, Z. , Shu, T. , & Niu, W. (2019). Comparison between movement‐cased and task‐based mirror therapies on improving upper limb functions in patients with stroke: A pilot randomized controlled trial. Frontiers in Neurology, 10, 288.
    1. Cavanna, A. E. , & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129, 564–583. 10.1093/brain/awl004
    1. Christie, B. (2000). Doctors revise Declaration of Helsinki. BMJ, 321, 913 10.1136/bmj.321.7266.913
    1. Cook, R. , Bird, G. , Catmur, C. , Press, C. , & Heyes, C. (2014). Mirror neurons: From origin to function. The Behavioral and Brain Sciences, 37, 177–192. 10.1017/S0140525X13000903
    1. Corbetta, M. , & Shulman, G. L. (2002). Control of goal‐directed and stimulus‐driven attention in the brain. Nature Reviews Neuroscience, 3, 201–215. 10.1038/nrn755
    1. Cui, X. , Bray, S. , Bryant, D. M. , Glover, G. H. , & Reiss, A. L. (2011). A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. NeuroImage, 54, 2808–2821. 10.1016/j.neuroimage.2010.10.069
    1. Cunningham, S. I. , Tomasi, D. , & Volkow, N. D. (2017). Structural and functional connectivity of the precuneus and thalamus to the default mode network. Human Brain Mapping, 38, 938–956. 10.1002/hbm.23429
    1. Deconinck, F. J. , Smorenburg, A. R. , Benham, A. , Ledebt, A. , Feltham, M. G. , & Savelsbergh, G. J. (2015). Reflections on mirror therapy: A systematic review of the effect of mirror visual feedback on the brain. Neurorehabilitation and Neural Repair, 29, 349–361. 10.1177/1545968314546134
    1. Dohle, C. , Kleiser, R. , Seitz, R. J. , & Freund, H. J. (2004). Body scheme gates visual processing. Journal of Neurophysiology, 91, 2376–2379. 10.1152/jn.00929.2003
    1. Ertelt, D. , Small, S. , Solodkin, A. , Dettmers, C. , McNamara, A. , Binkofski, F. , & Buccino, G. (2007). Action observation has a positive impact on rehabilitation of motor deficits after stroke. NeuroImage, 36(Suppl 2), T164–T173. 10.1016/j.neuroimage.2007.03.043
    1. Frankenstein, U. , Wennerberg, A. , Richter, W. , Bernstein, C. , Morden, D. , Rémy, F. , & Mcintyre, M. (2003). Activation and deactivation in blood oxygenation level dependent functional magnetic resonance imaging. Concepts in Magnetic Resonance, 16, 63–70. 10.1002/cmr.a.10054
    1. Freeze, B. S. , Kravitz, A. V. , Hammack, N. , Berke, J. D. , & Kreitzer, A. C. (2013). Control of basal ganglia output by direct and indirect pathway projection neurons. The Journal of Neuroscience, 33, 18531–18539. 10.1523/JNEUROSCI.1278-13.2013
    1. Fritzsch, C. , Wang, J. , Dos Santos, L. F. , Mauritz, K. H. , Brunetti, M. , & Dohle, C. (2014). Different effects of the mirror illusion on motor and somatosensory processing. Restorative Neurology and Neuroscience, 32, 269–280.
    1. Fukumura, K. , Sugawara, K. , Tanabe, S. , Ushiba, J. , & Tomita, Y. (2007). Influence of mirror therapy on human motor cortex. International Journal of Neuroscience, 117, 1039–1048. 10.1080/00207450600936841
    1. Funase, K. , Tabira, T. , Higashi, T. , Liang, N. , & Kasai, T. (2007). Increased corticospinal excitability during direct observation of self‐movement and indirect observation with a mirror box. Neuroscience Letters, 419, 108–112. 10.1016/j.neulet.2007.04.025
    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. Experimental Brain Research, 163, 118–122. 10.1007/s00221-005-2226-9
    1. Hamzei, F. , Lappchen, C. H. , Glauche, V. , Mader, I. , Rijntjes, M. , & Weiller, C. (2012). Functional plasticity induced by mirror training: The mirror as the element connecting both hands to one hemisphere. Neurorehabilitation and Neural Repair, 26, 484–496. 10.1177/1545968311427917
    1. Hoshi, Y. , Kobayashi, N. , & Tamura, M. (2001). Interpretation of near‐infrared spectroscopy signals: A study with a newly developed perfused rat brain model. Journal of Applied Physiology, 90, 1657–1662. 10.1152/jappl.2001.90.5.1657
    1. Huppert, T. J. , Diamond, S. G. , Franceschini, M. A. , & Boas, D. A. (2009). HomER: A review of time‐series analysis methods for near‐infrared spectroscopy of the brain. Applied Optics, 48, D280–D298. 10.1364/AO.48.00D280
    1. Inagaki, Y. , Seki, K. , Makino, H. , Matsuo, Y. , Miyamoto, T. , & Ikoma, K. (2019). Exploring hemodynamic responses using mirror visual feedback with electromyogram‐triggered stimulation and functional near‐infrared spectroscopy. Frontiers in Human Neuroscience, 13, 60 10.3389/fnhum.2019.00060
    1. Jankowska, E. , & Edgley, S. A. (2006). How can corticospinal tract neurons contribute to ipsilateral movements? A question with implications for recovery of motor functions. The Neuroscientist, 12, 67–79. 10.1177/1073858405283392
    1. Jegatheeswaran, G. , Vesia, M. , Isayama, R. , Gunraj, C. , & Chen, R. (2018). Increases in motor cortical excitability during mirror visual feedback of a precision grasp is influenced by vision and movement of the opposite limb. Neuroscience Letters, 681, 31–36. 10.1016/j.neulet.2018.05.026
    1. Kang, Y. J. , Ku, J. , Kim, H. J. , & Park, H. K. (2011). Facilitation of corticospinal excitability according to motor imagery and mirror therapy in healthy subjects and stroke patients. Annals of Rehabilitation Medicine, 35, 747–758. 10.5535/arm.2011.35.6.747
    1. Kumru, H. , Albu, S. , Pelayo, R. , Rothwell, J. , Opisso, E. , Leon, D. , … Tormos, J. M. (2016). Motor cortex plasticity during unilateral finger movement with mirror visual feedback. Neural Plasticity, 2016, 1–8. 10.1155/2016/6087896
    1. Lancaster, J. L. , Woldorff, M. G. , Parsons, L. M. , Liotti, M. , Freitas, C. S. , Rainey, L. , … Fox, P. T. (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping, 10, 120–131. 10.1002/1097-0193(200007)10:3<120:AID-HBM30>;2-8
    1. Lu, M. K. , Arai, N. , Tsai, C. H. , & Ziemann, U. (2012). Movement related cortical potentials of cued versus self‐initiated movements: Double dissociated modulation by dorsal premotor cortex versus supplementary motor area rTMS. Human Brain Mapping, 33, 824–839. 10.1002/hbm.21248
    1. Lundy‐Ekman, L. (2007). Neurocience: Fundamentals for rehabilitation (3rd ed.). St. Louis, MO: Saunders, Elsevier Inc.
    1. Marchand, W. R. , Lee, J. N. , Thatcher, J. W. , Thatcher, G. W. , Jensen, C. , & Starr, J. (2007). Motor deactivation in the human cortex and basal ganglia. NeuroImage, 38, 538–548. 10.1016/j.neuroimage.2007.07.036
    1. Matthys, K. , Smits, M. , Van der Geest, J. N. , Van der Lugt, A. , Seurinck, R. , Stam, H. J. , & Selles, R. W. (2009). Mirror‐induced visual illusion of hand movements: A functional magnetic resonance imaging study. Archives of Physical Medicine and Rehabilitation, 90, 675–681. 10.1016/j.apmr.2008.09.571
    1. Mehnert, J. , Brunetti, M. , Steinbrink, J. , Niedeggen, M. , & Dohle, C. (2013). Effect of a mirror‐like illusion on activation in the precuneus assessed with functional near‐infrared spectroscopy. Journal of Biomedical Optics, 18, 066001 10.1117/1.JBO.18.6.066001
    1. Michielsen, M. E. , Smits, M. , Ribbers, G. M. , Stam, H. J. , van der Geest, J. N. , Bussmann, J. B. , & Selles, R. W. (2011). The neuronal correlates of mirror therapy: An fMRI study on mirror induced visual illusions in patients with stroke. Journal of Neurology, Neurosurgery, and Psychiatry, 82, 393–398. 10.1136/jnnp.2009.194134
    1. Molenberghs, P. , Cunnington, R. , & Mattingley, J. B. (2009). Is the mirror neuron system involved in imitation? A short review and meta‐analysis. Neuroscience and Biobehavioral Reviews, 33, 975–980. 10.1016/j.neubiorev.2009.03.010
    1. Nachev, P. , Kennard, C. , & Husain, M. (2008). Functional role of the supplementary and pre‐supplementary motor areas. Nature Reviews Neuroscience, 9, 856–869. 10.1038/nrn2478
    1. Nojima, I. , Mima, T. , Koganemaru, S. , Thabit, M. N. , Fukuyama, H. , & Kawamata, T. (2012). Human motor plasticity induced by mirror visual feedback. Journal of Neuroscience, 32, 1293–1300. 10.1523/JNEUROSCI.5364-11.2012
    1. Pekna, M. , Pekny, M. , & Nilsson, M. (2012). Modulation of neural plasticity as a basis for stroke rehabilitation. Stroke, 43, 2819–2828. 10.1161/STROKEAHA.112.654228
    1. Raichle, M. E. (2015). The brain's default mode network. Annual Review Neuroscience, 38, 433–447. 10.1146/annurev-neuro-071013-014030
    1. Ramachandran, V. S. , Rogers‐Ramachandran, D. , & Cobb, S. (1995). Touching the phantom limb. Nature, 377, 489–490. 10.1038/377489a0
    1. Rizzolatti, G. , & Craighero, L. (2004). The mirror‐neuron system. Annual Review of Neuroscience, 27, 169–192. 10.1146/annurev.neuro.27.070203.144230
    1. Saleh, S. , Adamovich, S. V. , & Tunik, E. (2014). Mirrored feedback in chronic stroke: Recruitment and effective connectivity of ipsilesional sensorimotor networks. Neurorehabilitation and Neural Repair, 28, 344–354. 10.1177/1545968313513074
    1. Sheth, S. A. , Nemoto, M. , Guiou, M. , Walker, M. , Pouratian, N. , & Toga, A. W. (2004). Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic tesponses. Neuron, 42, 347–355.
    1. Shinoura, N. , Suzuki, Y. , Watanabe, Y. , Yamada, R. , Tabei, Y. , Saito, K. , & Yagi, K. (2008). Mirror therapy activates outside of cerebellum and ipsilateral M1. NeuroRehabilitation, 23, 245–252.
    1. Strangman, G. , Culver, J. P. , Thompson, J. H. , & Boas, D. A. (2002). A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. NeuroImage, 17, 719–731. 10.1006/nimg.2002.1227
    1. Thieme, H. , Morkisch, N. , Mehrholz, J. , Pohl, M. , Behrens, J. , Borgetto, B. , & Dohle, C. (2018). Mirror therapy for improving motor function after stroke. The Cochrane Database of Systematic Reviews, 7, Cd008449 10.1002/14651858.CD008449.pub3
    1. Toh, S. F. M. , & Fong, K. N. K. (2012). A systematic review of the effectiveness of mirror therapy in training upper limb hemiparesis after stroke. Hong Kong Journal of Occupational Therapy, 22(2), 84–95.
    1. Wang, J. , Fritzsch, C. , Bernarding, J. , Holtze, S. , Mauritz, K. H. , Brunetti, M. , & Dohle, C. (2013). A comparison of neural mechanisms in mirror therapy and movement observation therapy. Journal of Rehabilitation Medicine, 45, 410–413. 10.2340/16501977-1127
    1. Wang, J. , Fritzsch, C. , Bernarding, J. , Krause, T. , Mauritz, K. H. , Brunetti, M. , & Dohle, C. (2013). Cerebral activation evoked by the mirror illusion of the hand in stroke patients compared to normal subjects. NeuroRehabilitation, 33, 593–603.
    1. Xia, M. , Wang, J. , & He, Y. (2013). BrainNet viewer: A network visualization tool for human brain connectomics. PLoS ONE, 8, e68910 10.1371/journal.pone.0068910
    1. Yarossi, M. , Manuweera, T. , Adamovich, S. V. , & Tunik, E. (2017). The effects of mirror feedback during target directed movements on ipsilateral corticospinal excitability. Frontiers in Human Neuroscience, 11, 242 10.3389/fnhum.2017.00242
    1. Yavuzer, G. , Selles, R. , Sezer, N. , Sütbeyaz, S. , Bussmann, J. B. , Köseoğlu, F. , … Stam, H. J. (2008). Mirror therapy improves hand function in subacute stroke: A randomized controlled trial. Archives of Physical Medicine and Rehabilitation, 89, 393–398. 10.1016/j.apmr.2007.08.162
    1. Ye, J. C. , Tak, S. , Jang, K. E. , Jung, J. , & Jang, J. (2009). NIRS‐SPM: Statistical parametric mapping for near‐infrared spectroscopy. NeuroImage, 44, 428–447. 10.1016/j.neuroimage.2008.08.036
    1. Yeudall, L. T. , Fromm, D. , Reddon, J. R. , & Stefanyk, W. O. (1986). Normative data stratified by age and sex for 12 neuropsychological tests. Journal of Clinical Psychology, 42, 918–946. 10.1002/1097-4679(198611)42:6<918:AID-JCLP2270420617>;2-Y
    1. Zhang, J. J. Q. , Fong, K. N. K. , Welage, N. , & Liu, K. P. Y. (2018). The activation of the mirror neuron system during action observation and action execution with mirror visual feedback in stroke: A systematic review. Neural Plasticity, 2018, 1–14. 10.1155/2018/2321045

Source: PubMed

3
Tilaa