CASE REPORT

Modulation of Event-related Desynchronization during
Motor Imagery with Transcranial Direct Current Stimulation
in a Patient with Severe Hemiparetic Stroke: A Case Report
Takamichi Tohyama,1 Toshiyuki Fujiwara,1 Jun Matsumoto, 2 Kaoru Honaga,1 Junichi Ushiba, 3
Tetsuya Tsuji,1 Kimitaka Hase1 and Meigen Liu1
1Department of Rehabilitation Medicine, School of Medicine, Keio University, Tokyo, Japan

2School of Fundamental Science and Technology, Graduate School of Keio University, Kanagawa, Japan
3Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University,

Kanagawa, Japan(Received for publication on December 8, 2010)(Revised for publication on April 25, 2011)(Accepted for publication on May 19, 2011)

Recently, surface electroencephalogram (EEG)-based brain–machine interfaces (BMI) have been used
for people with disabilities. As a BMI signal source, event-related desynchronization of alpha-band
EEG (8–13 Hz) during motor imagery (mu ERD), which is interpreted as desynchronized activities of
the activated neurons, is commonly used. However, it is often difficult for patients with severe hemiparesis to produce mu ERD of sufficient strength to activate BMI. Therefore, whether it is possible to modulate mu ERD during motor imagery with anodal transcranial direct-current stimulation (tDCS) was
assessed in a severe left hemiparetic stroke patient. EEG was recorded over the primary motor cortex(M1), and mu ERD during finger flexion imagery was measured before and after a 5-day course of tDCS
applied to M1. The ERD recorded over the affected M1 increased significantly after tDCS intervention.
Anodal tDCS may increase motor cortex excitability and potentiate ERD during motor imagery in patients with severe hemiparetic stroke. (Keio J Med 60 (4) : 114–118, December 2011)

Keywords: cortical excitability, noninvasive brain stimulation, electroencephalogram, brain–machine interface

Introduction
Recently, the usefulness of a brain–machine interface(BMI) that controls external devices based on neural activity of the brain during motor intention and imagery
has been reported for people with disabilities.1 It has beensuggested that BMI might be used to restore severely paretic limbs, and its application to rehabilitation is attracting a great deal of attention.2,3The event-related desynchronization of the alpha-band(8–13 Hz) electroencephalogram (EEG) (mu ERD) is interpreted as the desynchronized activities of the activatedneurons appearing during motor imagery. It is well rec-ognized that motor imagery induces an ERD of 8–13 Hz
over the motor cortex.4 This mu ERD, which reflects motor preparation and appears during motor imagery, hasbeen used with BMI to control external devices such as
robotic hands and motor-driven orthoses.5
It is known that the magnitude of ERD varies among individuals, which means that not all subjects can use ERDbased BMI. In people with brain injuries, it is known thatmeasurement of stable ERD is often difficult;6 therefore,
use of BMI in patients with severe motor disabilities has
been limited.
Cortical excitability can be modulated with transcranial direct-current stimulation (tDCS). Anodal tDCS in-

Reprint requests to: Toshiyuki Fujiwara, MD, Department of Rehabilitation Medicine, School of Medicine, Keio University, 35 Shinanomachi,
Shinjuku, Tokyo 160-8582, Japan, E-mail: tofuji@xc5.so-net.ne.jp
Copyright © 2011 by The Keio Journal of Medicine
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Keio J Med 2011; 60 (4): 114–118

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Fig. 1 MRI (FLAIR) images of the patient.
Each of the arrows shows low-intensity areas in the right posterior limb of the internal capsule (A) and corona radiata (B).

creases excitability of the motor cortex, whereas cathodal
tDCS decreases it.7 If application of tDCS could enhancecortical signals such as mu ERD, it would be beneficial
for the use of BMI in persons with severe motor paralysis
due to central nervous system injury. In this case report,
mu ERD induced by motor imagery was assessed in apatient with severe left hemiparetic stroke, and its modulation with anodal tDCS was examined.
Case Description
The patient was a 61-year-old man who had sufferedleft hemiparesis secondary to thalamic hemorrhage due
to long-lasting hypertension 3 years earlier. He was able
to walk independently with a single cane and an ankle–
foot orthosis. He could raise his paretic hand up to nipple
height from the knee, and he could flex his paretic fingers
but not extend them. His Fugl-Meyer upper extremity
motor score was 17. Light touch and position sensation
were severely disturbed. The modified Ashworth scale(MAS)8 score for the finger flexor muscles was 2. He
could not use his left upper extremity practically in daily
life, except for placing it on a sheet of paper on a desk
to hold it in place. He did not exhibit apraxia, aphasia,
agnosia, or memory deficit. Fluid-attenuated inversion
recovery (FLAIR) magnetic resonance imaging (MRI)
showed low-intensity areas in the right posterior limb of
the internal capsule and corona radiata (Fig. 1).
The protocol of tDCS intervention was approved by the
ethical committee of Keio University School of Medi-cine, and the patient gave his written informed consent toparticipate in the study. The patient received anodal tDCS
for 5 days. The tDCS was applied for 10 min through rectangular, saline-soaked, sponge electrodes (50 × 70 mm 2)with a battery-driven stimulator (CX-6650, Rolf Schneider Electronics, Gleichen, Germany) while the patient
sat on a chair with his hands placed over the armrests.
The stimulation intensity was set at 1 mA. The anodal
electrode was placed on C4 according to the international
10–20 system for placement of EEG electrodes. The cathodal electrode was placed on the contralateral supraorbital area.
Assessment of ERD
One day before and 1 day after the 5-day tDCS session, mu ERD with finger flexion imagery was measured.
To assess the long-term effect of the 5-day tDCS session,
we measured mu ERD 1 year later. The patient sat on achair with his hands placed over the armrests, his shoulders flexed to 10° and elbows flexed to 90°. The patient
was asked to imagine flexion of his paretic finger for 5 s
initiated with a visual cue on a computer monitor. EEG
signals were recorded with 20 Ag/AgCl disc electrodes(1 cm in diameter) with binaural references according
to the international 10–20 system of electrodes. To determine the electrode pair showing the largest ERD, alladjacent pairs of bipolar derivations of EEG were used tocheck for the presence of mu ERD following motor imagery. The selected bipolar EEG showing the largest ERD

Tohyama T, et al: Modulation of ERD during Motor Imagery with tDCS

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Table 1 Change of mu event-related desynchronization (ERD) value (%) in the affected and unaffected hemispheres during motor
imagery

Affected hemisphere ERD (SE)
Unaffected hemisphere ERD (SE)

Motor imagery of paretic fingers
Before (T1)
After (T2)
4.1(8.8)
25.1(6.2)**
32.1(10.1)
13.0 (6.0)*

Motor imagery of non-paretic fingers
Before (T1)
After (T2)
−4.6 (11.5)−2.8 (7.2)
26.6 (6.5)
19.6 (7.0)

tDCS, transcranial direct-current stimulation; SE, standard error.
Mann-Whitney U test: **p=0.001, *p<0.05 compared with before (T1) value.

was used for further analysis. A surface electromyogram(EMG) was used to check that no activity of bilateral firstdorsal interosseous muscles (FDI) appeared during motor
imagery.
Event-related trials of 5 s during motor imagery wereselected for off-line data processing. All trials were visually assessed, and trials with artifacts (resulting from eye
movement), as well as those with increased EMG activityof the right FDI, were excluded. All trials were segmented into successive 1-s windows with 100 overlapping
samples, and Fourier transformation with the Hanningwindow was applied to each segment. The power spectrum densities of each segment were estimated over thetrials by Welch’s averaged periodogram method.9
The mu ERD was expressed as the percentage power
decrease in relation to a 1-s reference interval before thepatient was notified to be “ready.” The ERD was calculated for each time (resolution of 0.1 s) and frequency(resolution of 0.98 Hz) according to Equation (1):ERD(f, t)=[(R(f) − A (f, t)) / R(f)] × 100 (%)(1)

Where A is the power spectrum density of the EEG ata certain frequency f [Hz] and time t [s] after the imagery
task was started, and R is the power spectrum at the same
frequency f [Hz] of the baseline period (a 1-s interval before “Ready” was displayed). The largest power decreaseduring motor imagery in the alpha band (8–13 Hz) was
selected as the value of mu ERD. Before tDCS application, the values of mu ERD were compared in all adjacentpairs of bipolar derivations of the EEG to determine theelectrode pair showing the largest value of mu ERD.10
Results
Table 1 shows the mu ERD changes in both hemispheres during motor imagery of the paretic and nonparetic fingers before (T1) and after (T2) a 5-day tDCS
session. Anodal tDCS applied to the affected hemispherefor 5 days increased mu ERD induced by paretic hand
imagery in the affected hemisphere and decreased it in
the unaffected hemisphere.
One year after the 5-day tDCS session, the mu ERD
during motor imagery of the paretic finger flexion was
25.1 ± 3.8% in the affected hemisphere and 26.4 ± 5.1% in
the unaffected hemisphere. Clinically, the MAS score forthe finger flexor muscles decreased from 2 to 1+ and theFugl-Meyer upper extremity motor score increased from17 to 20. The patient used his paretic upper extremity forholding a bag, in addition to pressing a sheet of paper on
the desk in his daily life. The MAS score, Fugl-Meyer
score and his paretic upper extremity function in his daily
life had been maintained for 1 year after the 5-day tDCS
treatment. The patient did not experience any adverse
side effects during the course of the study.
Discussion
This is the first report demonstrating that anodal tDCS
applied to the affected hemisphere can increase mu ERD
induced with motor imagery of paretic finger movement.
At baseline, mu ERD induced with motor imagery of paretic fingers was low in the affected hemisphere, while
it was high in the unaffected hemisphere. We thought itdifficult for our patient to imagine paretic finger movement because he had suffered from severe hemiparetic
stroke more than 3 years before the time of the study.
Furthermore, it has been reported that disuse of the upper extremity reduces cortical excitability during motor
imagery.11
Anodal tDCS increases motor cortex excitability. Previous studies suggest that cortical excitability changes induced with tDCS are due to modifications of membranepolarization and the synaptic mechanism.7,12 The ERD
mechanism is attributed to a decrease in the synchrony of the underlying neuronal population.13 Therefore,
ERD changes after tDCS may be explained by changes
in the oscillatory behavior of cortical neurons, such as
membrane potentials in the primary motor area, and theprobability of neurons firing according to input signals
in response to motor imagery. Matsumoto et al. showedthat mu ERD significantly increased after anodal tDCS,
whereas it significantly decreased after cathodal tDCS in
healthy subjects.14 There was a significant correlation between mu ERD and motor cortex excitability. The ERD
is suggested to be generated by the neural interconnection of the feedback loop involving the thalamo-corticalor cortico-cortical loop.13,15 tDCS seems to activate theintermediate neurons projecting to pyramidal tract neurons (PTN) in the cortex.16 Therefore it is suggested that
mu ERD could be modulated by a change in excitabil-Keio J Med 2011; 60 (4): 114–118

ity of the intermediate neurons projecting to the PTNs.
Increased cortical excitability results in more activatedand desynchronized neurons, which results in an ERD
increase.
It has been reported that the after effects of tDCS for
10 min at 1 mA continue for 10 min to 1 h.7,12 Reis et al.
showed the existence of a consolidation mechanism susceptible to anodal tDCS.17 Long-term effects induced by
tDCS may include the build up of new synapses, with themechanism of long-term potentiation and long-term depression critically involved. The glutamatergic system,in particular NMDA receptors,18 seems to be necessary
for induction and maintenance of neuroplastic after-effectexcitability enhancement by tDCS.19 It was supposed,
therefore, that 5 days of tDCS intervention resulted in asignificant increase of ERD in the affected hemisphere.
We found that anodal tDCS applied to the affected
hemisphere for 5 days decreased the ERD in the unaffected hemisphere. Increased motor cortex excitability in theaffected hemisphere could increase the inter-hemisphericinhibition from the affected to the unaffected hemisphereand reduce the compensatory activity of the unaffected
hemisphere.20
Besides modulation of cortical activity, repeated application of tDCS reduced spasticity in paretic fingers inthis case. Recently, Roche et al. showed that anodal tDCS
increased disynaptic reciprocal inhibition.21 This might
explain the observed decrease in spasticity with tDCS.
It was supposed that increased motor cortex excitability and decreased spasticity might induce improvementof upper extremity motor function. The improvementof motor function allowed the patient to use his paretic
upper extremity more than before. It has been easier forthe patient to imagine paretic finger movement than before. That could be one of the reasons why the change of
ERD in the affected hemisphere during imagery has been
maintained for 1 year after the 5-day tDCS session.
In this patient with a thalamic lesion, mu ERD with motor imagery was increased after anodal tDCS. Cicinelli etal. suggested that the changes in imagery-induced cortical excitability were not different in respect to the location of the stroke lesion in patients whose primary motor cortex was spared.22 However, further study should
address whether stroke lesion location may influence the
ERD change with motor imagery.
If application of tDCS can enhance cortical signals
such as mu ERD, it would be beneficial for the use of BMI
in patients with severe motor disabilities due to central
nervous system injury. However, this present study is acase report, and further larger-scale and more systematicstudies are needed to test the usefulness of this approach.
Acknowledgments
This study was partially supported by the Strategic

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Research Program for Brain Sciences (SRPBS) and a
Grant-in Aid for Scientific Research (C) (20500465) from
the Ministry of Education, Culture, Sports, Science andTechnology of Japan.
References
1. Birbaumer N, Weber C, Neuper C, Buch E, Haagen K, Cohen L:
Physiological regulation of thinking: brain-computer interface(BCI) research. Prog Brain Res 2006; 159: 369–391. [Medline][CrossRef]
2. Pfurtscheller G, Muller GR, Pfurtscheller J, Gerner HJ, Rupp R:‘Thought’ – control of functional electrical stimulation to restore
hand grasp in a patient with tetraplegia. Neurosci Lett 2003; 351:
33–36. [Medline] [CrossRef]
3. Pfurtscheller G, Neuper C: Future prospects of ERD/ERS in thecontext of brain-computer interface (BCI) developments. Prog
Brain Res 2006; 159: 433–437. [Medline] [CrossRef]
4. Neuper C, Pfrutscheller G: Event-related dynamics of corticalrhythms: frequency-specific features and functional correlates.
Int J Psychophysiol 2001; 43: 41–58. [Medline] [CrossRef]
5. Kübler A, Birbaumer N: Brain-computer interfaces and communication in paralysis: extinction of goal directed thinking incompletely paralysed patients? Clin Neurophysiol 2008; 119:2658–2666. [Medline] [CrossRef]
6. Platz T, Kim IH, Pintschovius H, Winter T, Kieselbach A,
Villringer K, Kurth R, Mauritz KH: Multimodal EEG analysis in
man suggests impairment-specific changes in movement-related
electric brain activity after stroke. Brain 2000; 123: 2475–2490.
[Medline] [CrossRef]
7. Nitsche MA, Paulus W: Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation.
J Physiol 2000; 527: 633–639. [Medline] [CrossRef]
8. Bohannon RW, Smith MB: Interrater reliability of a modified
Ashworth scale of muscle spasticity. Phys Ther 1987; 67: 206–
207. [Medline]
9. Welch PD: The use of fast Fourier transform for the estimationof power spectra: A method based on time averaging over short,modified periodograms. IEEE Trans Audio Electroacoust 1967;
15: 70–73. [CrossRef]
10. Pfurtscheller G, Neuper C: Motor imagery activates primary sensorimotor area in humans. Neurosci Lett 1997; 239: 65–68. [Medline] [CrossRef]
11. Kaneko F, Murakami T, Onari K, Kurumadani H, Kawaguchi K:
Decreased cortical excitability during motor imagery after disuse of an upper limb in humans. Clin Neurophysiol 2003; 114:
2397–2403. [Medline] [CrossRef]
12. Nitsche MA, Paulus W: Sustained excitability elevations inducedby transcranial DC motor cortex stimulation in humans. Neurology 2001; 57: 1899–1901. [Medline]
13. Pfurtscheller G, Lopes da Silva FH: Event-related EEG/MEG
synchronization and desynchronization: basic principles. Clin
Neurophysiol 1999; 110: 1842–1857. [Medline] [CrossRef]
14. Matsumoto J, Fujiwara T, Takahashi O, Liu M, Kimura A, Ushiba
J: Modulation of mu rhythm desynchronization during motor imagery by transcranial direct current stimulation. J Neuroeng Rehabil 2010, 7: 27. [Medline] [CrossRef]
15. Lopes da Silva F: Neural mechanisms underlying brain waves:from neural membranes to networks. Electroencephalogr Clin
Neurophysiol 1991; 79: 81–93. [Medline] [CrossRef]
16. Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W: Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 2003; 114:
600–604. [Medline] [CrossRef]
17. Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E,

118
Celnik PA, Krakauer JW: Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 2009; 106: 1590–
1595. [Medline] [CrossRef]
18. Paulus W: Outlasting excitability shifts induced by direct current
stimulation of the human brain. Suppl Clin Neurophysiol 2004;
57: 708–714. [Medline] [CrossRef]
19. Liebetanz D, Nitsche MA, Tergau F, Paulus W: Pharmacological approach to the mechanisms of transcranial DC-stimulationinduced after-effects of human motor cortex excitability. Brain
2002; 125: 2238–2247. [Medline] [CrossRef]

Tohyama T, et al: Modulation of ERD during Motor Imagery with tDCS
20. Dimyan MA, Cohen LG: Neuroplasticity in the context of motor
rehabilitation after stroke. Nat Rev Neurol 2011; 7: 76–85. [Medline] [CrossRef]
21. Roche N, Lackmy A, Achache V, Bussel B, Katz R: Impact oftranscranial direct current stimulation on spinal network excitability in humans. J Physiol 2009; 587: 5653–5664. [CrossRef]
22. Cicinelli P, Marconi B, Zaccagnini M, Pasqualetti P, Filippi MM,
Rossini PM: Imagery-induced cortical excitability changes instroke: a transcranial magnetic stimulation study. Cereb Cortex
2006; 16: 247–253. [Medline] [CrossRef]