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Annals of Physical and Rehabilitation Medicine xxx (2015) xxx–xxx

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Update article

Repetitive transcranial magnetic stimulation and transcranial direct

current stimulation in motor rehabilitation after stroke: An update
W. Klomjai a, A. Lackmy-Vallée b, N. Roche c,d, P. Pradat-Diehl b,e, V. Marchand-Pauvert b,
R. Katz b,*,e
a
Faculty of Physical Therapy, Mahidol University, 73170 Nakonpathom, Thailand
b
Inserm, laboratoire d’imagerie biomédicale, Sorbonne universités, UPMC université Paris 06, CNRS, 75013 Paris, France
c
EA 4497, University Versailles-Saint-Quentin, Garches, France
d
Service d’explorations fonctionnelles, hôpital Raymond-Poincaré, AP–HP, 92380 Garches, France
e
Service de médecine physique et réadaptation, groupe hospitalier Pitié-Salpêtrière-Charles-Foix, AP–HP, France

A R T I C L E I N F O A B S T R A C T

Article history: Stroke is a leading cause of adult motor disability. The number of stroke survivors is increasing in
Received 26 March 2015 industrialized countries, and despite available treatments used in rehabilitation, the recovery of motor
Accepted 19 May 2015 functions after stroke is often incomplete. Studies in the 1980s showed that non-invasive brain
stimulation (mainly repetitive transcranial magnetic stimulation [rTMS] and transcranial direct current
Keywords: stimulation [tDCS]) could modulate cortical excitability and induce plasticity in healthy humans. These
rTMS findings have opened the way to the therapeutic use of the 2 techniques for stroke. The mechanisms
tDCS
underlying the cortical effect of rTMS and tDCS differ. This paper summarizes data obtained in healthy
Stroke
Plasticity
subjects and gives a general review of the use of rTMS and tDCS in stroke patients with altered motor
Motor control functions. From 1988 to 2012, approximately 1400 publications were devoted to the study of non-
invasive brain stimulation in humans. However, for stroke patients with limb motor deficit, only
141 publications have been devoted to the effects of rTMS and 132 to those of tDCS. The Cochrane review
devoted to the effects of rTMS found 19 randomized controlled trials involving 588 patients, and that
devoted to tDCS found 18 randomized controlled trials involving 450 patients. Without doubt, rTMS and
tDCS contribute to physiological and pathophysiological studies in motor control. However, despite the
increasing number of studies devoted to the possible therapeutic use of non-invasive brain stimulation
to improve motor recovery after stroke, further studies will be necessary to specify their use in
rehabilitation.
ß 2015 Elsevier Masson SAS. All rights reserved.

1. Introduction (rTMS < 1 Hz) reduces the excitability of the motor cortex, thus
decreasing the MEP amplitude, whereas high-frequency rTMS
Since the 1980s, the development of non-invasive techniques (>5 Hz) increases it (Fig. 1). Anodal transcranial direct current
(electrodes simply positioned on the scalp over the target brain stimulation (tDCS) increases the motor cortex excitability and
area) allowing for reversible manipulation of the cortex excitability cathodal tDCS decreases its excitability (Fig. 1). The effects of rTMS
has paved the way to physiological studies in healthy humans. In a and tDCS are not limited to the motor cortex target area but also
second step, these non-invasive techniques were introduced in affect distant interconnected brain and spinal networks [3–9]. Both
pathophysiological studies. To briefly summarize the main data rTMS and tDCS induce after-effects [3], which is a powerful
[1,2], these studies reveal that isolated transcranial magnetic argument to explore their possible therapeutic effects.
stimulation (TMS) applied over the motor cortex induces a motor Stroke is a leading cause of long-term adult disability, and the
evoked potential (MEP) in the target muscle recorded by surface number of patients with chronic motor deficit after stroke is
electromyography (EMG) (Fig. 1). Low-frequency repetitive TMS increasing in industrialized countries, despite classical rehabilita-
tion techniques. In the 2004 review by Dobkin, listing the current
strategies for stroke rehabilitation, only 60% of patients with
* Corresponding author. hemiparesis achieved functional independence in simple activities
E-mail address: rose.katz@upmc.fr (R. Katz). of daily living [10]. The author also stressed that the effect of

http://dx.doi.org/10.1016/j.rehab.2015.05.006
1877-0657/ß 2015 Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Klomjai W, et al. Repetitive transcranial magnetic stimulation and transcranial direct current
stimulation in motor rehabilitation after stroke: An update. Ann Phys Rehabil Med (2015), http://dx.doi.org/10.1016/
j.rehab.2015.05.006
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Fig. 1. Action of repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS). A–B. rTMS action. A. Low-frequency rTMS effects: the
upper line represents motor-evoked potential (MEP) in the target muscle. With increasing intensity of isolated TMS, the amplitude of MEP increases. The lower line represents
the MEP size after rTMS. Note that the MEP size decreases after low-frequency rTMS. B. High-frequency rTMS effects: upper line represents MEP in the target muscle. With
increasing intensity of isolated TMS, the amplitude of MEP increases. The lower line represents MEP amplitude after rTMS. Note that the MEP size increases after high-
frequency rTMS (adapted from Valero-Cabré et al., 2011 [22]). C–E. tDCS action C. Spontaneous discharge of cortical neurons before tDCS intervention. D. Decrease of the
spontaneous discharge after inhibitory cathodal tDCS. E. Increase of spontaneous discharge after anodal tDCS.

therapeutics is limited during the acute stage and the management subjects show no evidence of increased ipsilateral MEP amplitudes.
of stroke mainly focuses on secondary prevention and rehabilitation. The descending projections from upper motoneurones are not
The search to improve rehabilitation during the last decades has limited to the spinal motor neurones but are also propriospinal
led to different strategies to manipulate or induce brain plasticity. nuclei and spinal interneurons [4,7–9,16]. In a given hemisphere,
An increasing number of studies, involving rTMS and tDCS, are fMRI and magneto-encephalography studies have demonstrated
devoted to their possible therapeutic effects to improve motor that brain stimulation applied over the motor cortex may affect
functions after stroke [3,11–15]. These therapeutic trials consisted many brain regions at a distance involving other cerebral areas,
of excitatory stimuli applied on the motor cortex with a lesion to basal ganglia and cerebellum. Finally, the homologous cortical area
increase the efficacy of the remaining cells; inhibitory stimuli exhibits mutual inhibitory connections between the 2 hemispheres
applied on the non-lesioned cortex to decrease the inhibitory [3,17].
connections from the non-lesioned hemisphere to the lesioned In summary, it must be remembered that non-invasive brain
one; and both stimulations combined, with or without traditional stimulation over the motor cortex induces changes in the target
rehabilitation and with or without sham stimulation. These studies motor area but also in many cortico-subcortical and spinal
differ by the characteristics of the stimulation and number of structures. The likely excessive interhemispheric inhibition (IHI)
sessions. The outcome measures used to objectively determine the from the non-lesioned hemisphere after stroke has led to exploring
possible effect of these stimulations differed among studies, the possible therapeutic effects of inhibitory stimulation applied to
including in the assessment of the clinical motor function, muscle the non-lesioned hemisphere and also dual stimulation (excitatory
force or spasticity scales; appreciation of daily living; functional on the lesioned hemisphere and inhibitory on the non-lesioned
MRI (fMRI); and electrophysiology. They also differed in whether hemisphere) (Fig. 2). In recent years, 4 review articles [11–13,18]
the possible effect was tested during the intervention, immediately have summed up the therapeutic trials of rTMS and tDCS
after or at longer time after the end of the intervention. performed for about 10 years. In searching MEDLINE via PubMed
in February 2015 to identify the trials of rTMS and tDCS
2. Background summary interventions in stroke patients with limb motor deficit, we found
about 141 references for rTMS and 132 for tDCS. As reported in the
The mechanisms underlying the effects of rTMS and tDCS 4 reviews quoted above, about 1400 publications involved non-
applied over the motor cortex are fully described in this special invasive brain stimulation in humans, 180 of these devoted to
issue [1,2]. Here, we summarize the central nervous system stroke patients.
structures that these stimulations likely involve. Excitatory The criteria used by the authors of these 4 reviews to retain
stimulation enhances the excitability of the motor cortex under studies for meta-analysis differ as follows:
the electrodes, thus inducing a facilitatory effect on the contralat-
eral corticospinal tract and the spinal motor neurons. This effect is  Ayache et al. [11] retained all studies devoted to the possible
revealed by an increase in MEP amplitude (Fig. 1). The stimulation therapeutic effects of rTMS and tDCS on motor function in stroke
over the contralateral motor cortex also likely activates the patients. The authors excluded studies of only purely neuro-
ipsilateral corticospinal tract in stroke patients, but healthy physiological evaluation. Therefore, 66 studies involving

Please cite this article in press as: Klomjai W, et al. Repetitive transcranial magnetic stimulation and transcranial direct current
stimulation in motor rehabilitation after stroke: An update. Ann Phys Rehabil Med (2015), http://dx.doi.org/10.1016/
j.rehab.2015.05.006
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Fig. 2. rTMS and tDCS location. A. tDCS or rTMS is applied over the lesioned hemisphere: an excitatory stimulation is used. B. tDCS or rTMS is applied over the non-lesioned
hemisphere: an inhibitory stimulation is used to reduce the interhemispheric inhibition drive from the non-lesioned to the lesioned hemisphere. C. Dual stimulation:
excitatory stimulation on the lesioned hemisphere and inhibitory stimulation on the non-lesioned hemisphere.

1785 patients (1343 for rTMS studies and 442 for tDCS studies) 3.1. rTMS
were analyzed;
 the review by Hsu et al. [18] related to rTMS effects. The criteria The Cochrane review [12] included 588 patients aged 50 to
used were number of patients involved in each study >5 and 75 years; 30% to 80% were males (according to the different
only randomized controlled trials. Thus, the authors retained studies). The time between the stroke onset and the start of the
18 studies involving 392 patients; intervention varied from 4 hr to 6 years. The aim of the review was
 the Cochrane review [12] focused on the effects of rTMS for to assess efficacy and safety of rTMS for improving motor function
improving function after stroke. Randomized controlled trials in patients with stroke. The side effects were minimal, including
coupling rTMS therapeutics with sham or control interventions small headaches and local discomfort at the site of the stimulation.
were included. The studies reporting only laboratory parameters The possible rTMS efficacy was tested whatever the characteristics of
were excluded. After screening 2431 titles and abstracts, the the stroke (area, cortical or subcortical lesions, haemorrhagic or
authors included 19 papers involving 588 patients; ischemic origin), the characteristics of the stimulation (low frequency
 the Cochrane review [13] described the effects of tDCS. Only applied over the non-lesioned hemisphere or high frequency applied
randomized controlled trials and randomized controlled cross- on the lesioned hemisphere), and the time between stroke onset and
over trials were included. From 6231 records identified via intervention. The evidence did not support the routine use of rTMS for
database searching, the authors eliminated duplicate records the treatment of stroke. Subgroup analysis did not reveal any
(2726) and retained only studies meeting Cochrane criteria. difference between stimulation of the lesioned and non-lesioned
Thus, only 18 studies involving 450 patients were retained for cortex.
further analysis. The review by Hsu et al. published in 2012 [18] targeted upper-
limb motor-function studies in 392 stroke patients. Hence, the side
3. Main data effects were extremely limited (4 patients). The meta-analysis
suggested that rTMS had a positive effect on motor recovery,
Whatever the aim of the non-invasive brain stimulation especially for patients with subcortical stroke. Low-frequency
(excitatory or inhibitory) or type, rTMS or tDCS, the studies rTMS over the unaffected hemisphere may be more beneficial than
mostly dealt with upper-limb motor function. The possible rTMS over the affected hemisphere. However, the authors stressed
improvement of upper-limb motor function was assessed mainly that further studies in a larger population are required to better
by clinical tests and clinical scales of generic activities of daily elucidate the differential roles of various rTMS protocols in stroke.
living, improvement of hand functions, muscle force and The review by Ayache et al. published in 2012 [11] included
spasticity. More accurate tests such as neurophysiological and 1343 patients. The authors divided studies into 4 categories:
neuroimaging tools were rarely used even though clinical
assessment alone has low prognostic accuracy [19]. These studies  low-frequency rTMS (inhibitory effects applied on the non-
differed in number of patients (from <10 to >200), the stroke lesioned hemisphere) in the acute or post-acute phase (5 days to
onset, the presence of sham stimulation, the presence of 3 months after stroke), involving 139 patients;
traditional rehabilitation coupled with non-invasive brain stim-  the same inhibitory stimulation applied in the chronic phase
ulation, the type of stroke (cortical or sub-cortical), the time (4 months to 12 years), involving 682 patients;
between 2 sessions in case of repetitive sessions, and the time  high-frequency rTMS (excitatory stimulation applied on the
between the test and the end of the intervention. lesioned cortex) in the acute phase, involving 182 patients;

Please cite this article in press as: Klomjai W, et al. Repetitive transcranial magnetic stimulation and transcranial direct current
stimulation in motor rehabilitation after stroke: An update. Ann Phys Rehabil Med (2015), http://dx.doi.org/10.1016/
j.rehab.2015.05.006
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 the same excitatory stimulation in the chronic phase, involving 4.2. What is currently acquired?
327 patients.
Physiological studies of both animals and humans have
demonstrated that rTMS and tDCS (see corresponding papers in
Whatever the category, the studies were almost completely this issue [1,2]) reversibly modulate the excitability of the cortex
devoted to upper-limb motor function. However, the studies were and may induce after-effects. These findings have opened the way
heterogeneous given the characteristics of the stimulation, to pathophysiological studies in humans. By coupling non-invasive
number of patients, number of sessions when the intervention stimulation with electrophysiological and imaging studies, owing
was repeated, time between stroke onset and intervention, type of to neural connectivity, rTMS and tDCS modify the excitability of
stroke (cortical or subcortical), presence of traditional rehabilita- the target brain area and also at a distance (other brain areas,
tion coupled with rTMS intervention, and presence of sham cerebellum, spinal cord networks, contralateral brain area). For
stimulation. In a few cases, the clinical evaluation was coupled both rTMS and tDCS, changes induced at a distance from the motor
with electrophysiological tests. Most of the individual studies cortex area targeted by the stimulation have not been fully
reported clinical improvement of upper-limb motor function, more documented, and their possible role in the effects induced by the
commonly found in patients with subcortical lesions, when the stimulation over the motor cortex remain to be explored. To induce
rTMS intervention was coupled with traditional rehabilitation, and after-effects is likely important to favour the therapeutic effects.
when the stimulation was applied over the non-lesioned However, the stimulation parameters needed to regularly evoke
hemisphere. after-effects remain to be explored.

3.2. tDCS 4.3. Therapeutic trials

The Cochrane review [13] assessed the effects of tDCS on Therapeutic trials of rTMS and tDCS aim to increase the
activities of daily living and motor function in stroke patients. It excitability of the lesioned hemisphere to enhance the motor
included 455 patients, >18 years old, regardless of the initial level control originating from the lesioned hemisphere and decrease the
of impairment and duration of stroke. All kinds of tDCS (anodal, excitability of the non-lesioned hemisphere to reduce the IHI drive
cathodal or dual) were tested. Analysis of 6 studies involving from the non-lesioned to lesioned hemisphere. More recently, dual
326 patients regarding activities of daily living found an effect of stimulation (excitatory stimulation on the lesioned hemisphere
tDCS at follow-up but not at the end of the intervention. Regarding and inhibitory stimulation on the non-lesioned hemisphere) has
upper-limb function, the authors found an effect of tDCS at the end been introduced. Guidelines for non-invasive stimulations have
of the intervention but not at the end of follow-up. The authors been established, and thus side-effects are rarely reported. The
concluded low-quality evidence of the effectiveness of tDCS versus possibility of non-invasively modifying the brain cortex excitabil-
control for improving activities of daily living and functions after ity and the existence of after-effects have led to a number of
stroke. therapeutic trials of stroke patients with motor deficits, aphasia or
Ayache et al. [11] studied the effects of tDCS in 388 patients, spatial neglect and also patients with psychiatric diseases.
using the same classification as for rTMS: excitatory stimulation However, as stressed by Hao et al. [12] in their Cochrane review,
(anodal tDCS applied over the lesioned cortex) in the acute or post- the available evidence does not support the routine use of rTMS for
acute phase (2 days to 3 months), involving 169 patients; motor function treatment after stroke. The review by Elsner et al.
excitatory stimulation in the chronic phase (1–7 years), involving [13], of tDCS, points to low-quality evidence of the effectiveness of
67 patients; inhibitory stimulation (cathodal tDCS applied on the tDCS as compared with a control in stroke patients. The rather
non-lesioned hemisphere) in the acute or post-acute phase disappointing conclusions from these reviews differ from those of
(10 days to 4 months), involving 124 patients; and inhibitory individual studies, which predominantly indicate an improvement
stimulation in the chronic phase (1–7 years), involving 28 patients. with rTMS or tDCS. The discrepancy between individual studies
The authors also included dual tDCS studies of 54 patients in the and meta-analysis findings is likely linked to heterogeneity of
chronic phase (5 months to 7 years). The heterogeneity among patients, clinical tests and features of the intervention, which are
studies was similar to that for rTMS studies. The smaller number of not standardized. Indeed, the number of inhibitory rTMS pulses
patients (388 in tDCS studies vs 1343 in rTMS studies) does not varied from 150 to 1800 among studies [11] and the number of
allow for more detailed conclusions. All studies performed in the rTMS sessions from 1 to 30 [11]. For tDCS studies, the intensity of
chronic phase suggested an improvement in upper-limb motor the current varied from 1 to 2 mA and the duration of sessions from
function. The effects were more variable in the acute phase. 7 to 30 min [11]. The context of the therapeutic trials also varied
among studies: non-invasive stimulations were applied with or
4. Comments without traditional rehabilitation techniques and with or without
sham stimulation. The outcome measures used to detect the
4.1. rTMS versus tDCS possible effects of non-invasive stimulation also differed. In most
studies, various clinical tests were performed, including muscle
A recent study by Priori et al. [20] compared rTMS and tDCS in force and spasticity scales, functional tests and activity of daily
terms of technology and costs, the possibility of obtaining a true living assessments. Of note, the means used to detect the possible
sham stimulation, focality of stimulation, the possibility of effects of rTMS and tDCS different greatly in physiological and
obtaining stimulation during a motor or cognitive task, and therapeutic trial studies. Physiological tests may be more
stimulus intensity and safety. The authors cautioned the reader appropriate to detect subtle changes than are clinical tests.
about no strict recommendation on which of the 2 techniques is Therefore, the clinical tools used in most therapeutic studies may
better for specific use, but they suggested that the high temporal not be sufficiently sensitive to detect modifications induced by
and spatial resolution of rTMS is useful in experiments that probe non-invasive motor cortex stimulations, and physiological studies
neurophysiologic effects on specific neuronal networks. In may be more able to detect them. Different types of stroke are
contrast, the simplicity of low-cost tDCS may be better for involved; cortical or subcortical, ischemic or haemorrhagic. The
investigations that do not target a selective population of neurons time between stroke onset and therapeutic trials also varied.
because it may occur in various clinical studies. Finally, most studies were devoted to the possible modification of

Please cite this article in press as: Klomjai W, et al. Repetitive transcranial magnetic stimulation and transcranial direct current
stimulation in motor rehabilitation after stroke: An update. Ann Phys Rehabil Med (2015), http://dx.doi.org/10.1016/
j.rehab.2015.05.006
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Please cite this article in press as: Klomjai W, et al. Repetitive transcranial magnetic stimulation and transcranial direct current
stimulation in motor rehabilitation after stroke: An update. Ann Phys Rehabil Med (2015), http://dx.doi.org/10.1016/
j.rehab.2015.05.006