Journal of the International Neuropsychological Society (2016), 22, 1–9.

Copyright © INS. Published by Cambridge University Press, 2016.

doi:10.1017/S1355617716000345

Cerebellar, but not Motor or Parietal, High-Density Anodal

Transcranial Direct Current Stimulation Facilitates Motor Adaptation

Michael Doppelmayr,1,2 Nils Henrik Pixa,1 AND Fabian Steinberg1

1
Institute of Sport Science, University of Mainz, Germany
2
Centre for Cognitive Neuroscience, Salzburg, Austria
(RECEIVED October 28, 2015; FINAL REVISION March 29, 2016; ACCEPTED April 5, 2016)

Abstract

Objectives: Although motor adaptation is a highly relevant process for both everyday life as well as rehabilitation many
details of this process are still unresolved. To evaluate the contribution of primary motor (M1), parietal and cerebellar
areas to motor adaptation processes transcranial direct current stimulation (tDCS) has been applied. We hypothesized that
anodal stimulation of the cerebellum and the M1 improves the learning process in mirror drawing, a task involving fine
grained and spatially well-organized hand movements. Methods: High definition tDCS (HD-tDCS) allows a focal
stimulation to modulate brain processes. In a single-session double-blind study, we compared the effects of different
anodal stimulation procedures. The groups received stimulation either at the cerebellum (CER), at right parietal (PAR), or
at left M1, and a SHAM group was included. Participants (n = 83) had to complete several mirror drawing tasks before,
during, and after stimulation. They were instructed to re-trace a line in the shape of a pentagonal star as fast and accurate
as possible. Tracing time (seconds) and accuracy (deviation in mm) have been evaluated. Results: The results indicated
that cerebellar HD-tDCS can facilitate motor adaptation in a single session. The stimulation at M1 showed only a
tendency to increase motor adaptation and these effects were visible only during the first part of the stimulation.
Stimulating the right parietal area, relevant for visuospatial processing did not lead to increased performance.
Conclusions: Our results suggest that motor adaptation relies to a great extent on cerebellar functions and HD-tDCS can
speed up this process. (JINS, 2016, 22, 1–9)

Keywords: tDCS, Mirror drawing, Motor learning, Psychomotor performance, Motor skills, Electrical stimulation of the brain

INTRODUCTION At a first glance, at least two substantially different types of

motor learning can be distinguished and are implemented
Motor learning is one of the most fundamental process in
in partly overlapping, but nevertheless distinct, neuronal
everyday life, in which sustained practice of a movement networks. While motor sequence learning (to learn a new
leads to performance improvements of several relevant
sequence of movements, like on a piano) is represented
aspects such as accuracy and velocity. In a review, Halsband
in a cortico-basal ganglia-thalamo-cortical loop, motor
and Lange (2006) described the neuronal structures involved
adaptation (learn to adapt to environmental perturbations)
in motor learning in detail. While tertiary motor areas
relies mostly on a cortico-cerebello-thalamo-cortical loop
include the prefrontal cortex, the cingulate cortex, and
(Doyon, Penhune, & Ungerleider, 2003). In addition, motor
pre-supplementary motor area, the secondary motor areas
learning can be divided into distinct stages: an early,
consist of the supplementary motor area proper, the premotor
fast learning stage, followed by consolidation; a second,
cortex, the inferior frontal cortex, the inferior and superior– slow learning stage, followed by automatization; and finally,
posterior parietal cortex, as well as the cerebellum. Finally
after some delay, the retention. Except within the first
the primary motor areas include the primary motor cortex
learning stage, the cortical regions involved are almost
(M1) and the basal ganglia (Halsband & Lange, 2006).
identical including primary motor and parietal areas. At the
first stage, however, for sequence learning, M1 and the
striatum are more relevant, while motor adaptation is to a
Correspondence and reprint requests to: Michael Doppelmayr, Institute
of Sport Science, University Mainz, Albert Schweitzer Straße 22, 55128 greater extent based on the parietal cortex and the cerebellum
Mainz Germany. E-mail: doppelma@uni-mainz.de (Penhune & Steele, 2012).
1
2 M. Doppelmayr et al.
Jeuptner and Weiller (1998) described several different
learning processes and the related brain structures in detail.
They analyzed motor sequence learning, decision making
and selection of movements, repetitive finger movements,
overlearned motor tasks, visuo-motor co-ordination, and
several additional motor learning processes. However, with
respect to our study they also described the learning of fine
grained movements as re-tracing a line and reported that the
cerebellum but not the basal ganglia are involved.
One technique to investigate and to modulate the func-
tionality of motor learning related areas is the transcranial
direct current stimulation (tDCS). This is a non-invasive
technique that allows the modulation of brain processes
(Antal & Paulus, 2008; Nitsche & Paulus, 2000, 2001) by
the application of small amounts of direct electrical current
to the scalp. As a result, the activity of the neuronal
tissue between anode and cathode can be altered. Depending
on the specific setup of the stimulation, this induced
modulation of the respective neural membrane thresholds
can lead to in- or decreased signal processing efficiency
(Bolognini, Pascual-Leone, & Fregni, 2009; Liebetanz,
2002; Priori, 2003). Even more, it has been demonstrated that
anodal tDCS (atDCS) coupled with motor training (Reis &
Fritsch, 2011; Stagg et al., 2011) can enhance the response
properties of different neuronal networks involved in motor
learning.
Until recently in most studies tDCS has been applied using
two large sponge electrodes (approximately 35 cm2) located
on distant brain areas. However, meanwhile high definition
(HD-tDCS) stimulation with smaller electrodes and multiple
return positions can be used (Ruffini, Fox, Ripolles, Miranda,
& Pascual-Leone, 2014). For example Dmochowski, Datta,
Bikson, Su, and Parra (2011) reported that the use of small
1.2 cm diameter electrodes as compared to large (distant) pad
electrodes increases focality of up to 80%. Thus, this
approach allows a more focal stimulation of a targeted brain
area, a methodological advantage that has recently been
emphasized again by Herrmann, Rach, Neuling, and Strüber
(2013). As outlined, standard tDCS used large electrodes at
distant areas (as from parietal to prefrontal) and, thus,
induced a current flow over long distances within the brain
with, to some extent, unknown effects. The local stimulation
approach, however, allows narrowing the area of anodal
stimulation. Whether this emerging new method will lead
to different and more elaborate results as compared to
conventional stimulation is an open question.
As primary motor cortical areas are critically involved in
motor behavior, it is self-evident that these regions are of
interest for the investigation of motor learning. Several TMS-
studies evaluating the size of motor evoked potentials have
demonstrated that tDCS applied to the respective motor areas
modulates excitability in a polarity-specific way. While in
most cases, but depending on the strength of the current and
stimulation duration, atDCS facilitates motor responses
(Antal, Polania, Schmidt-Samoa, Dechent, & Paulus, 2011;
Paulus, 2011), cathodal stimulation can reduce it (Nitsche
et al., 2005).
Furthermore, it has frequently been reported that atDCS
at motor areas facilitates skill acquisition (Antal, Varga,
Kincses, Nitsche, & Paulus, 2004; Reis et al., 2009;
Vollmann et al., 2013). Positive effects have been found for
different types of motor tasks. For example, in motor
sequence learning Vines (Vines, Nair, & Schlaug, 2006) and
Nitsche et al. (2003) reported increased performance in serial
reaction time tasks. However, Stagg et al. (2011) outlined the
importance of the timing of the stimulation procedure. While
anodal stimulation during the learning phase led to increases
in performance, the same stimulation preceding the perfor-
mance led to slower learning. Similar for motor adaptation
different results have been reported regarding the respective
learning stage. While Antal and colleagues (Antal, Nitsche,
Kincses, et al., 2004) described increases already during the
early learning phase, Galea reported this only for a later
retention interval (Galea, Vazquez, Pasricha, Xivry, &
Celnik, 2011).
In addition to the M1, other brain areas such as the
cerebellum are substantially involved in motor perfor-
mance. Although the cerebellum is important in several
processes besides those related to motor control (Stoodley &
Schmahmann, 2009), research has substantially focused on
its fundamental involvement in motor execution and motor
learning processes. As reported by Grimaldi (2014), it has
been demonstrated that the electrical field of cerebellar
atDCS can reach the cerebellum and modulate its neural
activity (Grimaldi et al., 2014).
These results are supported by the findings of Parazzini
et al. (2014) who used a realistic human head model for
computing the electric field and current density for cerebellar
tDCS. Using atDCS, it was demonstrated that cerebellar but
not motor stimulation speeds up motor adaptation (Galea
et al., 2011). In addition, it has been reported that the motor
performance increase is due rather to online than to offline
learning and is based on a reduction in errors and not on an
increase in speed (Cantarero et al., 2015). Similarly, Jayaram
et al. (2012) reported that anodal cerebellar tDCS increased
the spatial but not the temporal adaptation processes.
However, for cerebellar tDCS, it has to be kept in mind that,
with respect to the motor domain, the cerebellum is involved
to a larger extent in ipsilateral movements (as compared to
the M1 which is activated contralateral).
Furthermore, fundamentally involved in motor adaptation
is the parietal cortex (Doyon et al., 2003), which is known to
be functionally related to spatial attention and sensomotoric
integration (Gottlieb & Snyder, 2010). While in older studies
(Mesulam, 1981), spatial attention is described as a function
mainly of the right parietal cortex, recent reports draw a more
detailed picture. It has been outlined (Bolognini, Fregni,
Casati, Olgiati, & Vallar, 2010) that visual search processes
are based to a large extent on a neuronal network comprising
the posterior parietal cortex.
Even more, they report that right parietal atDCS coupled
with a visual search training can enhance the response prop-
erties of this network. Participants receiving atDCS showed
positive effects for visual exploration and visuospatial
Cerebellar tDCS increases motor adaptation
orienting for right hemispheric stimulation only. Attempting
to inhibit neuronal processing, Vicario and colleagues
(Vicario, Martino, & Koch, 2013) used cathodal stimulation
and found reduced temporal accuracy after right hemispheric
stimulation. Thus, right parietal atDCS might significantly
influence the performance in a visuomotor task like mirror
drawing by modulating processing speed or accuracy.
The present study focusses on the changes in performance
in a mirror drawing task; a task that involves exact motor
performance as well as visuospatial integration. We investi-
gate the effects of atDCS at cerebellar, right parietal and left
M1 location and included a sham stimulation as control.
Based on the functional importance of the cerebellum for
learning of fine grained movements, we hypothesized that
both anodal cerebellar and M1 stimulation will increase
performance and accuracy in a mirror guided line re-tracing
task. Effects of parietal stimulation with respect to perfor-
mance have not been reported so far; however, the funda-
mental involvement of the right parietal cortex in visuospatial
processing leads to the assumption that a stimulation of these
area might facilitate those learning processes as well.
METHODS
Subjects
We conducted a single-session double-blind study with
90 healthy, right-handed volunteers without neurological
disorders. Seven of the participants had to be excluded
because they were not able to draw the picture as fast as
requested (within 90 s). The remaining 83 participants
(39 female) (age M = 24.17 years; SD = 2.19) were pseudo-
randomly assigned to one of four groups receiving different
stimulations at either cerebellar (CER; n = 21), right parietal
(PAR; n = 17) or primary left motor cortex (M1; n = 13)
areas, as well as one control group (SHAM; n = 32).1 The
double-blind design was implemented by a “double-blind
mode” in the stimulation software (NIC, Neuroelectrics,
Barcelona, Spain).
Before stimulation, all subjects signed an informed consent
and were informed about all relevant issues of this experi-
ment according to the Declaration of Helsinki. Ethical
approval was obtained from the Deutsche Gesellschaft für
Psychologie (DGPs). Furthermore, all participants were
verbally screened for neurological problems, or any severe
medical condition, as well as about drug intake, as described
in the safety criteria for non-invasive brain stimulation (Keel,
Smith, & Wassermann, 2000; Rossi, Hallett, Rossini, &
Pascual-Leone, 2009). Dominant right-handedness was tes-
ted using the shortened handedness inventory with 10 items
(Oldfield, 1971). After the experimental session, all
1
The presented study was originally designed as two separate experi-
ments which were collapsed later. In both of these experiments, a SHAM
condition was implemented; this is the reason for a substantially higher
number of participants in the SHAM group.
3
participants were asked to report any side-effects, but none
have been reported.
Visuo-motor Tasks
Participants were seated at a table approximately 60 cm in
front of a mirror sized 35 × 33.5 cm. A wooden board was
placed between the mirror and the subject in a way that only
the mirror but not the table was visible. In the task, geo-
metrical figures printed on a white paper were placed on the
table between the mirror and the board and, thus, visible only
via the mirror. Participants were requested to trace the lines
with a pencil held in the right hand as quickly and accurately
as possible without raising the pencil from the paper. The
participant could see his/her hand only via the mirror. All
drawings in this experiment had to be completed with the
mirror feedback only.
Besides the training pictures, two different types of draw-
ings, a geometric pentagonal star as well as an asymmetrical
figure, were used in this study.2 These were always presented
via the mirror only. First participants were instructed to
draw three different figures (circle, cross, triangle) for
familiarization and training with the visually mirrored
feedback. Then, for the first time the picture of the star was
presented in the mirror and had to be re-traced as fast and
accurately as possible. This was used as baseline measure.
As depicted in Figure 1, a 21-min stimulation began during
which the participants had to perform the following tasks. In
the first 9 min of the stimulation, the star had to be traced
(trained) six times with 90 s allowed to complete each trial.
After these 9 min, still receiving the stimulation, an online-
test for speed and accuracy, equally to baseline measurement
was performed. In addition to the star, the irregular figure had
to be drawn; these two online tests lasted 3 min. This was
followed by again tracing of six stars in the remaining 9 min
of stimulation. Immediately following the offset of the sti-
mulation after the second series of stars, a post-test was
conducted. The stimulation equipment was then removed,
and 20 min after termination of the stimulation a retention test
was performed.
High-Definition Anodal Transcranial Direct
Current Stimulation (HD-atDCS)
To apply the HD-atDCS, a mobile computer controlled brain
stimulation device, which allows a multichannel application
(Bolognini et al., 2011; Bolognini, Olgiati, Rossetti, &
Maravita, 2010) was used (Starstim, Neuroelectrics,
Barcelona, Spain). Electrodes were positioned in a non-
conductive neoprene cap. HD-atDCS was applied by one
stimulation electrode and four return electrodes (3.14 cm2
each) filled with conductive electrolyte-gel. To ensure a
focal stimulation, 4 × 1 electrode montages were applied.
2
Due to presentation errors during the experiment, the results for the
irregular figure were erroneous and, thus, cannot be analyzed.
4 M. Doppelmayr et al.

As depicted in Figure 2 for CER, the anode was placed
midline above the cerebellum 10% below Oz, for PAR at
right parietal area P4, and for M1 at C3 covering the primary
motor area of the right hand.
To exclude effects that are due to different return electrode
montages, in all groups Oz, O2, P8, and PO8 were used
as return sites. The montages were chosen to optimize
stimulation of the target areas and selected according to
a computational head model (Ruffini et al., 2013). Direct
current was delivered at an intensity of 1 mA (current density
0.319 mA/cm2) at the anodal stimulation electrode. The
stimulation software (NIC, Neuroelectrics, Barcelona, Spain)
offers to split the return current to the four return electrodes.
Although the exact values are unknown due to different tissue
resistances, this resulted in a computational intensity of
approximately –0.25 mA (current density -0.080 mA/cm2) at
each return electrode.
Compared to previous studies using substantially larger
electrodes (e.g., Antal, Nitsche, Kincses, et al., 2004; Antal,
Nitsche, & Paulus, 2006), we induced significantly lower
current density. Return sites were kept identical in all mon-
tages of our HD-tDCS protocols and for the alignment of the
generated electric field to reach the target area. In the control
group (SHAM), the same montage of four return-electrodes
was used and the position of the fifth electrode was counter-
balanced among CER, P4, and C3. The sham tDCS was
applied with only 30 s of real stimulation. Each stimulation
session started and closed with a 30-s ramp-up and ramp-
down phase and had a duration of 21 min to ensure to com-
plete the whole mirror drawing task.
Adaptation Measurement
For quantification of visuo-motor adaptation, two parameters
were measured. While drawing time (seconds) was recorded
by the experimenter, error evaluation was performed by a
neutral evaluator blind to the group assignment of the sub-
jects. Tracing time for each drawing was defined as the time
taken to trace the mirrored picture from the starting point to
the end point. Accuracy was evaluated after the
experimental-session by using a template. This template
consisted of a grid of adjacent 2 × 2 mm squares that were
added on both sides of the star (see Figure 1b). Deviations
within the first square (inside and outside the figure) were not
counted as errors. Each square outside this tolerance area was
counted as an error, and the errors were added up.
Statistical Analysis
All data were normally distributed as screened with
Kolmogorov-Smirnov tests. To evaluate baseline differences,
one-way analyses of variance (ANOVAs) were calculated for
tracing time and tracing accuracy. For adaptation perfor-
mance, two-way ANOVAs with TIME (Pre, Online, Post,
Follow Up) and GROUP (CER, PAR, M1, SHAM) were
conducted once for tracing time and once for accuracy. In the
event of significant results, Bonferroni post hoc analyses
were calculated for pairwise comparisons. In addition,
Spearman correlations were calculated for the mean values of
tracing time and accuracy separately for each stimulation
group as well as for the whole sample to analyze whether a

(a)

Baseline
1 x Star Training
6 x Star Online
1 x Star
1 x Irregular Training
6 x Star Post
1 x Star
Retention
1 x Star

(b)

Fig. 1. The experimental design and the drawing accuracy evaluation. (a) After a brief familiarization period to the mirror drawing, the
participants had to trace a star with the right hand receiving visual feedback only via a mirror. This was used as baseline for later
comparisons. Then, while stimulated they had to train this task six times for 90 s followed by an online test of drawing the star and an
irregular figure. Again and still under tDCS, the participants had to complete six further star tracings and were tested again immediately
after the termination of the stimulation. Finally, 20 min after the termination of the stimulation, the retention test was performed.
(b) Adjacent to the presented figure of the star, correction lines were added with 2 × 2 mm squares. While deviations from the original line
within the first 2 mm were seen as correct, all deviation exceeding this distance were counted as errors.
Cerebellar tDCS increases motor adaptation 5

Table 1a. Means and standard deviations (SDs) for the tracing times
in seconds for all groups as well as a grand average

Baseline Online Posttest Retention

M – M1: primary motor area in the left hemisphere
P – PAR: right parietal cortex at P4 Time/sec SD Time/sec SD Time/sec SD Time/sec SD
C – CER: cerebellar at 10% below Oz
R – Return electrodes: at Oz, O2, P8 and PO8
CER 47,63 10,63 27,58 4,58 22,45 6,95 20,83 5,11
PAR 46,23 5,27 36,08 7,05 28,76 6,21 27,70 4,67
M1 52,44 20,21 27,85 10,93 27,13 9,25 28,08 10,95
SHAM 49,51 14,54 32,57 7,85 28,79 6,70 29,62 7,89
Average 48,82 13,29 31,29 8,14 26,92 7,48 26,76 8,00

Fig. 2. Positions for anodal HD-tDCS stimulation and locations of

return electrodes. In the three stimulations conditions, left M1,
right parietal (P4), or cerebellar positions were used as anodal
stimulation locations. For all conditions, the four return positions Table 1b. Means and standard deviations (SDs) for tracing errors in
at Oz, O2, P8 and PO8 remained the same to have comparable millimeters for all groups as well as a grand average
cathodal effects.
Baseline Online Posttest Retention

decreased tracing time is related to in- or decreased accuracy. Error/mm SD Error/mm SD Error/mm SD Error/mm SD
The level of significance was set at p ≤ .05. CER 95,10 69,08 40,57 27,16 17,57 12,62 20,09 16,04
PAR 79,35 29,27 36,12 13,66 17,94 7,41 16,29 7,33
M1 111,46 65,75 23,31 14,11 19,76 18,59 16,77 15,05
SHAM 109,72 127,61 33,31 17,70 26,62 26,90 21,72 16,56
RESULTS Average 100,07 90,95 34,16 19,88 21,48 19,77 19,42 14,68

Table 1 depicts the mean and standard deviation for speed

and accuracy for all recordings and stimulation conditions.
Baseline measurement for tracing-time showed no differ-
ences between groups in the baseline. The two-way ANOVA
for tracing time revealed a highly significant effect
F(3,237) = 166.16, p ≤ .001, η2 = .678 for TIME, a
significant effect for GROUP F(3,79) = 2.99, p < .05,
η2 = .102, as well as a significant GROUP × TIME inter-
action F(9,237) = 2.50, p = .048, η2 = .087. As depicted in
Figure 3 the initial decrease (baseline to online test) in
tracing-time is most pronounced for CER and M1. This is
followed by a further decrease for CER while M1 remains
stable. PAR and SHAM, however, decrease equally and
Fig. 3. Besides the significant main effects for TIME and GROUP,
reach the values of M1 in the post-test and the retention test.
there was a significant interaction of GROUP and TIME for the
Bonferroni post hoc tests for the main effect GROUP
speed of the tracing. While there were no differences in speed at
showed only significant differences (i.e., improvement) in the baseline the CER group exhibited the best results as compared
tracing time between CER and SHAM (p < .05). Bonferroni to the other groups. The significant differences between the groups
post hoc comparisons for the interactions revealed that during are depicted for the respective test intervals. While an asterisk
the online-test both the results of CER (p = .006) and M1 denotes significant pairwise comparison at p < .05, two asterisks
(p = .026) were significantly lower as compared to PAR. In indicate a p < .01.
the post-test, CER differed significantly from PAR
(p = .049) and SHAM (p = .013). Finally, in the retention
test CER was significantly faster as compared to SHAM average r = 0.99, p = .001. This indicates that, for all types
(p < .001), to PAR (p = .031), and to M1 (p = .037). of stimulation, shorter tracing times are related to less tracing
The analyses for tracing accuracy showed a highly sig- errors.
nificant effect for TIME (F(3,237) = 54,697; p < .001;
η2 = .409), but no significant results for either GROUP or the
interaction. The number of errors significantly decreases with
DISCUSSION
time for all groups, but does not differ between the
stimulation types. The main findings of our study are that beside the expected
The correlations of tracing time and accuracy resulted in general learning induced decrease in tracing time and errors,
positive correlations for all correlations N = 4 with CER cerebellar HD-atDCS resulted in the best performance in
r = .995, p = .05, PAR r = .990, p = .01, M1 r = .997, tracing speed. This is significant (in comparison to SHAM) in
p = .003, SHAM r = .995, p = .005 and for the grand the post and in the retention test. However, using a more
6 M. Doppelmayr et al.
liberal approach as calculating least square difference (LSD)
instead of Bonferroni contrasts, we could report significant
differences (p = 0.22) between CER and SHAM already in
the online test. Most interestingly, in the retention test,
drawing time in the CER group is significantly decreased not
only in comparison to SHAM but also to PAR or M1
stimulation.
Cerebellar HD-atDCS facilitates motor adaptation, while
HD-atDCS at parietal areas does not. At the first glance, these
results fit well with recent findings as reported by Cantarero
et al. (2015), in which participants performed a visuo-motor
skill task in three training days with stimulation. Participants
receiving anodal cerebellar tDCS yielded the best learning
success already after the first day. Similarly, Galea et al.
(2011) reported best motor adaptation for cerebellar atDCS.
However, this better performance was due to a reduced error
rate, and the stimulation had no effect on a subsequent
retention test. In contrast, our data concerning the cerebellar
stimulation too indicate that performance is increased, but
(i) tracing speed instead of error reduction is significantly
improved and (ii) this effect is significant (with respect to
SHAM) only after the stimulation or after a short retention
interval of 20 min. Whether or not a longer-lasting stimula-
tion would have led to significant differences during stimu-
lation remains an open question.
Antal, Keeser, Priori, Padberg, and Nitsche (2015) have
recently made clear that meta-analyses focusing on the
effects of brain stimulation have to take into account the fact
that different stimulation sites and durations may lead to
divergent outcomes. In consequence to our results, we sug-
gest that the use of HD-atDCS might lead to results different
to those studies using conventional tDCS with less spatial
resolution. A more focal stimulation using an array of
pi-electrodes of 3.14 cm2 might differ substantially from the
stimulation procedure with 25 cm2 sponge electrodes with
return electrode placed at the right buccinators muscle
(inducing an electrical current almost throughout the brain).
Galea et al. (2011) reported a reduction in errors after cere-
bellar tDCS but not a reduction in movement time. Similar
results have been reported by Jayaram et al. (2012), who found
that the adaptation rate of only spatial but not of temporal
components was altered during anodal cerebellar tDCS. This is
in contrast to our findings that showed decreased tracing times
for the CER as compared to SHAM. However, the correlation
indicated that the decrease of tracing time is not due to less
accuracy. Even more, tracing time and errors correlated posi-
tively; thus, the observed decrease in tracing time is accom-
panied by better performance in accuracy (i.e., less errors).
One possible explanation is that tracing speed in mirror
drawing might not be comparable to movement speed per se,
as assessed in other studies (Galea et al., 2011; Jayaram et al.,
2012). Another possible explanation, at least in part and
rather speculative, could be the different stimulation applied.
While the intensity and duration might be comparable, the
location of the stimulation electrode and more importantly
the return electrodes differed. Reporting the results of cortical
tDCS, Miranda, Mekonnen, Salvador, and Ruffini (2013)
noted that the electric field induced by the stimulation could
be divided in a strong normal and a weaker tangential field.
The use of a more focal stimulation, however, resulted in a
significant increase of the focality of the tangential but not the
normally oriented component. To what extent this model is
valid for cerebellar stimulation has not been reported so far.
However, given the highly symmetric structure of the cere-
bellum the tangential component would exert stronger effects
on the parallel fibers of the cerebellum. This in turn might
modulate the long-term depression effects of the synapses
from parallel fibers to Purkinje cells.
The encountered increase in tracing speed after cerebellar
HD-atDCS is more likely due to better visuomotor integra-
tion than to pure movement speed. Thus, a stimulation of the
cerebrocerebellum (lateral hemispheres of the cerebellum)
should be relevant for this effect. Lesions of the cerebrocer-
ebellum can for example lead to prolonged reaction times.
We located the anode 10% below the inion and the return
electrodes on the right occipital lobe (Oz, O2, P8, and PO8).
Thus, the main current flow of the stimulation was on the
right cerebrocerebellum, exerting the strongest effect pre-
sumably at the respective lobuli VII and VIII. Riedel et al.
(2015) described four functional clusters of the cerebellum.
Most importantly, cluster 4 includes the lobuli VII and
VIII. This cluster is seen as a secondary motor representation
and important for motor processes that require perceptive
feedback and attentional control. Moreover, this cluster is
described as heavily involved in motor tasks, with strong
relation to the cognitive aspects necessary for execution;
furthermore, it may contribute to time-based expectancies.
We thus assume that the results achieved with HD-atDCS can
vary substantially from standard atDCS using return elec-
trodes at distant locations, and that more detailed studies have
to be performed on this issue.
Concerning the M1 stimulation, we expected increased
performance already after a short stimulation period similar
to Antal, Nitsche, Kincses, et al. (2004). As depicted, we
found a decreased tracing time during the online test after
12 min of stimulation, but the results were only significant
with respect to PAR, not to SHAM. However, Antal reported
these benefits already after 1 min of stimulation and lasting
only for a few minutes. Thus, an earlier online-test might
have replicated these findings. However, in contrast to Antal
Galea and colleagues (Galea et al., 2011) reported that only
cerebellar but not M1 stimulation increases motor adaptation.
However, it has to be kept in mind that these were quite
different experimental tasks.
Effects of parietal atDCS specifically on motor perfor-
mance or motor adaptation processes have not been reported
so far. Although the right parietal cortex is known to be, at
least to some extent, involved in spatial processing as
necessary in a mirror drawing task, the unilateral stimulation
at P4 may have been insufficient, whereas a bilateral stimu-
lation might have led to improvements. Bolognini et al.
(Bolognini et al., 2011; Bolognini, Olgiati, et al., 2010),
as an example reported that right parietal atDCS resulted
in enhanced orienting to contralateral stimuli. Furthermore,
Cerebellar tDCS increases motor adaptation
it has been noted that both hemispheres are involved in
spatial attention although left hemispheric spatial abilities
are to some extent subdominant (Suchan & Karnath,
2011).
Thus, our montage led to a current flow in the right hemi-
sphere only. One might consider that stimulation of both
hemispheres simultaneously might have changed these results.
However, given the possible influence on left motor areas
(M1), we restrained from stimulating at left parietal site (P3).
Concerning the positions of the return electrodes, we decided
to use the identical locations for all types of stimulations. In
fact, there are some reports indicating differential effects for
cathodal stimulation at visual sites. Although this is considered
an inhibitory stimulation, it does not necessarily result in per-
formance reduction (Pirulli, Fertonani, & Miniussi, 2014). The
behavioral effects of cathodal stimulation at visual areas are
dependent on the specificity of the experimental setting and are
contradictorily with some studies reporting positive and other
negative effects on visuo-motor skills.
As an example, Peters and colleagues reported positive
effects in an orientation discrimination task but only when
cathodal stimulation at V1 was applied before task perfor-
mance but not if applied during the task (Peters, Thompson,
Merabet, Wu, & Shams, 2013). Besides this evidence in
favor of possible positive cathodal effects on visual areas,
most other studies with cathodal stimulation targeted area V5
(Antal, Nitsche, Kruse, et al., 2004; Antal, Nitsche, Kincses,
et al., 2004; Antal et al., 2006) and reported no behavioral
effects with respect to a requested motor task. Nevertheless,
since no directly comparable study could be consulted, we
cannot definitely exclude that cathodal effects over visual
areas may in part be responsible for the effects in the present
approach. Furthermore, it is unresolved whether changing the
current direction (cerebellar – occipital vs. parietal – occipi-
tal) might have differential effects.
Although we cannot strictly rule out an effect due to
the cathodal stimulation, we strongly assume that these are
negligible in our setup. First, all participants receiving real
stimulation enhanced their performance as compared to the
baseline; thus, we can exclude a general decrease in visual
processing. Second, no significant differences in performance
were observed between SHAM and PAR at online, post, or
retention test. Similarly, no significant effects emerged
between SHAM and M1 for these time intervals. This too
suggests that basic visual processing is not deteriorated.
Although, we could not control possible effects directly, as for
example evaluated by VEPs induced via TMS, it seems not
very likely that the low current density might have resulted in
appreciable inhibitory effects at the stimulated visual areas.
All in all, our results support the earlier findings that cer-
ebellar tDCS can evidently facilitate motor adaptation. The
use of HD-tDCS might modulate these effects in a more focal
way. Parietal HD-tDCS, however, yielded no positive effects,
and a stimulation at M1 resulted only in a tendency to
increased performance, but only during an early learning
stage. This highlights the specific function of the cerebellum
in motor adaptation.
7
ACKNOWLEDGMENTS
The authors thank F. Meud for the implementation of a pilot study
and preliminary data recording. No grants nor any conflict of interest
of any author has to be mentioned.
REFERENCES
Antal, A., Keeser, D., Priori, A., Padberg, F., & Nitsche, M.A.
(2015). Conceptual and procedural shortcomings of the systema-
tic review “evidence that transcranial direct current stimulation
(tDCS) generates little-to-no reliable neurophysiologic effect
beyond mep amplitude modulation in healthy human subjects:
A systematic review” by Horvath and Co-workers. Brain
Stimulation, 8, 846–849. doi:10.1016/j.brs.2015.05.010
Antal, A., Nitsche, M.A., Kincses, T.Z., Kruse, W., Hoffmann, K., &
Paulus, W. (2004). Facilitation of visuo‐motor learning by
transcranial direct current stimulation of the motor and extrastriate
visual areas in humans. The European Journal of Neuroscience,
19, 2888–2892. doi:10.1111/j.1460-9568.2004.03367.x
Antal, A., Nitsche, M.A., Kruse, W., Kincses, T.Z., Hoffmann, K.-P.,
& Paulus, W. (2004). Direct current stimulation over V5 enhances
visuomotor coordination by improving motion perception
in humans. Journal of Cognitive Neuroscience, 16(4), 521–527.
doi:10.1162/089892904323057263
Antal, A., Nitsche, M.A., & Paulus, W. (2006). Transcranial direct
current stimulation and the visual cortex. Brain Research
Bulletin, 68(6), 459–463. doi:10.1016/j.brainresbull.2005.10.006
Antal, A., & Paulus, W. (2008). Transcranial direct current
stimulation and visual perception. Perception, 37(3), 367–374.
doi:10.1068/p5872
Antal, A., Polania, R., Schmidt-Samoa, C., Dechent, P., & Paulus,
W. (2011). Transcranial direct current stimulation over the
primary motor cortex during fMRI. Neuroimage, 55(2), 590–596.
Antal, A., Varga, E.T., Kincses, T.Z., Nitsche, M.A., & Paulus, W.
(2004). Oscillatory brain activity and transcranial direct current
stimulation in humans. Neuroreport, 15(8), 1307–1310.
Bolognini, N., Fregni, F., Casati, C., Olgiati, E., & Vallar, G. (2010).
Brain polarization of parietal cortex augments training-induced
improvement of visual exploratory and attentional skills. Brain
Research, 1349, 76–89. doi:10.1016/j.brainres.2010.06.053
Bolognini, N., Olgiati, E., Rossetti, A., & Maravita, A. (2010).
Enhancing multisensory spatial orienting by brain polarization of
the parietal cortex. The European Journal of Neuroscience,
31(10), 1800–1806. doi:10.1111/j.1460-9568.2010.07211.x
Bolognini, N., Pascual-Leone, A., & Fregni, F. (2009). Using non-
invasive brain stimulation to augment motor training-induced
plasticity. Journal of Neuroengineering and Rehabilitation, 6, 8.
doi:10.1186/1743-0003-6-8
Bolognini, N., Vallar, G., Casati, C., Latif, L.A., El-Nazer, R.,
Williams, J., … Fregni, F. (2011). Neurophysiological and
behavioral effects of tDCS combined with constraint-induced
movement therapy in poststroke patients. Neurorehabilitation and
Neural Repair, 25(9), 819–829. doi:10.1177/1545968311411056
Cantarero, G., Spampinato, D., Reis, J., Ajagbe, L., Thompson, T.,
Kulkarni, K., … Celnik, P. (2015). Cerebellar direct current
stimulation enhances on-line motor skill acquisition through an
effect on accuracy. The Journal of Neuroscience, 35(7), 3285–3290.
doi:10.1523/JNEUROSCI.2885-14.2015
Dmochowski, J.P., Datta, A., Bikson, M., Su, Y., & Parra, L.C.
(2011). Optimized multi-electrode stimulation increases focality
8 M. Doppelmayr et al.
and intensity at target. Journal of Neural Engineering, 8(4),
46011. doi:10.1088/1741-2560/8/4/046011
Doyon, J., Penhune, V., & Ungerleider, L.G. (2003). Distinct
contribution of the cortico-striatal and cortico-cerebellar systems
to motor skill learning. Neuropsychologia, 41(3), 252–262.
doi:10.1016/S0028-3932(02)00158-6
Galea, J.M., Vazquez, A., Pasricha, N., de Xivry, J.J., & Celnik, P.
(2011). Dissociating the roles of the cerebellum and motor cortex
during adaptive learning: The motor cortex retains what the
cerebellum learns. Cerebral Cortex, 21(8), 1761–1770.
doi:10.1093/cercor/bhq246
Gottlieb, J., & Snyder, L.H. (2010). Spatial and non-spatial
functions of the parietal cortex. Current Opinion in Neuro-
biology, 20(6), 731–740. doi:10.1016/j.conb.2010.09.015
Grimaldi, G., Argyropoulos, G.P., Boehringer, A., Celnik, P.,
Edwards, M.J., Ferrucci, R., … Ziemann, U. (2014).
Non-invasive cerebellar stimulation–A consensus paper.
Cerebellum, 13(1), 121–138. doi:10.1007/s12311-013-0514-7
Halsband, U., & Lange, R.K. (2006). Motor learning in man:
A review of functional and clinical studies. Journal of Physiology,
Paris, 99(4–6), 414–424. doi:10.1016/j.jphysparis.2006.03.007
Herrmann, C.S., Rach, S., Neuling, T., & Strüber, D. (2013).
Transcranial alternating current stimulation: A review of the
underlying mechanisms and modulation of cognitive processes.
Frontiers in Human Neuroscience, 7, 279. doi:10.3389/
fnhum.2013.00279
Jayaram, G., Tang, B., Pallegadda, R., Vasudevan, E.V.L., Celnik,
P., & Bastian, A. (2012). Modulating locomotor adaptation with
cerebellar stimulation. Journal of Neurophysiology, 107(11),
2950–2957. doi:10.1152/jn.00645.2011
Jeuptner, M., & Weiller, C. (1998). A review of differences between
basal ganglia and cerebellar control of movements as revealed by
functional imaging studies. Brain, 121, 1437–1449.
Keel, J.C., Smith, M.J., & Wassermann, E.M. (2000). A safety
screening questionnaire for transcranial magnetic stimulation.
Clinical Neurophysiology, 112, 720.
Liebetanz, D. (2002). Pharmacological approach to the mechanisms
of transcranial DC-stimulation-induced after-effects of human
motor cortex excitability. Brain, 125(10), 2238–2247.
doi:10.1093/brain/awf238
Mesulam, M.M. (1981). A cortical network for directed attention
and unilateral neglect. Annals of Neurology, 10(4), 309–325.
doi:10.1002/ana.410100402
Miranda, P.C., Mekonnen, A., Salvador, R., & Ruffini, G. (2013). The
electric field in the cortex during transcranial current stimulation.
Neuroimage, 70, 48–58. doi:10.1016/j.neuroimage.2012.12.034
Nitsche, M.A., & Paulus, W. (2000). Excitability changes induced
in the human motor cortex by weak transcranial direct current
stimulation. Journal of Physiology, 527(3), 633–639.
doi:10.1111/j.1469-7793.2000.t01-1-00633.x
Nitsche, M.A., & Paulus, W. (2001). Sustained excitability
elevations induced by transcranial DC motor cortex stimulation
in humans. Neurology, 57(10), 1899–1901. doi:10.1212/
WNL.57.10.1899
Nitsche, M.A., Schauenburg, A., Lang, N., Liebetanz, D., Exner, C.,
Paulus, W., … Tergau, F. (2003). Facilitation of implicit motor
learning by weak transcranial direct current stimulation of the
primary motor cortex in the human. Journal of Cognitive
Neuroscience, 15(4), 619–626. doi:10.1162/089892903321662994
Nitsche, M.A., Seeber, A., Frommann, K., Klein, C.C., Rochford,
C., Nitsche, M.S., … Tergau, F. (2005). Modulating parameters
of excitability during and after transcranial direct current
stimulation of the human motor cortex. Journal of Physiology,
568(1), 291–303. doi:10.1113/jphysiol.2005.092429.
Oldfield, R.C. (1971). The assessment and analysis of handedness:
The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.
doi:10.1016/0028-3932(71)90067-4
Parazzini, M., Rossi, E., Ferrucci, R., Liorni, I., Priori, A., &
Ravazzani, P. (2014). Modelling the electric field and the current
density generated by cerebellar transcranial DC stimulation
in humans. Clinical Neurophysiology, 125(3), 577–584.
doi:10.1016/j.clinph.2013.09.039
Paulus, W. (2011). Transcranial electrical stimulation (tES - tDCS;
tRNS, tACS) methods. Neuropsychological Rehabilitation, 21,
37–41.
Penhune, V.B., & Steele, C.J. (2012). Parallel contributions of
cerebellar, striatal and M1 mechanisms to motor sequence
learning. Behavioural Brain Research, 226(2), 579–591.
doi:10.1016/j.bbr.2011.09.044
Peters, M.A., Thompson, B., Merabet, L.B., Wu, A.D., & Shams, L.
(2013). Anodal tDCS to V1 blocks visual perceptual learning
consolidation. Neuropsychologia, 51(7), 1234–1239.
doi:10.1016/j.neuropsychologia.2013.03.013
Pirulli, C., Fertonani, A., & Miniussi, C. (2014). Is neural
hyperpolarization by cathodal stimulation always detrimental at
the behavioral level? Frontiers in Behavioral Neuroscience,
8(110), 387. doi:10.3389/fnbeh.2014.00226
Priori, A. (2003). Brain polarization in humans: A reappraisal of an
old tool for prolonged non-invasive modulation of brain
excitability. Clinical Neurophysiology, 114(4), 589–595.
doi:10.1016/S1388-2457(02)00437-6
Reis, J., & Fritsch, B. (2011). Modulation of motor performance and
motor learning by transcranial direct current stimulation. Current
Opinion in Neurology, 24(6), 590–596. doi:10.1097/
WCO.0b013e32834c3db0
Reis, J., Schambra, H.M., Cohen, L.G., Buch, E.R., Fritsch, B.,
Zarahn, E., … Krakauer, J.W. (2009). Noninvasive cortical
stimulation enhances motor skill acquisition over multiple days
through an effect on consolidation. Proceedings of the National
Academy of Sciences of the United States of America, 106(5),
1590–1595. doi:10.1073/pnas.0805413106
Riedel, M.C., Ray, K.L., Dick, A.S., Sutherland, M.T., Hernandez,
Z., Fox, P.M., … Laird, A.R. (2015). Meta-analytic connectivity
and behavioral parcellation of the human cerebellum. Neuro-
image, 117, 327–342. doi:10.1016/j.neuroimage.2015.05.008
Rossi, S., Hallett, M., Rossini, P.M., & Pascual-Leone, A. (2009).
Safety, ethical considerations, and application guidelines for the
use of transcranial magnetic stimulation in clinical practice and
research. Clinical Neurophysiology, 120(12), 2008–2039.
doi:10.1016/j.clinph.2009.08.016
Ruffini, G., Fox, M.D., Ripolles, O., Miranda, P.C., & Pascual-
Leone, A. (2014). Optimization of multifocal transcranial current
stimulation for weighted cortical pattern targeting from realistic
modeling of electric fields. Neuroimage, 89, 216–225.
doi:10.1016/j.neuroimage.2013.12.002
Ruffini, G., Wendling, F., Merlet, I., Molaee-Ardekani, B.,
Mekonnen, A., Salvador, R., … Miranda, P.C. (2013).
Transcranial current brain stimulation (tCS): Models and
technologies. IEEE Transactions on Neural Systems and
Rehabilitation Engineering, 21(3), 333–345. doi:10.1109/
TNSRE.2012.2200046
Stagg, C.J., Jayaram, G., Pastor, D., Kincses, Z.T., Matthews, P.M.,
& Johansen-Berg, H. (2011). Polarity and timing-dependent
effects of transcranial direct current stimulation in explicit motor
Cerebellar tDCS increases motor adaptation
learning. Neuropsychologia, 49(5), 800–804. doi:10.1016/j.
neuropsychologia.2011.02.009
Stoodley, C.J., & Schmahmann, J.D. (2009). Functional
topography in the human cerebellum: A meta-analysis of neuro-
imaging studies. Neuroimage, 44(2), 489–501. doi:10.1016/j.
neuroimage.2008.08.039
Suchan, J., & Karnath, H.-O. (2011). Spatial orienting by left
hemisphere language areas: A relict from the past? Brain,
134(Pt 10), 3059–3070. doi:10.1093/brain/awr120
Vicario, C.M., Martino, D., & Koch, G. (2013). Temporal
accuracy and variability in the left and right posterior
9
parietal cortex. Neuroscience, 245, 121–128. doi:10.1016/j.
neuroscience.2013.04.041
Vines, B.W., Nair, D.G., & Schlaug, G. (2006). Contralateral and
ipsilateral motor effects after transcranial direct current stimula-
tion. Neuroreport, 17(6), 671–674.
Vollmann, H., Conde, V., Sewerin, S., Taubert, M., Sehm, B.,
Witte, O.W., … Ragert, P. (2013). Anodal transcranial direct
current stimulation (tDCS) over supplementary motor area
(SMA) but not pre-SMA promotes short-term visuomotor
learning. Brain Stimulation, 6(2), 101–107. doi:10.1016/j.
brs.2012.03.018