Original Article

Perceptual and Motor Skills

2020, Vol. 127(5) 803–822
Effects of Transcranial ! The Author(s) 2020
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DOI: 10.1177/0031512520935695
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Dorsolateral Prefrontal
Cortex (PFC) on
Cognitive-Motor Dual
Control Skills

JaeHyuk Lee1, SungHee Dong2,

JiChai Jeong2, and
BumChul Yoon1,3

Abstract
This randomized crossover study investigated whether anodal transcranial
direct current stimulation (tDCS) over the dorsolateral prefontal cortex (dlPFC)
modulates memory-guided finger isometric maintenance during single motor and
dual cognitive-motor tasks, based on electroencephalogram (EEG) signals. Twenty-
three healthy participants (14 female; M age ¼ 29.130 years, SD ¼ 10.918) underwent
both sham and 2-mA stimulation sessions over the dlPFC for 20 minutes,
with a minimum washout period of seven days. We analyzed finger-force isometric
maintenance and event-related spectral perturbation (ERSP) of the EEG during
early and later phases of both tasks. We observed a significant motor accuracy
improvement (p ¼ .014) and significant variation of force output (p ¼ .027) with sig-
nificant decrease in ERSP on the dorsomedial prefrontal cortex (dmPFC)
(early phase, p ¼ .027; later phase, p ¼ .023) only after 2 mA stimulation.

1
Major in Rehabilitation Science, Graduate School, Korea University
2
Department of Brain and Cognitive Engineering, Korea University
3
Department of Physical Therapy, College of Health Science, Korea University
Corresponding Author:
BumChul Yoon, Department of Physical Therapy, College of Health Sciences, Korea University, Hana
Health Science B BLD, 670 145 Anam-ro, Sungbuk-gu, Seoul 136-701, Korea.
Email: yoonbc@korea.ac.kr
804 Perceptual and Motor Skills 127(5)

Thus, anodal tDCS over the dlPFC may improve memory-guided force control
during cognitive-motor dual tasks.

Keywords
cognitive-motor dual-task, event-related spectral perturbation, force maintenance,
memory guidance, transcranical direct current stimulation

Introduction
In daily life, maintaining precise finger forces without visual guidance is essential
for various cognitive-motor dual performance tasks, as this enlarges visual fields
and permits simultaneous secondary cognitive tasks to be accomplished as, for
example, when manipulating a fragile object while also calculating a math for-
mula. Generally, this dual task force control requires one to give adequate
cognitive attention first to ongoing precise forces that depend on tactile and
proprioceptive information (Johansson & Cole, 1992) and then to short-term
motor representations (also called motor memory) (Fowler & Notterman, 1975).
If the cognitive loads of the secondary task increase to the point that they exceed
the individual’s cognitive capacity, the ongoing motor control deteriorates in
both healthy people (Bray et al., 2012) and in patients with cognitive deficits
(Neely et al., 2017; Z. Wang et al., 2014).

Roles of the Prefrontal Cortex in Cognitive-Motor Dual Tasking

In addition to managing basic cognitive skills, such as arithmetic processing, the
prefrontal cortex (PFC) has a primary motor control function associated with
its direct involvement with cognitive controls such as attention and memory that
are essential for response inhibition in goal-directed behavior (Menon et al.,
2002; Poon et al., 2012). Other studies have also demonstrated the PFC’s func-
tional contributions to motor control, reporting its activation during memory-
guided motor actions and cognitive-motor dual tasking (Goldman-Rakic et al.,
1992; Holtzer et al., 2011). Specifically, the PFC has a well-defined major role in
executive function during motor control, encompassing attention, memory, and
inhibition (Funahashi, 2001; Miller & Cohen, 2001) while interacting with the
motor cortex during goal-directed motor behavior (Diamond, 2013; Royall
et al., 2002) and dual-tasking (Coppin et al., 2006). Several studies have identi-
fied connective executive function and dual tasking, in that dual-task training
has been shown to improve executive function through the normal aging process
(Falbo et al., 2016; Gregory et al., 2017). Furthermore, the dorsolateral region
of the brain’s prefrontal cortex (dlPFC) is a major component of the fronto-
parietal neural network for executive control (Collette & Van der Linden, 2002);
Lee et al. 805

lesions in this area have been seen to cause clinical deficits in short-term (non)
visuospatial memory and attentional control (Müller & Knight, 2006; Spiegel
et al., 2013) during dual-task performance (Kimura et al., 2017).
The PFC is also associated with precise goal-directed motor control such as
pinch force (Neely et al., 2013). Clinically, aging or cognitive-related dysfunc-
tion related primarily to the PFC cause pathological force control problems
(Kim et al., 2016; Poston et al., 2008; Pradhan et al., 2010). For example, in
pinch force maintenance without visual feedback among healthy individuals, the
force output decays progressively as a normal motor response immediately after
removing visual feedback, regardless of muscle fatigue (Vaillancourt & Russell,
2002). This phenomenon occurs more rapidly in people with PFC-related cog-
nitive disorders (Neely et al., 2016, 2017). To study these natural or pathological
phenomena, recent studies have used emotional regulation tasks to modulate
PFC activity and have reported a delay in pinch force output decay, implying
altered force control ability due to modulation of PFC excitation (Beatty et al.,
2014; Blakemore et al., 2016).

Effects of Anodal tDCS Over the dlPFC on Memory Processes in Dual Tasks
For about five decades, research with transcranial direct current stimulation
(tDCS), considered a safe tool for modulated cortical excitation, have examined
whether anode or cathode stimulation over the dlPFC affects cognitive control
in normal individuals or patients (Dedoncker et al., 2016). Although fewer tDCS
polarity effects have been evident in the cognitive domain (Jacobson et al.,
2012), there is emerging evidence of enhanced executive function from tDCS
anodal stimulation over the dlPFC (Bogdanov & Schwabe, 2016; Zaehle et al.,
2011). Especially, among the five basic cognitive processes (i.e., attentional con-
trol, cognitive inhibition, inhibitory control, working memory and cognitive
flexibility) of executive function (Diamond, 2013), most studies on tDCS have
reported positive effects of anodal tDCS on dlPFC on working memory (defined
as the ability to hold information temporarily during dual-task performance)
(Bogdanov & Schwabe, 2016; Cesp
on et al., 2017; Fregni et al., 2005; Zaehle
et al., 2011), except for a few studies that did not find any effects (Nilsson et al.,
2015; J. Wang et al., 2018). Moreover, it is generally accepted that cognitive-
motor dual task performance markedly depends on working memory, as move-
ment errors are consciously corrected by working memory (Fuster, 1997;
Maxwell et al., 2003). However, the direct effects of anodal tDCS over the
dlPFC on cognitive-motor dual tasking are not well-known to date.
Regarding the effects of tDCS over the dlPFC on cognitive-motor dual task-
ing, only a few studies have reported improved cognitive-motor dual function
(Manor et al., 2018; Zhou et al., 2014) while a study reported no effects of tDCS
over the dlPFC on cognitive-motor functioning (Vancleef et al., 2016). A recent
tDCS intervention study found that anodal tDCS over the dlPFC improved
806 Perceptual and Motor Skills 127(5)

significantly the cognitive-motor function among the elderly (Manor et al.,

2018). However, the mechanism (i.e., with respect to the electrical modulation
of brain activity) underlying the changes in the cognitive-motor function
induced on application of tDCS over the dlPFC is still not clear. Also, the
consistency of the effects of tDCS over the dlPFC on cognitive-motor dual
functions must be assessed by expanding the age groups assessed or evaluating
other types of experimental cognitive-motor dual tasks.
Therefore, in the current study, we investigated the effects of anodal tDCS
over the dlPFC on cognitive-motor function by measuring the temporal changes
in the memory-guided pinch force output with and without concurrent second-
ary cognitive tasks, using simple arithmetic tasks (Noteboom et al., 2001; Weeks
et al., 2003). As noted, in previous studies, secondary cognitive tasks were used
to minimize any potential ceiling effects on task performance that may be pre-
sent, as the study population comprised healthy participants, and to observe any
apparent real effects of tDCS (McGeehan et al., 2017; Weeks et al., 2003).
Furthermore, as evidence regarding the brain activity changes underlying
these cognitive-motor functions is sparse, we performed electroencephalography
(EEG) on the PFC simultaneously with when the memory-guided pinch force
task was performed. We hypothesized that left dlPFC tDCS would alter the
force output only after the real tDCS period and not during a sham period and
that these alterations would be evident through EEG changes on the left dlPFC.

Method
Study Design
This study employed a randomized, double-blind, sham-controlled crossover
research design. Participants were engaged in both sham and real tDCS sessions,
with at least seven-day washout periods between sessions.

Participants
We recruited 23 healthy participants (14 female; M age ¼ 29.130 years,
SD ¼ 10.918) through an online community bulletin of Korea University. All
participants were right-handed according to the Edinburgh Handedness
Inventory (Oldfield, 1971). We excluded participants for abnormal hand sense
or movement due to (a) central or peripheral neurological deficits, (b) muscu-
loskeletal pain, or (c) history of injury or burn; additionally, for the motor-
cognitive dual-tasks in the study, we also excluded participants for (d) severe
difficulty in performing basic arithmetic calculations and (e) headache Prior to
baseline evaluation, all participants had to have had sufficient sleep duration
(>6 hr) and no intake of alcohol or caffeine before the testing day. Each par-
ticipant was scheduled at the same time for both sham and real tDCS sessions.
Lee et al. 807

tDCS and Sham Applications

We used a battery-powered stimulator (Y brain, Korea) to apply in counter
balanced order either (a) a real 2 milliampere mA stimulation simultaneously
over the left dlPFC (F3 of the international 10-20 system) by anode elecromes
and the sinous process of C7 by cathode electrodes for 20 minutes or (b) a sham
condition of no stimulation (see below) over the same area with the same elec-
trodes. We positioned saline-soaked 5  5 cm sponges under each electrode to
transfer the current. For the sham stimulation, we ramped a transient current to
less than 1 mA and ramped this down to “off” for 30 seconds to avoid placebo
effects. We used a minimum of seven days as the washout period between the 2
mA and the sham stimulations.

Apparatus
The participants sat on a chair with their knees bent at approximately 90
degrees, their dominant hands placed on the table with their shoulders abducted
to approximately 45 degrees, and their elbows flexed to approximately 90
degrees and supported by the table. We assessed pinch grip using the thumb
and index finger placed with the wrist pronated approximately 20 degrees from
the neutral position. The participants were instructed to comfortably flex the
other three fingers; i.e., the 3rd, 4th, and 5th fingers. We used a piezoelectric
force sensor (Model 208M182, PCB Piezoelectric, Inc., USA) to measure the
force output during pinch grip. The position of the sensor was adjusted for each
participant’s posture, as detailed in the following experimental procedure. The
compression force signals of the index fingers recorded by the sensors were
processed by separate AC/DC conditioners (482C, PCB Piezoelectric, Inc.,
USA). The signals were acquired at 1000 Hz by a 16-bit A/D board (NI 9215,
National Instrument, USA). The real-time acquisition of raw data; i.e., visual
feedback, was coordinated using LabView (LabView 2010, National
Instruments, USA) by the assessor while recording signals to check for signal
errors from the apparatus. The participants were provided visual feedback only
during the practice period and the initial five seconds of each evaluation.

Experimental Procedure
All participants underwent the following experimental procedure (see Figure 1).
Each participant conducted three trials of the 5-second maximal isometric vol-
untary force (MVF) pinch grip task with 30-second rest intervals to avoid
fatigue between trials. To perform the single and dual tasks, we averaged the
three MVF values and calculated the 10% MVF for each participant.
Participants were then allowed a practice period lasting approximately five
minutes, during which they experienced one trial of isometric force maintenance
by pinch grip with 10% MVF for 30 seconds with visual feedback to familiarize
808 Perceptual and Motor Skills 127(5)

Figure 1. A: Experimental processes; all participants performed the same process during
each real and sham tDCS session, with a washout period of at least seven days. B: Simplified
experimental task protocols; all figures above the gray dotted line were those displayed to the
participants. The figures in the first row indicate the process of cognitive-motor dual task in
which seven arithmetic trials were conducted, while the figures in the second row indicate the
process of motor single task in which the eye was fixated on the cross symbol. The rest of the
figures below the gray dotted line in the display allowed assessors to check the signal errors
from the apparatus.

themselves with the magnitude of their individual 10% MVF. Next, participants
were allowed one trial each of single and dual tasks in order to understand the
entire experimental process. For the single task, the participants were instructed
to maintain the force output for 25 seconds while fixing their visual focus on a
cross symbol displayed in the middle of the computer screen; immediately after
the task, the visual feedback was removed. The dual-task consisted of seven
trials of subtraction arithmetic calculations on the computer screen (instead of
looking at the cross symbol) during the 25-second force maintenance task. These
calculations used the psychtoolbox provided in MatLab (R2017a, MathWorks
Inc., Natick, MA, USA). Each trial was shown for 3.5 seconds, with 1.5 seconds
to solve the subtraction problem, one second to check the answer, and one
second to prepare for the next question. The participants were instructed to
verbally report in a low voice whether the problem was right or wrong imme-
diately after checking the answer displayed on the monitor. After the practice
period, participants performed a total of 22 blocks in a randomized order of 11
blocks for each of these single and dual tasks. The participants were instructed
to perform the tasks while maintaining the early wrist posture.
Lee et al. 809

Outcome Measures
Isometric Pinch Force Under Memory Guidance. Memory-guided pinch force control
was measured for 25 seconds and evaluated in four domains: (a) accuracy, (b)
variability, (c3 regularity, and (d) force drop rate. For each domain, the
25-second force data were calculated along with root mean square error
(RMSE) to assess accuracy, coefficient of variation (CV) for variability, approx-
imate entropy (ApEn) for regularity, and the slope of the regression line for
force drop rate, as previously described (Hong et al., 2008; Kang & Cauraugh,
2015; Li et al., 2015).

Event-Related Spectral Perturbation (ERSP) in the PFC. To investigate brain activity

change mechanisms related to the functional role of the PFC and the aftereffects
of tDCS, we recorded electroencephalography (EEG) data by wireless dry elec-
trode EEG (DSI-24, Wearable Sensing Inc., USA), using 21 electrodes placed
according to the 10–20 system (Klem et al., 1999). The EEG data were filtered
online (0–200 Hz) and sampled at 300 Hz. To avoid contamination of the data
with eye movement artefacts, we also recorded the electrooculogram (EOG)
using the same filter and sampling rate as for the EEG; artifacts from eye
blinking were removed using artifact subspace reconstruction methods in
EEGLAB. The signal was then high-pass filtered at 0.5 Hz to remove DC
offset and slow change using Hamming windowed-sinc finite impulse response
(FIR) filter. Finally, we resampled the signal to 250 from 300 Hz and then
segmented from -3–30 sec when the task onset was 0 seconds. The baseline
was set from -3–0 sec, a range that included the cue and was considered as
the preparation period for the task. The recorded data were calculated as
event-related spectral perturbations (ERSPs), defined as the rate of relative
changes in event-related brain activity compared to the baseline, in the PFC,
including F3, Fz, and F4 as the regions of interest (ROIs). After we calculated
the ERSP of four frequency bands (i.e., low alpha, 7.5–8 Hz; high alpha, 8–12.5
Hz; low beta, 12.5–16 Hz; and high beta, 16–30 Hz waves), each pre-tDCS
ERSP and one post-tDCS were compared for the same frequency band.

Data and Statistical Analysis

The sample size was calculated using G*Power 3.1.9.2, considering power of
0.95, a correlation among the measurements of 0.85, nonsphericity correction
 ¼ 1 and a Cohen’s d of 0.25. Then, the calculation resulted in a sample size of
18 participants. All finger force and EEG raw data were filtered and calculated
using MATLAB (R2017a, The MathWorks Inc., USA). For each total
25-second memory-guided force and EEG raw data, we divided the 25-second
recorded phase into two phases, in which half of the data were considered the
early phase and the remaining half of the data were the later phase. Shapiro–
Wilk tests were conducted to identify the normality of the distribution data
810 Perceptual and Motor Skills 127(5)

using baseline MVF values. Next, the baseline MVF in each stimulation session
was compared using paired t-tests. Except for the slope of the regression line, the
RMSE, CV, and ApEn for finger force data were analyzed using three-way
repeated measures (RM) analysis of variance (ANOVA) for two current types
(sham and 2 mA stimulations), two task conditions (single motor and dual
cognitive-motor tasks), and two evaluation periods (pre and post-tDCS). The
ERSP of the EEG data was also analyzed using four-way RM ANOVA (two
current types x two task conditions x two evaluation periods x 3 ROIs [F3, Fz,
F4]) in the early and later phases of finger force. We then performed a paired t-
test as subgroup analyses to determine the significance of each factor. All sta-
tistical analyses were conducted using IBM SPSS Statistics for Windows, ver-
sion 20.0 (USA). We used p-values less than 0.05 for determining statistical
significance.

Results
No participants reported adverse effects after tDCS application, and none
noticed any differences in the feeling of stimulation between the sham and the
real tDCS sessions. The baseline MVF between the sham (M ¼ 35.74,
SD ¼ 9.258 N) and real tDCS (M ¼ 36.39, SD ¼ 10.703 N) sessions were not
significantly different.

Effects of Anodal DLPFC tDCS on Isometric Pinch Force

For the regression line, RMSE, CV, and ApEn variables, the three-way RM
ANOVA reported significant main effects of task conditions in the RMSE
(F(1,22) ¼ 4.750, p ¼ .04) and ApEn of the early phase (F(1,22) ¼ 14.194,
p ¼ .001) and the evaluation periods in the RMSE of the later phase
(F(1,22) ¼ 5.286, p ¼ .031), CV of the early phase ([F(1,22) ¼ 5.908, p ¼ .024), and
ApEn of the early phase (F(1,22) ¼ 4.927, p ¼ .037).
Significant interactions were also found between current types and task con-
ditions in the CV of the initial phase (F(1,22) ¼ 5.227, p ¼ .032); among current
types and evaluation periods in the regression line (F(1,22) ¼ 14.888, p ¼ .001) and
the ApEn of the later phase (F(1,22) ¼ 13.492, p ¼ .001); between task conditions
and evaluation periods in the regression line (F(1,22) ¼ 5.330, p ¼ .031]); and
among current types, task conditions, and evaluation periods in the RMSE
(F(1,22) ¼ 7.553, p ¼ .012) and CV of the later phase (F(1,22) ¼ 4.696, p ¼ .041),
indicating that the significant difference in RMSE and CV of the later phase was
dependent on the tDCS current types and task types. Subgroup analyses using
paired t-tests across each factor revealed significant decreases in RMSE
(p ¼ .014, Cohen’s d ¼ 0.438) and CV (p ¼ .027, Cohen’s d ¼ 1.282) in the later
phase during dual cognitive-motor task in the real tDCS session (Table 1) while
there were no changes in all factors in the sham tDCS session (Table 2).
 Table 1. Finger Force Outputs During Motor Single and Cognitive-Motor Dual Tasks After Real tDCS.

Single motor task Cog-motor dual task

Pre Post P Pre Post P

Regression slope 0.121 (0.038) 0.101 (0.031) 0.088 0.119 (0.035) 0.102 (0.030) 0.006*
Early phase
RMSE 1.090 (0.471) 1.179 (0.756) 0.675 1.113 (0.492) 1.203 (0.820) 0.393
CV 0.213 (0.095) 0.201 (0.124) 0.744 0.213 (0.088) 0.201 (0.141) 0.591
ApEn (x103) 0.766 (0.364) 1.135 (0.736) 0.072 0.682 (0.307) 0.929 (0.528) 0.033
Later phase
RMSE 2.420 (0.844) 2.235 (1.074) 0.567 2.310 (0.740) 2.117 (0.835) 0.014*
CV 0.366 (0.186) 0.341 (0.333) 0.784 0.412 (0.230) 0.200 (0.308) 0.027*
ApEn (x103) 0.889 (0.667) 1.387 (1.777) 0.274 0.780 (0.574) 0.849 (0.598) 0.570
Values are expressed as means (standard deviation).
Data were analyzed using paired t-test.
ApEn: approximate entropy; CV: coefficient of variation; RMSE: root mean square error
*P < 0.05.

811
812
Table 2. Finger Force Outputs During Motor Single and Cognitive-Motor Dual Tasks After Sham tDCS.

Single motor task Cog-motor dual task

Pre Post P Pre Post P

Regression slope 0.120 (0.035) 0.118 (0.034) 0.844 0.125 (0.033) 0.112 (0.029) 0.230
Early phase
RMSE 1.099 (0.505) 1.175 (0.443) 0.632 1.230 (0.521) 1.189 (0.533) 0.819
CV 0.227 (0.112) 0.230 (0.103) 0.946 0.245 (0.093) 0.222 (0.102) 0.425
ApEn (x103) 0.820 (0.459) 0.850 (0.580) 0.932 0.636 (0.359) 0.716 (0.449) 0.501
Later phase
RMSE 2.431 (0.834) 2.412 (0.798) 0.205 2.454 (0.921) 2.198 (0.929) 0.234
CV 0.846 (1.647) 0.341 (0.157) 0.762 0.523 (0.522) 0.356 (0.222) 0.571
ApEn (x103) 0.970 (1.104) 0.816 (0.533) 0.598 0.420 (1.708) 0.596 (0.243) 0.808
Values are expressed as means (standard deviation).
Data were analyzed using paired t-test.
ApEn: approximate entropy; CV: coefficient of variation; RMSE: root mean square error.
*P < 0.05.
Lee et al. 813

Effects of Anodal DLPFC tDCS on ERSP on ROIs

For the ERSP, four-way RM ANOVA revealed significant main effects on ROIs
in the low alpha band of the later phase (F(1,22) ¼ 16.712, p ¼ .001), high alpha
band of the early phase (F(1,22) ¼ 12.607; p ¼ .004), and low beta band of the
later phase (F(1,22) ¼ 9.478, p ¼ .009), indicating the significant differences
between each ROI regardless of the other three factors (i.e., current type, task
condition, and evaluation period) and also on task conditions in the high alpha
of the early phase (F(1,22) ¼ 5.211, p ¼ .04).
There were significant interactions between ROIs and task conditions
(F(1,22) ¼ 5.154, p ¼ .041); between current types and evaluation periods in the
low beta band of the early phase (F(1,22) ¼ 7.618, p ¼ .016) and the high beta
band of the later phase (F(1,22) ¼ 8.424, p ¼ .012); and among current types, task
conditions, and evaluation periods in the high beta band of the later phase
(F(1,22) ¼ 6.486, p ¼ .024). Therefore, we conducted paired t-tests as subgroup
analyses to identify the significant effects across the factors with significant
changes in the high beta band on F3 during the later phase of the dual task
in both 2 mA tDCS (p ¼ .002; Cohen’s d ¼ 1.172) and sham tDCS (p ¼ .017;
Cohen’s d ¼ 1.147) sessions and in the high beta band on Fz during the early
(p ¼ .027; Cohen’s d ¼ 1.050) and later (p ¼ .023; Cohen’s d ¼ 1.488) phases of
the dual task only in the 2 mA tDCS session (Figures 2 and 3).

Discussion
The current study investigated whether anode tDCS over the left dlPFC would
alter memory-guided finger force control and brain activities during single
motor or dual cognitive-motor tasks. We assessed the control of finger force
maintenance in four domains. Furthermore, to explain the underlying physio-
logical basis of the possible finger force changes by tDCS, we simultaneously
measured EEG data of the PFC as regions of interest (ROI) because of its
functional roles in cognitive control such as working memory and dual tasking
by calculating the time-frequency data (ERSP) of three ROIs (i.e., F3, Fz, F4),
as previously described. We found that anodal tDCS over the left dlPFC may
offer increased stabilization of memory-guided force maintenance than pre-
stimulation trials while performing a dual task, with changes in PFC activity.
Most previous tDCS studies have investigated whether tDCS over cortical
areas directly associated with movement execution such as the primary or sup-
plementary motor cortices changed motor performance. These studies demon-
strated that anodal tDCS over the motor-related brain cortex enhanced motor
learning of precise movement and manipulation dexterity in both upper and
lower limbs (Jacobson et al., 2012). However, although many brain studies
demonstrated that the prefrontal cortex is involved in motor control for com-
pleting intended movements requiring cognitive control such as executive
814 Perceptual and Motor Skills 127(5)

Figure 2. Plots Depicting the Changes in Event-Related Spectrum Perturbation (ERSP) on

the Regions of Interest (ROI) (F3, Fz, and F4) After Real 2 mA Transcranial Direct Current
Stimulation (tDCS) That Analyzed by Paired t Test as a Post-Hoc Analysis. The graphs on the
upper row line (A) indicate cognitive-motor dual tasking while those on the lower line (B)
indicate motor single tasks. The white bar graph indicates low alpha (7.5–8 Hz). The light gray
bar graph indicates high alpha (8–12.5 Hz). The dark gray bar graph indicates low beta (12.5–
16 Hz). The black-gray bar graph indicates high beta (16–18 Hz). The oblique line bar graph on
each phase indicates the post-tDCS ERSP.

function, including attention and memory (Collette et al., 2002; Kimura et al.,
2017; Neely et al., 2013), there has been insufficient research into whether tDCS
over the prefrontal cortex changed motor output.
Especially, previous studies reported that the PFC played important roles in
motor performance by modulating executive function and retaining motor
memory (also called motor representation) (Shadmehr & Holcomb, 1997).
For example, when conducting more than two tasks simultaneously (i.e., dual
tasking) or when conducting a task without corrective visual feedback (i.e.,
memory-guided tasking), there is increased activation of the prefrontal cortex
to trigger attention and memory assists in stabilizing the motor output (Ohsugi
et al., 2013; Woollacott & Shumway-Cook, 2012). However, the few studies that
have investigated the effects of tDCS over the PFC on motor output have
reported confusing results on motor performance, with some reporting positive
tDCS effects (Manor et al., 2018; Zhou et al., 2014) and others reporting no
tDCS effects (Nilsson et al., 2015; Vancleef et al., 2016; J. Wang et al., 2018). To
examine the definite effects of tDCS over the PFC on motor outputs, we used a
precise motor control task (i.e., pinch force maintenance) and cognitively chal-
lenging two-task conditions - no visual feedback and dual tasking.
Lee et al. 815

Figure 3. Plots Depicting the Changes in Event-Related Spectrum Perturbation (ERSP) on

the Regions of Interest (ROIs) (F3, Fz, and F4) After Sham Transcranial Direct Current
Stimulation (tDCS) Analyzed by Paired t Test as a Post-Hoc Analysis. The graphs on upper row
line (A) are cognitive-motor dual tasking while those on the lower line (B) indicate motor
single tasks. The white bar graph indicates low alpha (7.5–8 Hz). The light gray bar graph
indicates high alpha (8–12.5 Hz). The dark gray bar graph indicates low beta (12.5–16 Hz). The
black-gray bar graph indicates high beta (16–18 Hz). The oblique line bar graph on each phase
indicates the post-tDCS ERSP.
The experimental procedure was approved by the Institutional Review Board at Korea
University (KU-IRB-17-126-A-2) and all participants provided written informed consent.

Effects of Anodal DLPFC tDCS on Isometric Pinch Force

In the rehabilitation field, the finger force isometric maintenance task has been
used with many participants, from healthy to disabled individuals, to investigate
both natural and pathologic fine motor control skills by observing the accuracy
and constancy of the force output (Kang et al., 2015). The dependence on motor
memory to generate isometric force without visual feedback has been investi-
gated to examine initial force magnitude effects on sensory-motor
integration with proprioceptive sensory and short-term memory. According to
previous studies, the accuracy of memory-guided force generally dropped unin-
tentionally immediately after visual information was removed, as evidenced by
the drifting of the force output to lower values (Vaillancourt et al., 2002, 2003).
Our findings also showed this force drift in our healthy participants when visual
feedback was removed, regardless of the tDCS application and task types (i.e.,
single or dual tasks). Furthermore, we considered the magnitude of force drift as
a clinical indicator, because abnormal finger force output is manifested in
cognitive-related disease and dysfunction when compared with the force in
816 Perceptual and Motor Skills 127(5)

healthy individuals. For example, in disabled individuals with cognitive deficits,

force control accuracy was markedly decreased, variability was increased, reg-
ularity was increased, and force drifts were faster. In this context, we observed a
significant interaction between three factors (current types, task conditions, and
evaluation periods) that was ultimately interpreted as an alteration of memory-
guided pinch force maintenance affected by real 2mA tDCS only during the
cognitive-motor dual task. Specifically, through the sub-group analysis by
paired t-test, among various force-related variables, we found significant
changes in RMSE and CV, indicating a significant decrease in force accuracy
and variability only during the later phase of dual tasks after real tDCS; there
was no significant change after the sham tDCS applications. In accordance with
the underlying physiological mechanism, our finding of significant reduction in
force variation during the later phase of the dual task after real tDCS occurred
because, in the early phase, healthy participants normally produce a stable force
control without large challenges to their attention and memory, ultimately
resulting in a ceiling effect. This finding indicated that anodal tDCS over the
dlPFC in healthy individuals improved stability in the later phase of memory-
guided force production, challenging the larger cognitive loads compared to
those in the early phase. Further studies are necessary to validate whether clin-
ical uses of tDCS over dlPFC improves abnormal finger force control in patients
with cognitive deficits related to PFC lesions.

Effects of Anodal DLPFC tDCS on ERSP on ROIs

After we found a significant interaction between four factors (current types, task
conditions, evaluation periods, ROIs) that we ultimately interpreted as the alter-
ation of brain activity in specific brain areas caused by real 2mA tDCS only
during the cognitive-motor dual task, additional subgroup analysis by paired t-
test showed that ERSP on the left dlPFC (F3), where we applied tDCS, showed
a significant decrease in the amplitude of ERSP (also called event-related
desynchronization, ERD) for higher beta frequencies during the later phase of
the dual task both in real and sham tDCS sessions when compared to that at
baseline. Typically, ERD of beta frequency indicates an activation of cortical
neurons underlying cognitive and motor processes (Neuper & Pfurtscheller,
2001). We speculated that the ERD in F3 during the later phase of the dual
task both in real and sham stimulation sessions resulted from the load of atten-
tional control over time, one of the previously mentioned executive functions
(Corbetta & Shulman, 2002), and this interpretation was supported by another
observation in this study, showing ERD trends during the early phase of only
the dual task in both real and sham tDCS sessions which were not observed
during the single motor task (Figures 2A and 3A).
Interestingly, we also found that only real tDCS sessions provoked the addi-
tional ERD of higher beta frequencies during the dual task in the dorsomedial
Lee et al. 817

prefrontal cortex (dmPFC, Fz) when compared to that at baseline. Then, we

speculated that this change in dmPFC excitation after real tDCS would result in
changes in force accuracy and variability for two reasons; (a) the coincidence
between the time of change in ERSP of dmPFC and the one in the force var-
iables (i.e. force accuracy and variability in the current study), and (b) reports of
dmPFC anatomical functions in previous reports. According to a few studies
that investigated the functional roles of the dmPFC for motor control, a study
reported that dmPFC was involved in temporal inhibition of inappropriate
responses during motor performance (Narayanan & Laubach, 2006). Another
study reported that the dmPFC interacted with the premotor cortex to maintain
force production in various emotional contexts (Coombes et al., 2012). That is,
the decrease in force variation and increase in force accuracy during cognitive-
motor dual task in our study may have resulted from an increase in dmPFC
excitation by real tDCS.
Regarding the cause of the changes in dmPFC excitation, although it was
outside the scope of the present study, there is a rational inference based on
previous studies. A recent study investigating the positive effect of tDCS over
the left dlPFC on executive function and its correlation with changes in event-
related potentials (ERP), which was not measured in this study, found that the
improvement in working memory by anodal tDCS resulted from increased P300
ERP amplitude in the frontal region (Cesp
on et al., 2017). Another study
reported that the dorsolateral and dorsomedial PFC had anatomical and func-
tional connections for cognitive control when making a decision between two
competing responses (Taren et al., 2011). Thus, we cannot exclude the possibility
that changes in dlPFC ERP activity by anodal tDCS over the left dlPFC affect-
ed the changes in ERSP of the dmPFC, ultimately resulting in changed force
control ability.
Lastly, in motor learning theory, repetitive task practice has typically been
used to enhance motor control, based on the concept of changing and adapting
brain activity. Physiological effects reported in earlier studies suggest that long-
term potentiation or depression, is based on the neuroplasticity principle.
Likewise, since tDCS has demonstrated effectiveness for modulating brain activ-
ity and, thereby, enhancing motor learning, many studies have demonstrated
tDCS feasibility for improving motor control deficits among individuals with
impairment from such disorders as stroke or cerebral palsy (Bolognini et al.,
2009). Most of these studies have relied on stimulating the primary motor cortex
(M1). The present study provides new evidence of the feasibility of applying
tDCS over the dlPFC for force control ability, based on EEG changes reflecting
brain activation in this brain reigion. Further studies are needed to next inves-
tigate whether the application of tDCS over the PFC provides a double clinical
effect to improve both cognitive and motor tasks simultaneously in healthy
patients and/or the elderly.
818 Perceptual and Motor Skills 127(5)

This study has several limitations related to generalizing these results. First,
although we applied stimulation to the left dlPFC according to a 10-20 EEG
system, tDCS has a shadow effect due to low spatial focality such that other
brain regions could have been affected by the current. Second, uncontrolled
variability in each participant’s emotional state might have affected PFC acti-
vation. Lastly, because we investigated healthy participants who may have
reached a ceiling effect on some measures, future studies should perform repli-
cating research with patients with cognitive deficits.

Conclusion
In the current study, we assessed the effect of a single application of tDCS over
the left DLPFC on cognitive-motor dual control by measuring performance on
the memory-guided finger force task with or without dual task arithmetic ques-
tions. Simultaneously, we also measured event-related spectral perturbation in
the frontal cortex. The accuracy and stability of memory-guided force mainte-
nance during arithmetic processing improved after applying 2-mA tDCS with
ERD in the beta frequency band on the dorsomedial prefrontal cortex (dmPFC)
but did not improve after sham tDCS. These results indicated that anodal tDCS
over the dlPFC may improve the memory-guided force control during cognitive-
motor dual tasks, due to alteration of brain activation.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research,
authorship, and/or publication of this article.

Funding
The author(s) received no financial support for the research, authorship, and/or publi-
cation of this article.

ORCID iD
BumChul Yoon https://orcid.org/0000-0001-7564-479X

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Author Biographies
JaeHyuk Lee: PhD, PT (physical therapist), Department of Rehabilitation science, Korea
University, Seoul, Korea.

SungHee Dong: PhD, Department of Brain and Cognitive Engineering, Korea University, Seoul,
Korea.

JiChai Jeong: PhD, Professor, Department of Brain and Cognitive Engineering, Korea University,
Seoul, Korea.

BumChul Yoon: PT(physical therapist), PhD, Professor, Department of Physical therapy, Korea
University, Seoul, Korea.