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Brain stimulation modulates the autonomic
nervous system, rating of perceived exertion
and performance during maximal exercise
Alexandre Hideki Okano,
1
Eduardo Bodnariuc Fontes,
2
Rafael Ayres Montenegro,
3
Paulo de Tarso Veras Farinatti,
3
Edilson Serpeloni Cyrino,
4
Li Min Li,
2
Marom Bikson,
5
Timothy David Noakes
6
▸Additional material is
published online only. To view
please visit the journal online
(http://dx.doi.org/10.1136/
bjsports-2012-091658).
1
Physical Education
Department, Federal University
of Rio Grande do Norte
(UFRN), Natal, Rio Grande do
Norte, Brazil
2
Department of Neurology,
University of Campinas
(UNICAMP), Campinas,
São Paulo, Brazil
3
Physical Education and Sports
Institute, Rio de Janeiro State
University (UERJ), Rio de
Janeiro, RJ, Brazil
4
Center of Physical Education
and Sport, State University of
Londrina (UEL), Londrina,
Parana, Brazil
5
Department of Biomedical
Engineering, The City College
of New York of CUNY,
New York, New York, USA
6
MRC/UCT Research Unit for
Exercise Science and Sports
Medicine, University of Cape
Town (UCT), Cape Town,
Western Cape, South Africa
Correspondence to
Professor Alexandre Hideki
Okano, Departamento de
Educação Física, Universidade
Federal do Rio Grande do
Norte, Campus Universitário
BR 101, Lagoa Nova,
CEP 59072-970, Natal,
Rio Grande do Norte, Brazil;
emaildookano@gmail.com
Received 6 August 2012
Revised 22 October 2012
Accepted 30 January 2013
Published Online First
27 February 2013
To cite: Okano AH,
Fontes EB, Montenegro RA,
et al.Br J Sports Med
2015;49:1213–1218.
ABSTRACT
Background The temporal and insular cortex (TC, IC)
have been associated with autonomic nervous system
(ANS) control and the awareness of emotional feelings
from the body. Evidence shows that the ANS and rating
of perceived exertion (RPE) regulate exercise
performance. Non-invasive brain stimulation can
modulate the cortical area directly beneath the electrode
related to ANS and RPE, but it could also affect
subcortical areas by connection within the cortico-
cortical neural networks. This study evaluated the effects
of transcranial direct current stimulation (tDCS) over the
TC on the ANS, RPE and performance during a maximal
dynamic exercise.
Methods Ten trained cyclists participated in this study
(33±9 years; 171.5±5.8 cm; 72.8±9.5 kg; 10–11
training years). After 20-min of receiving either anodal
tDCS applied over the left TC (T3) or sham stimulation,
subjects completed a maximal incremental cycling
exercise test. RPE, heart rate (HR) and R–R intervals (as
a measure of ANS function) were recorded continuously
throughout the tests. Peak power output (PPO) was
recorded at the end of the tests.
Results With anodal tDCS, PPO improved by ∼4%
(anodal tDCS: 313.2±29.9 vs 301.0±19.8 watts: sham
tDCS; p=0.043), parasympathetic vagal withdrawal was
delayed (anodal tDCS: 147.5±53.3 vs 125.0±35.4 watts:
sham tDCS; p=0.041) and HR was reduced at
submaximal workloads. RPE also increased more slowly
during exercise following anodal tDCS application, but
maximal RPE and HR values were not affected by cortical
stimulation.
Conclusions The findings suggest that non-invasive
brain stimulation over the TC modulates the ANS activity
and the sensory perception of effort and exercise
performance, indicating that the brain plays a crucial role
in the exercise performance regulation.
INTRODUCTION
‘Classical’mechanisms determining exercise toler-
ance have focused on the cardiovascular, respira-
tory, metabolic and neuromuscular mechanisms of
muscle fatigue
1–3
and produced a brainless model
of human exercise performance. ‘Contemporary’
studies have challenged the current paradigm of
exercise physiology by emphasising the crucial role
played by the brain in the regulation of exercise
performance.
4–9
Studies integrating peripheral and
central responses should help to clarify this debate,
which is still open.
710–13
Non-invasive brain stimulation has been increas-
ingly used by clinicians and neuroscientists to delib-
erately alter the status of the human brain.
Transcranial direct current stimulation (tDCS) is
considered a neuromodulatory intervention that
induces excitability changes in the human motor
cortex.
14 15
The exposed tissue is polarised, and
tDCS modifies spontaneous neuronal excitability
and activity by a tonic depolarisation or hyperpolar-
isation of resting membrane potential.
16
The nature
of these modulations depends on stimulation polar-
ity: Anodal stimulation increases excitability, which
is decreased by cathodal stimulation.
17
If the stimu-
lation is applied for 9 min or longer, these changes
in excitability may persist for an hour or more.
15
A possible mechanism underlying the tDCS
effects might be associated changes in cortical neur-
onal activity. Pharmacological studies have shown
that tDCS-related effects depend on changes of
N-methyl-D-aspartate (NMDA) receptor-efficacy.
17
Using magnetic resonance spectroscopy, Stagg
et al
18
demonstrated changes in gamma-
aminobutyric acid (GABA) levels after anodal tDCS,
suggesting that this stimulation alters both
GABAnergic inhibition as well as the NMDA recep-
tors. Although tDCS stimulates the cortical area dir-
ectly beneath the electrode, it could also modulate
subcortical structures since there are connections
within the cortico-cortical neural networks.
19 20
It
has already been shown that tDCS can improve
implicit motor learning,
21
motor performance
22 23
and may be valuable in the treatment of depres-
sion,
24
of the symptoms of Alzheimer’s
25
and
Parkinson’s disease,
26
chronic pain,
27
stroke
28
and
regulation of appetite sensations.
29
Even though
tDCS is an attractive, non-invasive neuromodulatory
technique for a diverse range of applications, its
effect on the dynamic motor performance and toler-
ance to physical strain has yet to be studied.
It is well known that the autonomic nervous
system (ANS) plays a key role in homeostatic
control in humans,
30 31
especially when under high
metabolic demand as occurs during physical activ-
ity.
32 33
There is some evidence that ANS responses
are associated with exercise performance in healthy
subjects
34
and with the development of fatigue in
patients with some specific diseases.
35
Healthy sub-
jects with high aerobic capacity seem to have sig-
nificantly higher vagal modulation of the heart rate
(HR) and, consequently, longer parasympathetic
withdrawal as demonstrated by greater heart rate
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variability (HRV) when compared to subjects with lower fitness
levels.
32
These findings suggest that the ANS may be highly
related to the mechanisms underlying physical exercise perform-
ance and fatigue.
Assessment of HR and blood pressure (BP) variability
36–38
has implicated the temporal cortex (TC) as one of the cerebral
regions involved in the control of cardiac autonomic function.
Changes in HR and BP accompany the -ictal discharges in
humans with temporal lobe epilepsy.
39
There is also evidence
that the TC is involved in motor control perception
40
and is
part of a sensory system that detects emotional stimuli.
41 42
In
addition, studies suggest that the left cerebral hemisphere is
usually associated with pleasant feelings as occurs, for example,
when subjects either see or make a smile,
43
or listen to happy
voices,
44
or hear pleasant music.
45
On the other hand, negative
perceptions, such as heat-related pain sensation,
46 47
subjective
cooling
48
and elevated perceived exertion during dynamic
cycling exercise,
49
are more usually associated with right hemi-
sphere function.
The insular cortex (IC) has been implicated in the control of
cardiac autonomic function in humans and animals.
50–52
In
humans, right anterior insular stimulation increased sympathetic
cardiovascular responses, whereas left insular stimulation
reduced parasympathetic cardiovascular effects.
50
Additionally,
there is evidence that the IC is primarily responsible for the
awareness of several subjective feelings from the body.
53 54
For
example, activation of the right anterior IC is associated with
heat-related pain sensation,
46 47 55
subjective cooling
48
and per-
ceived exertion during dynamic cycling exercise.
49
On the other
hand, activation of the left AIC was reported in mothers
viewing photos of their own child
56
; in subjects who were
either seeing or making a smile
43
; listening to happy voices
44
or
hearing pleasant music.
45
In summary, the left anterior IC is
activated mainly by positive and affiliated emotional feelings,
while stimuli that activate the right IC are generally evoked by
the body in response to negative and unpleasant sensations.
We have recently shown that anodal tDCS over the TC is able
to modulate the ANS in athletes at rest by increasing the para-
sympathetic activity, as shown by the HRV responses.
57
However, the related effects during a highly demanding cardio-
vascular exercise, such as a maximal cycling test to exhaustion,
have not been described. Since the TC can be associated with
both autonomic nervous control
37 58 59
and emotional feel-
ings
41 42
we hypothesise that anodal tDCS over the left TC
immediately prior to maximal exercise might enhance parasym-
pathetic activity, increase tolerance to physical strain by decreas-
ing the rating of perceived exertion (RPE) and improve exercise
performance. Hence, the purposes of the present study were to
verify the effects of a neuromodulation tool (anodal tDCS) on
exercise performance, HR, HRV and RPE during an incremental
exercise test performed until exhaustion by trained cyclists.
METHODS
Subjects
Ten male national-level road cyclists with 10–11 years of train-
ing experience volunteered to participate in this study (33±9
years; 171.5±5.8 cm; 72.8±9.5 kg). Each participant was
informed of the procedures and risks before giving written
informed consent to participate in the study. In addition, the
volunteers were instructed to refrain from vigorous activities
and the ingestion of beverages containing caffeine and alcohol
or of using tobacco for 24 h prior to each test. This study was
approved by the local Institutional Research Ethics Committee.
Experimental design
After arriving at the laboratory, subjects first rested for 15 min
before receiving either of the experimental conditions—anodal
tDCS or sham (see tDCS procedures)—for 20 min. They then
performed the maximal incremental exercise test. HR and HRV
were recorded continuously throughout the experiment. Both
test conditions were completed at the same time of the day and
in a counterbalanced randomised order with a minimal 48 h
interval between trials. From the data collected during the incre-
mental test, SD1 using Poincaré plots were calculated every
minute and HRV 3 ms threshold (HRV
TH
) was determined.
60
The evaluators and cyclists were blinded to the test conditions.
The cyclists received strong verbal encouragement from the
same researcher during all tests in order to achieve the highest
possible performance.
tDCS procedures
The direct electric current was applied through a pair of
sponges humidified with saline solution (150 mMols of NaCl
diluted in water Milli-Q) on the electrodes (35 cm2).
14
The
electrodes (anode and cathode) were connected to a continuous
electric stimulator, with three energy batteries (9 V) connected
in parallel. The maximum energy output was 10 mA and was
controlled by a professional digital multimeter (DT832, WeiHua
Electronic Co., Ltd, China) with a standard error of ±1.5%.
For anodal polarity stimulation over the left TC, the anodal
electrode was placed over the scalp on the T3 area located at
40% of the distance on the left from the Cz point, according to
the international standards for EEG 10–20 system. The cathode
electrode was placed over the contralateral supraorbital area
(Fp2). Thereafter, a constant electric current of 2 mA was
applied for 20 min. For the sham condition, the electrodes were
placed at the same positions as for the anodal tDCS. However,
the stimulator was turned off after 30 s of stimulation, according
to the methods of Gandiga et al.
61
As a result, the cyclists
reported the same sensory feelings from the beginning of the
real tDCS conditions, specifically itching and tingling feelings
on the scalp for the first few seconds of tDCS, but not there-
after, whether or not the stimulation was continued or stopped.
This procedure ensured that subjects remained ‘blinded’to the
condition they had received, since no sensory feelings were
reported from any subjects after the initial 30 s period during
either condition. Additionally, we asked the cyclists if they could
discern any difference between conditions, but none could.
High-resolution computational model
Using a previously developed finite element (FE) model,
62 63
we
analysed the effect of our electrode montage on the current
flow in the brain, taking into consideration the electrical proper-
ties of the cortical and subcortical structures. The human head
model was derived from a high spatial resolution (1 mm
3
)3T
MRI of a healthy male adult subject, and segmented into com-
partments representing the scalp, skull, cerebrospinal fluid, eye
region, muscle, grey matter, white matter and air. Sub-cortical
and brain stem structures including the insula, cingulate, thal-
amus, midbrain, pons and medulla oblongata were also segmen-
ted (Custom Segmentation, Soterix Medical, New York,
New York, USA). Sponge-based electrode stimulation pads as
used experimentally were imported as computer-aided design
models and placed onto the segmented head to mimic the
experimental montage: from the segmented data, volumetric
mesh was generated and exported to an FE solver (COMSOL
Multiphysics 3.5a, COMSOL Inc., Massachusetts, USA). The
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following isotropic electrical conductivities (in S/m) were
assigned: scalp: 0.465; skull: 0.01; cerebrospinal fluid: 1.65;
eye region: 0.4; muscle: 0.334; grey matter: 0.276; white
matter: 0.126; air: 1e-15; synthetic region: 0.17; sponge: 1.4;
electrode: 5.8e7. The cingulate cortex, insula and the thalamus
were assigned the grey matter conductivity while the midbrain,
pons and the medulla oblongata were assigned the white matter
conductivity. The Laplace equation was solved, and current
density corresponding to 2 mA total current was applied.
Induced cortical surface electric field magnitude was determined
and plotted across the cortex and insula.
Maximal incremental exercise test
The maximal incremental exercise test began at an initial work-
load of 15 W with increments of 25 W/min until the subjects
voluntarily terminated the test or were unable to sustain the
cadence (80 rpm) for longer than 5 s. All tests were performed
on an electronic braked cycle ergometer (ERGO-FIT model 167
cycle, Pirmansens, Germany) with similar riding position
(saddle and handlebar height and position), and the cadence
was kept at 80 rpm. The peak power output (PPO) was defined
as the highest intensity sustained by the cyclist on the cycle erg-
ometer for longer than 1 min.
HR and HRV recordings
The HR and HRV were recorded by an HR monitor (S810i,
PolarTM, Finland) with an acquisition rate set at 1000 Hz. The
R–R interval data were downloaded by Polar Precision
Performance Software (Polar, Finland). The SD1 was calculated
using Poincaré plots for every minute by Kubios HRV software
(Kuopio, Finland). The HRV
TH
was considered as the first
workload during the maximal incremental exercise test, in
which SD1 was less than 3 ms.
60
RPE responses
RPE was defined as the subjective intensity of effort, strain, dis-
comfort or fatigue that was felt during exercise.
64
The Borg
6-20 RPE scale was used to estimate whole-body perceived exer-
tion during exercise. RPE anchoring was: ‘number 7 represents
unloaded cycling while number 19 indicates an exertion similar
to exhaustive cycling’.
65
The RPE scale was displayed in front of
the participants during the tests and instructions about reporting
their perceived exertion were given before each test in both con-
ditions. Participants were asked to accurately report the RPE at
the end of each minute of the tests.
Statistics
All analyses were performed using the SPSS software (V.19.0,
Chicago, USA). Data are reported as means and SD. The distri-
bution of the data was analysed by the Shapiro–Wilk test, and
the results showed a normal Gaussian distribution. Mauchly’s
test of sphericity was used to test this assumption, and a
Greenshouse–Geisser was used when necessary. A two-way (RPE
and HR measured at different moments during incremental test
and stimulation procedure) analysis of variance with repeated
measures was applied. Bonferroni’s multiple comparisons test
was used to check where were the differences previously
detected by the analysis of variance. A paired Student’st-test
was used to compare PPO, HRV
TH
and TE in anodal tDCS and
sham conditions.
RESULTS
Table 1 lists the power outputs corresponding to HRV
TH
and
the PPO as well as the TE during the maximal incremental tests
for the anodal and sham conditions. HRV
TH
, PPO and TE were
all significantly higher for anodal tDCS compared to the sham
condition.
The calculated SD1 using Poincaré plots for every minute
during the maximal incremental test for anodal or sham tDCS,
as well as the HRV
TH
, is presented in figure 1.
The HR during exercise in both tDCS conditions is shown in
figure 2. There was an interaction effect between the stimulation
condition and time of measurement for HR (F
(10,90)
=3.60;
p=0.00047). Anodal tDCS produced significantly lower HR
during submaximal exercise compared to the sham condition.
Differences between experimental conditions occurred at
125 W (p=0.00053), 150 W ( p=0.00007), 175 W
(p=0.00006), 200 W (p=0.00007), 225 W ( p=0.00001),
250 W ( p=0.00345) and 275 W (p=0.04188).
Figure 3 shows the RPE during maximal incremental exercise in
both experimental conditions. The top graph (A) is plotted against
power, whereas the bottom figure (B) is against % exercise dur-
ation. For RPE plotted against power, there was an interaction
effect between stimulation conditions and time of measurement
(F
(10,90)
=5.43; p=0.00000). RPEs at 50 W ( p=0.01774), 75 W
(p=0.00000), 100 W (p=0.00003), 125 W (p=0.00000), 150 W
(p=0.00000) and 175 W (p=0.00003) of anodal stimulation were
lower than during the sham condition. The maximal RPE was not
different across the conditions, and nor were the RPE values when
plotted against % exercise duration (F
(3,27)
=0.45; p=0.71686).
Consistent with previous modelling studies,
66
tDCS produces
current flow in the brain under and between electrodes
(figure 4). In addition to diffuse clustering in parietal and
frontal regions, our montage resulted in current hotspots in the
IC of comparable magnitude to cortical peaks. The relatively
Table 1 Power output (W) at the heart rate variability threshold
(HRV
THR
), peak power output (PPO) and time to exhaustion (TE)
during incremental maximal cyclist test with anodal or sham
transcranial direct current stimulation (tDCS)
Anodal
tDCS SHAM
Degrees
of
freedom t p Value
PPO (W) 313.2±29.9 301.0±19.8 9 −2.358 0.043
TE (s) 751.4±71.5 723.7±45.0 9 −2.261 0.050
HRV
TH
(W) 147.5±53.3 125.0±35.4 9 −2.377 0.041
Figure 1 Heart rate variability responses (SD1) and respective heart
rate variability threshold during the maximal incremental cycling test
for the anodal transcranial direct current stimulation and sham
conditions. The dotted line represents the 3 ms of heart rate variability
threshold.
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high current density in this deeper structure represents the com-
bination of the electrode montage and neuroanatomy where
highly conductive cerebrospinal fluid can guide current to adja-
cent deeper brain regions.
DISCUSSION
To the best of our knowledge, this is the first study to show the
influence of tDCS on ANS, RPE and performance during a
maximal dynamic exercise test. Our main findings indicated that
anodal tDCS applied over the left TC of cyclists for 20 min
before exercise modulated ANS by delaying vagal withdrawal
and improved performance by ∼4% during a maximal incre-
mental exercise test. In addition, HR was reduced during the
initial submaximal portion of the maximal exercise test. The
RPE increased more slowly during exercise that followed anodal
tDCS application. However, maximal RPE and HR values were
not influenced by cortical stimulation.
Autonomic nervous system
We have recently shown that tDCS applied over T3 targeting
the left IC increases the parasympathetic modulation in athletes
at rest.
57
The present study extends this finding by showing that
the anodal tDCS effect remains during light and moderate exer-
cise, as shown by the delayed vagal withdrawal. Previous
research has shown that the TC and IC are associated with auto-
nomic cardiovascular control.
37 38 67–69
Besides the direct
effects of anodal tDCS on TC, this stimulation might also have
reached subcortical areas, such as the IC located just below the
TC as demonstrated in figure 1. Thus, anodal tDCS over the left
TC may have increased the parasympathetic modulation and
increased the HRV
TH
. The HRV
TH
HRV
TH
is strongly asso-
ciated with indices of human aerobic capacity.
32
Indeed, the
SD1 changes during the incremental exercise measured in the
present study were associated with a greater capacity to continue
to a higher work rate during maximal exercise.
Additionally, our data found that HR was decreased at sub-
maximal exercise intensities. Since cardiovascular control has a
strong feedforward component,
33 70
it can be speculated that
the anodal tDCS might have increased the parasympathetic
modulation or reduced the sympathetic modulation and, conse-
quently, decreased the HR. Hence, it seems quite likely that
anodal tDCS may induce improvements in cardiac autonomic
control and cardiac efficiency during aerobic exercise.
71
This
possibility certainly invites further study.
Rating of perceived exertion
The present study showed that anodal tDCS reduced the RPE
during the initial and submaximal phases of the maximal exer-
cise test. It has been proposed that the RPE is a psychophysio-
logical construct based on peripheral/central and cognitive
cues.
64 65 72
tDCS has been shown to provide an analgesic
effect when applied over the motor cortex.
27
fMRI studies of
the neural mechanisms of pain showed an increased signal in
the temporal gyrus.
73
Furthermore, verum acupuncture signifi-
cantly altered the brain response to pain stimuli by decreasing
the activation of the temporal gyrus.
74
In addition, the pain
modulation system is influenced by factors such as cognition
and emotion,
75 76
which also modulate the ANS activity
77
and
can alter the perception of pain. Moreover, there is evidence
that the left hemisphere is related more to positive emotional
feelings
43–45
and that vagal nerve stimulation induces high levels
of pleasant sensations.
67
Thus, since the RPE is also under the
influence of cognitive factors,
69
and since tDCS might induce
similar effect as vagal nerve stimulation, it follows that tDCS
may improve exercise tolerance by lessening the discomfort
levels and consequently decreasing the RPE.
The IC acts as the main brain site responsible for the aware-
ness of subjective feelings from the body
53 54
and is related to
Figure 2 Heart rates at the different power outputs during the
maximal incremental cycling test with either anodal or sham
transcranial direct current stimulation. *p<0.05.
Figure 3 Rating of perceived exertion (RPE) during the maximal
incremental cycling test in the anodal and sham transcranial direct
current stimulation conditions. (A) RPE versus workload. (B) RPE versus
%exercise duration. *p<0.05.
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the RPE during dynamic exercise.
49
The IC has pathways from
the premotor and parietal cortex
78
but also receives homeostatic
afferent signals, which provide the basis for the insular stream
of integration towards the ‘sentient self ’.
79
Then the ongoing
decision process during the exercise exertion (‘How do I feel
now?’;‘Do I go on?’;‘Do I try harder?’;‘Am I near the end?’),
based on ‘willpower’, must provide the subjective sense of
engagement that underlies the feeling of ‘effort’.
49 53
Thus,
anodal tDCS might also have modulated IC (figure 4) and prob-
ably affected the subjective feelings of effort, decreasing the
RPE during the submaximal part of the maximal exercise test
(figure 3A).
Also, experiments that have induced muscle pain produce an
increase in neural activity within widespread regions of both the
insular and cingulate cortices.
80
Furthermore, the IC is involved
not only in pain processing but also in the evaluation of other
homeostatic processes.
81
Under adverse conditions, the rate at
which the RPE increases during exercise can be elevated by pre-
vious strenuous exercise,
82
by hot environment
83
and by
reduced muscle glycogen stores.
84
However, in these studies
when the RPE slopes were plotted as a function of the percent-
age of exercise duration, the differences disappeared, as also
shown in our data between anodal tDCS and sham conditions
(figure 3B). Noakes and colleagues
13 85
suggest that the teleoan-
ticipation phenomenon would explain this response. This idea
was first suggested by Ulmer
86
who associated this concept to
the existence of an extracellular controller of the sustainable
metabolic rate during exercise. Therefore, our findings might
indicate the roles of the TC and the IC in integrating the
homeostatic and emotional tolerance control for more demand-
ing maximal exercise performance.
Exercise performance
Our findings indicated that anodal tDCS applied over the left
TC before exercise modulated improved performance by ∼4%
during a maximal dynamic exercise (incremental exercise test).
We speculated that anodal tDCS have modulated TC and prob-
ably the IC. Thus, affected by the subjective feelings of effort,
decreasing the RPE during the submaximal intensities improved
the performance in maximal exercise test. Studies investigating
the neural activity during a maximal 2 min handgrip contraction
reported that the activity of brain structures such as the IC and
cingulate cortex can be associated with the integration of inhibi-
tory influences arising from group III and IV muscle afferents.
87
Hilty and colleagues
88
have shown that, during an isometric
muscle fatiguing handgrip contraction until exhaustion, the IC
mediated the task failure, probably alerting the organism of
impending homeostatic imbalance.
Cogiamanian and colleagues
22
applied anodal tDCS over the
motor cortex and improved the performance of a submaximal
isometric motor task at 35% of the maximum voluntary con-
traction. It has been suggested that these results could be due to
an increase in cortical excitability. Since the present study evalu-
ated tDCS during a more demanding activity, we propose that
the enhancement in the performance could be related to a dif-
ferent mechanism, in which the delayed vagal withdrawal or
sympathetic activity attenuation shown by the reduced HR
could play an important role in the homeostatic regulation.
Even though a different brain region than the motor cortex was
targeted in the present study (ie, T3 and IC), the tDCS was
effective in modulating dynamic exercise performance.
In summary, together with the evidences provided by
Cogiamaniam, our data indicate the role of the brain in the
regulation of exercise. Although there is still a debate about ‘per-
ipheral’and ‘central’mechanisms determining exercise toler-
ance,
710–13
the brainless model of human exercise physiology,
solely, may not explain exercise performance.
Electrode montage
The selection of electrode montage (tDCS dose) in tDCS
governs the underlying brain current flow; computational
models of current flow are a standard tool in the analysis and
optimisation of resultant brain current flow.
66
Although the
focality of tDCS is limited by the electrode dimensions and
current flow physics (anatomy and tissue resistivity), the tDCS
montage used in the present study was selected to optimise
current flow to the IC. While influence from current flow in col-
lateral brain regions cannot be ruled out, the outcomes of the
present study are consistent with our hypothesis and predictions
of current flow in IC.
Figure 4 Computational model of
brain current flow during transcranial
direct current stimulation (tDCS). The
model development workflow
preserved the high resolution of the
MRI scans (1 mm
3
). tDCS produces a
diffused clustering of electric fields
across the parietal and frontal brain
regions. Importantly, using this
montage, the electric field peak in the
insula cortex was comparable to the
maximum electric fields produced on
the superficial cortex. The false colour
map indicates the electric field
magnitude.
Original article
Okano AH, et al.Br J Sports Med 2015;49:1213–1218. doi:10.1136/bjsports-2012-091658 5 of 7
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With regard to the electrodes montage used in this study
(bi-cephalic), the ‘active/stimulating’electrode was placed over
T3 and the ‘reference’electrode over the contralateral orbita,
14
both of which receive similar currents. This is a functional defin-
ition that does not imply that the ‘reference’electrode is physio-
logically inert. It is possible that the cephalic reference electrode
might also have modulated the brain regions involved in the cor-
tical cardiovascular regulation and decision making,
89
such as
the prefrontal cortex,
90
to tolerate high levels of effort.
Additionally, frontal lobe afferents to TC come from the orbital
cortex,
78
which may also have been influenced the ‘reference’
electrode, accounting for additional cardiac autonomic and RPE
modulation.
Limitations
The present results are the first to present the potential effects
of tDCS as a non-invasive and ergogenic method to enhance
dynamic exercise performance. However, some limitations of
the present study must be acknowledged. The use of bipolar
electrodes and the assessment of physiological responses (such
as muscle activity, cerebral oxygenation, and pulmonary oxygen
consumption) could have helped to better describe the mechan-
isms of action of tDCS on exercise performance.
CONCLUSIONS
In conclusion, non-invasive brain stimulation applied over the
TC induces electrical fields to IC and modulates the ANS activ-
ity and RPE during submaximal exercise. It also improves the
maximal exercise performance. This study indicates how the
brain plays a crucial role in the exercise performance regulation
by integrating physiological and psychological cues.
What this study adds
▸Novel way to improve maximal exercise performance using a
non-invasive brain stimulation technique.
▸Brain stimulation modulates the autonomic nervous system
and the sensory perception of effort.
▸Brainless model of human exercise physiology, solely, cannot
explain the exercise performance.
Acknowledgements The authors gratefully acknowledge Prof. Dr. Michael Nitsche
and Dr. Arthur (Bud) Craig for read the manuscript and provided critical comments.
The authors highly appreciate Renata Leite for engineering assistance (tDCS device)
and the cooperation of the cyclists who volunteered their time to participate in this
project.
Contributors AHO and EBF contributed to the conception and study design,
analysis and interpretation of data, as well as the writing and review of this
manuscript. RAM contributed to the acquisition and analysis of data, and writing.
TD, LLM, MB, ESC and PTVF contributed to the interpretation of data and revised it
critically for important intellectual content.
Funding Supported by the National Council for Scientific and Technological
Development (CNPq), Coordination for the Improvement of Higher Education
Personnel (CAPES), São Paulo Research Foundation - FAPESP, National Institute of
Health, The Wallace H Coulter Foundation and BrainGear.
Competing interests None.
Patient consent Obtained.
Ethics approval The National Commission of Research Ethics approved this study.
Provenance and peer review Not commissioned; externally peer reviewed.
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Original article
Okano AH, et al.Br J Sports Med 2015;49:1213–1218. doi:10.1136/bjsports-2012-091658 7 of 7
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and performance during maximal exercise
nervous system, rating of perceived exertion
Brain stimulation modulates the autonomic
Min Li, Marom Bikson and Timothy David Noakes
Montenegro, Paulo de Tarso Veras Farinatti, Edilson Serpeloni Cyrino, Li
Alexandre Hideki Okano, Eduardo Bodnariuc Fontes, Rafael Ayres
doi: 10.1136/bjsports-2012-091658
27, 2013 2015 49: 1213-1218 originally published online FebruaryBr J Sports Med
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