The Effects of Direct Current Stimulation and Random Noise Stimulation On Attention Networks

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com/scientificreports
OPEN The effects of direct current

stimulation and random noise
stimulation on attention networks
Alberto Lema1, Sandra Carvalho1,5, Felipe Fregni2, Óscar F. Gonçalves3 & Jorge Leite4*
Attention is a complex cognitive process that selects specific stimuli for further processing. Previous
research suggested the existence of three attentional networks: alerting, orienting and executive.
However, one important topic is how to enhance the efficiency of attentional networks. In this
context, understanding how this system behaves under two different modulatory conditions, namely
transcranial direct current stimulation (tDCS) and transcranial Random Noise Stimulation (tRNS), will
provide important insights towards the understanding of the attention network system. Twenty-seven
healthy students took part on a randomized single-blinded crossover study, testing the effects that
involved three modalities of unilateral stimulation (tRNS, anodal tDCS, and sham) over the DLPFC,
during the performance of the attention network test (ANT) in three different conditions: standard,
speed and accuracy. Results showed that tRNS was able to increase attention during more complex
situations, namely by increasing alerting and decreasing conflict effect in the executive network.
Under the Speed condition, tRNS increased efficiency of the alerting network, as well as under the
more demanding conflict network, tRNS overall increased the performance when comparing to
sham. No statistical significant effects of tDCS were observed. These results are compatible with the
attention requiring the synchronization of pre-existing networks, rather the reinforcement or creation
of new pathways.
Attention is a complex core cognitive function, responsible for prioritizing the selection for further process-
ing of internal and/or external sensory s timuli1. Attention can act through a bottom-up process in response
to externally driven salient stimuli or by a top-down approach, guided by previous knowledge, planning and
goals2. As a process, attention relies on multiple brain networks. According to Posner and Peterson3,4, attention
encompasses three brain networks: alerting, orienting and executive. Alerting network is activated to maintain
a state of readiness and is linked to thalamic and frontoparietal areas of the left hemisphere5,6. The orienting
network is associated with spatial orientation, as well as to covertly direct attention to focus on specific s timuli7
and is linked to the activation of the frontal eye field (FEF) and superior parietal cortex, mainly on the right-
hemisphere3. The executive control network refers to the process of conflict resolution associated with a g oal8
and is dependent on the activation of the dorsal anterior cingulate (ACC) and dorsolateral prefrontal cortex
(DLPFC)8–11. Although early studies suggested the independence of these three n etworks8, there are also reports
of that the three networks rather act in an inter-dependent m anner12, at least when participants are performing
the attention network test (ANT).
The ANT8 is a task, in which several warning cues and flankers targets are combined, in order to probe the
efficiency of each attention network, which has been widely used with h ealthy8,13,14 and clinical p
opulations15–17.
In each trial, 5 arrows are presented on screen and participants are required to make a left or right decision based
on the direction that the middle arrow is pointing at. Flankers can point towards the same direction of the central
arrow (i.e. congruent), or in the opposite direction (incongruent). And there can be also warning cues before
the target, that could either be in the center, and thus replacing the fixator, above or below the fixator, or even
double cues (i.e. above and below). This combination of no cues with spatial cues and congruent and incongruent
etworks8.
flankers allows to test the three attentional n
1
Psychological Neuroscience Laboratory, CIPsi, School of Psychology, University of Minho, Campus de
Gualtar, 4710‑057 Braga, Portugal. 2Spaulding Neuromodulation Center, Department of Physical Medicine
and Rehabilitation, Spaulding Rehabilitation Hospital & Massachusetts General Hospital, Harvard Medical
School, Boston, USA. 3Proaction Laboratory, Faculty of Psychology and Educational Sciences, University
of Coimbra, Coimbra, Portugal. 4I2P-Portucalense Institute for Psychology, Portucalense University, Porto,
Portugal. 5Department of Education and Psychology, University of Aveiro, Campus Universitário de Santiago,
Aveiro, Portugal. *email: [email protected]
Scientific Reports | (2021) 11:6201 | https://doi.org/10.1038/s41598-021-85749-7 1
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Age BDI STAI-Y state STAI-Y trait

Stimulation N Mean (SD) Mean (SD) Mean (SD) Mean (SD)
Female 19 22.16 (3.99) 4.11 (3.41) 33.68 (8.76) 35.42 (9.72)
Male 5 22.40 (2.51) 3.60 (3.78) 34.40 (9.13) 34.60 (8.29)
Total 24 22.21 (3.68) 4.00 (3.41) 33.83 (8.64) 35.25 (9.27)
Table 1. Sociodemographic and clinical information.
Interestingly enough attention is not a static process. Instead it relies on successful interregional
communication18. Interregional correlation time series between brain regions, or functional connectivity (FC)
showed that attention is a process involved in large scale brain network modulation, which includes within and
between network modulation19,20, as well as reoccurring patterns of network modulation21,22. Thus, it is not
surprising that these large scale FC modulations immediately preceding stimuli presentation are a predictor
of subsequent r esponse23,24. Moreover, by using a paced finger tapping paradigm, these moment-to-moment
fluctuations in large scale brain networks were also shown to be significant for attention. For instance, spontane-
ous increase in tap variance (i.e. out of the zone) was associated with dorsal attentional and salience networks,
while decreases in tap variance (i.e., in the zone) was associated with the default brain n etwork25. This has been
interpreted as being attentionally focused or in a mind wandering state26.
The dorsolateral prefrontal circuit is a suitable area for targeting attention enhancement, as it shares many
connections with cortical and subcortical structures such as the caudate nucleus, globus pallidus, substantia
nigra and the t halamus10,27. The DLPFC has an important role in top-down processing as well as inhibition of
irrelevant stimuli28. Neuroimaging studies have shown greater activation of left hemisphere during tasks related
to rapid changes as well as conflict r esolution3. Namely, the left hemisphere seems more involved in attention
cued paradigms whereas the right hemisphere seems more involved in slower responses over time, such as sus-
tained attention3,11. Therefore, attention paradigms such as the ANT are more likely to involve left hemisphere
activation, especially to attend to warning cues and conflict resolution among conflicting targets. Moreover, the
left DLPFC has already been used as a target area for the study of attention in combination with transcranial
electric stimulation (tES)29,30. And, as such attention has been a target for cognitive training alone in healthy31,
opulations32,33.
or in clinical p
Transcranial direct current stimulation (tDCS) is one of the most used tES techniques, which has been shown
to increase working memory34, cognitive flexibility35,36, inhibition37, and attention38, among other cognitive
functions. In tDCS, a weak electric current is delivered to the scalp that is able to induce neuromodulatory (i.e.
change the likelihood of firing) and neuroplastic effects (by LTP and LTD)39,40. For instance, anodal tDCS over the
right inferior frontal gyrus (i.e., 2 mA for 30 min) significantly increased performance in the alerting network38.
Similarly, the orienting network has also been successfully modulated by anodal tDCS over the posterior parietal
cortex (PPC) at 1.5 mA for 20 m inutes41. Recently, offline anodal tDCS over the left DLPFC at 2 mA for 20 min
showed a significant increase performance in the executive n etwork29. Moreover, tDCS over the prefrontal
cortex was able to increase performance in the orienting and executive networks in people with fi bromyalgia17.
Another tES technique that can modulate large-scale n etworks42 is transcranial random noise stimulation
(tRNS), a stimulation technique based on alternating current delivered at random normally distributed frequen-
cies ranging from 0.1 to 640 Hz43. Terney and colleagues were among the first to demonstrate the tRNS excitatory
effects on the motor cortex (M1)44. Since the first studies on motor cortex, tRNS has also proven to be effective
in increasing performance in visual discrimination of faces45 and e motions46, numerical cognition, especially on
complex scenarios47, as well as working m emory48. Despite the fact that tRNS is able to modulate large-networks
within the brain, and the fact that attention relies of several large scale networks in the brain, there was one
previous attempt to study the effects of tRNS on affect, pain and attention was conducted on people suffering
from multiple s clerosis49. However, the authors only showed that tRNS over the left dorsolateral prefrontal cortex
(DLPFC) was only able to decrease pain. Thus, to the best of our knowledge, no previous studies have suggested
specific frequency bands or applied full spectrum tRNS on attention, in healthy population.
Previous studies have shown that both t DCS29,38 and tRNS47 may actually improve performance, however
potentially through different mechanisms such as creation of new connection or the development of new learning
circuits in the case of tDCS, or better functional connectivity at critically across the pre-existent neural circuitry50.
In this context, understanding how the attentional system would behave under two different modulatory condi-
tions (tDCS and tRNS). would provide important insights towards the understanding of the attention network
system. Therefore, the objective of this study was to study the effects of anodal tDCS and full spectrum tRNS on
attentional network efficiency, as assessed by the attention network test (ANT).
Methods
Participants. A total of twenty-seven student volunteers, aged between 20 to 32 years old (M 22.78; SD
3.89; 7 males), recruited on campus, participated in this study (see Table 1). All participants reported to be
healthy, with normal or corrected-to-normal vision and were right-handed (Edinburgh Handedness Inventory:
EHI ≥ 80)51. Participants were excluded if they had any contraindication to receive tDCS/tRNS (such as metal in
the head, implanted brain medical devices, scalp injuries prior experience of active tDCS/tRNS adverse effects,
seizures, frequent headaches or migraines, use of medication, history of epilepsy, history of psychiatric/neu-
rologic disorders, and any uncontrolled health conditions likely to worsen patient’s functional status in next
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Figure 1. Study design. Cross-over controlled study with three experimental sessions: anodal tDCS, tRNS, and
sham tDCS/tRNS randomized and counterbalanced across participants. The interval between each session was
of, at least, 72 h.
6-months such as cancer, terminal heart, kidney, or liver disease). Additionally, we excluded participants who
reported extreme fatigue due to insufficient sleep in any stimulation session. All participants reported compli-
ance with the experiment’s initial recommendations to avoid alcohol, cigarettes and caffeinated drinks on the day
of the experiment and none reported fatigue due to insufficient sleep. The study was performed in accordance
with the Declaration of Helsinki, and all participants gave their written informed consent prior to their inclusion
in the study. The study was approved by the local ethics committee.
Design. Overall procedure. This is a randomized, single-blinded and crossover controlled study in which
participants were randomized to receive both anodal tDCS, tRNS, and sham tDCS/tRNS. In order to decrease
inter-individual effects, all participants received the 3 stimulation conditions. The stimulation order was fully
randomized and counterbalanced across participants. The interval between each session was of, at least, 3 days
to account for any carry-over stimulation effects43. We assessed the presence and severity of mood and anxi-
ety symptoms in the initial screening using the Beck Depression Inventory—BDI52 and the State-Trait Anxiety
Inventory—STAI-Y53,54. In the pre- and post-stimulation assessments, participants were screened about discom-
fort, fatigue, pain, itching, humor, tingling, burning, headache and sleepiness (among others) using a continuous
Visual Analog Scale (VAS). Participants also responded to a modified version of the Positive and Negative Affect
Schedule (PANAS)55 to assess changes in mood associated with the stimulation. At the end of each session, we
assessed the blinding procedure’s efficacy with a blinding questionnaire. The duration of each session was ap-
proximately 45 min.
Please see Fig. 1 for a schematic representation of the study.
Experimental task. We administered a modified version of the attention network test described by Fan
et al.8. In this task, participants were asked to press a key indicating the direction (i.e., left or right) of a cen-
tral arrow flanked by distracters pointing to the same or opposite direction (i.e., neutral “- -> - -”, congruent
“ > > > > > ” or incongruent trials “ < < > < < ”)56. Before the target presentation, participants could be cued with
an “*”, which could appear at an up, down or both (i.e., double) position from the central fixator, signaling a
probable location of the following target or no cue (See Fig. 2A). Each trial consisted of a stochastic fixator
period (400–1600 ms), a brief cue presentation(100 ms), a fixation period (400 ms) and a target presentation
until participant response (max. 1700 ms), and an inter-trial interval with a variable duration, in order to ensure
that each trial lasted for a total of 4000 ms (See Fig. 2).
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Figure 2. Attention network test (ANT) description and task design. (a) Cues, targets and trial sequence.
(b) Task design: instructions were always given in the same order: first Standard Condition (regular task
instructions), then, after a short break, Speed Condition (participants were asked to respond as fast as possible)
and finally, after a new break, Accuracy Condition (participants were asked to respond as accurate as possible)
followed.
The ANT had four blocks: a full-feedback 24 trials practice block and three experimental blocks. Each experi-
mental block had 96 trials which were determined by: target directions (left, right) × target locations (up, down)
× flanker congruencies (neutral, congruent, incongruent) × cue types (no cue, center cue, double cue and spatial
cue), all repeated twice. Hence, 288 experimental trials were completed per session. The duration of the task was
about 20 min. We modified the instructions of the ANT by presenting a new instruction before each experimen-
tal block, during the breaks. Instructions for each block followed a fixed sequence: (i) first experimental block,
participants were given standard instructions to “respond as fast as possible, without committing errors” (i.e.,
Standard-ANT); (ii) second experimental block, participants were asked to “respond as fast as possible” (i.e.,
Speed-ANT); (iii) third block, instruction was changed to “respond as accurate as possible” (i.e., Accuracy-ANT).
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Figure 3. Electrode placement and stimulation parameters. (a) Electrode placement. 35 cm2 electrodes were
used for both anode and cathode. Red dot represents the anode, over the left DLPFC (F3) while the blue dot
represents the cathode, over the contra-lateral supra-orbital area (FP2). All stimulation conditions (sham,
anodal-tDCS and tRNS) followed the same montage. (b) Stimulation parameters: tDCS for 20 min at 2 mA
with a ramp in/out of both 15 s; tRNS current intensity was of 2 mA, with full-spectrum frequency 0.1–600 Hz;
sham-tDCS was delivered at the beginning and at the end of 20 min applying 45 s of real stimulation (15 s
ramp-up, 15 s stimulation and 15 s ramp-down).
This was done in order to induce a change in participant´s response strategy, by increasing their focus on response
speed or on accuracy. Before the beginning of each experimental block, participants were given a short break and
the new set of instructions. The presentation order of the instructions was kept constant throughout all sessions
and participants (i.e., Standard ANT, Speed-ANT, and Accuracy-ANT conditions) to allow for comparisons
between blocks and stimulation duration (See Fig. 2B).
The ANT used in this study was programmed with E-Prime version 2.0 SP1 (Psychology Software Tools,
Sharpsburg PA, US) and presented using a desktop computer running Windows 10 with a 17-in LCD (Fujitsu
DVI-VGA) monitor with a 1280 × 1024 pixels’ resolution and a 75 Hz frame rate. Participants seated at approxi-
mately 60 cm of the screen and were required to respond by pressing the right or left mouse buttons.
Stimulation protocols. Electric current was delivered by a 5 × 7 (35 cm2) cm pair of rubber electrodes in
saline-soaked sponges placed over the left DLPFC (F3; anode) and the contralateral supraorbital area (Fp2; cath-
ode), in accordance to the International 10–20 EEG System57 (See Fig. 3A). 2 mA of anodal tDCS was delivered
for 20 min (with 15 s of ramp in/out). tRNS was delivered at 2000 μA with full-spectrum frequencies ranging
from 1 to 640 Hz, for 20 min. Both stimulations were delivered continuously for 20 min during the completion
of the task. Sham-tDCS consisted of 45 s of stimulation delivered at the beginning and at the end of the 20 min
(i.e., 15-s for each phase: ramp-up, stimulation, and ramp-down). We applied this blinding procedure, with
15-s of verum stimulation in the beginning and in the end, in order to minimize the difference between the
sensations induced by the active stimulation (especially the tRNS) when compared to the sham condition (see
Fig. 3B). Previous studies have shown that the blinding may be compromised in repeated measures designs with
a high current intensity such as 2 mA58–60. All stimulation techniques were applied using a Magstim Eldith DC
Stimulator Plus (Neuroconn, DE).
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Assessments. The Edinburgh Handedness Inventory—EHI51 was used to measure hand preference for
common manual tasks. Participants are asked to rate 10 statement on the use of the right or left hand when
performing a specific action (e.g., writing or using scissors). Scores range from − 100 to 100 for left and right-
handed, respectively. To be included as right-handed in the study, participants needed to score above 80.
To measure the presence and severity of depressive symptoms across affective, cognitive, motivational, and
functional domains, we used the Beck Depression Inventory—BDI52. The BDI is a 21-item rating inventory to
assess how the subjects feel “at that moment” about each statement on a four-point scale (symptoms severity
increases from 0 to 3). Participants with scores above 9 (i.e., symptomatic), were excluded due to known effects
of depression on cognition and reaction times.
State-Trait Anxiety Inventory—STAI-Y53,54 is a 40-item scale used to measure trait anxiety (e.g., “I worry too
much over something that really does not matter”) and state anxiety (e.g., “at that moment” anxiety feelings such
as “I am tense”). Items are rated on a four-point scale, with higher ratings indicating greater anxiety. Scores for
each subtest ranges from 20 to 80 with a cut-off score of 40 for clinically significant anxiety symptoms.
The Positive and Negative Affect Scale—PANAS55 is a 20-item scale that measures the affective disposition
composed by two mood scales: positive (PA) and negative affect (NA). PA is defined as activation or engagement
and is represented by positive mood items like “Interested” and “Excited.” In contrast, NA is defined by lethargy
or sadness and is represented by negative mood items like “Irritable” and “Afraid”. Participants are asked to rate
the extent to which they experience each item within a specified period (e.g., “right now” or “over the past week”)
on a five-point scale (from 1—Very slightly or not at all to 5—Extremely). Scores range from 10 to 50 for each
subscale, with higher scores indicating higher PA or NA levels.
The Visual Analog Scale/tES—VAS. The VAS is a 10-item scale that measures potential adverse effects of tES
on a continuous scale (from 0 to 10). Adverse effects are assessed on several domains: tiredness, anxiety, sadness,
agitation, sleepiness, itch, headache, pain, tingling, and metallic taste. This scale was administered before and
after the intervention to control for potential adverse effects of the stimulation.
Adult Safety Screening Questionnaire. This questionnaire was administered to determine the participants’
suitability to undergo tDCS and tRNS interventions. It is a 16-item instrument that assesses the prior contact
with tDCS or other tES techniques, past adverse effects, occurrence of convulsions, stroke, serious head injury,
frequent or severe headache, implanted medical devices, medication, pregnancy and epilepsy. All items are
answered by a yes/no. If yes to any of the items, more detailed information was asked.
We used a blinding Questionnaire to measure the efficacy of the blinding procedure, as perceived by the
subjects. Participants were asked to indicate if they think the tDCS/tRNS intervention was active, sham, or do
not know the answer. Additionally, they were required to mention how confident they feel about their response
on a five-point scale (from not confident at all to extremely).
Data analysis. All data analyses were performed using SPSS version 25 (IBM, United States). From the 27
participants enrolled in the study, a total of three participants were excluded. Two of them were excluded due
to the presence of psychiatric symptoms as indexed by BDI scores of 13 and 14 and one of them due to high
scores in VAS (i.e., > 8) for fatigue and anxiety across all sessions. Therefore, final analyses were performed with
24 participants.
Prior to computing the network scores from the ANT, we selected only correct responses, resulting in a loss
of 1.98% of the data. We also removed outliers with response time (RT) < 200-ms and > 1200-ms, which ended
up in an additional loss of 0.28% data. The remaining data base was used for both RT and Accuracy analyses. For
RT, we calculated the ANT scores using the median of correct responses as a measure of central tendency61,62.
We calculated all networks scores according to Westlye and c olleagues62 formula, by subtracting the RT from
relevant network-conditions and scaled to percentage by dividing the network score by the center cue (alerting
network), spatial cue (orienting network) and congruent target (executive network). Please see the following
formulas for more details on the percentage scaled results.
RT(nocue) − RT(center)
Alerting = ,
RT(center)

RT(centercue) − RT spatial
Orienting = ,
RT spatial

RT incongruent − RT congruent
Executive = .
RT congruent
For alerting and orienting ANT scores, higher scores indicate better performance (i.e., benefits from cue
presentation), whereas for executive network ANT scores, lower scores indicate better performance (i.e., less cost
related to the filtering of incongruent target). We performed an additional analysis on RT of no cue condition
under standard condition to verify the effects of the stimulation techniques at a motor level. For accuracy, we
computed the mean percent of correct response (ACC) of the cues involved in each network.
The statistical analyses for both RT and ACC followed these steps: normality of the distribution was assessed
by Kolmogorov–Smirnov test; main analyses consisted of GLM repeated measures ANOVAs with instruction
condition (standard, speed, accuracy) and stimulation condition (sham, tDCS, tRNS) as within-subject factors;
data sphericity was assessed by the Mauchly test and corrected using Greenhouse–Geisser when appropriate;
post-hoc comparisons were performed using LSD whenever significant effects were found (p < 0.05). As indexed
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Figure 4. Response time effects on all attention networks. (a) Stimulation main effect for all attention networks.
Only executive network showed a significant effect of tRNS improving conflict resolution when compared
to sham (p = 0.022). (b) Interaction effects for all attention networks. Alerting network showed a significant
interaction effect, namely, under Speed Condition, tRNS showed a facilitating effect when compared to tDCS
(p = 0.005) but not compared to sham (p = 0.055). *p < 0.05 Error bars show Standard Error. +p < 0.10, *p < 0.05,
**p < 0.01, ***p < 0.001.
by PANAS and VAS before and after stimulation scores, adverse effects were computed with paired-samples
t-tests.
Ethical approval and informed consent. All procedures performed in the study were in accordance
with the ethical standards of the Declaration of Helsinki (1964). All participants gave written informed consent
before they participated in the study. The study was approved by the local ethics committee, Ethics Committee
for Research in Life and Health Sciences (CEICVS), at Minho University.
Results
Attention network test. Response time. For the alerting network, the main analysis showed that there
was no statistical significant effects for condition [F(2, 46) = 0.22, p = 0.801, ηp2 = 0.010] or stimulation [F(2,
46) = 0.67, p = 0.517, ηp2 = 0.028]. However, there was a statistically significant interaction effect between condi-
tion and stimulation [F(4, 92) = 3.53, p = 0.010, ηp2 = 0.133]. Pairwise comparisons showed that under speed con-
dition, tRNS increased ANT score as compared to anodal tDCS (p = 0.005), but not to sham (p = 0.330). Anodal
tDCS marginally decreased the ANT score when compared to sham (p = 0.055) (see Fig. 4B).
For the orienting network, the main analysis showed that there was no statistically significant effect for con-
dition [F(2, 46) = 0.33, p = 0.716, ηp2 = 0.014], stimulation [F(2, 46) = 0.29, p = 0.744, ηp2 = 0.013], nor interaction
[F(4, 92) = 0.66, p = 0.616, ηp2 = 0.028].
For the executive network, analyses showed significant effects for the condition [F(2, 46) = 12.20, p < 0.001,
ηp2 = 0.347] and stimulation, [F(2, 46) = 3.72, p = 0.032, ηp2 = 0.139], yet no interaction effect was found [F(4,
92) = 1.29, p = 0.281, ηp2 = 0.053]. For the condition main effect, as expected, speed condition increased the ANT
score when compared to standard (p < 0.001) and accuracy conditions (p = 0.001), resulting in worse RT per-
formance. For stimulation main effect, tRNS showed a decrease in the ANT score when compared to sham
(p = 0.022), thus improving efficiency of the executive network by reducing the time needed to solve the conflict
between congruent and incongruent target (see Fig. 4A and Table 2 for scores). Other comparisons were not
statistically significant.
Additionally, we analyzed no cue RT as a probe for possible changes at the motor level. We analyzed the effects
of stimulation condition on no cue RT under standard instruction using one way repeated measures ANOVA.
Results showed no effect of stimulation [F(2, 46) = 2.33, p = 0.108, ηp2 = 0.092]. Therefore, stimulation conditions
did not change the RT of participants when no cue were presented. We also highlight in the discussion that the
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Stimulation
Sham (N = 24) a-tDCS (N = 24) tRNS (N = 24)
Instruction
Attention effect condition RT Mean (SD) Acc % RT Mean (SD) Acc % RT Mean (SD) Acc %
Standard 20.94 (30.34) 98.00 (3.16) 17.25 (38.05) 97.57 (3.45) 6.88 (27.50) 98.61 (1.90)
Alerting Speed 17.19 (37.65) 95.14 (5.12) 0.17 (26.99) 97.22 (2.92) 27.06 (31.66) 97.48 (3.24)
Accuracy 13.83 (32.14) 98.35 (1.37) 19.75 (40.27) 97.83 (3.71) 5.54 (28.48) 98.18 (2.90)
Standard 42.54 (40.01) 98.18 (2.63) 32.31 (33.52) 98.00 (2.97) 42.08 (32.19) 98.70 (1.82)
Orienting Speed 31.56 (42.31) 95.31 (5.18) 40.73 (37.44) 97.40 (3.89) 29.58 (37.51) 97.57 (3.45)
Accuracy 34.52 (37.04) 98.52 (1.56) 43.77 (33.18) 98.26 (3.67) 44.00 (28.45) 98.87 (2.13)
Standard 99.17 (41.24) 97.92 (3.65) 100.85 (35.87) 96.81 (4.18) 92.29 (38.53) 98.24 (1.80)
Executive Speed 133.67 (60.21) 93.75 (6.65) 117.46 (36.66) 95.96 (4.54) 104.25 (42.73) 96.55 (4.22)
Accuracy 116.25 (33.75) 97.92 (1.88) 105.85 (47.04) 97.07 (4.43) 89.54 (39.12) 97.59 (3.26)
Table 2. RT and ACC for each attention network effects by instruction condition and stimulation. Attention
networks effects are derived from the ANT.
Figure 5. Accuracy effects on all attention networks under speed condition. Under speed condition (“respond
as fast as possible”), tDCS and tRNS significantly improved mean percent of correct response when compared to
sham across all attention networks. Error bars show Standard Error. *p < 0.05, ** p < 0.01, ***p < 0.001.
effects may be also due to motor components related to task performance, however, the data from the simple RT
does not suggest that these effects are purely motor.
Accuracy: ACC. For Alerting, analyses showed that there was a statistical significant main effect for condi-
tion [F(1.49, 34.48) = 6.46, p = 0.008, ηp2 = 0.219, ɛ = 0.75], but not for stimulation [F(2, 46) = 2.58, p = 0.086,
ηp2 = 0.101]. An interaction effect was also found [F(4, 92) = 2.96, p = 0.024, ηp2 = 0.114]. Post hoc analysis for the
interaction effect revealed that under the Speed condition, both active tRNS (p = 0.003) and tDCS (p = 0.008)
showed a significant increase in accuracy when compared to sham (see Fig. 5; see Table 3 for more information).
Other comparisons were not statistically significant.
Orienting network analyses showed statistically main effects of condition [F(1.41, 32.46) = 5.81, p = 0.013,
ηp2 = 0.202, ɛ = 0.70] and stimulation [F(2, 46) = 4.67, p = 0.014, ηp2 = 0.169], as well as an interaction effect [F(2,
46) = 2.86, p = 0.028, ηp2 = 0.111]. The interaction effect showed that under Speed Condition, both active tRNS
(p = 0.002) and tDCS (p = 0.001) increased accuracy when compared to sham (see Fig. 5; see Table 3 for more
information).
For the executive network, analyses showed a statistically significant main effect for condition [F(1.34,
30.98) = 7.70, p = 0.005, ηp2 = 0.251, ɛ = 0.67]; but not for the stimulation conditions [F(2, 46) = 3.02, p = 0.059,
ηp2 = 0.116].An interaction effect was also found [F(2.90, 66.77) = 4.09, p = 0.0115, ηp2 = 0.151, ɛ = 0.72]. Post hoc
analysis for the interaction effect revealed that under the Standard condition, active tDCS showed a decrease in
conflict accuracy when compared to sham (p = 0.035) and tRNS (p = 0.038). Under Speed Condition, however,
both active tRNS (p = 0.003) and tDCS (p = 0.012) increased conflict accuracy when compared to sham. Other
comparisons were not statistically significant (see Fig. 5; see Table 3 for more information).
Exploratory analysis based on the effects of instruction blocks on accuracy. Post-hoc tests for the condition
main effect did reveal statistically significant decrease in accuracy during Speed when compared to Standard
(p > 0.001) and to Accuracy conditions (p = 0.019) in the alerting network. Post-hoc analyses for condition main
effect for the orienting network showed that under Speed Condition, accuracy decreased significantly when
Vol:.(1234567890)
Instruction condition
Standard Speed Accuracy
Stimulation Cues and targets RT (M, SD) Acc (%, SD) RT (M, SD) Acc (M, SD) RT (M, SD) Acc (M, SD)
No cue 554.50 (79.91) 99.61 (2.92) 521.04 (58.85) 96.01 (4.68) 556.58 (60.88) 98.61 (2.35)
Center cue 533.56 (75.14) 97.40 (4.73) 503.85 (69.48) 94.27 (6.93) 542.75 (68.68) 98.09 (2.74)
Double cue 526.23 (69.24) 98.96 (3.53) 510.46 (67.22) 95.66 (7.00) 541.90 (69.69) 97.92 (3.25)
Sham
Spatial cue 491.02 (61.89) 98.96 (1.84) 472.29 (70.65) 96.35 (5.26) 508.23 (73.87) 98.96 (1.84)
Congruent 498.15 (71.62) 99.61 (1.06) 466.02 (60.34) 99.48 (1.19) 504.77 (58.96) 100.00 (0.00)
Incongruent 596.31 (87.98) 96.22 (7.37) 599.69 (98.78) 88.02 (12.52) 621.02 (79.65) 95.83 (3.76)
No cue 529.31 (66.55) 97.40 (4.22) 515.19 (51.85) 97.92 (3.25) 562.17 (67.09) 97.57 (4.58)
Center cue 512.06 (61.56) 97.74 (3.68) 515.02 (66.20) 96.53 (4.86) 542.42 (65.13) 98.09 (3.47)
Double cue 513.06 (57.39) 97.57 (3.67) 506.25 (60.15) 96.18 (5.20) 540.54 (59.68) 97.40 (2.96)
a-tDCS
Spatial cue 476.25 (58.70) 98.26 (3.23) 474.29 (59.18) 98.26 (3.67) 498.65 (59.83) 98.44 (4.57)
Congruent 478.13 (53.46) 99.22 (2.11) 472.46 (52.65) 99.61 (1.40) 510.63 (60.78) 99.48 (1.19)
Incongruent 578.98 (74.50) 94.40 (8.54) 589.92 (57.76) 92.32 (8.19) 616.48 (76.09) 94.66 (8.37)
No cue 532.15 (60.10) 98.78 (2.29) 524.75 (62.97) 97.92 (3.25) 540.44 (57.09) 97.92 (3.48)
Center cue 525.27 (68.30) 98.44 (2.40) 497.69 (66.37) 97.05 (4.16) 534.90 (59.88) 98.44 (3.21)
Double cue 519.58 (58.11) 98.61 (2.35) 498.81 (61.51) 97.05 (4.34) 532.90 (53.52) 97.22 (3.82)
tRNS
Spatial cue 483.19 (57.22) 89.96 (2.22) 468.10 (70.78) 98.09 (3.47) 490.90 (58.63) 99.31 (1.59)
Congruent 488.75 (55.65) 100.00 (0.00) 468.44 (60.27) 99.74 (0.88) 502.75 (52.28) 99.87 (0.64)
Incongruent 581.04 (83.41) 96.48 (3.61) 576.71 (66.77) 93.36 (8.56) 592.29 (61.04) 95.31 (6.58)
Table 3. Mean (SD) RT and ACC for each cue and target by instruction condition and stimulation.
Before (N = 24) After (N = 24)

Stimulation Dimensions Mean (SD) Mean (SD) t (23)
Itching 0.39 (1.03) 1.17 (1.53) 2.27*
Sham
Tingling 0.00 (0.00) 0.35 (0.65) 2.58*
Itching 0.58 (1.38) 2.21 (2.57) 3.49**
a-tDCS Tingling 0.08 (0.28) 0.79 (1.41) 2.38*
Headache 0.46 (1.06) 0.75 (1.11) 2.07+
Itching 0.25 (0.85) 0.88 (1.65) 1.97+
tRNS
Headache 0.63 (1.38) 1.17 (2.06) 2.18*
Table 4. VAS self-report differences before and after experimental protocol. Visual analogue scale (VAS).
We only report symptoms that present a statistically significant increase between before and after the sessions
(all symptoms assessed: tiredness, anxiety, sadness, agitation, sleepiness, itching, headache, pain, tingling and
metallic flavor). + p < 0.10, *p < 0.05, **p < 0.01, *p < 0.001.
compared to Standard (p = 0.006) and Accuracy conditions (p = 0.022). Similarly, for the executive networks,
post hoc tests for condition main effect did reveal statistically significant decrease in accuracy when Speed Con-
dition was compared to Standard Condition (p > 0.001) and to Accuracy Condition (p = 0.019).
Adverse effects. Regarding the effects of each stimulation condition in affect (positive or negative)
as assessed by the PANAS, there was no statistically significant difference in any stimulation condition (all
P’s > 0.083). Results for adverse effects as indexed by VAS scores showed a statistically significant increase in itch-
ing [t(23) = 3.49, p = 0.002)] and tingling [t(23) = 2.37, p = 0.026], for anodal tDCS when comparing before and
after stimulation. For tRNS, we only found a statistically significant increase in headache [t(23) = 2.18, p = 0.039].
As expected, anodal tDCS produced the highest itching score (See Table 4). However, it is important to highlight
that these effects were mild, not averaging 3 on a 10-point scale. No phosphenes were reported by participants.
Blinding efficacy. In order to assess if participants were able to correctly guess the stimulation condition to
which they were subjected to in that particular session (i.e., active or sham), participants responses about their
guessed allocation were asked at the end of each session. Participants were able to correctly guess their allocation
to sham and active conditions in 38 out of 72 sessions, which translates to 52.78%. Most of participants rated
their confidence level on the responses as moderate (34.21%) or considerable (31.58%).
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Discussion
The aim of the present study was to examine the effects of tRNS and anodal tDCS over the left DLPFC, as
compared to sham stimulation, on the alerting, orienting and executive networks of attention. Additionally, in
order to probe potential effects on the ANT, we used three distinct blocks: standard, focus on speed and focus
on accuracy.
Under the speed condition, participants who received tRNS performed better in terms of the alerting network
ANT score by responding faster, when compared to tDCS. It has already been shown that tRNS applied to the
visual cortex enhances p erception63,64, or affects the binocular rivalry p henomenon65. As attention requires a
transient long phase synchronization in the theta band between fronto-parietal-temporal r egions66, intra and
inter-regional modulation seems to be required in order to modulate attention. As synchronization between
regions depend on several factors such as frequency, anatomical distances, axon conduction velocity, among
others, effective communication requires a favorable signal to noise ratio. However, not all the neurons that
are responsible for signal transmission will reach a threshold that will allow them to depolarize. In this sense,
random noise stimulation may help to improve inter-regional transmission by the mechanisms of stochastic
resonance64,67, in which the noise added to neural processing improves the signal in the attention network. For
instance, using a global motion task, it has been suggested that high frequency tRNS was able to tune in neurons
near the directional signal and improved signal pooling of the local cues, by an increased signal-to-noise ratio,
which in turn increased the overall sensitivity for the global motion68.
On linear systems, noise induction impairs performance, however in non-linear systems, adding noise can
actually increase performance69. Adding a subthreshold noise to a weak signal can increase its detection44,67,
especially because stochastic resonance has been shown to modulate intra and inter regional neural
synchronization63,65,67,70. This is especially relevant for tasks in which the synchronization of different brain
regions is required, such as in the attention system. Therefore, it is possible that under the speed condition,
increased network demands in the brain (which is a non-linear system), allowed for additional neurons to tune
in by the mechanism of stochastic resonance, thus increasing performance in the alerting network.
Our exploratory analysis of accuracy suggests that speed emphasis actually decreased accuracy, in what is
called a speed accuracy tradeoff (SAT). Moreover, compared to other conditions, the speed condition signifi-
cantly increased the conflict effect in the executive network, thus, resulting in participants adopting a different
response criterion under a time-constraint speed instruction (i.e., “Respond as fast as possible”). Therefore, the
condition changed participants’ behavior.
First of all, it is important to explain this SAT process71. Typically, when speed of response is favored, accu-
racy is decreased, whereas, when accuracy is favored, a decrease in speed is expected. More than changes in
participant’s strategy, neuroimaging studies suggest that SAT is mediated by an interplay between cortical and
subcortical structures72–75. Namely, SAT seems to rely on cortical integrators76 (e.g. pre-supplementary motor
area) and at the subcortical level through basal ganglia inhibitory a ctivity75,77. Under speed it is possible that
these cortical integrators receive additional excitatory inputs, which results in increased baseline activity; or that
increases in striatal activity will decrease the inhibitory control of the basal ganglia over the brain73.
These theories highlight the importance of the relationship between cortical and subcortical regions. Regard-
less of the fact that the present study cannot provide insights about how the brain changes during the SAT, it is
important to highlight that tDCS and tRNS had very distinct effects on the ANT scores, especially under speed
instructions. Moreover, according to the speed-accuracy tradeoff, in the condition in which speed is favored,
accuracy is decreased71. In other words, it is harder to maintain accuracy, with shorter response times. In this
sense, with a focus on response time, accuracy decreases, simply because it is ubiquitously harder to maintain
accurate performance (as demonstrated by the present data on the accuracy under the speed condition).
tRNS seems to have counteracted this increased difficulty demand over the network and, indeed, improved
RT when the task complexity increased—especially on the case of the executive network. This phenomenon has
already been shown b efore47,63,78. For instance, beneficial effects of tRNS during an arithmetic learning task have
been shown previously, but only on the difficult condition when the number of repetitions was l ower47. Moreover,
random noise applied to the earlobes was also able to induce an effect on an arithmetic task, but only for the
complex version50. More specifically, tRNS improved participant´s performance by decreasing response time
for incongruent targets for the executive network. It is important to highlight that the executive network is the
most demanding in terms of the cognitive resources required to perform the ANT, as it requires the filtering of
task conflicting stimuli. In this sense, it is possible that tRNS may improve the filtering of relevant and irrelevant
information related to the t ask79,80. Speed further increases cognitive demands due to the need to adjust the
response threshold to faster responses when less information is available to make a decision, which has already
been shown to induce greater activation in frontal regions, such as striatum, supplementary motor area (pre-
SMA) and DLPFC73,77,81. As these changes rely on more efficient intra and inter regions communication, the
facilitatory effects of tRNS may have occurred through subthreshold stochastic resonance, in which the added
random noise to the neural system may have improved the detection of the signal by facilitating its processing
and detection at critically44,82. According to the at critical brain hypothesis, brain networks operate near phase
transition called at criticality, which lies between states of increased or decreased activation and therefore is not
unique83. In this context, the presence of non-zero noise will add a subthreshold noise to the signal and, there-
fore, facilitate its transmission by reaching the at criticality p oint84. In this at critically point there is increased
similarity between the input signal and the one that travels throughout the system, which can result, for instance,
in increased target detection64. In this sense, tRNS was able to increase overall performance over the executive
network by increasing the similarity between the input and the signal throughout the task related network, due
to the stochastic resonance p henomenon70,85. However, this hypothesis of stochastic resonance should be further
Vol:.(1234567890)
explored, especially by assessing stimulation-induced changes in the spontaneous brain oscillatory activity, as
well as in the intra and inter-regional functional connectivity.
Anodal tDCS did not showed any effect on executive network, as previously found by Miler and colleagues in
a similar experiment29. The instruction conditions in our study may have negatively affected tDCS ANT score due
to changes in participants strategy as well as functional connectivity demands as shown by a decrease in accuracy
on the executive network under the standard instructions. tDCS effects on attention may require constant instruc-
tion conditions or the combination with cognitive training to increase the efficiency in the orienting or executive
networks17. This is compatible with the rationale underlying the effects of tDCS, namely modulation of cortical
activity and excitability, which leads to secondary changes to synaptic connectivity (i.e., new learning)86,87. tDCS
seems therefore to facilitate new learning (rather than consolidate it)34,88,89. Interestingly, studies have shown
that timing of tDCS application is critical for its effects as well as tDCS is more effective during the encoding
phase than the consolidation p hase88,90; thus tDCS seems to increase task accuracy (especially when baseline is
34,91–93
low), and not e fficiency which is a core feature during visual perception and across attentional networks.
However, Anodal tDCS over the left DLPFC only showed a marginally significant decrease in alerting net-
work efficiency under speed condition when compared to sham stimulation. In this particular case, anodal tDCS
seems to have decreased network efficiency for the alerting network, but only under the speed condition. One
hypothesis here is that, under speed, response thresholds may be lowered and will depend on more effective
brain connectivity94. Anodal tDCS has been shown to increase connectivity near the stimulation site, as well to
other intra and inter-hemispheric regions95–97. However, the effects of tDCS and regions to be affected by it are
dependent on the task being performed and the network involved98. Furthermore, these task dependency effects
may be more important than polarity e ffects99,100. In this sense, it is not the first time that anodal tDCS impairs
response times101, or that there are no effects of anodal tDCS on RT102, or even that tDCS has distinct effects due
to the level of expertise when performing the t ask103. Therefore, in order to fully explain these findings, future
studies should study how different levels of cognitive load, expertise, even the effects of single site Vs dual site
tDCS104,105 impacts the oscillatory activity between intra and inter hemispheric regions, and how that is related to
performance in order to surpass the physiological effects of tDCS and to better understand the task related effects.
However, this study is not without limitations. First of all, it is not possible to identify if the effects of stimu-
lation are network specific, as ANT performance probably relies on interdependent, rather that independent
network performance106. Second, in the current design, participants performed the three instruction conditions
in a fixed sequence in order to allow for a comparison across stimulation times. Third, it is not possible to dis-
entangle the present results from the motor component of response time, even if our ancillary analysis does not
show effects of type of stimulation the RT level per se. Furthermore, the present study does not allow to assess
potential differences between low and high frequency tRNS. In fact, previous studies suggested that low and
high frequency tRNS may have opposite e ffects107. Or even that only high frequency tRNS was able to increase
performance in perceptual l earning78. However it is also true that the authors did not show statistical significant
differences between low and high frequency t RNS78, which led other authors to suggest that tRNS effects may
indeed be stimulus dependent and as such, lower intensities will induce inhibitory effects (i.e., less than 0.4 mA),
while higher intensities will induce excitatory effects (i.e. 1 mA)108.
Finally, SAT effects in the present protocol are more evident on the speed condition, however they are not as
evident under accuracy condition. As such, the effects of these types of stimulations need to be further explored
using tasks with distinct speed and accuracy conditions, which allow a better isolation of the task-dependent
networks.
Moreover, studies probing the mechanism of tRNS and tDCS, with varying stimulus intensity and frequen-
cies (in the case of tRNS) using online electroencephalography and/or neuroimaging methods are required to
explore stochastic resonance effects through phase synchronization as well as intra and interregional effects of
the stimulation.
Conclusions
Taken together, our current findings showed that tRNS and anodal tDCS over the left DLPFC had differential
effects on attention, as measured by the ANT network scores. Overall, we found a recurrent interaction between
tRNS and task difficulty in different networks. In the Alerting network, under the Speed instruction, tRNS
increased efficiency of the network. Under the more demanding conflict network, tRNS overall increased the
performance when comparing to sham. No statistical significant effects of tDCS were observed. These results are
compatible with the attention requiring the synchronization of pre-existing networks, rather than the reinforce-
ment or creation of new pathways.
Received: 6 October 2020; Accepted: 25 February 2021
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Author contributions
J.L., A.L., S.C., O.F.G. conceived and designed the study. A.L. acquired and analyzed the data. A.L. and J.L. inter-
preted the data and drafted the manuscript. S.C., O.F.G. and F.F. gave substantial intellectual contributions and
critical revision of the manuscript. All authors approved the final version of the manuscript.
Funding
AL is supported by the Portuguese Foundation for Science and Technology and the Portuguese Ministry of
Science, Technology and Higher Education through national funds, and co-financed by FEDER through COM-
PETE2020 under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007653). OFG and SC were sup-
ported by the Portuguese Foundation for Science and Technology and the Portuguese Ministry of Science,
through national funds and co-financed by FEDER through COMPETE2020 under the PT2020 Partnership
Agreement (POCI-01-0145-FEDER-007653) and along with JL were also funded through the grants: PTDC/PSI-
ESP/30280/2017 and PTDC/PSI-ESP/29701/2017, SC was also funded by the individual Grant IF/00091/2015.
FF is supported by a NIH grant (1R01AT009491-01A1). This work was partially supported by National Funds
through the Portuguese Foundation for Science and Technology (FCT) and co-funded through COMPETE
2020 – PO Competitividade e Internacionalização/Portugal 2020/União Europeia, FEDER (Fundos Europeus
Estruturais e de Investimento – FEEI) under the number:PTDC/PSI-ESP/30280/2017.
Competing interests
The authors declare no competing interests.
Additional information
Correspondence and requests for materials should be addressed to J.L.
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OPEN The effects of direct current

Scientific Reports | (2021) 11:6201 | https://doi.org/10.1038/s41598-021-85749-7 1

Age BDI STAI-Y state STAI-Y trait

Table 1. Sociodemographic and clinical information.

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Before (N = 24) After (N = 24)

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Received: 6 October 2020; Accepted: 25 February 2021

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© The Author(s) 2021

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Table 1. Sociodemographic and clinical information.