Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortex

Ryan B Savoury; Armin Kibele; Kevin E Power; Nehara Herat; Shahab Alizadeh; David G Behm

doi:10.1371/journal.pone.0280129

. 2023 Jan 6;18(1):e0280129. doi: 10.1371/journal.pone.0280129

Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortex

Ryan B Savoury ^1,^#, Armin Kibele ^2,^#, Kevin E Power ^1,^#, Nehara Herat ^1,^#, Shahab Alizadeh ^1,^#, David G Behm ^1,^*,^#

Editor: Xin Ye³

PMCID: PMC9821721 PMID: 36608054

Abstract

Background

The goal of this study was to determine if 10-min of anodal transcranial direct current stimulation (a-tDCS) to the motor cortex (M1) is capable of modulating quadriceps isometric maximal voluntary contraction (MVC) force or fatigue endurance contralateral or ipsilateral to the stimulation site.

Methods

In a randomized, cross-over design, 16 (8 females) individuals underwent two sessions of a-tDCS and two sham tDCS (s-tDCS) sessions targeting the left M1 (all participants were right limb dominant), with testing of either the left (ipsilateral) or right (contralateral) quadriceps. Knee extensor (KE) MVC force was recorded prior to and following the a-tDCS and s-tDCS protocols. Additionally, a repetitive MVC fatiguing protocol (12 MVCs with work-rest ratio of 5:10-s) was completed following each tDCS protocol.

Results

There was a significant interaction effect for stimulation condition x leg tested x time [F_(1,60) = 7.156, p = 0.010, ηp² = 0.11], which revealed a significant absolute KE MVC force reduction in the contralateral leg following s-tDCS (p < 0.001, d = 1.2) and in the ipsilateral leg following a-tDCS (p < 0.001, d = 1.09). A significant interaction effect for condition x leg tested [F_(1,56) = 8.12, p = 0.006, ηp² = 0.13], showed a significantly lower ipsilateral quadriceps (to tDCS) relative MVC force with a-tDCS, versus s-tDCS [t(15) = -3.07, p = 0.016, d = -0.77]. There was no significant difference between the relative contralateral quadriceps (to tDCS) MVC force for a-tDCS and s-tDCS. Although there was an overall significant [F_(1,56) = 8.36, p < 0.001] 12.1% force decrease between the first and twelfth MVC repetitions, there were no significant main or interaction effects for fatigue index force.

Conclusion

a-tDCS may be ineffective at increasing maximal force or endurance and instead may be detrimental to quadriceps force production.

Introduction

Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation technique that can induce both excitatory and inhibitory cortical effects depending on the polarity of the stimulation administered [1]. The effectiveness of tDCS for clinical use has shown positive results involving the treatment of depression, anxiety, schizophrenia, Parkinson’s disease, chronic pain, stroke, and other neural-related problems [2–7]. However, the tDCS research on athletic performance is not as consistent.

There is conflict in the literature as to whether tDCS can augment muscle strength and endurance performance. There are many studies that have demonstrated that tDCS is effective at increasing maximal muscle force and endurance [8–25] as well as strength training volume [26]. Brief applications of anodal tDCS (a-tDCS) increased maximal voluntary force production in both lower and upper limbs [10], pinch grip in stroke patients [27], and intramuscular coherence in sustained low force hand muscle activity [28]. This augmented strength can be sustained for 60 minutes after 20 minutes of tDCS over M1 [19] and has been attributed to an enhancement of cortical motor drive to spinal motor pool [29].

However, many others report no significant effects or decreases of muscle force or endurance when stimulating the motor cortex [9, 21, 28–37]. There were also no significant effects on jump height [38], or single or repeated sprint performance [39, 40] when stimulating the dorsolateral prefrontal cortex. Others have also reported that the significant decrease in maximal voluntary isometric force was accompanied by no significant differences in motor evoked potentials (i.e., corticospinal excitability) [28] or voluntary muscle activation with t-DCS stimulation targeting M1 [41]. Thus, in contrast to the aforementioned studies that show strength increases, they indicate that cortical motor drive is not enhanced. This contradiction in the literature may be reflective of the diverse protocols utilized in these studies making comparisons very difficult [42].

Meta-analyses of the overall literature tend to suggest small magnitude improvements in muscle strength [43–46] and endurance [45–47]. The small magnitude benefits might have been affected by low quality studies and selective publication bias [45]. Shyamali Kaushalya et al. [47] in their meta-analysis on tDCS effects on cycling and running endurance showed a positive effect on time to exhaustion, which they suggested may have resulted from increased corticospinal excitability may influence ratings of perceived exertion. Increases in corticomotoneuronal excitability and decreases in short interval intracortical inhibition (SICI) were also suggested to influence strength improvements in a tDCS training study [48].

Almost all tDCS studies provide stimulation contralateral to the tested muscle. A 2-week strength training program with a-tDCS to the ipsilateral M1 provided prolonged (48 hours) improvements in strength [48]. Only one study [19] has investigated the acute effect that tDCS of the M1 can have on muscles ipsilateral to the site of stimulation reporting no changes in knee extensors (KE) maximal force production. No studies to date have tested the acute effects of a-tDCS on fatigue/endurance in muscles ipsilateral to the site of stimulation.

Examinations of cortical and spinal excitability of the contralateral, non-exercised limb after an acute session of unilateral fatiguing exercise (monitoring of ipsilateral corticospinal influences) have revealed conflicting results with both decreases [49, 50] and increases in cortical excitability [51, 52] as well as increases [49, 50], decreases [51] and no significant change [52] in spinal excitability. Indeed Cabibel et al. [53] did discover cross facilitation or interhemispheric interactions with tDCS targeting the left M1 inducing both excitatory and inhibitory processing of the left M1. Similarly, a single session of strength training with a-tDCS increased strength, decreased SICI, and increased motor evoked potentials in the contralateral wrist extensor muscles [54]. In their review, Cabibel et al. [55] explained that tDCS-induced cross activation both reduces intracortical inhibition and increases interhemispheric excitatory inputs in the ipsilateral M1. This transfer could result in performance enhancements in muscles ipsilateral to the site of stimulation. Studies have also found evidence of interhemispheric facilitation of the motor cortices using sub-motor threshold intensity TMS stimulation, which suggests the existence of an underlying facilitatory neuronal circuit [56, 57]. One study using a single pulse supra-threshold TMS design demonstrated that a-tDCS could increase excitability of the contralateral motor cortex [58]. It is also possible that uncrossed corticospinal fibres that target ipsilateral motor neurons (10–30%) [59] and branched corticospinal fibres projecting to motor neurons bilaterally are affected. Although, this is less likely since these projections are strongest to axial muscles and may not be present for distal limb muscles [60].

A previous study reported that cathodal tDCS effects were greater in magnitude and duration for female participants when compared to males [61]. Similarly, a multivariate meta-regression revealed that women demonstrated greater magnitude responses to tDCS, which might be attributed to sex differences in the precise cortical anatomical locations, cognitive task strategies, as well as hormonal differences affecting brain stimulation [62]. Furthermore, the heterogeneity and genetic diversity of overall (both sexes) muscle strength, endurance, and corticospinal excitability findings is likely a result of variation in protocols [43].

The main goal of this study was to determine whether unihemispheric a-tDCS of the left M1 is capable of modulating maximal force production or fatiguability of either the contralateral or ipsilateral KE. It was hypothesized that there would be an increase in maximal force production and fatigue resistance in the contralateral and ipsilateral KE in relation to the site of tDCS. Due to the lack of literature on sex dependent effects of a-tDCS effects on motor function, this research question was exploratory.

Materials and methods

Participants

A priori power analyses (software package, G* Power 3.1.9.7: University of Dusseldorf, Germany) conducted using the results from studies by Hazime et al. [18] and Lattari et al. [14] with statistical power set at 0.8 and an effect size of 0.5 (moderate magnitude), suggested a required sample size of 10 and 8, respectively. Therefore, 16 healthy, participants were recruited for this study (8 males; age = 24.1 ± 2.8 years, height = 173.2 ± 8.3 cm, mass = 86.1 ± 13.3 kg and 8 females; age = 21.9 ± 1.6 years, height = 163.2 ± 8.6 cm, mass = 70.0 ± 14.7 kg). Participants were recreationally active with no history of musculoskeletal disorders and were screened for their suitability to receive tDCS based on tDCS checklist recommendations by Thair et al. [63], which included personal and family history of epilepsy, metal implants, implanted medication pump, pacemakers, recurring headaches, serious head injuries/surgeries, pregnancy, heart disease, and various medications. Participants were asked “which leg they would use to kick a ball at a target” to determine lower limb dominance [64]. All participants were determined to be right leg dominant. Each participant was required to read and sign a consent form and verbally consent to the researcher in order to participate in the study. This study was approved by the Interdisciplinary Committee on Ethics in Human Research at Memorial University of Newfoundland (ICEHR No. 20201316-HK) in accordance with the Declaration of Helsinki.

Experimental design

This study utilized a fully randomized, crossover, repeated measures design, with all participants completing four protocols. The four protocols involved the participant receiving: 1) a-tDCS targeting the left M1, with testing of the contralateral (right) leg, 2) a-tDCS targeting the left M1 with testing of the ipsilateral (left) leg, 3) sham tDCS (s-tDCS) targeting the left M1, with testing of the contralateral (right) leg, and 4) s-tDCS targeting the left M1 with testing of the ipsilateral (left) leg. At least one week of recovery was allocated between each session to ensure that no effects from prior stimulations carried over to the next session (Fig 1) [63].

Fig 1 — Abbreviations: KE: knee extensors, KF: knee flexors, MVC: maximal voluntary isometric contraction, tDCS: transcranial direct current stimulation.

tDCS intervention

A similar stimulation protocol as the only other study to test ipsilateral tDCS effects [19]. Using random allocation, participants underwent four sessions of tDCS (two a-tDCS and two s-tDCS) delivered via a direct current stimulator (TCT Research Limited, Hong Kong) using saline-soaked sponge electrodes. For all sessions, the anode (5 x 5cm) was placed at the left M1, contralateral to the participant’s dominant limb, with the cathode (5 x 7cm) placed on the shoulder area of the same side [8, 9, 28]. The M1 was located via the C3/C4 locations according to the 10–20 electroencephalography (EEG) electrode placement system [18–20, 29, 30]. a-tDCS protocols had a constant stimulation intensity of 2 milliamps (mA) with a duration of 10 minutes [21, 31, 33]. The s-tDCS protocols involved participants receiving 2 mA stimulation for the initial 30 seconds, followed by an additional 9.5 minutes of no stimulation [21]. Participants were not informed during the s-tDCS that the stimulator was not providing stimulation for the final 9.5 minutes. Prior research from our lab suggested that participants typically could not accurately differentiate between s-tDCS and a-tDCS protocols with 2mA stimulation. As described below, we also included a tDCS questionnaire to determine if the s-tDCS was an effective, blinding protocol.

MVC and fatigue tests

Prior to any performance measurements, participants completed a five-minute warm up using a cycle ergometer at 70 revolutions per minute and 1 kilopond.

To measure force, a cuff with a non-extensible strap was attached to a strain gauge (Omega Engineering Inc., LCCA 500 pounds; sensitivity = 3 mV/V, OEI, Canada) and placed around the ankle of the participant. Knee joint angles were measured using a goniometer (90⁰), since it has previously been shown that knee angle can affect isometric maximal voluntary contraction force (MVC) [65]. Before MVCs, participants were instructed to complete three warm-up contractions at what they perceived to be 50% of their maximum capability for five seconds each. Prior to each tDCS protocol, participants performed a minimum of two, four second MVCs for both the ipsilateral (left) and contralateral (right) KE. A third MVC was completed if the second MVC resulted in more than a five percent greater force than the initial contraction. One minute of recovery was provided between the MVCs. Participants were instructed to contract “as hard and as fast as possible”, with consistent verbal encouragement being provided during the contractions [66]. Immediately following the final pre-test MVC, the intervention commenced. Immediately post-tDCS 10-minute protocol, participants performed a single KE MVC of either the ipsilateral or contralateral KE. Only a single MVC was performed to minimize the effect on the following fatigue protocol. Peak MVC forces were analyzed for the KE of the tested leg. All force data was sampled at 2000 Hz and analyzed with the software program (AcqKnowledge III, Biopac Systems Inc., Holliston, MA). Force was normalized by comparing the post-test tDCS MVC forces to pre-test tDCS values.

Following the post-tDCS MVC, participants performed a repeated contraction (fatigue) protocol consisting of 12 KE MVCs with a work to rest ratio of 5:10 seconds [67]. During this protocol, participants were not told how many contractions had been completed in order to minimize pacing effects [68–70]. All participants were similarly verbally exhorted to maximize each contraction [71], with a consistent form of encouragement, which involved stating “Go, Go, Go” once for each contraction. A fatigue index (FI: Eq 1) was calculated and analyzed.

F I = \frac{(M e a n f o r c e o f r e p e t i t i o n s 1 & 2) - (M e a n f o r c e o f r e p e t i t i o n s 11 & 12)}{M e a n f o r c e o f r e p e t i t i o n s 1 & 2} / 100

(1)

tDCS blinding questionnaire

Before and after receiving tDCS (either a-tDCS or s-tDCS), participants were given a questionnaire, where they were asked to rate perceived sensations (e.g., itching, tingling, scalp irritation) on a scale from 1–10 (Likert scale: 1 = absent, 10 = severe) [63].

Statistical analysis

Statistical analyses were calculated using SPSS software (Version 27.0, SPSS, Inc. Chicago, IL). Normality and homogeneity of variances tests were conducted for all dependent variables. If the assumption of sphericity was violated, the Greenhouse-Geiser correction was employed. For absolute MVC force, a three-way repeated measures ANOVA (2x2x2) with factors including time (pre-/post-tDCS), tDCS protocol (anodal/sham), and tested leg ((ipsilateral to tDCS) / contralateral to tDCS) was conducted. Sex was not included in the absolute data analysis as it is well established that men typically exert greater forces than women. However, for relative measures, sex was incorporated as a factor. For the fatigue index, a three-way repeated measures ANOVA (2x2x2) with factors including sex, tDCS protocol (anodal/sham), and leg tested was also completed. For the fatigue test, another 3-way repeated measures ANOVA (2x2x2) with factors including first and last (12) repetition, two legs and tDCS protocol (anodal/sham).

If significant interactions were detected, post-hoc t-tests corrected for multiple comparisons were conducted to determine differences between values. Significance was set at p ≤ 0.05. Cohen’s d effect size was calculated to compare measures. Effect sizes were qualitatively interpreted as: (trivial <0.2, small 0.2 ≤ d < 0.5; medium 0.5 ≤ d < 0.8; large: d ≥ 0.8) [72]. Day to day reliability for pre-test MVC was assessed with Cronbach’s alpha intraclass correlation coefficient (ICC) [72].

Friedman’s ANOVA was utilized to detect significant effects for scales related to headache, neck pain, blurred vision, scalp irritation, tingling, itching, burning sensation, acute mood change, fatigue, and anxiety. For significant effects post-hoc Wilcoxon Signed Ranks tests corrected for multiple comparisons were performed.

Results

Absolute force measures

Coefficient of variations (CV) less than 10% of the mean and excellent reliability described as an ICC: >0.9 were found between pre-test measurements for the contralateral (α = 0.943, a-tDCS CV: 31.6 = 6.5% of mean, s-tDCS CV: 30.5 = 6.3% of mean) and ipsilateral (α = 0.964, a-tDCS: 36.4 = 7.5% of mean, s-tDCS: 36.2 = 7.4% of mean) KE.

There was a significant [F_(1,60) = 38.85, p < 0.001, ηp² = 0.39] main effect for time with a small magnitude, 8.7% (d = 0.27) decrease in KE MVC (both KE combined) from pre- to post-test, with no significant interaction effects found for condition (condition x time), or leg tested (leg tested x time), nor main effects for condition.

A significant [F_(1,60) = 7.156, p = 0.010, ηp² = 0.11] interaction effect was found for condition and leg tested (condition x leg tested x time) (Fig 2). Participants’ maximal ipsilateral KE MVC force was reduced 14% (large effect size magnitude), following a-tDCS when compared to the pre-stimulation values [t(15) = 4.35, p < 0.001, d = 1.09], but no significant change for s-tDCS. There was also a significant [t(15) = 4.84, p < 0.001, d = 1.21] MVC force reduction of 10.7% in the contralateral KE (contralateral to tDCS) following the s-tDCS protocol, but no significant difference following a-tDCS (Fig 2).

Relative (normalized) MVC force

A significant interaction effect for condition x leg tested [F_(1,56) = 8.12, p = 0.006, ηp² = 0.13], showed a significantly lower ipsilateral quadriceps (ipsilateral to tDCS) relative MVC force with a-tDCS (85.92 ± 12.75%), versus s-tDCS (96.2 ± 10.5%) [t(15) = -3.07, p = 0.016, d = -0.77]. There was no significant difference between the relative contralateral quadriceps (contralateral to tDCS) MVC force for a-tDCS and s-tDCS. No other significant main or interaction effects were observed. No significant sex effects were evident.

Fatigue test

There were no significant main or interaction effects for fatigue index force (Fig 3). There was a significant main effect of the first and last repetitions with a moderate magnitude 12.05% (d = 0.54) decrease in force overall [F_(1,56) = 8.36, p < 0.001] (see Fig 4 for all 12 repetitions).

Fig 4 — Asterisk highlights a significant (p<0.0001) decrease in force from repetition #1 to #12. Columns and bars represent mean force values and standard deviations in Newtons.

tDCS blinding questionnaire data

Only minor side effects were reported following tDCS, including headache, scalp irritation, tingling, itching, burning sensation, and fatigue. Friedman’s ANOVA revealed no significant differences in these variables between the four protocols (all p values ≥ 0.056) suggesting that participants were sufficiently blinded to which type of stimulation they were receiving.

Discussion

The main objective of this study was to determine if a-tDCS targeting the left M1 could modulate maximal force production or muscle fatiguability in either the right (contralateral to tDCS) or left (ipsilateral to tDCS) quadriceps. This study demonstrated significant force impairments (s-tDCS with testing of contralateral KE MVC, and a-tDCS with testing of ipsilateral KE MVC) and no significant changes (a-tDCS with testing of the contralateral KE MVC and s-tDCS with testing of the ipsilateral KE MVC) in discrete (single repetition) MVC tests.

Since four meta-analyses [43–46] report at least a small positive effect of tDCS on strength, we hypothesized an a-tDCS-induced increase in contralateral KE MVC force. However, this effect was not observed in the present study. The lack of significant change in normalized MVC force of the contralateral KE (contralateral to tDCS) following a-tDCS, in comparison to s-tDCS was contradictory to many studies which have reported force increases following anodal stimulation of the M1 [10–12, 18, 19]. Although only one of the studies that reported increases tested the KE [19], a larger number of studies testing the KE following a-tDCS reported no significant changes in comparison to the control [29, 30, 32, 73]. Additionally, following a-tDCS in the present study, 4/16 (2 males, 2 females) and 2/16 (2 females) participants experienced increased MVC force in their contralateral and ipsilateral quadriceps, respectively. This inter-individual variability likely contributed to some of the non-significant results of this study, and in combination with previous research suggests that a-tDCS is not a consistently effective ergogenic aid when the goal is to increase maximal KE force for a discrete contraction. This lack of reliability and high variability in the literature may be also related to the great diversity of implemented protocols (e.g., differences in electrode location, size, number, current density, polarity, and stimulation duration) [42].

The anodal and sham tDCS post-test protocols were conducted after approximately 10 minutes of physical inactivity. While the pre-test MVCs were performed shortly after a warm-up, the beneficial effects of this warm-up may have been reduced after 10 minutes of inactivity [74, 75]. The reported significant force losses with contralateral s-tDCS, and ipsilateral a-tDCS might be attributed to a diminished warm-up-induced post-activation potentiation enhancement that can increase force through phosphorylation of myosin light chains, and increased muscle temperature [76]. However, a previous studies involving a-tDCS of the contralateral leg motor cortex reported improved foot pinch force for 30 minutes post-a-tDCS [10], as well as increased KE MVC force for 60 minutes after a-tDCS [19]. Similarly, the positive effects of warm-up activities on subsequent performance have been reported to be sustained for 8–12 min [77, 78], 10–15 min [79], 18 minutes (with adolescents) [80], and 20 minutes [81, 82].

While a-tDCS in the literature has shown the ability to increase M1 excitability, it has also been hypothesized that a-tDCS could attenuate the reduction in output from the M1 contributing to supraspinal fatigue [21, 83]. While there were no significant fatigue index interactions between legs or stimulation conditions, there was a significant overall (main effect for contractions) 12.05% force decrease between the first and last contractions of the protocol (Fig 4). It has previously been demonstrated that a-tDCS can delay the onset of fatigue for a prolonged submaximal contraction [9, 21, 24, 25], although again, only one of these studies tested the KE [21]. Numerous other studies also reported no significant changes in KE fatiguability following a-tDCS [21, 30, 31] with one study also reporting increased muscle fatiguability [32]. While Angius et al. [21] suggested an extracephalic electrode montage was more effective at inducing a-tDCS effects on muscle fatigue than cephalic montages, our study found that an extracephalic montage was ineffective in modulating muscle fatigue. It is possible that the difference in the fatigue test used may have led to this discrepancy, with our study utilizing a 12 x 5s MVC protocol while Angius et al. [21] utilized a submaximal 20% MVC force time to exhaustion test. Furthermore, Shyamali Kaushalya et al. [47], only demonstrated tDCS induced effects with a time to exhaustion test during running and cycling endurance activities. Additionally, anodal tDCS did not influence performance during repeated “all out” efforts (4–6 sec) interspersed with 30 sec rests [39]. Although the fatigue protocol in the present study involved 12 5-s MVCs with 10-s rest, the accumulated fatigue only reduced the post-test MVC by a moderate magnitude 12.05% (d = 0.54). This suggests that a-tDCS is more effective for delaying the effect of muscle fatigue for low intensity activities, while those requiring maximal exertions may not experience similar benefits.

This study found no significant differences between male and female participants for relative force production or fatigue index. This suggests that tDCS affects male and female participants to a similar extent. A review by Dedoncker [62] suggested that women demonstrated greater accuracy on cognitive tasks with a-tDCS. A previous study that retrospectively re-analyzed data collected from previous transcranial direct current stimulation studies did not report significant cortical excitability differences between the sexes for a-tDCS. However, the effects of cathodal tDCS on neuroplasticity were greater, lasted longer and demonstrated more inhibition for female participants in comparison to males, suggesting that female participants may experience increased effects of tDCS possibly due to the effects of sex hormones [61]. These sex differences might be attributed to differences in identifying cortical anatomical locations, sex-dependent cognitive task strategies, and hormonal differences affecting brain stimulation. Our findings suggest that a-tDCS had similar performance effects for both male and female participants. More research is needed to explore possible sex differences.

Limitations

It might be suggested that the recruitment of 16 participants in this study involving a more variable intervention might have led to low statistical power even though the power analysis indicated that 8–10 participants should provide sufficient power. This lower power may have diminished the possibility of revealing any sex differences. Furthermore, as only the KE (quadriceps) were tested, future studies should aim to determine if other muscle groups ipsilateral to the site of stimulation are affected in a similar manner, while also utilizing transcranial magnetic stimulation (TMS) to determine potential changes in corticospinal excitability. When combined with transmastoid electrical stimulation which activates axons in the spinal cord, effects can be distinguished between cortical and spinal excitability or inhibition. Finally, as reviewed by Savoury et al. [42], differences in stimulation protocols (e.g., duration, intensity, electrode location, blinding efficacy, individual expectations and others) make it difficult to make direct comparisons with other studies. A series of comprehensive studies are needed to determine optimal stimulation protocols suitable for various populations (e.g., possible differences between sexes, age), specific performance enhancement (e.g., strength, endurance, or cognitive) and more research targeting areas other than the M1 (e.g., temporal cortex and prefrontal cortex).

Conclusions

This study found that 10 minutes of 2 mA of a-tDCS is not an effective or consistent method for increasing maximal force production or reducing fatigue in the KE either contralateral or ipsilateral to the stimulated M1. Furthermore, the decrements with the contralateral s-tDCS also contributed to the inconsistent findings with tDCS. With many athletes looking to devices such as those for administering tDCS to provide performance enhancements, it is important to caution that tDCS may not be beneficial but could instead be detrimental to exercise performance.

Acknowledgments

The experiments comply with the current laws of the country in which they were performed.

Data Availability

The datasets generated during and/or analyzed during the current study are publicly available from the Dryad database (https://doi.org/10.5061/dryad.brv15dvcn).

Funding Statement

This research was partially funded by the Natural Science and Engineering Research Council of Canada David Behm: RGPIN-2017-0328.

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PLoS One. doi: 10.1371/journal.pone.0280129.r001

Decision Letter 0

Xin Ye

12 Jul 2022

PONE-D-22-11905Reduced Isometric Knee Extensor Force Following Anodal Transcranial Direct Current Stimulation of the Ipsilateral Motor CortexPLOS ONE

Dear Dr. Behm,

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David Behm: RGPIN-2017-0328”

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Reviewer #2: No

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Reviewer #1: The manuscript is a technically sound piece of scientific research with data that supports the conclusions. It appears that all appropriate statistical analyses were utilized to reach the authors' conclusions.

Reviewer #2: The aim of this study was to determine if anodal transcranial direct current stimulation (a-tDCS) to the motor cortex (M1) modulates quadriceps isometric maximal voluntary contraction (MVC) force or fatigue contralateral or ipsilateral to the stimulation site. Authors main conclusions are that a-tDCS may be ineffective at increasing maximal force or endurance and instead may be detrimental to quadriceps force production.

Because of the rise in popularity of a-tDCS as a tool with potential to influence sport performance, the aims of the present study could be considered relevant to the field. However, the manuscript has some limitations that decreased the initial enthusiasm.

First of all, a single blind approach (with only subjects blinded to condition) could not be the best way to perform this research. Double blind is recommended in this kind of study in which investigators can inadvertently influence the experiment’s results due to hypothesis expectations (i.e., for example, with differences in the way subjects are encouraged during the session).

Another question, is the protocol used to induce KE fatigue, which from my point of view does not work well (induced only a 12% decrease in force overall). A time to exhaustion test (TTE) would have been desirable, or at least, a large number of repetitions to increase the perception of effort to a greater extent, since it has previously been argued that modulation of RPE could underpin the tDCS induced beneficial effects on endurance performance.

The other main weaknesses of the study are related to the way it is written. There is a lack of explanations of arguments to support a priori hypothesis and a rather superficial discussion about the results. There are also some inconsistencies between the statistical analysis done and the way results are interpreted and the conclusions raised does not align well with results.

Introduction

Introduction is confusing and the rationale is not clear at all. Overall, introduction needs reorganization of content and a better justification of the aims of the study.

For example, there is no proper explanation of the physiological rationale for the effects of a-tdcs over M1 on muscle force. All the justification is based on the effects of a-tdcs on MEP amplitude. Although elucidating the mechanisms of a-tdcs is not the aim of the present study, a proper justification of the selection of stimulating areas, explaining possible physiological mechanisms by which they might influence motor behavior, should be included. Furthermore, it should be better physiologically justified the interaction between both motor cortices and its reciprocal influences, both in terms of facilitation and inhibition, when altering the “excitability” of one hemisphere. The rationale of cross education does not fit well in the intro, or at least at the main argument.

Lines 137 – 140: This is too speculative Hard to believe that tDCS may exert an effect on the reticulospinal system. My recommendation is to delete this sentence.

There is a need to actualize the citing literature, because there is a lot of missing references regarding the effects of TDCS on maximal force production and endurance performance. See some of them:

The Effect of Anodal Transcranial Direct Current Stimulation on Quadriceps Maximal Voluntary Contraction, Corticospinal Excitability, and Voluntary Activation Levels.

Kristiansen M, Thomsen MJ, Nørgaard J, Aaes J, Knudsen D, Voigt M.

J Strength Cond Res. 2021 Mar 3. doi: 10.1519/JSC.0000000000003710. Online ahead of print.

Anodal transcranial direct current stimulation enhances strength training volume but not the force-velocity profile.

Alix-Fages C, García-Ramos A, Calderón-Nadal G, Colomer-Poveda D, Romero-Arenas S, Fernández-Del-Olmo M, Márquez G.

Eur J Appl Physiol. 2020 Aug;120(8):1881-1891. doi: 10.1007/s00421-020-04417-2.

Transcranial Direct Current Stimulation Does Not Improve Countermovement Jump Performance in Young Healthy Men.

Romero-Arenas S, Calderón-Nadal G, Alix-Fages C, Jerez-Martínez A, Colomer-Poveda D, Márquez G.

J Strength Cond Res. 2019 Jul 31. doi: 10.1519/JSC.0000000000003242. Online ahead of print.

Transcranial direct current stimulation and repeated sprint ability: No effect on sprint performance or ratings of perceived exertion.

Alix-Fages C, Romero-Arenas S, Calderón-Nadal G, Jerez-Martínez A, Pareja-Blanco F, Colomer-Poveda D, Márquez G, Garcia-Ramos A.

Eur J Sport Sci. 2021 Feb 25:1-10. doi: 10.1080/17461391.2021.1883124. Online ahead of print.

Acute effects of transcranial direct current stimulation on cycling and running performance. A systematic review and meta-analysis.

Shyamali Kaushalya F, Romero-Arenas S, García-Ramos A, Colomer-Poveda D, Marquez G.

Eur J Sport Sci. 2021 Jan 7:1-13. doi: 10.1080/17461391.2020.1856933. Online ahead of print.

Effects of Anodal Transcranial Direct Current Stimulation on Training Volume and Pleasure Responses in the Back Squat Exercise Following a Bench Press.

Rodrigues GM, Machado S, Faria Vieira LA, Ramalho de Oliveira BR, Jesus Abreu MA, Marquez G, Maranhão Neto GA, Lattari E.

J Strength Cond Res. 2021 May 5. doi: 10.1519/JSC.0000000000004054. Online ahead of print.

Transcranial Direct Current Stimulation Does Not Affect Sprint Performance or the Horizontal Force-Velocity Profile.

Alix-Fages C, Garcia-Ramos A, Romero-Arenas S, Nadal GC, Jerez-Martínez A, Colomer-Poveda D, Márquez G.

Res Q Exerc Sport. 2021 Nov 4:1-9. doi: 10.1080/02701367.2021.1893260. Online ahead of print.

Methods

There are some concerns regarding some questions of the methods and design:

Why authors have chosen a single blind approach (only subjects blinded to condition)? Double blind is needed in this type of research because the authors´ a priory expectation could influence the results of the study (e.g.: via changes in the feedback provided, etc).

For sample size estimation authors have chosen the effect size based on previous literature (Hazime et al. (2017) and Lattari et al. (2020a)) who found very large effect sizes. However, all the meta-analysis that studied the effects of a-TDCS on motor performance (strength and endurance) found much lower effect sizes (SMD: 0.20 to 0.40). Please justify this decision, and how it would influence the selection of lower ES.

Regarding the stimulation site, it has been located at the C3/C4 according to the 10-20 electrode placement system. However, leg representation is located in Cz (just in the sulcus), so it is rather difficult to argue that it is possible to focally stimulate left leg M1 using a 5 x 5 cm anode placed over C3. If we take this into account, the “a priory hypothesis” of this study could not be tested.

Line 207 -211: Why authors use different protocols before and after the application of tDCS (anodal/sham)? Subjects warmed-up in the PRE but not after 10 minutes of rest (while applying tDCS). Furthermore, they performed 2 to 3 MVCs in the PRE, but only one in the POST. This could influence the results obtained.

Line 222: please revise the Fatigue Index equation (and the obtained results), it is wrong. It should be as follow:

FI= ((a-b)/a)*100, where “a” is the initial performance and “b” the final performance.

Discussion

Discussion needs substantial improvement. Overall arguments and explanations exposed by the authors are rather superficial and imprecise. As with the rest of the manuscript, writing needs a thoughtful revision. See some specific comments below:

Line 303: fatigability

Line 308-3318: I do not understand why it is hypothesized an increase in the MVC while most of the papers who tested 1RM or MVC failed to demonstrate an effect of tDCS on maximal force production, regardless of the muscle tested (please see Alix-Fages et al., 2019). Kristiansen et al., 2021 previously found a lack of increase in MEP amplitude and MVC in a KE MVC after a-tDCS. It should be better addressed and discussed.

Line 334-337: This is mere speculation. First, M1 excitability has not been measured. Second, it is not well stablished a causal link between M1 increased excitability and force enhancement. Furthermore, this is not aligned with the main interpretation and conclusion of the paper, which is completely opposed to this result.

Line 352-354: This is important, because the task could influence results. See Kaushalya et al., who showed that only TTE test are affected by TDCS during running and cycling endurance activities. Furthermore, recent papers found that aTDCS does not influence performance during repeated “all out” efforts (4-6 sec) interpesed with 30 sec rests (i.e.: RSA test: Alix-Fages et al., 2021). Moreover, as previously commented, the task used in this study only produced a 12% reduction in force overall. This should be discussed further.

Acute effects of transcranial direct current stimulation on cycling and running performance. A systematic review and meta-analysis.

Shyamali Kaushalya F, Romero-Arenas S, García-Ramos A, Colomer-Poveda D, Marquez G.

Eur J Sport Sci. 2021 Jan 7:1-13. doi: 10.1080/17461391.2020.1856933. Online ahead of print

Transcranial direct current stimulation and repeated sprint ability: No effect on sprint performance or ratings of perceived exertion.

Alix-Fages C, Romero-Arenas S, Calderón-Nadal G, Jerez-Martínez A, Pareja-Blanco F, Colomer-Poveda D, Márquez G, Garcia-Ramos A.

Eur J Sport Sci. 2021 Feb 25:1-10. doi: 10.1080/17461391.2021.1883124

Conclusions

“This study found that 10 minutes of 2 mA of a-tDCS is not an effective or consistent method for increasing maximal force production or reducing fatigue in the KE either contralateral or ipsilateral to the stimulated M1.”

This conclusion contrast with those mentioned in lines 334-337.

Reviewer #3: This reviewer is thankful for the opportunity to review this submission by Savoury et al. The aim of the study was to measure the effect of anodal transcranial direct current stimulation (a-tDCS) of the left motor cortex (M1) on both ipsilateral and contralateral knee extension strength and fatigue using a sham-controlled crossover study design. The authors concluded that, contrary to their initial hypothesis, the use of a-tDCS did not significantly increase strength of muscle contraction with contralateral knee extension and significantly decreased muscle contraction with ipsilateral knee extension. They additionally found no significant effect of a-tDCS on muscle fatigue. This work contributes to a growing collection of publications on a-tDCS, all with inconsistent findings regarding its efficacy on muscle contraction augmentation. While the topic is interesting and has promise to translate into clinical space, its findings add to overall ambiguity within the current science. The work is generally well-written, although there is opportunity to provide more clear and consistent use of right/left and contralateral/ipsilateral as shifting between the two sets of terms leads to an unnecessary cognitive burden for the reader. This work provides findings contrary to many published studies, which may be noteworthy, but the authors do not sufficiently reconcile issues they raise in their introduction regarding inconsistency in published tDCS protocol. Consequently, it is difficult to conclude if their contrary findings are a true finding or a result of poorly controlled method with small sample size. With some modifications this work may be fit for publication.

ABSTRACT

Minor Comments

1. Break into sections: Background, Methods, Results, and Conclusion (See Plos One criteria)

INTRODUCTION

Major Comments

1. The authors spend a paragraph describing variables that contribute to the efficacy of tDCS. Even when they describe previously used methods in muscle force production and fatigue, they highlight heterogeneity (i.e., contralateral M1 vs temporal cortex vs prefrontal cortex). It is not well resolved what approach might be the most efficacious. Based on what is written, there seems to be insufficient knowledge to support methodological choices.

2. Moreover, the introduction is hard to follow, unfocused, and too lengthy. The previous research is presented without flow and how it relates to the current study as well as muscular force specifically. Additionally, much of the details should be reserved for the Discussion Section.

3. Lines 148-150: Sex differences did not seem to be an active area for investigation. Authors may add background for this or exclude this hypothesis, as no meaningful investigation was conducted to actually observe differences and as of now seems out of place.

Minor Comments

1. Line 148: Due TO the lack…

2. Throughout the paper, this reviewer suggests using the wording “targeting the left M1” instead of “of the” as it is more reflective of the administration of tDCS

3. Line 79-81: If this sentence remains in the article, make wording clearer with more detailed outcomes.

4. Issues with sentence structure and clearly presenting the previous literature to introduce the topic to the reader.

METHODS

Major Comments

1. Although the authors refer to Thair et al., 2017 paper for screening, it is important to spell out for the reader in the methods the specific Inclusion/exclusion criteria used to enroll participant.

2. Works cited in the methods session regarding intervention design are not addressed in the introduction. Why were particular protocols chosen as opposed to others?

3. The introduction states that this work builds upon the work of Vargas et al. (2018), but this study chose to stimulate and then test versus test at 13 minutes in a 20-mintue stimulation. It is unclear why the authors strayed from this established protocol.

4. Cogiamanian et al. (2007), Kan et al. (2013), Abdelmoula et al. (2016), and Lampropoulou & Nowicky (2013) all use tDCS to measure changes in elbow flexion. The knee and elbow are distinct areas of the motor strip with leg and knee sitting more midline/parasagittal. Montenegro et al. (2015) measured knee flexor, but this was a negative study. Explanation for why this protocol is applicable for your knee flexion study would be helpful.

5. It was noted that measurements of the knee joint were acquired as knee angle can affect the isometric MVC, however the angles were not documented.

6. It is understandable that post-tDCS, participants performed only one MVC to minimize the effect on fatigue protocol, but this leads to a comparison of pre-tDCS measurements after 2 -3 attempts that took participant related effort (change of +5%) into account.

7. Tables mentioned EMG MVC data but were not explicitly stated in the paper; only a strain gauge.

8. Typically blinding of tDCS conditions are implemented in protocols. It does not appear the testing was double-blinded. If so, authors will need to comment on this limitation.

Minor Comments

1. Experimental design noted to be crossover in abstract. Similar verbiage not used in the body of the manuscript. The authors do say, “repeated measures design, with all participants completing four protocols,” which is the equivalent, but there may be some value to maintain consistency.

2. Line 183: 10–20 electroencephalography (EEG) electrode placement system.

3. While testing order was randomized, given the sample size was small, did randomization protocol actually result in equal variances?

4. The Supplementary questionnaire could be improved by asking the participants if they believe they just received the a-tDCS or s-tDCS, but again blinding should be made clearer.

5. Authors should consider reviewing sentence structure, as run-on and missing words make the narrative hard to follow.

RESULTS

Major Comments

1. It would be helpful to report the specific main effects that were not significant

2. Line 282: The title should be more specific. Also, the two paragraphs should be more concise. Moreover, this reviewer does not think this section adds much to the overall aim of the study.

3. Tables 1-3: Discrepancy with Tables and reporting. Table 3 is referenced in-text (Line 290), but as Table 1 in Line 300. Tables 1 and 2 (at the end of the manuscript) are not referenced in-text at all and does not have a Table legend.

4. Figures 2-4: Authors should add more details of the figures to captions

Minor Comments

5. Define a very good and excellent reliability score outside of parentheses.

6. Line 262: the results are presented as ipsilateral with a-tDCS then s-tDCS followed by contralateral with s-tDCS then a-tDCS. Would recommend reversing the order of s-tDCS and a-tDCS in the contralateral group so that the ipsilateral and contralateral are presented using a similar convention.

DISCUSSION

Major Comments

1. First paragraph, it is not commonplace to re-report statistics (i.e., the p-values) in the discussion section. This reviewer suggests removing.

2. First paragraph should include specific details of the results. For example, it appears the authors are including both results of maximal force production and muscle fatiguability in “force impairment.” Please rectify.

3. Lines 320-321: “a-tDCS is not a consistently effective ergogenic aid when the goal is to increase maximal KE force for a discrete contraction”. Is the variation in outcomes (specifically an increase in maximal KE force) a product of the technology or a product of experimental designs with small sample sizes and numerable uncontrolled, confounding variables? (as stated in the next sentence).

4. This reviewer is not sold on the importance of Lines 365-380. These statements can be concise enough to mention in the limitations section (which needs more exploration) due to the fact the participants were not directly asked if they believe they received a-tDCS or s-tDCS.

5. Limitation section needs to be developed. Potentially the comments provided in this review will trigger additional limitations of the study besides the small sample size (e.g., blinding efficacy/expectancy beliefs, other regions of the brain that the authors mention). Other considerations would be the 10-min stimulation, could it be that the length of stimulation inadequate to produce a change?

6. In the conclusion section, the authors mention athletes and performance enhancements, but this was not previously mentioned as a potential impetus of this study. This should be rectified.

7. Lines 392-392 offers a limitation to only studying quadriceps/KE. This should be moved up to the limitations section. Again, same comments for Lines 392-397 are recommendations to limitations and should be discussed in the Limitations section.

Minor Comments

1. Restatement of hypothesis on line 308 is hard to follow. Consider rewording to say, “the hypothesis that …” or adding another hyphen in “a-tDCS-induced..”

2. Would consider changing work reported on line 317 – MVC is measured not reported.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

**********

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PLoS One. 2023 Jan 6;18(1):e0280129. doi: 10.1371/journal.pone.0280129.r002

Author response to Decision Letter 0

20 Aug 2022

Revisions re: data availability have been made as requested. There are no ethical restrictions on data availability. Data has been uploaded to Dryad web site and the DOI is provided.

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PLoS One. doi: 10.1371/journal.pone.0280129.r003

Decision Letter 1

Xin Ye

4 Oct 2022

PONE-D-22-11905R1Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortexPLOS ONE

Dear Dr. Behm,

Please submit your revised manuscript by Nov 18 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Xin Ye, Ph.D.

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #3: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Partly

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: I Don't Know

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: Yes

**********

6. Review Comments to the Author

Reviewer #3: Summary of feedback:

This reviewer appreciates the consideration of previous feedback and revision of the manuscript. The manuscript has improved, however, this reviewer found it difficult and time-consuming to identify what changes the authors made. On any subsequent revisions, the authors should include a “tracked changes” version, so that reviewers can easily follow the revisions. This reviewer still found sentence structure, clarity issues, and punctuation errors. Attention to detail is imperative. Lastly, more detail should be included in the methods section as to the measures used to assess MVC.

ABSTRACT:

Minor Comments

1. As mentioned in this Reviewer’s previous comments, there is inconsistent use of right/left and contralateral/ipsilateral as shifting between the two sets of terms leads to an unnecessary cognitive burden for the reader. (Lines 42-47 and throughout the manuscript)

2. Line 37, was MVC force tested <immediately> following the a-tDCS and s-tDCS? If so, please specify.

3. Line 40 – remove “The main finding of this study..” and simply say “There was a ….”

4. Line 48 – remove the comma after “Although”

5. Line 50 – remove “Hence”

INTRODUCTION:

Major Comments

1. Third paragraph and fourth paragraph describe positive results and negative results of tDCS, respectively. The third paragraph speaks generally about studies that showed increased muscle force and endurance. The fourth paragraph speaks specifically about tDCS applied to the dorsolateral prefrontal cortex/M1. While the conclusion the authors draw starting on line 77 is likely sound, comparing a general pool of studies to those in a particular area may not be comparing the same phenomenon. The authors discuss this in the final line of paragraph four. If the point to be communicated with the reader is that there is likely heterogeneity in results likely as a result of variation in protocols, this point could likely be made more succinctly.

2. Appreciate the addition of discussion around mechanism and selection of tDCS target added from last version

3. Clear stated aim in final paragraph is helpful - would consider adding ‘left’ prior to M1 in this sentence.

4. The inclusion of sex differences, while appreciated, seems to emerge suddenly. Consider providing some additional context.

5. SICI was not introduced previously to line 112.

6. The differences in sex was outlined without including why this should be studied, despite the lack of research.

Minor comments

1. Errors in punctuation: Lines 64, 70, 72

2. Line 74: prefrontal is generally not hyphenated

3. In line 81, the word “reviews” should be removed and state “meta-analyses” instead.

4. Line 99, a-tDCS was already introduced, and should be used.

5. Line 102: It is unclear to this reader what you mean by “acute studies”. Perhaps, “No studies to date have tested the acute effects of a-tDCS on fatigue/endurance…”?

6. Line 124: Neurones -> neurons (twice)

METHODS:

Minor Comments

1. Appreciate the inclusion of the tDCS Questionnaire in methods. While the results may be in supplementary data, using ‘supplementary’ in the title is confusing. Would consider retitling to “tDCS Blinding Questionnaire”

2. Punctuation Errors: Lines 146, 235

3. Either session or protocol should be used in line 162.

4. Line 182: Consider a different word than “deceptive” – “blinding protocol” would be more appropriate

5. Line 193: use of semi-colon between two and four is unclear. Consider using comma “two, four-second…”

RESULTS:

Minor Comments:

1. Line 243-244 for clarity, consider leading the sentence with “Coefficient of variations …”

2. Line 285: Similar concern about removing supplementary from title, and if truly supplemental, direct readers to the supplemental material within the body of the paragraph

3. Define a very good and excellent reliability score outside of parenthesis.

DISCUSSION:

Major Comments:

1. There is opportunity to discuss more about the gender differences and recommendations for future tests based on why gender was included as exploratory in this study. The introduction referred to a lack of literature, however the discussion noted a previous study. Additionally, in the conclusion that there is no difference between males and females is perhaps overstated. Was the experiment actually powered to observe this? Agree that it is worth noting, but that a recommendation for further research with a specific aim on sex differences is warranted.

2. Line 312: you reiterate the point, “this lack of reliability and high variability in the literature may be also related to the great diversity of implemented protocols (e.g., differences in electrode location, size, number, current density, polarity, and stimulation duration) [42].” after reading the introduction and discussion I am still left wondering how your study attempts to address this. Ideally stronger commentary should be provided as to why your method is optimal and why others should continue to apply this method in future studies.

3. Addition of expanded limitations section is appreciated

4. Lines 350-353 should be included in the introduction as well.

5. Final sentence of your last paragraph again noted heterogeneity in protocol - what is your recommendation?</immediately>

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #3: No

**********

PLoS One. 2023 Jan 6;18(1):e0280129. doi: 10.1371/journal.pone.0280129.r004

Author response to Decision Letter 1

31 Oct 2022

Reviewer #3: Summary of feedback:

Response: Based on your and the other reviewer comments we hope this revised version will be acceptable.

ABSTRACT:

Minor Comments

Response: We have now emphasized the use of ipsilateral and contralateral rather than left and right limbs or muscles throughout the manuscript.

2. Line 37, was MVC force tested following the a-tDCS and s-tDCS? If so, please specify.

Response: As stated in the abstract:

“Knee extensor (KE) MVC force was recorded prior to and following the a-tDCS and s-tDCS protocols. Additionally, a repetitive MVC protocol (12 MVCs with work-rest ratio of 5:10-s) was completed following each tDCS protocol.”

3. Line 40 – remove “The main finding of this study..” and simply say “There was a ….”

Response: Done.

4. Line 48 – remove the comma after “Although”

Response: Done.

5. Line 50 – remove “Hence”

Response: Done.

INTRODUCTION:

Major Comments

Response: We have added another sentence as suggested to the second last paragraph of the introduction (prior to the objectives and hypothesis paragraph). Based on your suggestion we state:

“Furthermore, the heterogeneity and diversity of overall (both sexes) muscle strength, endurance, and corticospinal excitability findings is likely a result of variation in protocols.”

2. Appreciate the addition of discussion around mechanism and selection of tDCS target added from last version

Response: Thank you for the supportive comment.

3. Clear stated aim in final paragraph is helpful - would consider adding ‘left’ prior to M1 in this sentence.

Response: Done.

4. The inclusion of sex differences, while appreciated, seems to emerge suddenly. Consider providing some additional context.

Response: We have added the following contextual information to the introduction.

“There may be sex differences to consider with tDCS. A previous study reported that cathodal tDCS effects were greater in magnitude and duration for female participants, suggesting that female participants may experience increased effects of tDCS when compared to males [82]. Similarly, a multivariate meta-regression by Dedonker et al. (2016) revealed that women demonstrated greater magnitude responses to tDCS, which might be attributed to sex differences in the precise cortical anatomical locations, cognitive task strategies, as well as hormonal differences affecting brain stimulation. A review by Chinzara et al. [43] suggested that the participants’ heterogeneity in terms of sex and genetic diversity requires consideration. Furthermore, the heterogeneity and diversity of overall (both sexes) muscle strength, endurance and corticospinal excitability findings is likely a result of variation in protocols.”

5. SICI was not introduced previously to line 112.

Response: SICI was defined in line 106.

6. The differences in sex was outlined without including why this should be studied, despite the lack of research.

Response: We have added the following contextual information to the introduction.

Minor comments

1. Errors in punctuation: Lines 64, 70, 72

2. Line 74: prefrontal is generally not hyphenated

3. In line 81, the word “reviews” should be removed and state “meta-analyses” instead.

4. Line 99, a-tDCS was already introduced, and should be used.

5. Line 102: It is unclear to this reader what you mean by “acute studies”. Perhaps, “No studies to date have tested the acute effects of a-tDCS on fatigue/endurance…”?

6. Line 124: Neurones -> neurons (twice)

Response: All minor comments revised as suggested.

METHODS:

Minor Comments

2. Punctuation Errors: Lines 146, 235

3. Either session or protocol should be used in line 162.

4. Line 182: Consider a different word than “deceptive” – “blinding protocol” would be more appropriate

5. Line 193: use of semi-colon between two and four is unclear. Consider using comma “two, four-second…”

Response: All minor comments revised as suggested.

RESULTS:

Minor Comments:

1. Line 243-244 for clarity, consider leading the sentence with “Coefficient of variations …”

2. Line 285: Similar concern about removing supplementary from title, and if truly supplemental, direct readers to the supplemental material within the body of the paragraph

3. Define a very good and excellent reliability score outside of parenthesis.

Response: All minor comments revised as suggested.

DISCUSSION:

Major Comments:

Response: We have expanded the discussion paragraph on sex differences as well as adding a sentence in the limitations section regarding a possible lack of statistical power to detect sex differences.

Response: Our methods were based on the prior review recommendations of Savoury et al. Based on the variability in the literature and inconsistent results in the present study there may not be an overall “optimal” method. As discussed in greater detail in the discussion in this revised version, there are sex differences in responses as well as interindividual responses. We previously stated:

“This inter-individual variability likely contributed to some of the non-significant results of this study, and in combination with previous research suggests that a-tDCS is not a consistently effective ergogenic aid when the goal is to increase maximal KE force for a discrete contraction.”

We have added the following sentence based on your suggestion:

“These inconsistent results occurred even though the present study implemented the a-tDCS stimulation recommendations of the Savoury et al. [42] review for the methodological variables that were most likely to produce the greatest exercise performance (i.e., muscle strength, endurance) enhancement.”

3. Addition of expanded limitations section is appreciated

Response: We appreciate the supportive comment.

4. Lines 350-353 should be included in the introduction as well.

Response: This information has been moved to the introduction as suggested.

5. Final sentence of your last paragraph again noted heterogeneity in protocol - what is your recommendation?

Response: We have added the following recommendation:

“A series of comprehensive studies are needed to determine optimal stimulation protocols suitable for various populations (e.g., possible differences between sexes, age), specific performance enhancement (e.g., strength, endurance, or cognitive) and more research targeting areas other than the M1 (e.g., temporal cortex and prefrontal cortex).”

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PLoS One. doi: 10.1371/journal.pone.0280129.r005

Decision Letter 2

Xin Ye

22 Nov 2022

PONE-D-22-11905R2Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortexPLOS ONE

Dear Dr. Behm,

Please submit your revised manuscript by Jan 06 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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Kind regards,

Xin Ye, Ph.D.

Academic Editor

PLOS ONE

Journal Requirements:

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Partly

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: I Don't Know

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4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: No

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6. Review Comments to the Author

Reviewer #3: Summary of feedback:

This reviewer thanks the author for addressing most of the previous comments. This reviewer, however, still identified issues in organization, sentence structure, clarity, and references, especially in the Introduction. This reviewer suggest that the authors recruit a few other researchers, outside of the authors, to review and provide feedback. I offer the additional suggestions, although not exhaustive, below.

ABSTRACT:

Minor Comments

1. Methods: Label the fatigue protocol.

2. Line 44: Replace “impairments” with “reduction” to specify direction of the change.

INTRODUCTION:

Major Comments

1. The Introduction is too long for the information provided. This reviewer suggests being more succinct in reporting information. For example, Lines 82-98 has unnecessary and repetitive details in which the information can be reduced to about 2 sentences. The authors can reserve some of the details for the discussion.

2. Lines 58-62 should be better linked. For example, use of “however” or some other revision to which it would tell the reader, this is what is known clinically without much discrepancy in the literature, however, when investigating the effects of tDCS on exercise and sport performance there appears to be mixed results. This would be a better transition in

3. There are over 60 references in the Introduction alone, which leads to an indication that the information in the introduction is unfocused. The authors should focus in on only articles specific to their research study. For example, are the effects of tDCS on elbow flexion necessary when the current study focuses on lower limb force and endurance? Are studies that target the dlPFC necessary to compare to a study targeting M1?

Minor Comments

1. Lines 139-143: use active voice or make line 139-140 its stand-alone sentence after the stated aim.

METHODS:

Minor Comments

1. Lines 185-187: It is unclear why the authors are using 5 study references just say that M1 is located at C3/C4 on EEG placement. Are the authors trying to say something else? If not, this reviewer thinks 1 major reference of an EEG placement paper is sufficient.

2. Line 194: Remove double word.

RESULTS:

Minor Comments:

1. It would be helpful to restate the statistical models for each analysis in the results since the variables of the ANOVA vary.

DISCUSSION:

Minor Comments:

1. Line 336-338: Make the sentence more detailed based on the references provided (i.e., #10 and #19). For example, the target of tDCS and MVC, etc in these articles.

2. Line 364: Make the effects on sex more specific to the current studies protocol, parameters and variables and not so general.

3. Lines 365-369: Authors should highlight the a-tDCS results first, since it relevant to the current study and then introduce that cathode tDCS generated different results.

4. Line 382: The authors introduced TMS without defining it or providing insight into how TMS may determine potential changes in M1 excitability.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #3: No

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PLoS One. 2023 Jan 6;18(1):e0280129. doi: 10.1371/journal.pone.0280129.r006

Author response to Decision Letter 2

1 Dec 2022

Reviewer #3: Summary of feedback:

Authors’ response: We thank the reviewer for their contributions to improving the manuscript.

ABSTRACT:

Minor Comments

1. Methods: Label the fatigue protocol.

Authors’ response: We have added the descriptor “fatiguing” to clarify that the repetitive MVC protocol was a fatigue protocol. The revision is as follows:

“Additionally, a repetitive MVC fatiguing protocol (12 MVCs with work-rest ratio of 5:10-s) was completed following each tDCS protocol.”

2. Line 44: Replace “impairments” with “reduction” to specify direction of the change.

Authors’ response: The term impairment is defined as “diminishment or loss of function or ability.” Hence it does specify the direction of the change. Hence a KE MVC force impairment would be defined as a diminishment or decrease in MVC force function or ability. But if the reviewer likes the word “reduction” better then we have made that change as requested.

INTRODUCTION:

Major Comments

Authors’ response: We have integrated the information in the suggested paragraph to just 4 sentences. We have also reduced the introduction from about 4 to 3 pages.

Authors’ response: We have attempted to better link the information as follows:

“The effectiveness of tDCS for clinical use has shown positive results involving the treatment of depression, anxiety, schizophrenia, Parkinson’s disease, chronic pain, stroke, and other neural-related problems [2-7]. However, the tDCS research on athletic performance is not as consistent.”

Authors’ response: Nineteen (19) of the citations are provided for one statement which demonstrated:

“…that tDCS is effective at increasing maximal muscle force and endurance [8-25] as well as strength training volume [26].”

Another two sentences illustrate the expansiveness of the non-significant literature with 15 citations:

“…However, many others report no significant effects or decreases of muscle force or endurance when stimulating the motor cortex [9,21,28-37]. There were also no significant effects on jump height [38], or single or repeated sprint performance [39,40] when stimulating the dorsolateral prefrontal cortex.”

Hence, 34 of the citations are focussed on either the performance improvements or the reductions associated with tDCS. We feel it is necessary to comprehensively cover the literature so the reader is familiar with the disparity and conflicts in the prior publications and what has been examined before.

Based on the reviewer’s comment we have reduced the introduction by approximately a page.

Minor Comments

1. Lines 139-143: use active voice or make line 139-140 its stand-alone sentence after the stated aim.

Authors’ response: We have removed the first part of the sentence regarding the type of stimulation protocol. We have moved this information to the methods section.

METHODS:

Minor Comments

Authors’ response: We would like to illustrate to the reader that this stimulation protocol has been widely used. Thus, the reader should now have confidence that this protocol is valid and reliable.

2. Line 194: Remove double word.

Authors’ response: The second repeated word (i.e., protocol) was removed as suggested.

RESULTS:

Minor Comments:

1. It would be helpful to restate the statistical models for each analysis in the results since the variables of the ANOVA vary.

Authors’ response: A 3-way repeated measures ANOVA was employed for all testing.

1. Absolute MVC force

2. Relative MVC force

3. Fatigue test.

Hence stating that it was a 3-way repeated measures ANOVA for each measure would be redundant or repetitive with the information already provided in statistical analysis section and would not provide any greater clarity.

With each interaction in the results, we state the variables tested. Below are just 3 examples:

“…with no significant interaction effects found for condition (condition x time), or leg tested (leg tested x time), nor main effects for condition.”

“A significant [F(1,60) =7.156, p = 0.010, ηp2 = 0.11] interaction effect was found for condition and leg tested (condition x leg tested x time)(Fig 2).”

“A significant interaction effect for condition x leg tested [F(1,56) = 8.12, p = 0.006, ηp2 = 0.13], showed…”

DISCUSSION:

Minor Comments:

1. Line 336-338: Make the sentence more detailed based on the references provided (i.e., #10 and #19). For example, the target of tDCS and MVC, etc in these articles.

Authors’ response: We have added the following details as suggested.

“However, a previous studies involving a-tDCS of the contralateral leg motor cortex reported improved foot pinch force for 30 minutes post-a-tDCS [10], as well as increased KE MVC force for 60 minutes after a-tDCS [19].”

2. Line 364: Make the effects on sex more specific to the current studies protocol, parameters and variables and not so general.

Authors’ response: Line 364 is the last sentence of the previous paragraph and does not discuss sex differences. However, the following paragraph does discuss sex differences and we have added some greater detail. For example: we have added the following information to that paragraph.

A review by Dedoncker [62] suggested that women demonstrated greater accuracy on cognitive tasks with a-tDCS. A previous study that retrospectively re-analyzed data collected from previous transcranial direct current stimulation studies did not report significant cortical excitability differences between the sexes for a-tDCS. However, the effects of cathodal tDCS on neuroplasticity were greater, lasted longer and demonstrated more inhibition for female participants in comparison to males, suggesting that female participants may experience increased effects of tDCS possibly due to the effects of sex hormones [61].

3. Lines 365-369: Authors should highlight the a-tDCS results first, since it relevant to the current study and then introduce that cathode tDCS generated different results.

Authors’ response: We have changed the order as suggested.

4. Line 382: The authors introduced TMS without defining it or providing insight into how TMS may determine potential changes in M1 excitability.

Authors’ response: We have added the following explanation:

“Furthermore, as only the KE (quadriceps) were tested, future studies should aim to determine if other muscle groups ipsilateral to the site of stimulation are affected in a similar manner, while also utilizing transcranial magnetic stimulation (TMS) to determine potential changes in corticospinal excitability. When combined with transmastoid electrical stimulation, which activates axons in the spinal cord, effects can be distinguished between cortical and spinal excitability or inhibition.”

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PLoS One. doi: 10.1371/journal.pone.0280129.r007

Decision Letter 3

Xin Ye

21 Dec 2022

Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortex

PONE-D-22-11905R3

Dear Dr. Behm,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Xin Ye, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #3: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: I Don't Know

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: Yes

**********

6. Review Comments to the Author

Reviewer #3: This Reviewer thinks that the manuscript has improved greatly since initial review. This Reviewer does not have any other MAJOR comments, and just a few MINOR comments. Once those are fixed, this Reviewer believes it has reached a point for acceptance.

1. Page 5 Line 105 AND Page 15 Line 363: The Page 5 can be used to define TMS and Page 15 can be moved to abbreviation.

2. Page 7 Line 161: Revise for clarity. This sentence is missing a word or two.

3. Page 9 Line 201-101 Revise for clarity.

4. Page 13 Line 35: Revise to "....may also be related to greater diversity..."

5. Page 15 Line 346: Authors can use the abbreviation tDCS here.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #3: No

**********

PLoS One. doi: 10.1371/journal.pone.0280129.r008

Acceptance letter

Xin Ye

27 Dec 2022

PONE-D-22-11905R3

Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortex

Dear Dr. Behm:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Xin Ye

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

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Data Availability Statement

The datasets generated during and/or analyzed during the current study are publicly available from the Dryad database (https://doi.org/10.5061/dryad.brv15dvcn).

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PERMALINK

Reduced isometric knee extensor force following anodal transcranial direct current stimulation of the ipsilateral motor cortex

Ryan B Savoury

Armin Kibele

Kevin E Power

Nehara Herat

Shahab Alizadeh

David G Behm

Roles

Abstract

Background

Methods

Results

Conclusion

Introduction

Materials and methods

Participants

Experimental design

Fig 1. Experimental design.

tDCS intervention

MVC and fatigue tests

tDCS blinding questionnaire

Statistical analysis

Results

Absolute force measures

Fig 2. Mean participant absolute contralateral and ipsilateral knee extensor force following anodal transcranial direct current stimulation (a-tDCS) or sham tDCS (s-tDCS).

Relative (normalized) MVC force

Fatigue test

Fig 3. Participant contralateral and ipsilateral knee extensor force fatigue index following anodal transcranial direct current stimulation (a-tDCS) or sham tDCS (s-tDCS).

Fig 4. Mean participant contralateral and ipsilateral knee extensor (KE) force for each contraction of the fatigue protocol.

tDCS blinding questionnaire data

Discussion

Limitations

Conclusions

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Xin Ye

Roles

Author response to Decision Letter 0

Decision Letter 1

Xin Ye

Roles

Author response to Decision Letter 1

Decision Letter 2

Xin Ye

Roles

Author response to Decision Letter 2

Decision Letter 3

Xin Ye

Roles

Acceptance letter

Xin Ye

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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