Abstract
Objectives
The purpose of this study is to examine the effects of applying anodal tDCS (2 mA for 20 min) over the scalp from T3 (anodal-tDCS) to Fp2 (cathodal-tDCS) on the perceptual, physiological and performance responses during maximal incremental and constant-load exercise (CLE) in trained cyclists.
Methods
Eleven male cyclists performed maximal incremental exercise (MIE) on a cycle ergometer under either tDCS or sham, with power output, heart rate (HR), oxygen uptake (V̇O2), ratings of perceived exertion (RPE) assessed throughout, and blood samples collected before and after MIE. On two separate occasions, nine subjects performed CLE at 62 % of the peak power output followed by a 15 km time trial under either tDCS or sham (n=8 for the time trial).
Results
HR, V̇O2, RPE and blood samples were collected at regular intervals. There were no differences between tDCS and sham in any variable during the MIE. tDCS elicited a decreased HR (F (4,8)=9.232; p=0.016; η p 2 =0.54), increased V̇O2 (F (4,8)=8.920; p=0.015; η p 2 =0.50) and increased blood non-esterified fatty acids (F (6,8)=11.754; p=0.009; η p 2 =0.60) and glycerol (F (6,8)=6.603; p=0.037; η p 2 =0.49) concentrations during the CLE when compared to sham. tDCS also improved 15 km time trial performance by 3.6 % (p=0.02; d=0.47) without affecting RPE, HR and blood lactate.
Conclusions
The application of tDCS over the temporal cortex in trained cyclists improved cycling performance during a self-paced time trial but did not enhance performance during maximal incremental exercise. These results are encouraging and merit further investigation of the ergogenic effects of tDCS in trained athletes.
Introduction
Transcranial direct current stimulation (tDCS) is a non-invasive modality of cerebral neuromodulatory technique that can alter brain excitability and the autonomic nervous system [1, 2]. While the electrical current is applied to the scalp over the cortical area beneath the electrode, tDCS is thought to reach subcortical brain regions since there are connections within the cortico-cortical neural networks [3]. tDCS involves the application of a low-intensity electrical current (1–2 mA) over the scalp that flows from an anode to a cathode electrode to induce excitability changes within the stimulated cortex. The change in excitability is dependent on both the placement and polarity of the stimulation [4]. Anodal stimulation depolarizes the resting membrane potential of neurons and increases cortical excitability, whereas cathodal stimulation elicits a hyperpolarization of the membrane and reduces cortical excitability [5].
An extensive introduction of tDCS in the medical setting has occurred over the last two decades as a supplementary treatment to alleviate pain and enhance mood states in patients suffering from epilepsy [6], schizophrenia [7] and other neurological disorders. While the precise physiological mechanism(s) for the analgesic effect of electrical stimulation remains to be determined, previous evidence suggests that the stimulation of specific areas of the brain triggers the modulation of activity in specific pain-related regions such as the medial thalamus, the insula and the anterior cingulate gyrus [8]. For example, Dos Santos et al. demonstrated that the application of tDCS targeting the primary motor cortex (M1 area) induced the activation of the µ-opioid system [9]; a system heavily involved in analgesia, which might play an important role reducing the perception of effort during exercise. In addition to this analgesia, the stimulation of the left insular cortex has been shown to increase parasympathetic activity, delay vagal withdrawal, and affect cardiac autonomic control and cardiac efficiency during aerobic exercise [1, 2]. The stimulation of the left insular cortex together with surrounding cortical areas (e.g., nucleus tractus solitarii or rostral ventrolateral medulla) has been shown to induce favorable effects on the autonomic control of the heart [2].
The systematic application of tDCS in healthy individuals was introduced by Cogiamanian et al. over a decade ago [10]. These authors reported a reduction in fatigue-related muscle soreness and improved muscle endurance following tDCS (1.5 mA for 10 min). These promising initial results encouraged others such as Okano et al. [1] to assess the impact of tDCS, using different electrode montages. Okano et al. examined the effect of tDCS over the left temporal cortex (2 mA for 20 min) on the rating of perceived exertion (RPE), the cardiovascular response and peak power output (PPO) during maximal incremental exercise (MIE) in trained cyclists. These authors found a significant reduction in HR and RPE during submaximal intensities, as well as a 4 % improvement in PPO during maximal incremental exercise following tDCS [1]. These pioneering early findings encouraged the publication of numerous studies examining the effects of tDCS on performance-related phenotypes such as time to exhaustion (TTE) at a fixed work load in cycling [11], [12], [13], [14], [15], [16] and cycling time trial [15] with conflicting effects on performance. Notably, the promising methodology reported by Okano et al. in 2015 (anodal tDCS at 2 mA for 20 min over the T3 area) has not been replicated in trained athletes and there are only two other studies to have used the same tDCS procedures [15, 16]. A recent systematic review and meta-analysis [17] summarized the acute effects of tDCS on cycling and running performance, revealing a significantly higher time to exhaustion performance for the tDCS group when compared to sham, but no significant impact in time trial or sprint performance [17]. However, the different tDCS set-up characteristics (e.g., stimulated brain area, electrodes montage, stimulation duration, current intensity and density, electrode size), fitness level of cyclists, and reduced number of publications likely biased the pooled findings. Nowadays the impact of tDCS on time trial performance is controversial, as well as the impact on exercise efficiency at submaximal intensities. It is possible that the original and promising electrode montage proposed by Okano et al. [1], could reveal novel insights during these exercise modalities.
In our study, we hypothesize that anodal tDCS over the left temporal cortex would elicit physiological and perceptual modulations, as well as performance improvements in trained cyclists. Therefore, the objectives of the present study were to explore the effects of anodal tDCS over the left temporal cortex (from T3 to Fp2) on the physiological, perceptual and performance responses during 1) maximal incremental cycling exercise; 2) constant-load submaximal cycling; and 3) a 15 km time trial in trained cyclists (Figure 1).
Graphical representation of the study. Keys points: 1) Anodal tDCS improved 15 km cycling performance; 2) Anodal tDCS modulated cardiac function during constant-load submaximal cycling; 3) Energy expenditure during a constant-load submaximal cycling exercise was increased following anodal tDCS. Figure created with BioRender.teaser-image.
Materials and methods
For the present study, cyclists were required to attend the laboratory a total of six occasions: VO2max test, familiarization with the CLE and time trial tests, 2 × maximal incremental tests (tDCS or sham in a randomized order), 2 × CLE and time trial tests (tDCS or sham in a randomized order). Athletes rested for a minimum of three days and maximum of seven days between the different exercise tests. According to their availability, tests were always performed at the same time of the day for each athlete. All tests were performed using a fan and with an ambient temperature of 20–24 °C. Further details for each test are specified below.
Subjects
Twelve trained male cyclists (30.0 ± 5.2 years; 178.9 ± 7.6 cm; 73.1 ± 6.4 kg; BMI=22.8 ± 1.5; PPO=366 ± 44 w; PO at the first ventilatory threshold=173 ± 30 w; PO at the second ventilatory threshold=298 ± 30 w; relative PPO=5.1 w·kg−1) volunteered to participate in this study. According to previously published guidelines, the cyclists included in the present project are classified as “trained athletes” or performance level 3 [18]. All cyclists were informed of the procedures and risks of the study and provided informed consent. They were required to avoid strenuous exercise during the testing period and to replicate their individual diets 24 h prior to each test. This study was approved by the Ethics Committee of Aragón, Spain (CEICA; Num. 22/2018).
tDCS procedures
The electrical current was applied with a portable and wireless device (Starstim, Neuroelectrics Barcelona SLU, Barcelona, Spain) with a maximum current per channel of ±2 mA, a current accuracy of 1 % and a maximum voltage of ±15 V per electrode.
A neoprene head cap with 39 possible electrode positions (based on the EEG 10-10 system) was used to precisely position the electrodes, with the Cz point aligned to the vertex of the head. Two sponges (25 cm2) were soaked in saline solution (NaCl 0.9 %) and wrapped around the electrodes. In order to optimize the transmission of the electrical current through the electrodes, a highly conductive and water-soluble gel was applied on the contact surface between the electrode and the scalp (Signagel, Parker Laboratories Inc., New York, USA). The active anodal electrode was placed over the left temporal cortex at T7 area according to the EEG 10-10 system (T3 area according to the traditional EEG 10–20 international system) targeting the left insular cortex. The return electrode was positioned over the contralateral supraorbital area (Fp2 position). Brain stimulation following this electrode montage was selected to target the insular cortex, which has been implicated in autonomic nervous system control [19] and also in the awareness of subjective bodily feelings [20]. Electrode impedance check was performed before and during the stimulation period to ensure the electrical current was being transmitted correctly throughout all the stimulation periods. Thereafter, a constant electrical current of 2 mA was applied (total current density of 0.08 mA·cm−2) for 20 min. For the sham condition, the head cap and electrodes were positioned in the same manner but the electrical current gradually turned off after 30 s of real tDCS, as previously described [21], in order to mimic the tDCS sensations and allow for blinding. In order to check the effectiveness of the sham condition and thus to ensure the lack of placebo effect, subjects were required to indicate the stimulation condition they thought was being applied each time.
Maximal incremental exercise
Cyclists attended the laboratory in the morning (approximately at 10 am) or evening (approximately at 6 pm) in a consistent manner according to their availability in order to avoid any influence of circadian rhythm, as this has shown to have a direct impact on sports performance [22]. They were fasted for a minimum of 3 h prior to arrival, having abstained from coffee, alcohol and strenuous exercise 24 h before the test. The protocol followed a step format, and was performed on a cycle-ergometer (Ergoselect 200 K, Ergoline; Bitz, Germany) and, following a 5-min warm-up at 70 W, subjects performed constant load exercise at 100 W for 5 min. This first phase was followed by increments of 25 W·min−1 until voluntary exhaustion or until the cyclist was unable to maintain a cadence of 70 rpm for longer than 5 s. Cyclists self-selected their preferred cadence in the range of 70–100 rpm. RPE was measured every minute using the 20-point Borg scale, HR (H9, Polar, Kempele, Finland) and cardiorespiratory variables (Oxycon Pro, Jaeger/Viasys, Hoechberg, Germany) were assessed throughout the test. A 3 mL blood sample was collected in a K3EDTA tube before and immediately after the MIE and blood used for the analysis of lactate concentrations. The PPO achieved by the cyclists represented the maximum load that they could complete during 1 min (i.e., athletes had to complete the 1-min step to consider that load as reached).
Constant-load exercise and time trial
Subjects were required to attend the laboratory in the morning in a fasted state and refrained from strenuous exercise, caffeine and alcohol consumption 24 h before the test. Prior to attending to the laboratory, subjects were required to drink approximately 500 mL of water to ensure a standardized state of euhydration at the commencement of each test. After a standardized warm-up, subjects pedaled at a constant work load (225 ± 22 W; 62 % of their PPO; 76 ± 2 % of their V̇O2max) for 30 min on a cycle ergometer and subsequently performed a 15 km time trial on a cycle simulator with a 3 min rest in between to change trainers to cycling cleats and mount their own road-bike (protocol displayed in Figure 2). A constant load at 62 % of their PPO was selected given a previous work of our group with a similar protocol [23], ensuring that respiratory quotients were under one to avoid an excessive anaerobic contribution. Road-bikes were connected to an electromagnetic cycle-simulator (Spintrainer, Technogym, Gambettola, Italy) and, prior to each test, tire pressure was set at 8 bars and the road-bike calibrated on the simulator (calibration process described elsewhere [24]) with HR and RPE being assessed throughout the test. At the commencement of the trial (immediately after anodal tDCS/sham stimulation), a 20-gauge cannula (Introcan Safety, B. Braun, Melsungen, Germany) was inserted into the right antecubital vein and blood collected on five occasions (specified in Figure 2) to assess lactate, glucose, non-esterified fatty acids (NEFAs), and glycerol concentrations. Breath-by-breath analysis (Oxycon Pro, Jaeger/Viasys, Hoechberg, Germany) was intermittently performed every 2.5 min for 2.5 min using a mouthpiece.
Perceptual and physiological measurements during the constant-load exercise and 15 km time trial.
Cyclists were asked to complete the 15 km distance as quickly as possible and to use the same pacing strategy during all trials. Three km splits were recorded to assess the pacing strategy, and communicated these split times to the cyclist during all trials. Subjects were required to remain in a seated position at all times and were allowed to drink water ad libitum (all subjects consumed 200–500 mL of water during trials).
Mood state and pain assessment
Subjects completed the a-POMS questionnaire before and immediately after the tDCS stimulus during MIE sessions, which was previously validated in an athletic population [25]. This 24-item questionnaire is categorized into six main domains: anger, confusion, depression, fatigue, tension and vigor. The adjective responses and scores were measured on a 0–4 scale (0=not at all; 4=extremely) and this data standardized using the normative values for factor loading proposed in a 6-factor model of the a-POMS questionnaire [25]. Additionally, a 10-point visual analog scale (VAS) for pain was completed immediately after the tDCS/sham stimulus. VAS has been widely used to assess pain during numerous intervention studies in the field of brain stimulation [26].
Statistical analyses
The distribution of the data was determined by the Shapiro–Wilk statistic and the results showed a normal distribution. The sample size calculation was performed through the G*Power software (version 3.1.9.3) using the 15 km performance time collected during a pilot study previously performed in four cyclists. A two-tail t-test assessing the difference between two dependent means with a power of 80 and 5 % alpha level was performed. The power calculation revealed a minimum sample size of nine subjects. Greenhouse–Geisser was used to correct the p-value when the Mauchly’s test of sphericity was significant (p≤0.05).
A paired Student’s t-test was used to compare lactate concentrations, PPO, TTE, and pain scores between tDCS and sham during the MIE, and also to compare lactate concentrations and cycling performance in the 15 km time-trial. A two-way analysis of variance with repeated measures (ANOVARM) was applied with two main factors including condition (tDCS, sham) and time (12 time-points for the MIE, six time-points for the CLE, and five time-points for the 15 km time trial).
Bonferroni’s multiple comparisons test was used to check the differences previously detected in the group-effect analysis by the ANOVARM. Partial eta squared (η p 2 ) was used to report effect size from the ANOVARM analysis considering the following thresholds: small effect (>0.01), medium effect (>0.06) and large effect (>0.14). Cohen’s d was calculated for the effect size from multiple comparisons using the classic thresholds proposed by Cohen: small effect (>0.2), medium effect (>0.5), and large effect (>0.8). All analyses were performed using SPSS (version 24.0, Chicago, USA).
Results
The final subject numbers were: 11 cyclists for the MIE, nine for the CLE and eight for the 15 km time trial. One cyclist decided not to continue after the familiarization trial, two suffered an injury before completing the CLE and a fourth cyclist suffered technical problems with the cycle simulator during the 15 km time trial (the rear tire rubbed against a metal part of the cycle-simulator, and we found out at the end of the test). In terms of blinding of the study, subjects were unable to correctly distinguish between tDCS and sham conditions. No adverse effects were experienced by any of the volunteers in the present study. The results from the ANOVARM including the a-POMS assessment showed no differences for anger (η p 2 =0.09; p>0.05), confusion (η p 2 =0.02; p>0.05), depression (η p 2 =0.01; p>0.05), fatigue (η p 2 =0.00; p>0.05), tension (η p 2 =0.255; p>0.05) or vigor (η p 2 =0.05; p>0.05). In addition, the 10-point VAS for levels of pain from all testing sessions showed no differences between tDCS and sham (0.2 ± 0.4 vs. 0.1 ± 0.3, respectively; p>0.05).
Maximal incremental exercise
No significant differences were observed for PPO, TTE and lactate concentrations between treatment groups during the MIE (Table 1). The group-effect detected by the ANOVARM revealed that HR (F (3,10)=0.365; η p 2 = 0.04), RPE (F (3,10)=0.173; η p 2 = 0.02), V̇O2 uptake (F (3,10)=0.717; η p 2 = 0.07) and lactate concentrations (t=−0.14) were not different between sham and anodal tDCS throughout the MIE.
Peak power output (PPO), power output (PO) at the ventilatory thresholds, time to exhaustion (TTE) and lactate concentrations during the maximal incremental exercise with sham or transcranial direct current stimulation (tDCS).
| Variable | Sham (mean ± SD) | tDCS (mean ± SD) | t | p |
|---|---|---|---|---|
| PPO, W | 370.5 ± 46 | 370.5 ± 49 | 0.000 | 1.000 |
| PO at VT1, W | 170.0 ± 30.7 | 175.0 ± 23.0 | 0.000 | 1.000 |
| PO at VT2, W | 295.0 ± 28.4 | 282.5 ± 40.9 | −1.86 | 0.096 |
| TTE, s | 968 ± 108 | 955 ± 114 | 0.932 | 0.373 |
| Lactate pre-test, mmol·L−1 | 1.0 ± 0.6 | 1.1 ± 0.4 | −0.720 | 0.488 |
| Lactate post-test, mmol·L−1 | 10.1 ± 4.2 | 9.9 ± 5.0 | 0.140 | 0.891 |
Constant-load exercise and time trial
During the CLE, a significant group-effect difference was observed for HR (F (4,8)=9.232; p=0.016; η p 2 =0.54), V̇O2 uptake (F (4,8)=8.920; p=0.015; η p 2 =0.50), blood NEFAs (F (6,8)=11.754; p=0.009; η p 2 =0.60) and blood glycerol (F (6,8)=6.603; p=0.037; η p 2 =0.49). Nevertheless, RPE, blood glucose and lactate did not show a significant group-effect difference between tDCS and sham. Figure 3 shows the between-treatment group comparisons followed by Bonferroni post hoc test for those variables that showed a significant treatment group-effect in the ANOVARM. The application of tDCS significantly decreased HR at 10 min (−2.9 bpm; d=0.38, p=0.03), 15 min (−4.3 bpm; d=0.58, p=0.05), 20 min (−4.5 bpm; d=0.50, p=0.03), 25 min (−6.3 bpm; d=0.73, p=0.02) and 30 min (−5.3 bpm; d=0.55, p=0.05) when compared to sham. The effects of tDCS on V̇O2 uptake showed a small increase in V̇O2 uptake at 5 min (+111 mL·min−1; d=0.32, p=0.02), at 20 min (+89.8 mL·min−1; d=0.28 p=0.01), at 25 min (+83.8 mL·min−1; d=0.27, p=0.04) and at 30 min (+117.4 mL·min−1; d=0.40, p=0.01). It is worth noting that this increase in V̇O2 uptake was not accompanied by any changes in V̇CO2, V̇E and RER. There was an increase in NEFAs concentration on the tDCS trial at 0 min (+96.9 mg·dL−1; d=0.81, p=0.04), 10 min (+81.3 mg·dL−1; d=0.96, p=0.00), 20 min (+109.8 mg·dL−1; d=0.83, p=0.01) and 30 min (+133.1 mg·dL−1; d=0.85, p=0.02) when compared to sham. Finally, blood glycerol concentration was significantly higher for the tDCS group at 20 min (+43 mmol·L−1; d=0.70, p=0.02) and 30 min (+78 mmol·L−1; d=0.98, p=0.00) when compared to sham.
Effects of transcranial direct current stimulation (tDCS; black dots) on heart rate (A), V̇O2 uptake (B), blood non-esterified fatty acids (C) and blood glycerol (D) concentrations, when compared to sham (black line) during the constant-load protocol. *p≤0.05.
During the 15 km time trial, ANOVARM revealed no significant treatment group-effect for HR (F (5,7)=1.677; η p 2 =0.173) and RPE (F (5,7)=4.806; η p 2 =0.375) between tDCS and sham. Additionally, there were no significant differences in post-exercise blood lactate between conditions (mean difference=0.3 ± 2.0 mmol·L−1). However, a paired t-test revealed that the tDCS group improved 15 km performance (improvement of 3.6 %; d=0.47, p=0.02; Figure 4) when compared to sham (effect size of 0.884). The pacing strategy for each condition is displayed in Figure 4, showing a consistently similar improvement during each 3 km split for the tDCS group (mean improvement in 0–3 km split=−10.1 s; 3–6 km split=−11.8 s; 6–9 km split=−10.1 s; 9–12 km split=−10.3 s; and 12–15 km split=−8.0 s; Figure 4).
Effects of transcranial direct current stimulation (tDCS) on 15 km cycling performance (A), the time performed on every 3 km split (B), and the individual performance change in response to tDCS when compared to sham (C). *p≤0.05.
Individual response in performance
There was substantial inter-individual variability in performance outcome in the present study, as shown in Figure 4. From the eight subjects included in the 15 km time trial, six improved their performance while two subjects had similar performance times (subjects 1 and 2 showed a decreased performance of 1 and 12 s, respectively) after anodal tDCS. Among the six subjects who improved their cycling performance, four subjects showed similar improvements (improvement range: 3–4.8 %) while two cyclists (subject 3 and 5) showed much larger improvements (8.9 and 10.8 %, respectively).
Discussion
The main findings of our study revealed that anodal tDCS (2 mA for 20 min from T3 to Fp2) improved performance during a 15 km time trial in trained cyclists despite showing no differences in any of the measured physiological or perceptual responses when compared to sham. In our study, we did not observe any effect of tDCS during maximal incremental exercise, although we did observe a reduced cardiovascular strain and improved cardiac efficiency during the constant-load exercise.
Effects of tDCS on MIE. Our findings do not support the performance improvements previously observed with maximal incremental exercise [1]. For the maximal incremental exercise, we replicated the protocol design and tDCS procedures previously used by Okano et al. with trained cyclists [1], but did not reproduce the previously reported performance effects. Notably, the total duration from the end of the tDCS stimulus to the completion of the maximal incremental test was approximately 24 min (approximately 3 min to complete the a-POMS questionnaire + 5 min warm-up + approximately a 16 min test). When examining the effects of tDCS during the CLE, the first significant differences in HR between tDCS and sham were observed after approximately 22 min from the end of the tDCS stimulus (approximately 5–6 min to complete the cannulation process + 6 min warm-up + 10 min test). This occurrence and the gradual increase observed in the differences in HR response throughout the 30 min CLE (Figure 3) suggests a delayed increase in the cardiac autonomic nervous system modulation after anodal tDCS over the temporal cortex. The excitability elevations caused by anodal cortical stimulation are thought to last up to 2 h, depending on the stimulation duration, intensity and direction of current flow [5, 27]. However, the optimal time when neural plasticity is maximized seems less clear. Hoy et al. [28] revealed that 2 mA over the left dorsolateral prefrontal cortex (DLPFC) increased cognitive performance when compared to sham but only 20 and 40 min after tDCS [28]. Further studies have also found an approximate 30 min delay in the corticospinal plasticity after anodal tDCS over the primary motor cortex (M1 area) in elderly [29], and also in younger subjects over the left motor cortex [30]. This presumed delay in the physiological response after tDCS needs to be explored in future studies to identify the optimal time when tDCS effects are potentiated.
Effects of tDCS on CLE. During the constant-load exercise, CLE, tDCS reduced cardiovascular strain and improved cardiac efficiency as reflected in Figure 3. These findings are in agreement with previous research stating that the application of tDCS over the left temporal cortex triggers an increase in the autonomic modulation via parasympathetic pathways altering HR at rest and during exercise in athletes [1, 2]. Contrary to these findings, Barwood et al. showed no effects on HR response during a CLE in non-trained cyclists [15], although the use of untrained individuals might have masked the tDCS effects as a reduced parasympathetic activity and an increased sympathetic activity have been previously observed in untrained individuals compared to well-trained athletes [2, 31]. This suggests that well-conditioned athletes may have specific adaptations in cardiovascular brain-related areas such as the insular cortex, which might be explained due to a more plastic neural environment [2].
In addition to this modulation in the HR response during constant-load cycling, we observed a small but significant increase in V̇O2 uptake after tDCS throughout the 30 min CLE. This finding is in agreement with previous research showing a significant increase in V̇O2 uptake following tDCS, concluding that anodal tDCS might be able to modulate cerebral areas related to respiratory centers [32]. These authors attributed these findings to potential increases in cerebral concentrations of oxygenated hemoglobin (HbO2) [33] and a higher regional cerebral blood flow (rCBF) after activating specific brain regions [3]. While this rCBF increase seems to be widespread in different brain areas, further research suggested that the hemodynamic effect of anodal tDCS is relatively focal [34], showing that the increase in HbO2 occurs proximate to the stimulated area but notably diminishes in other brain regions (e.g., the contralateral hemisphere). Nevertheless, the focal brain alterations caused by tDCS seem to influence downstream metabolic systems regulated by the brain. Accordingly, Binkofsi et al. [35] showed that an increased cerebral energy consumption upon neural excitation (anodal tDCS of 1 mA for 20 min over M1) improved glucose tolerance in healthy subjects. These authors hypothesized that by stimulating the brain it could be possible to influence systemic metabolic features, evoking a transient ATP decrease, which in turn could lead to hypothalamic KATP channel activation and therefore increase systemic glucose uptake in humans [35]. In agreement with these findings, we observed significantly higher blood NEFAs and glycerol concentrations which might reflect the increased energy expenditure and a greater utilization of NEFAs than blood glucose due to the fasted state of the present subjects.
Effects of tDCS on 15 km TT. In the present study, anodal tDCS was accompanied by an improved 15 km performance despite exhibiting equivalent HR, RPE and blood lactate concentrations when compared to sham. This improvement in performance was not related to a change of mood state, which is in agreement with Vitor-Costa et al., who witnessed an improved TTE after anodal tDCS with unaffected levels of mood [13]. It is interesting to note that HR was decreased during the CLE but not during the time trial. The explanation for this might be because exercise during the CLE was performed at or slightly under the second ventilatory threshold (VT; i.e., anaerobic threshold), whereas the 15 km time trial was performed at a higher intensity. As previously stated, the relative contribution of the sympathetic nervous system increases when exercise exceeds VT while the parasympathetic activity is reduced [36]. Exercising at this higher intensity during the time trial might have inhibited the potential effectiveness of tDCS on cardiac autonomic modulation, given that anodal tDCS over the left insular cortex controls the parasympathetic activity of HR [37]. Accordingly, Okano et al. found an improved cycling performance during maximal incremental exercise although the differences in RPE and HR between tDCS and sham disappeared at very high intensities [1]. In our study, cycling performance was enhanced by 3.6 % for the same HR and RPE, when compared to the sham condition. These observations suggest that cyclists under tDCS effects were able to perform consistently harder throughout the 15 km test (as displayed Figure 4) despite reporting the same perception of effort at each time point. However, this improved performance is not supported by the findings of Barwood et al., who found no differences in performance during a 20 km time trial. As stated previously, the lower fitness (PPO=235 vs. 370 W in our study) of subjects in this study may potentially have concealed the true effectiveness of tDCS.
There are several limitations in the present study. Although we initially recruited a sample of 12 trained cyclists, four cyclists dropped out of the 15 km time trial, which resulted in the study of one less subject than the nine subjects indicated by a priori sample size calculation. However, the data derived from the difference between tDCS/sham from the eight subjects revealed a large effect size (0.884) on the main outcome variable. The variable duration between the end of tDCS and both testing protocols (MIE and CLE) complicates the interpretation and comparison of our results. This limitation should be considered in future studies given the undulating dynamics of the motor evoked potential (MEP) observed after tDCS [38]. In our study, the insular cortex was targeted by positioning the anodal electrode over the T3 area (i.e., through the temporal cortex), however, previous neuroimaging studies demonstrated that the electrical current might propagate to adjacent brain areas [39], thus making it impossible to focus the electrical current on specific areas of interest. Future research implementing neuroimaging techniques such as electroencephalography or functional magnetic resonance imaging might aid understanding cause-effect relationships after tDCS. In accordance with the literature, we observed markedly different individual responses to tDCS. The inter-individual variability in response to tDCS was previously examined [40] and approximately 50 % of subjects were classified as non-responders to anodal tDCS (1 mA for 13 min over M1). Within the responder group, there were individuals with a 300 % increase in MEP amplitude at 60 min post tDCS [40]. It is currently unknown whether repeated exposure to tDCS can impact response; an area of future investigation.
To conclude, this study revealed that anodal tDCS (2 mA for 20 min from T3 to Fp2) improves performance during a 15 km time trial in trained cyclists despite showing no differences in any of the measured physiological or perceptual responses when compared to sham. Subjects were able to exercise at a higher intensity consistently throughout the 15 km despite showing an equal RPE, lactate and HR response following tDCS. Our study was not designed to investigate mechanisms so the etiology for the improvement in performance with tDCS can only be speculated but likely due to some central modulation of perception of effort and physiological response as reflected in the observed alterations in HR, V̇O2 uptake and blood NEFAs and glycerol concentrations. While we did not observe any effect of tDCS during maximal incremental exercise, the after-effect timing and the inter-individual variability associated with the timing of tDCS needs to be further examined.
Practical applications
The main findings shown in the present study supports the use of specific tDCS procedures (i.e., anodal-tDCS of 2 mA for 20 min over the scalp from T3 to Fp2) to improve exercise performance during a time trial. The present work, when reinforced with further research, may assist coaches and trainers in selecting an effective ergogenic method to acutely improve exercise performance. Nonetheless, future research should consider the existing limitations of using tDCS and explore individual responses in designing personalized tDCS protocols to optimize performance.
Acknowledgments
The authors would like to thank the volunteers of the present study for their invaluable effort during all trials.
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Research ethics: This study was approved by the Ethics Committee of Aragón, Spain (CEICA; Num. 22/2018). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013).
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Informed consent: All cyclists were informed of the procedures and risks of the study and provided informed consent.
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Author contributions: BMP, EG, LM and YP conceived the idea and designed the experimental procedures. BMP, JSP and JAC performed the tests. The author(s) have (has) accepted responsibility for the entire content of this manuscript and approved its submission.
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Competing interests: The authors state no conflict of interest.
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Research funding: This study was funded by a grant from CIDIMU group and the Sub2 Foundation.
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Data availability: Data will be available upon request to the first author.
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