Anodal transcranial direct current stimulation enhances response inhibition and attention allocation in fencers

Participants

This study enrolled 16 female fencers (age: 21.18 ± 1.32 years, height: 173.50 ± 5.81 cm, weight: 63.62  ± 7.73 kg, training years: 9.75 ± 1.18) from the Jiangsu Provincial Fencing Team of Nanjing Sports Institute. All subjects were right-handed, had good overall health, no history of mental illness or brain injury, were not allergic to direct current and volunteered to participate in the trial. G*power program was used to compute a priori sample size with a test family = F-tests, statistical test = analysis of variance (ANOVA): repeated measures between factors. Based on previous studies (Codella et al., 2021; Maeda et al., 2017), power, alpha, and effect size were set at 0.80, 0.05, and 0.4, respectively, calculating that 14 subjects were required for a single group. To allow for an anticipated dropout rate of 10%, there were 16 subjects for a single group. The subjects were informed of the basic test procedure and potential risks before the trial, and all signed an informed consent form. The study protocol was approved by the Ethics Committee of the Nanjing Sports Institute (Approval no. RT-2022-06) and was conducted in accordance with the tenets of the Declaration of Helsinki.

Study design and procedures

All the enrolled fencers underwent a-tDCS and sham stimulation one week apart in a crossover, randomized, single-blind manner to investigate the effects of anodal and sham stimulation on reaction time, response inhibition, and attention (Fig. 1). To minimize the effects of circadian rhythm changes, subjects were tested at the same time of day. Prior to each test, subjects were instructed to abstain from alcohol, caffeine, theophylline, drugs or supplements, and to get a good night’s sleep. A standard experimental procedure is described as follows: the subjects came to the laboratory in the Physical Fitness Centre and sat in silence for 5 min to regain their composure (resting phase). A Stop Signal Task (SST) was then started, this will take approximately five minutes. After the end of the SST test, a Neuro tracker (NT) test was conducted in three modes: core (four balls), dynamic (four balls), and selective (two balls), with a 2-min interval between each test, each test takes approximately six minutes. The athletes were given five attempts to familiarize themselves with the test in each mode before starting the actual test. After completion of the whole test, an anodal tDCS intervention was carried out with a current strength of 2 mA for 20 min or sham stimulation (Bashir et al., 2022; Gu et al., 2022). Another SST test was performed immediately after the stimulation. After the end of the SST test, NT test was conducted in three modes: core, dynamic, and selective, with a 2-min interval between each test. However, the NT test in each mode was directly tested without attempts.

tDCS intervention

The tDCS intervention was carried out using the 1300A&4x1-C3A multichannel tDCS apparatus (Soterix Medical, New York, NY, USA). The 16 athletes were randomly assigned numbers, and each athlete had to undergo both anodal and sham stimulation. A crossover randomized design was used to determine the condition of stimulation for the first round of 16 athletes, followed by the second round of stimulation in the opposite condition, 1 week later. tDCS was administered by personnel familiar with the operation of the instrument, but they were not involved in this study, and the subjects were blinded to the type of stimulation received. For the safety of the subjects, the procedures related to the use of tDCS were designed based on the study by Muthalib et al. (2018). The left M1 primary motor area was selected and electrodes were placed on C3, FC1, FC5, CP5, and CP1 based on the International 10-10 system, with C3 being the central electrode (Fig. 2). Five silver chloride sintered circular electrodes (one cm²) were connected to a 4 x 1 adapter; the adapter was then attached to the tDCS device using a cable, and the electrode fixation caps were attached to the electrode caps at C3, FC1, FC5, CP5, and CP1.

The subjects were asked to sit quietly on a back-rest chair. An experimenter then left the subject’s scalp exposed, injected conductive gel into the five electrode fixation caps, and positioned the electrodes in place. When anodal stimulation was performed, the operator pressed the conductivity test button to check the conductivity and then pressed the start button to perform tDCS. The current strength was gradually increased to 2 mA within 30 s and lasted 20 min, and then the current gradually decreased to 0 mA in the last 30 s. The current intensity, stimulation time, and current acceleration of the sham stimulation were the same as those of the anodal stimulation, except that the current accelerated to 2 mA in the first 30 s and then gradually decreased to 0 mA automatically in 30 s (Gu et al., 2022; Guo et al., 2022). The tDCS was stopped immediately if the subject felt any discomfort other than the normal mild tingling sensation of stimulation throughout the tDCS procedure.

Data collection

SST test

The SST program was written using the E-Prime 3.0 software (Psychology Software Tools, Inc., Sharpsburg, PA, USA), it is widely used to test the subjects’ response inhibition ability (Guo et al., 2022; Sandrini et al., 2020). The Go task reaction time (Go RT) and Stop-signal reaction time (SSRT) were selected as indicators of reaction time and response inhibition. The GO RT was determined by measuring the time interval between the time when go signal appeared and time when participants made the correct response. A total of 240 trials were performed, including 180 (75%) Go trials, 20 (8.3%) NoGo trials, and 40 (16.7%) stop-signal trials. Trials were presented randomly, and the number and type of tasks were equally divided between the two blocks, with an intergroup interval of no more than 2 min. Prior to the start of the experiment, the subjects were informed of the testing procedure and proceeded with 25 trial attempts until they were familiar with the task, fully understood the task, and became proficient in its operation. In the Go trial, the central position was initially calibrated with a cross on the computer screen, and the subjects used the keyboard to press the appropriate left and right keys according to the left and right black arrows that appeared in the center of the computer screen. The arrows were presented for 1,000 ms. The next trial would appear after the response (regardless of its accuracy) or if no response was recorded within 1,000 ms. In the SST trial, the left/right black arrows appeared on the screen initially, but after the stop-signal delay (SSD), the arrows changed color to red, to which the subject is to inhibit their response and did not respond. The initial value of SSD was 250 ms, and a 50% success suppression was maintained by a 50-ms incremental correct/50-ms decremental incorrect algorithm, which has been widely used in stop-signal studies (Friehs & Frings, 2019; Huijgen et al., 2015; Parkin & Walsh, 2017). The SSRT calculation was simplified as follows: mean SSRT = mean Go RT - mean SSD. SSRT represents an estimate of how long it takes a person to successfully inhibit their prepotent response and that a shorter SSRT indicates better response inhibition. In the NoGo trial, A red arrow appears on the screen but the subjects did not respond to the red arrow (1,000 ms) (Fig. 3).

NT test

Subjects’ attention was tested using the Neuro Tracker multi-task tracking neuro-perceptual system (Faubert Applied Research Centre, Toronto, Canada). To increase stereoscopy and the demands of attentional tracking, the NT test involves tracking multiple targets among distractors in a 3D environment. Thus, NT involves multifocal attention and requires a high level of processing that includes the brain’s ability to ignore distractors and maintain focus (Cavanagh & Alvarez, 2005; Meyerhoff, Papenmeier & Huff, 2017). NT is based on a multi-target tracking task (MOT), Originating with Pylyshyn & Storm (1988), MOT is a well-established paradigm for studying attention. The MOT task has been used to assess sustained, distributed, dynamic, and selective attention and has proven to be one of the most useful and popular tools in attention research (Doran and Hoffman, 2010; Drew et al., 2009; Koldewyn et al., 2013; Meyerhoff, Papenmeier & Huff, 2017; Meyerhoff & Papenmeier, 2020). In the NT test, speed threshold scores measured in the core, dynamic, and selective modes were selected as a measure of attention. The NT test was conducted sequentially in three modes: core, dynamic, and selective. Subjects were tested once for each mode, and 20 trials were performed each time. In the core mode, the subject was seated in a back-rest chair with 3D glasses, and her line of sight was aligned with the center of the cube. Eight small yellow-green static balls appeared in the cube’s field of view. The four target balls to be tracked by the subject appeared in red for 2 s and then turned back to the original yellow-green color. The eight balls then began to move and collide at their initial velocity in an irregular pattern in the cube’s field of view, changing direction of motion when they collided with each other or with the walls. After 8 s, the balls stopped moving and were marked from 1 to 8. The subject was required to say the number corresponding to the target ball and was judged to be correct only if all the numbers of the target balls were reported correctly. The correct target balls were shown in red for 2 s after the subject reported the number, after which the next trial began.

After each trial, the ball speed automatically adjusted based on the correctness of the responses, with correct answers increasing the speed of the ball and incorrect answers decreasing it. Thus, the correct rate was controlled at around 50%. At the end of the test, the subject was given a speed threshold score as a test indicator. Dynamic mode differed from the core mode in that the sphere moved in an irregular manner at variable speed. In the dynamic mode, the ball speed slowed down and then returned to the initial speed over the course of 8 s, with the remaining procedure identical to the core mode. Selective mode differed from the core mode in that there were only two target balls, one blue and one red ball, and at the end of the trial, the subject reported the blue ball first and then the red ball. The rest of the procedure was the same as that in the core mode.

Statistical analysis

All data were statistically analyzed using JMP, version 16 (SAS Institute, Inc., Cary, NC, USA) and index data were expressed as the mean standard deviation (M ± SD). A two-factor analysis of variance (ANOVA) with repeated measures was used to analyze the effects of stimulation condition (anodal and sham stimuli) and time (pre-stimulation and post-stimulation) on reaction time (Go RT), response inhibition (SSRT), and attention ability (speed threshold scores). Post-hoc analysis with LSD was used if significant main or interaction effects were observed. A value of P < 0.05 was considered to indicate significant difference. The effect size (ES) analysis was used to report the magnitude of the pre-post differences for all measures in each condition, and the ES was expressed as Cohen’s d. The criteria for interpreting ES size were: <0.19 for a weak effect, 0.20–0.49 for a low effect, 0.50–0.79 for a medium effect, and >0.8 for a high effect (Cohen, 1992).

Go RT

Two-factor repeated measures ANOVA was used to analyze the effect of Stimulation conditions and time (pre-stimulation and post-stimulation) on reaction time. The results indicated that the main effect of stimulation conditions [F (1,30) = 0.030, P = 0.862, ${\eta }_p^2=0.001$] and main effect of time [F (1,30) =0.083, P = 0.774, ${\eta }_p^2$ = 0.003] were both not significant. The interaction between time and stimulation conditions was insignificant [F (1,30) =0.001, P = 0.974, ${\eta }_p^2$ <0.001]. Post-hoc analysis showed no significant differences in Go RT from pre to post stimulation for anodal or sham stimulation (Fig. 4).

SSRT

Two-factor repeated measures ANOVA was used to analyze the effect of Stimulation conditions and time (pre-stimulation and post-stimulation) on SSRT. The results showed that the main effect of stimulation conditions was not significant [F (1, 30) =0.008, P = 0.928, ${\eta }_p^2$ <0.001], while the main effect of time was significant [F (1,30) =4.711, P = 0.038, ${\eta }_p^2$ =0.135]. The interaction between time and stimulation conditions was significant [F (1, 30) = 5.299, P = 0.028, ${\eta }_p^2$ =0.150]. Results of post-hoc analysis demonstrated that SSRT was significantly reduced after a-tDCS (P < 0.05) (Table 1, Fig. 5).

Speed threshold scores

A two-factor repeated measures ANOVA was used for the analysis of the speed threshold score in the core mode. We found that a main effect of stimulation condition was not significant [F (1,30) = 0.134, P = 0.716, ${\eta }_p^2$ =0.004], a main effect of time was significant [F (1,30) = 9.764, P = 0.003, ${\eta }_p^2$ =0.246], and an interaction between time and stimulation condition was significant [F (1,30) = 4.849, P = 0.035, ${\eta }_p^2$ =0.139]. Results of post-hoc analysis demonstrated that core mode speed threshold score increased significantly after a-tDCS (P < 0.05) (Table 2).

A two-factor repeated measures ANOVA was used for the analysis of the speed threshold score in the dynamic mode. We found no significant main effect of stimulation condition [F (1,30) = 2,140, P = 0.153, ${\eta }_p^2$ =0.067], a significant main effect of time [F (1,30) = 11,955, P = 0,001, ${\eta }_p^2$ =0.285] and an interaction between time and stimulation condition was not significant [F (1, 30) = 0.204, P = 0.654, ${\eta }_p^2$ =0.007]. Results of post-hoc analysis demonstrated that dynamic mode speed threshold score increased significantly after a-tDCS (p < 0.05, Fig. 6).

A two-factor repeated measures ANOVA was used for the analysis of the speed threshold score in the selective mode. We found that a main effect of stimulation condition was not significant [F (1,30) =2.963, P = 0.095, ${\eta }_p^2$ =0.090], a main effect of time was not significant [F (1,30) =3.0985, P = 0.088, ${\eta }_p^2$ =0.094], and an interaction between time and stimulation condition was also not significant [F (1,30) =0.007, P = 0.930, ${\eta }_p^2$ <0.001]. Post-hoc analysis showed no significant differences in selective mode speed threshold from pre to post stimulation for anodal or sham stimulation (Fig. 7).