Hemodynamic and autonomic responses after a single session of ...

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Isokinetics and Exercise Science -1 (2016) 1–8 DOI 10.3233/IES-160653 IOS Press

Hemodynamic and autonomic responses after a single session of resistance exercise following anodal motor cortex tDCS Antonio H.G. Soaresa, Rafael A. Montenegrob, Bruno R. Cavalcantea, Wagner Ribeiroc , Paulo F.M. de Limaa , Annelise L. Menêsesd, Tarciso R.M. Almeidae , Alexandre H. Okanof and Raphael M. Ritti-Diasa,g,∗ a

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Associated Graduated Program UPE/UFPB, Pernambuco, Brazil Physical Activity and Health Promotion Laboratory, Physical Education and Sports Institute, Rio de Janeiro State University, Rio de Janeiro, Brazil c Associated Graduated Program in Physical Education UEM/UEL, Paraná, Brazil d School of Health and Sport Sciences, University of the Sunshine Coast, Queensland, Australia e Department of Physical Education, University of Pernambuco, Pernambuco, Brazil f Research Group of Integrative Biology of Exercise, Physical Education Department, Rio Grande do Norte Federal University, Rio Grande do Norte, Brazil g Albert Einstein Hospital, São Paulo, Brazil

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Received 26 May 2016

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Accepted 3 December 2016

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Abstract. BACKGROUND: Transcranial direct current stimulation (tDCS) seems to modulate cardiac autonomic function and blood pressure (BP) at rest and during exercise. Therefore, it is possible that anodal tDCS could influence post-exercise hypotension. OBJECTIVE: To investigate whether anodal tDCS applied over the motor cortex would affect cardiac autonomic modulation and BP after resistance exercise. METHODS: Twelve apparently healthy young men performed two experimental sessions: anodal tDCS or sham condition followed by resistance exercise. Blood pressure (BP), heart rate (HR), rate-pressure product (RPP), and HR variability (HRV) were obtained before and during post-exercise recovery (at 20 and 60 minutes). RESULTS: Compared to pre-exercise, systolic BP decreased at 20 and at 60 minutes of post-exercise recovery only in anodal tDCS condition (p = 0.03), with no statistical differences in sham condition (p > 0.05). Diastolic and mean BP reduced after both anodal tDCS and sham conditions with no differences between them (P > 0.05). In comparison with anodal tDCS, there were slower HR recovery (tDCS vs. sham: −2 ± 14 vs. 14 ± 8 bpm) and higher RPP (tDCS vs. sham: −1083 ± 1846 vs. 1672 ± 1275 mmHg × bpm) after exercise following sham condition (P < 0.01). No differences were found in any of the HRV analyzed parameters (P > 0.05). CONCLUSION: A single session of primary motor cortex tDCS is capable of decreasing the systolic BP and HR responses, as well as the cardiac work after a resistance exercise session in young normotensive subjects regardless of any changes in cardiac autonomic modulation. Keywords: Post-exercise hypotension, tDCS, motor cortex, resistance exercise

∗ Corresponding

author: Raphael Mendes Ritti-Dias, Albert Einstein Hospital. Albert Einstein Avenue, 627, ZIP-code: 05652-900, Sao Paulo, Brazil. Tel.: +5519 99940 6878; E-mail: raphaelritti@ gmail.com.

1. Introduction

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Physical exercise has been extensively acknowledged as a non-pharmacological strategy in the preven-

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c 2016 – IOS Press and the authors. All rights reserved ISSN 0959-3020/16/$35.00 

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at [17,18], during exhaustive exercise [19] and after exercise (i.e. excess-post oxygen consumption – EPOC) were modulated by tDCS [18], however, the effects of brain stimulation techniques upon cardiovascular and hemodynamic responses after exercise (i.e. PEH) are not fully understood. Previous studies that investigated the effects of anodal tDCS (polarity of current that has been increased and facilitated the neuronal membrane depolarization and neuron firing rate [20,21]) on autonomic nervous system (ANS) have stimulated different cortices (i.e. motor, frontal or temporal cortices) through different electrode montage (i.e. bi-cephalic or extra-cephalic), which might preclude comparisons between studies and may explain in parts the controversial findings. For example, Vernieri et al. [16], Montenegro et al. [17] and Clancy et al. [22] reported favorable tDCS effects upon both sympathetic and parasympathetic autonomic nervous system, while Raimundo et al. [23] and Vandermeeren et al. [24] failed to detect any tDCS influence upon ANS, BP or cardio-respiratory responses at rest. Despite these mixed results, our group recently observed interesting findings regarding the anodal tDCS effects on the autonomic cardio-respiratory system during exercise and recovery. When the exhaustive ramp cardiopulmonary exercise test was preceded by anodal tDCS, young male cyclists achieved lower submaximal responses of heart rate, ratings of perceived effort and longer time to achieve the heart rate variability (HRV) threshold than in sham condition [19]. Higher EPOC after submaximal aerobic isocaloric bouts (energy expenditure during exercise fixed in 200 kcal at 70% oxygen uptake reserve) was also observed [18]. Considering the crucial role exerted by the sympathovagal balance upon post-exercise BP and heart rate responses and the capability of tDCS of modulating the neuronal excitability of cortical and subcortical areas related to BP and HRV regulation [17,22,25,26], it is plausible that tDCS may be useful to enhance the PEH response, and accelerate the heart rate recovery after exercise. Hence, this randomized crossover- study aimed to investigate whether anodal tDCS over motor cortex would be capable of either potentiating the PEH or modulating the sympathetic and/or parasympathetic ANS assessed by spectral analysis of HRV. Since 20 min of anodal motor cortex tDCS seems to be capable of modulating neuronal excitability of brain area related to cardio-respiratory responses at rest, during and after exercise [17–19,26], we hypothesized that anodal tDCS would be capable of inducing greater decreases upon sympathovagal balance, increasing the magnitude of PEH when compared to sham condition.

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tion and treatment of hypertension [1]. Recently, it has been demonstrated that a single bout of either aerobic [2], resistance [3] or concurrent exercise (i.e. association between aerobic and resistance bouts) [4] could be effective to reduce blood pressure (BP) for several hours, which has been referred to as post-exercise hypotension (PEH). The PEH would be a desirable phenomenon in the context of hypertension management since there is evidence that exercise-related chronic reduction of BP results from acute (single session) PEH [5]. The mechanisms underlying PEH are not fully understood. However, central and peripheral factors seem to explain, at least in part, a decrease of cardiac output and/or systemic vascular resistance. This response is initiated through the central command from the somatic motor cortex and muscle chemoreceptive and mechanoreceptive inputs [6]. Centrally, both mechanisms are mediated by changes in the baroreflex control due to afferent information from active muscles (exercise pressor response or ergoreflex) [6]. Changes in barosensitivity are induced by inhibition stimuli mediated by the nucleus tractus solitarium (NTS) and rostral ventrolateral medulla (RVM), with consequent attenuation of neuronal activity within higher brain centers at thalamic and insular regions [7,8]. In this context, the insular cortex (IC) has been proposed as a major center of autonomic cardiac responses, baroreflex activity and BP control [9]. This premise was confirmed by Oppenheimer et al. [10] who observed parasympathetic nervous activity modulation, bradycardia and hypotension when the left IC was directly stimulated, while higher sympathetic activity, tachycardia and hypertension were observed when right IC was stimulated. Moreover, a reduction in right IC blood flow was reported after exercise only when PEH was observed [11]. Hypotension also was observed when the primary motor cortex was directly stimulated. This means that motor cortex following muscular activity may initiate and transmit stimulus to cardiac and vasomotor spinal preganglionic neurons regulating cardiovascular function [12]. Based on the abovementioned information, Coggiamanian et al. [13] highlighted non-invasive brain stimulation techniques (i.e. transcranial magnetic stimulation – TMS or transcranial direct current stimulation – tDCS) as a promising therapeutic tool for treating hypertension, given its capability of inducing excitatory or inhibitory effects upon either sympathetic nervous system or BP in healthy subjects or patients [14–16]. It has been shown that cardio-respiratory responses

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2.2. Procedures

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Familiarization – Prior to the experimental sessions, participants underwent two familiarization sessions designed to standardize resistance exercises execution. In these sessions, they performed an exercise routine as follows: leg press 45◦ , bench press, unilateral knee extension, seated row, knee curl and frontal raise. In each exercise, three sets of 10 repetitions with the minimum load allowed by the machines were performed. 8–12 repetitions maximum (RM) test – At least 48 hours following the familiarization sessions, participants performed 8–12 RM tests in order to determine the workload to be used in the experimental sessions [27]. After warming-up at a comfortable load, participants attempted each exercise once (leg press 45◦ , bench press, unilateral knee extension, seated row, knee curl, and frontal raise) with a workload estimated to elicit 8–12 RM. If the target load was not obtained in the first attempt (number of repetitions below or above 8–12 RM), the load was progressively readjusted and subjects were allowed to perform a second attempt after 10-min rest intervals, until the 8–12 RM could be determined. An interval of 5 min was respected between tests for each exercise. If the load was not obtained in the second attempt, another test session in another day was scheduled. Experimental session – All participants underwent two experimental sessions (anodal tDCS or sham condition followed by resistance exercise session) in a random counterbalanced order. Before and after exercise

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Twelve apparently healthy young men right-side dominant were recruited from local community of Pernambuco University, Brazil through advertisement. Prior to the enrollment, each participant was informed about the procedures of the study and were given a written consent. The Ethics Committee of the University of Pernambuco approved the study’s procedures. Each participant completed a detailed health history questionnaire and were included in the study if they had no signs or symptoms of disease, were not under medication or using ergogenic substances, and had no orthopedic or neurological injuries or prosthesis. This study was conducted in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki).

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sessions, the BP and HRV were obtained. Prior to the experimental sessions, subjects were instructed to have a light meal, to avoid physical exercise in the prior 24 h and alcohol or caffeine ingestion in the prior 12 h, and to maintain their sleeping hours routine and daily activities. Before the exercise sessions, the participants remained at rest for instrumentation and then randomly received either anodal tDCS or sham condition over the left primary motor cortex for 20 min. The exercise sessions performed after both anodal tDCS and sham condition were similar in terms of total volume of repetitions. In both sessions, the subjects initiated with a warm-up set of 10 repetitions at 50% of 8–12 RM. Subsequently, three sets of 10 repetitions of each exercise with load corresponding to 85% of 8–12 RM were performed, with the same exercise order described in 8– 12 RM testing. Resting intervals between sets and exercises were set at 2 min and 1 min, respectively. A washout period of 48–72 h between experimental sessions was respected to avoid tDCS carryover effects. Transcranial direct current stimulation (tDCS) – Direct current was transferred through a saline-soaked pair of surface sponge electrodes (35 cm2 ) and was delivered using a battery-driven constant current stimulator and the electrical current delivered by the stimulator was confirmed using a digital multimeter (ICELTM, Manaus, AM, Brazil). The tDCS electrode montage for this study followed the configuration chosen by Montenegro et al. [28] where the anode electrode was positioned over M1 (C3) and the cathode over the contralateral supraorbital area (Fp2) in accordance with the International Electroencephalography (EEG) 10–20 system [29]. A direct electrical current with 2 mA of intensity was applied for 20 min in both experimental sessions. In sham conditions, the electrodes took place in the same positions used for the anodal tDCS, however, the electrical current was turned off after two min of stimulation since this time of stimulation is considered to cause no prolonged changes in neuronal excitability [20]. On the other hand, the subjects were capable of feeling an initial itching sensation due to electrical direct current on scalp. This procedure allowed the subjects to remain ‘blind’ in respect of the tDCS polarity stimulation received assuring a sham control effect.

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2. Methods

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2.3. BP and HRV measurements

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BP was measured using an oscillometric monitor (Dyna-MAPA, Cardios, Brazil). The cuff was adjusted to the circumference of the right arm, 2–3 cm above

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a Data

presented in median interquartile range; b Data presented in mean and standard deviation. Table 2 Comparison of the hemodynamic and autonomic variables in the preexercise between experimental sessions

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Anodal tDCS Sham p-value Systolic blood pressure 114 ± 11 110 ± 12 0.248 (mmHg) Diastolic blood pressure 67 ± 7 66 ± 6 0.315 (mmHg) Mean blood pressure 83 ± 8 81 ± 7 0.192 (mmHg) Heart rate (bpm) 78 ± 10 67 ± 5 0.001 Rate-pressure product 8888 ± 1568 7375 ± 1156 0.002 (mmHg × bpm) RR interval (ms) 908 ± 97 879 ± 69 0.192 LF (nu) 58 ± 13 67 ± 17 0.175 HF (nu) 42 ± 13 33 ± 17 0.175

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Normality and homoscedasticity of the data were confirmed by the Shapiro-Wilk and Levene’s test, respectively. The comparisons of the hemodynamic and autonomic variables in the pre-exercise between sessions, as well as the differences of delta changes in heart rate and RPP were performed using a paired Ttest. The pre- to post-exercise responses in the hemodynamic and autonomic variables were compared by a two-way ANOVA for repeated measures including condition (sham x tDCS) and time (pre, 20 min, and

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Values 19 ± 3 70 ± 10 173 ± 4 23.3 ± 2.8 120 ± 13 74 ± 9

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Variables Age (yrs)a Body mass (kg)b Height (m)a body mass index (kg/m2 )b Systolic blood pressure (mmHg)b Diastolic blood pressure (mmHg)b

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2.4. Statistical analysis

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Table 1 General characteristics of the participants (n = 12)

Data presented as mean ± standard deviation.

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the cubital fossa at heart level. Measurements were performed at rest and after 20 and 60 minutes of resistance exercise session cessation. Rate-pressure product (RPP), an indicator of cardiac workload, was calculated by multiplying systolic BP and heart rate. All procedures followed the recommendations of the VI Brazilian Guidelines on Arterial Hypertension [30]. HRV was recorded using a heart rate monitor (Polar R RS800cx , Polar Electro Oy, Finland; sampling frequency = 1000 Hz) and them it was assessed using Kubios HRV software (Biosignal Analysis and Medical Imaging Group, Finland) by a single evaluator blinded to the other study variables, in accordance with the recommendations of the Task Force [31]. This software allows filtering all signals and eliminating the noises. Time domain analysis included the RR intervals, whereas for the frequency stationary periods of the tachogram with at least 500 beats were broken down into bands of low (LF) and high (HF) frequencies using the autoregressive method with a model order of 12. Frequencies between 0.04 and 0.4 Hz were taken to be physiologically significant. The LF component was represented by oscillations between 0.04 and 0.15 Hz and HF was represented by oscillations between 0.15 and 0.4 Hz. The power of each spectral component was normalized by dividing the power of each spectrum band by the total variance, minus the value of the very low frequency band (< 0.04 Hz), and multiplied by 100. To interpret the results, the LF and HF normalized components of HRV were considered as representative of predominantly sympathetic and parasympathetic modulation of the heart, respectively [31]. Although the respiratory rate is commonly controlled in HRV studies, this approach could disrupt the natural return of HR to baseline during recovery and for this reason, we chose not to do it and opted for a self-control study. However, the respiratory rate remained between 0.15–0.4 Hz.

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60 min) as factors. When necessary, the post-hoc of Newman-Keuls was performed for pairwise comparisons. For all analyses, a p value  0.05 was considered as statistically significant. Data were processed using the STATISTICA software version 10.0 (STATASOFT INC., Tulsa, OK, USA).

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3. Results

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Table 1 summarizes the characteristics of the participants enrolled in this study. None of the twelve volunteers reported any adverse events during or post-tDCS procedures such as headache, nauseas or vomit. Table 2 summarizes the comparisons of the hemodynamic and autonomic variables before each experimental session. No differences were observed for systolic, diastolic, and mean BP, as well as for any of the HRV parameters (p > 0.05), except for heart rate and RPP (p < 0.05). Figure 1 shows the systolic, diastolic and mean BP responses after resistance exercise sessions preceded by anodal tDCS or sham condition. In comparison with pre-exercise, systolic BP decreased in both 20th and 60th minutes after resistance exercise in tDCS condi-

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Fig. 2. Absolute changes of heart rate (panel A) and rate pressure product (panel B) after resistance exercise preceded by tDCS (black bars) or sham condition (white bars). *Different from sham condition.

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C Fig. 1. Systolic (panel A), diastolic (panel B), and mean BP (panel C) before and after resistance exercise preceded by tDCS (black bars) or sham condition (white bars). *Different from pre-exercise within tDCS condition.

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tion, however no changes were found in sham condition (F2,22 : 4.3; P < 0.03). In addition, individual results revealed that 5 out 12 subjects who did not experience hypotension in sham condition, experienced it in anodal tDCS condition. Diastolic (F2,22 = 1.28; p = 0.30) and mean BP (F2,22 = 1.97; p = 0.16)

presented similar responses within and between pre- to post-exercise comparisons. Figure 2 illustrates the absolute changes (post- minus pre-exercise) heart rate and RPP variations between anodal tDCS and sham conditions. It was observed faster HR (tDCS vs. sham: −2 ± 14 vs. 14 ± 8 bpm; t = −3.23; 95% CI: −25 to −8; P = 0.008) and RPP recovery to baseline (tDCS vs. sham: −1083 ± 1846 vs. 1672 ± 1275 mmHg × bpm; t = 4.65; 95% CI: −4059 to −1452; P = 0.01) in anodal tDCS than in sham condition. Figure 3 shows the autonomic responses after resistance exercise session followed or not by anodal tDCS. All HRV parameters responded similarly when resistance exercise was or was not preceded by anodal tDCS, with no interaction for LF (F2,16 = 1.045; P = 0.374), HF (F2,16 = 1.045; P = 0.374) and R-R intervals (F2,16 = 1.349; P = 0.287).

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4. Discussion

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The present study is perhaps the first to demonstrate the capability of a non-invasively brain stimu-

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by higher reductions in systolic BP when compared to pre-exercise responses and sham condition; and (ii) lowered heart rate variation and rate pressure product after resistance exercise session was observed in anodal tDCS condition, which means a lowered cardiac work to recovery in comparison with sham condition. The systolic BP has been shown to decrease after resistance exercise [3], but this might not occur in normotensive subjects [32,33]. Actually, greater PEH has been observed in subjects showing high baseline or pre-exercise BP levels [3], therefore normotensive subject are less inclined to be affected by PEH. Our results corroborate with these findings since no changes in systolic BP during post-resistance exercise recovery were observed compared to pre-exercise responses in sham condition. On the other hand, a single session of anodal tDCS over primary motor cortex targeting the left insular cortex was able to induce PEH. In this context, previous studies have been shown bradycardia and hypotension when the left cerebral hemisphere was directly stimulated [10]. Furthermore, decreases in neuronal activity of the right IC due to exercise have been indicated as a significant neural factor contributing to the PEH since low cerebral blood flow in IC was positively correlated to mean blood pressure reductions (r2 = 0.74) [11]. Our findings concur with these studies since the left motor cortex was non-invasively stimulated by anodic current polarity, while simultaneously the right cerebral hemisphere was depressed by cathodic current polarity through bi-cephalic tDCS montage. Taking into account that motor or temporal direct current stimulations were capable of modulating the neuronal activity of sub- and cortical projections to the heart (i.e. IC, nucleus of solitary tract and rostral ventrolateral medulla) [12,19,25], it is feasible to speculate that anodal tDCS over motor cortex was able to induce high neuronal excitability of cardiac autonomic centers and therefore, lowered systolic blood pressure responses and faster cardiac recovery after resistance exercise session were observed. However, these findings were not followed by modulations upon cardiac autonomic nervous system as seen by spectral analysis of HRV after exercise, which is in contradiction with our hypothesis. Considering the controversial effects of tDCS upon ANS [16,17,23,24], the mechanisms explaining how anodal tDCS applied over primary motor cortex could influence PEH regardless of cardiac autonomic control are only speculative. However, the exercise recovery in a seated position might elicit an accumulation of blood in the lower limbs, reducing venous return, and, con-

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C Fig. 3. Low frequency (panel A), high frequency (panel B), and RR interval (panel C) before and after resistance exercise preceded by tDCS (black bars) or sham condition (white bars). *Different from pre-exercise within condition.

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lation technique (i.e. anodal tDCS) in modulating the cardiac and hemodynamic responses induced by a single bout of resistance exercise. The main findings of the present study were: (i) a single anodal tDCS session applied over the left motor cortex during 20 min can potentiate the post-exercise hypotension as seen

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5. Conclusion

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The results of the present study indicated that releasing a single session of anodal tDCS over left motor cortex of the normotensive young subjects was able to induce a greater decrease in both systolic blood pressure and rate pressure product followed by faster heart rate recovery after resistance exercise. Additional studies should be encouraged to ratify these results and to help clarify the physiological mechanisms that underlie the modulations upon hemodynamic responses at rest and after exercise due to brain stimulation techniques.

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Acknowledgments

Financial support was provided by “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ)” and “Fundação de Ciência e Tecnologia do Estado de Pernambuco. (FACEPE)”.

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Conflict of interest The authors have no conflict of interest. References [1]

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sequently, decreasing BP. As a result, there is an increase in sympathetic drive to the heart and vasculature leading to vasoconstriction and tachycardia in order to compensate for the decrease in cardiac output. It is possible that the lower systolic BP, HR and RRP responses after resistance exercise induced by anodal tDCS (as seen in Figs 1 and 2) were likely due to a decrease in sympathetic vasoactivity. This speculation is based on findings by Clancy et al. [22] who observed the effectiveness of anodal tDCS applied over motor cortex in augmenting the sympathetic nerve activity to the muscle (assessed by microneurography). Unfortunately, the present study did not investigate the tDCS effects upon ANS in the vasculature or muscle sympathetic nerve activity, which limits any robust conclusion in regards to the potential tDCS effect on peripheral ANS. Perhaps the tDCS effects on cardiac autonomic centers may be dependent on physical fitness, and therefore the ANS of athletes may be more susceptible to tDCS effects than non-athletes, as revealed by previous study of our group [17]. Additional research is needed to confirm these findings.

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