The effect of tDCS applied to the dorsolateral prefrontal cortex on cycling performance and the modulation of exercise induced pain

Highlights

• Anodal tDCS is proposed to reduce naturally occurring pain associated with exercise.

• The effects of DLPFC tDCS on the rating of exercise-induced pain have not been examined.

• Two studies were conducted to assess differences in DLPFC electrode montage.

• Neither DLPFC electrode montage reduced pain or improved time trial performance.

Abstract

Transcranial direct current stimulation (tDCS) is a neuromodulatory tool purported to enhance endurance performance through reducing fatigue related perceptions, including exercise-induced pain (EIP). We examined whether tDCS of the left DLPFC (1) can reduce EIP during a fixed intensity cycling trial (FI), (2) can improve cycling time trial (TT) performance, and (3) whether this was affected by a bilateral or an extracephalic montage. This investigation was comprised of two parts (study one and two). In both studies, participants completed a 10-minute FI trial and a 15-minute TT after 10 min of 2 mA anodal left DLPFC tDCS, SHAM or no stimulation. In study one, 11 participants received tDCS via a bilateral montage. In study two, 20 participants received tDCS using an extracephalic montage. Pain was recorded throughout the FI and TT trials, with power output (PO) monitored during the TT. Study one saw no significant changes in pain (tDCS 4.3 ± 2.0; SHAM 4.0 ± 1.8; control 3.8 ± 1.4) during the FI trial and no significant differences in distance covered, pain or PO in the TT. In study two there were no differences in pain reported in the FI trial, or distance covered (P = 0.239), pain or PO in the TT. In summary, tDCS of the DLPFC did not induce analgesia and provided no ergogenic effect for TT performance, moreover these observations were consistent across both the extracephalic and bilateral montage. These findings are in line with an increasing number of studies demonstrating the inconsistent effects of tDCS.

Introduction

Transcranial direct current stimulation (tDCS) is often used in the treatment of various neuropsychiatric disorders [1]. In healthy populations, tDCS is also used to investigate cognitive functions [2] and enhance physical performance [3]. Originally it was presumed that tDCS influences neuronal excitability in a polar dependent fashion [4]. However, the response to tDCS is more complex than this due to the intricate relationship between the non-linearity of the dose response and a multitude of inter-and-intra-individual differences [[5], [6], [7]]. Changes in neuronal excitability are presumed to produce an ergogenic effect through enhancing synergistic muscle coupling and attenuation of decline in motor cortex (M1) excitability [8]. However, due to inconsistencies within research design and reported outcomes, the exact mechanisms remain inconclusive [3].

Tolerance of exercise-induced muscle pain (EIP) influences time trial performance [9], with improvements in performance shown when pain is reduced [10,11]. As tDCS of the M1 and the dorsolateral prefrontal cortex (DLPFC) in a cephalic montage (anode over left M1 or DLPFC, cathode over right supraorbital area) has been successfully used to treat acute and chronic pain in patient groups [12,13] it is plausible that tDCS induced analgesia could confer an ergogenic effect in exercise with healthy individuals. Applying tDCS to the M1 in an extracephalic montage (Anode: M1, cathode: ipsilateral shoulder) can improve exercise tolerance through a reduction in perceptual stimuli such as the sense of effort [14], but tDCS may be less effective in reducing EIP [15]. Indeed, analgesia during a cold pressor test [15] and enhanced conditioned pain modulation [16] has been observed following conventional [15] and high-definition [16] M1 tDCS, despite no changes in EIP [15,16]. However, experimental pain and EIP are different [17] so M1 tDCS may be more effective in moderating pain of type III afferent origin [18]. Indeed, EIP is commonly described as an aching or burning (akin to type IV afferent stimulation) so M1 tDCS may be less effective in reducing EIP [15]. However, stimulating the dorsolateral prefrontal cortex (DLPFC) can induce analgesia [19,20], and has been used to treat chronic pain disorders [20], increase pain tolerance and empathy to experimental pain [19]. The DLPFC is a fundamental structure for nociceptive control, modulation of emotional valences, attention and working memory [18,[21], [22], [23]] and houses reciprocal connections to the M1 [18]. tDCS applied to the left DLPFC in a cephalic montage has been shown to reduce effort/pain related perceptions during resistance exercise [24], so anodal tDCS applied to the DLPFC may serve as an effective means to reduce EIP and thus enhance endurance performance.

The direction of current flow is determined by the montage of the tDCS electrodes. Finite Element Method modelling studies have demonstrated that traditional M1 cephalic montages (anode: placed over left M1, cathode: placed over the right supraorbital area) induces greater current densities within the prefrontal cortex [25]. Therefore, the cephalic montage used by Angius et al. [15] could have induced unintended reductions in excitability of the right DLPFC, and produced changes in performance unrelated to EIP. Alternatively, using an extracephalic (one electrode placed over the brain region of interest with the other placed on a non-brain area such as the deltoid) and/or bilateral (placement of the electrodes symmetrically across both hemispheres) montage could maintain a localised current flow in the targeted area [25,26]. Indeed, when an extracephalic montage was used, tDCS improved isometric [8,14] and dynamic [27] exercise time to exhaustion.

This study tested whether anodal left DLPFC tDCS would enhance performance of a 15 min cycling time trial. An additional 10 min fixed intensity trial was used to examine whether tDCS would improve EIP tolerance, as time trials do not usually identify perceptual changes arising from ergogenic interventions [11]. Finally, this study explored whether a bilateral or extracephalic montage changed the response to these tests.