Neither Cathodal nor Anodal Transcranial Direct Current Stimulation on the Left Dorsolateral Prefrontal Cortex alone or Applied During Moderate Aerobic Exercise Modulates Executive Function

Highlights

• Testing synergies between tDCS and exercise.

• No replication of current findings regarding the effects of tDCS or aerobic exercise on executive functions.

• Multimodal approach (tDCS+aerobic exercise) did not lead to any further improvements.

• Cathodal tDCS during aerobic exercise modulated perceived exertion.

Abstract

There is converging evidence that both aerobic exercise (AE) and transcranial direct current stimulation (tDCS) can acutely modulate executive functions (EF). In addition, recent studies have proposed the beneficial effects of applying tDCS during AE on physical performance. This study aimed to investigate whether tDCS applied during an AE session additionally or differently effects EF. Therefore, five experiments were conducted in a counterbalanced pre-post-retention crossover design to explore the acute effects of tDCS and AE on EF (inhibition and updating) once in isolation (i.e., either cathodal, anodal tDCS or AE alone as controls) and once in a combined application (i.e., anodal and cathodal tDCS during AE versus sham tDCS during AE). No differences were found in any experiment in the cognitive test parameters. However, in the case of anodal tDCS vs. sham during AE, heart rate was significantly affected. For cathodal tDCS vs. sham during AE, a significant Anova interaction indicated that cathodal tDCS during AE slightly reduced ratings of perceived exertion. The nonsignificant effects of tDCS on EFs are in contrast to previous studies, as no replication of existing observations could be achieved. Thus, the protocol applied in this study does not provide any strong evidence that a combination of AE and tDCS has any effects on EFs, but indicates effects on physiological parameters and subjective exhaustion ratings. Further research should consider changes in AE and tDCS parameters (e.g., intensity or exercise mode) and sequence of applications (online vs. offline).

Introduction

Executive functions (EF) such as the three EFs inhibition, updating and switching defined by Miyake et al. (2000) are essential abilities in mental and physical health. They play a pivotal role in cognitive, social, and psychological development and are needed to accomplish daily tasks. Quality of life can decline in the case of impaired EFs, e.g., due to neurological or psychiatric disorders or age-related decline. Due to such examples, recently, an increasing need for noninvasive, harmless, and easily applicable methods has emerged (De Hert et al., 2012), to not only treat EF deficits but maintain and even train EF performance. Despite cognitive training approaches, transcranial direct current stimulation (tDCS) (Dedoncker et al., 2016, Imburgio and Orr, 2018) and physical exercise (Verburgh et al., 2014, Northey et al., 2018) are methods that can positively modulate executive functioning. However, given small effect sizes and limited evidence for long-term changes in both treatments, it would be desirable to increase the effectiveness of both methods, such as that proposed by multimodal treatment approaches (Hendrikse et al., 2017, Ward et al., 2017). Indeed, multimodal intervention experiments (e.g., Ward et al., 2017) combining brain stimulation (tDCS) and physical exercise have shown superior effects compared to single interventions on cognitive functions. However, despite potential benefits, a direct combined treatment, such as the application of tDCS during exercise, has not been systematically performed in the context of EF improvements (Steinberg et al., 2019), although effectivity on combining tDCS and physical exercise has been shown to reduce pain (e.g., Medonca et al., 2016) and increase sport performance (e.g., Angius et al., 2019).

tDCS is a noninvasive neuromodulatory brain stimulation technique that delivers a weak electrical current directly and continuously to the target brain area by electrodes positioned on the scalp (Nitsche and Paulus, 2000, Lattari et al., 2016). The primary effects of tDCS seem to originate from polarity-specific membrane polarization of cortical neurons. Anodal tDCS (a-tDCS) is associated with increased cortical excitability, while cathodal tDCS (c-tDCS) produces the reversed effect (Nitsche and Paulus, 2000). Despite justified objections by Horvath et al. (2015), there is some evidence in the present literature that a single session of a-tDCS leads to an improvement in cognitive functions in health and disease (Jacobson et al., 2012, Flöel, 2014, Tremblay et al., 2014, Dedoncker et al., 2016, Summers et al., 2016, Strobach and Antonenko, 2017, Imburgio and Orr, 2018). Following this line, Strobach and Antonenko (2017) reviewed that the performance of all three core EFs (inhibition, updating, and shifting) can be enhanced with tDCS over the prefrontal cortex (PFC). More specifically, when tDCS is applied for 10–30 min over the dorsolateral prefrontal cortex (DLPFC) with a current between 1 mA and 2 mA, a-tDCS improved the working memory performance (Fregni et al., 2005, Andrews et al., 2011, Teo et al., 2011, Zaehle et al., 2011, Hoy et al., 2013, Meiron and Lavidor, 2013). Moreover, a-tDCS over the DLPFC lasting 10–30 min improved inhibition (i.e., faster reaction time [RT]) in a flanker task, go/no-go task, stop task, and stroop task paradigms (Jacobson et al., 2012, Kwon et al., 2013, Loftus et al., 2015, Hogeveen et al., 2016, Angius et al., 2019, Dubreuil-Vall et al., 2019), while, for both left and right DLPFCs and different stimulation protocols, effects on EFs have been documented (Strobach and Antonenko, 2017, Steinberg et al., 2019).

Several reviews and meta-analyses indicate that EFs benefit from bouts of AE (Lambourne and Tomporowski, 2010, Chang et al., 2012, Ludyga et al., 2016, Basso and Suzuki, 2017, Mandolesi et al., 2018). For EF inhibition, 20 min of moderate AE resulted in significantly better task performance for the stroop test (Chang et al., 2015) and the Flanker task (Davranche et al., 2009). Regarding updating, Pontifex et al. (2009) showed a significant decrease in RT after 30 min of running at 60–70 % of VO_2max in the modified Sternberg working memory task compared to resistance training or inactivity. Furthermore, Weng et al. (2015) demonstrated increased accuracy in a 2-back task after 30 min of moderate-intensity aerobic cycling.

So far, a few studies have investigated whether a combination of both methods is applicable to synergize effects on study outcomes. Mendonca et al. (2016) observed optimized analgesic responses (pain relief) in fibromyalgia when tDCS was applied while running on a treadmill with significant effects on pain, anxiety, and mood compared to single interventions. Ward et al. (2017) demonstrated the effects of combined methods on cognition during a 16 week intervention. Their multimodal training (computerized game training + physical exercise + tDCS) led to significantly enhanced performance in updating and shifting tasks compared to unimodal pieces of training.

Recently, Steinberg et al. (2019) postulated that AE might be capable of positively interacting with tDCS. One of their hypotheses is that AE may serve as a brain primer to enhance the effect of tDCS interventions, possibly through an increased brain-derived neurotrophic factor (BDNF) level, and that other levels of neurochemicals, such as dopamine, may create optimal conditions for brain plasticity (Huang et al., 2014). AE performed directly before (or during) tDCS application over the DLPFC could therefore result in better cognitive outcomes compared to each method alone. To date, only one recent study by Hendy et al. (2019) tested this hypothesis but the combined protocol did not lead to enhanced post-exercise cognitive performance, potentially due to the selected high-intensity AE protocol and/or the participants tested (sedentary lifestyle; people with a high fitness level were more likely to exhibit greater post-exercise increase in EFs; Basso and Suzuki, 2017).

Given the current findings of the modulating capacity of either acute moderate AE intensity sessions and tDCS on EFs, this study primarily aimed to systematically explore whether the combined intervention (tDCS concurrent with AE) affects EFs differently compared to single interventions (tDCS/AE alone) and control conditions (inactivity/sham tDCS). We hypothesized that 20 min of moderate AE with simultaneous tDCS improves EF beyond the level of single interventions, while control conditions have no effect on cognitive performance. More specifically, we expect that a-tDCS + AE increases cognitive performance, while c-tDCS + AE could lead to either maintained or decreased cognitive performance compared to the single interventions (i.e., sham tDCS + AE).