Elsevier

Neuroscience Letters

Volume 687, 20 November 2018, Pages 131-136
Neuroscience Letters

Research article
Differential effects of high-definition transcranial direct current stimulation on verbal working memory performance according to sensory modality

https://doi.org/10.1016/j.neulet.2018.09.047Get rights and content

Highlights

  • High definition tDCS can target the area more definitely than conventional tDCS.

  • HD-tDCS was applied to the DLPFC on two different modality of verbal working memory.

  • Visual but not auditory verbal working memory was improved by the stimulation.

Abstract

Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation technique that modulates cortical excitability in a polarity-dependent manner. The diffuse nature of tDCS makes it difficult to investigate the optimal stimulation parameters for more effective and specific cognitive enhancement; to address this deficit, a more focalized stimulation technique, high-definition tDCS (HD-tDCS), has been developed. To date, only a few studies have examined the effects of HD-tDCS on cognitive functions; and none has investigated the effects of HD-tDCS on different sensory modalities of verbal working memory. Therefore, the present study compared the effects of prefrontal HD-tDCS on visual and auditory working memory tasks. Twenty healthy participants completed three sessions of each modality task, and additionally a sustained attention task. Anodal or sham HD-tDCS was administered to the dorsolateral prefrontal cortex (DLPFC) during the second session of the task in a parallel, single-blind design. Anodal stimulation to the DLPFC significantly enhanced the visual verbal working memory accuracy during and 20 min after the stimulation. In contrast, auditory verbal working memory performance was not modulated by anodal stimulation. Anodal stimulation to the DLPFC showed no effect on any other cognitive functions. The present study revealed the differential effects of HD-tDCS on two different modalities (visual vs. auditory) of working memory performance: important preliminary findings for the establishment of a more effective and specific use of tDCS.

Introduction

Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation technique characterized by portable size, relatively low cost and safety. In conventional tDCS, a weak direct current (1–2 mA) is delivered between two large pad electrodes (25 – 35 cm2) attached to the scalp (positively charged anode and negatively charged cathode). A single session of tDCS has been reported to modulate cortical excitability for over an hour in a polarity-dependent manner [[1], [2], [3]]. Two mechanisms of the effects of tDCS have been proposed. The first involves depolarization and hyperpolarization of the resting membrane potential during anodal and cathodal stimulation. The second involves long-term potentiation (LTP) -like and long-term depression (LTD) -like neuroplastic changes after anodal and cathodal stimulation [4]. These neuromodulatory effects are also thought to underlie enhancement in learning and memory by tDCS. Extensive research has demonstrated that tDCS can enhance multiple cognitive functions such as executive function, learning and memory in both neuropsychiatric and healthy individuals [5,6,7]. However, the conventional large-pad electrode montage produces diffuse current flow through the brain [8,9], making it difficult to investigate the causal relationship between brain activity in the targeted region and behavior.

Recently, high-definition tDCS (HD-tDCS) has been developed to achieve more focalized stimulation using a 4 × 1 ring electrode configuration with an active center electrode on the targeted area surrounded by 4 reference electrodes [8,10]. HD-tDCS has also been shown to modulate cortical excitability in a polarity-dependent manner, and the excitability change lasted longer than conventional tDCS [3,11]. Although these findings in the motor cortical excitation have been established, only a few studies have examined the effects of HD-tDCS on cognitive functions, reporting that HD-tDCS to the dorsolateral prefrontal cortex (DLPFC) facilitated the rate of verbal learning, working memory speed [12], memory monitoring [13] and adaptive cognitive control [14] in comparison to the sham stimulation condition. More studies are needed to acquire detailed evidence about the effects of HD-tDCS on different cognitive functions and the optimal stimulation protocols for more effective and specific cognitive enhancement.

In the present study, we targeted the DLPFC because of its critical role for executive functions, especially working memory. The DLPFC is responsible for the maintenance, manipulation and integration of information in working memory [15,16]. Although working memory is an especially critical cognitive function [17,18] and the effects of tDCS on working memory have been explored in a number of studies [7,16,19], no published study has explored the potential differences in modality effects, e.g., visual versus auditory. The present study investigated the effects of prefrontal HD-tDCS on two different types (visual vs. auditory) of verbal working memory (VWM) as well as sustained attention. To this end, participants were randomly selected to receive active (excitatory anodal) or sham (placebo) stimulation; in addition, they performed visual and auditory VWM tasks before, during and 20 min after the stimulation to reveal the modality specificity in the effects of prefrontal HD-tDCS. Participants also performed a sustained attention task, as prefrontal tDCS enhanced sustained attention performance in several studies, and sustained attention may affect working memory task performance [20,21]. The results obtained in the present experiments will be useful for the establishment of more effective and tolerable use of tDCS required for basic studies to understand the cognitive processing in specific brain areas as well as clinical applications in neuropsychiatric patients such as attention-deficit hyperactivity disorder and schizophrenia. Moreover, the present study provided, to our knowledge, the first direct comparison of modality specificity in the effects of tDCS on working memory by assessing prefrontal HD-tDCS effects on both visual and auditory VWM performance using the same experimental paradigm.

Section snippets

Participants

Twenty healthy right-handed participants (age 22.7 years ± 4.2, 10 females) were recruited for the experiment. The participants were randomly assigned to either sham (n = 10) or active (n = 10) conditions. Exclusion criteria were as follows: history of adverse reactions to transcranial magnetic stimulation (TMS) or tDCS, history or family history of seizure or stroke, history of severe head injury or brain surgery, any current psychiatric or neurological disorders, concurrent medication that

Participants and blinding

Twenty participants completed the study and all data were included in the analysis. Gender (sham, 5 females; active, 5 females) and age (sham, 22.2 ± 4.9; active, 23.1 ± 3.5) were closely matched between conditions. There was also no significant difference in baseline cognitive performance between sham- and active-condition participants. Cognitive performance data for all tasks are shown in the supplementary material (Table S1). Blinding was also assessed, asking participants to guess whether

Discussion

The present study revealed the effects of prefrontal HD-tDCS on different modalities of verbal working memory. HD-tDCS to the left DLPFC enhanced visual but not auditory 3-back task accuracy during and after the stimulation. There was a trend towards improved reaction time in visual 3-back task, suggesting that the significant enhancement of visual VWM accuracy by prefrontal HD-tDCS was not due to a speed-accuracy trade-off. Sustained attention assessed by the modified version of RVIP task

Declaration of interest

The authors declare no conflicts of interest with regard to this manuscript.

Acknowledgements

The authors would like to thank MS. Rieko Kimura and Ms. Aya Kato for their research assistance. The authors are also grateful for the funding from the Academic Contributions from Pfizer Japan Inc.

References (29)

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    18 studies addressed the effect of anodal tDCS on N-Back performance. Although two studies found a positive effect of anodal tDCS on N-Back performance (Fregni et al., 2005; Lally et al., 2013), 13 studies (Dumont et al., 2018; Friehs and Frings, 2019b; Keshvari et al., 2013; Lukasik et al., 2018; Mashal and Metzuyanim-Gorelick, 2019; Naka et al., 2018; Nikolin et al., 2017; Ohn et al., 2008; Röhner et al., 2018; Talsma et al., 2017; Teo et al., 2011; Trumbo et al., 2016; Xu et al., 2015) found no effect. Surprisingly, four studies (Keshvari et al., 2013; Steenbergen et al., 2016; Trumbo et al., 2016; Wang et al., 2018) found that anodal tDCS negatively affected N-Back performance.

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