Cognitive neuroscience and neuropsychology 1433

Beta-frequency EEG activity increased during transcranial direct current stimulation Myeongseop Songa,b, Yungjae Shinb and Kyongsik Yunb,c Transcranial direct current stimulation (tDCS) is a technique for noninvasively stimulating specific cortical regions of the brain with small (< 2 mA) and constant direct current on the scalp. tDCS has been widely applied, not only for medical treatment, but also for cognitive and somatosensory function enhancement, motor learning improvement, and social behavioral change. However, the mechanism that underlies the effect of tDCS is unclear. In this study, we performed simultaneous electroencephalogram (EEG) monitoring during tDCS to understand the dynamic electrophysiological changes throughout the stimulation. A total of 10 healthy individuals participated in this experiment. We recorded EEGs with direct current stimulation, as well as during a 5-min resting state before and after the stimulation. All participants kept their eyes closed during the experiment. Anode and cathode patches of tDCS were placed on the left and the right dorsolateral prefrontal cortex, respectively. In addition, an EEG electrode was placed on the medial prefrontal cortex. The betafrequency power increased promptly after starting the stimulation. The significant beta-power increase was maintained during the stimulation. Other frequency bands

Introduction Transcranial direct current stimulation (tDCS) is a method that can noninvasively stimulate specific cortical regions of the brain with weak and constant direct current (DC) on the scalp [1]. tDCS has been used for the treatment of various brain disorders, including Alzheimer’s disease [2], depression [3], attention deficit hyperactivity disorder [4], and different kinds of addictions, including alcohol and substance abuse [5]. tDCS has also been applied for cognitive enhancement, including that of working memory [6] and motor learning [7]. Recent advances in tDCS studies include cortical–subcortical network stimulation and [8] application to social behavioral change [9]. However, the underlying mechanisms of tDCS have rarely been investigated. A previous study found that DC stimulation increased brain-derived neurotrophic factor levels, which induces synaptic plasticity [10]. The most accepted theory so far is that tDCS induces polaritydriven alterations in resting membrane potentials, which can result in spontaneous depolarization (anode) or hyperpolarization (cathode) [11]. Moreover, we have no clue about what is happening in the brain while stimulating it. There is one study that showed that the number of epileptiform electroencephalogram 0959-4965 © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins

did not show any significant changes. The results indicate that tDCS of the left dorsolateral prefrontal cortex changed the brain to a ready state for efficient cognitive functioning by increasing the beta-frequency power. This is the first attempt to simultaneously stimulate the cortex and record the EEG and then systematically analyze the prestimulation, during-stimulation, and poststimulation EEG data. NeuroReport 25:1433–1436 © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins. NeuroReport 2014, 25:1433–1436 Keywords: electroencephalogram, resting state, transcranial direct current stimulation a Department of Bio and Brain Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon, bYbrain Research Institute, Seoul, South Korea and cComputation and Neural Systems, California Institute of Technology, Pasadena, California, USA

Correspondence to Kyongsik Yun, PhD, Computation and Neural Systems, California Institute of Technology, 1200 E. California Blvd. MC139-74, Pasadena, CA 91125, USA Tel: + 1 626 415 7556; fax: + 1 626 792 8583; e-mail: [email protected] Received 1 September 2014 accepted 23 September 2014

(EEG) discharges reduced while patients with focal refractory epilepsy were stimulated with DC [12]. This study is, as far as we know, the first to analyze the EEG signal with concomitant DC stimulation. They used multichannel EEG to observe the interaction between current stimulation and the neural network. However, they just counted the number of epileptiform EEG discharges with raw EEG data, without analyzing detailed EEG dynamics, such as EEG power spectra and frequency coupling. They collected EEG data from just two patients requiring further study [12]. In this study, we concomitantly recorded EEG changes with tDCS in the prefrontal cortex. We hypothesize that the beta-frequency EEG activity would be enhanced during and after stimulation. Beta rhythms have been known to operate cognitive functions [13], and the cognitive performance enhancement is one of the main tDCS effects [6].

Methods Ethics statement

All participants submitted written informed consent after receiving a detailed explanation of the experimental procedures. This study was approved by the Institutional Review Board of the Ybrain Research Institute. DOI: 10.1097/WNR.0000000000000283

Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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After the experiment, the participants were interviewed about their feelings, such as discomfort and pain during and after the stimulation.

skin preparation, anode and cathode hydrogel patches were placed on the left (F3) and right (F4) dorsolateral prefrontal cortices (DLPFCs), respectively (EEG 10–20 system), whereas an EEG recording electrode was positioned on the medial prefrontal cortex (MPFC) in between Fp1 and Fp2 (EEG 10–20 system; Fig. 1a). We placed the reference and ground electrodes on the right mastoid. In this experiment, the current intensity of 1 mA was maintained for 10 min; the current was slowly increased up to 1 mA for 15 s at first and was slowly decreased for 15 s and turned off at the end of the stimulation. EEGs of the participants were recorded for a total of 30 min, separated by three periods. For the first 10 min, EEGs were recorded at the resting state. For the next 10 min, EEGs were measured during DC stimulation. Finally, the resting state EEGs were recorded for 10 min. During every period, participants kept their eyes closed. EEGs were recorded in 500 Hz, and the recording impedance was kept under 10 kΩ. We used OpenViBE software (Campus de Beaulieu, Rennes Cedex, France) for EEG data acquisition [15].

Transcranial direct current stimulation and electroencephalogram recording

Data analysis

DC stimulation was applied through hydrogel patches (rectangular shape: 5 cm × 5 cm = 25 cm2). Scalp preparation included investigation of skin condition and reduction of skin impedance. When investigating skin condition, we checked for rashes or pre-existing lesions to avoid skin burns by DC stimulation. Second, we used wet tissue to reduce impedance of the skin to under 40 kΩ (during tDCS, impedance was maintained under 20 kΩ), resulting in pain reduction on tDCS and decreased noise for cleaner EEG recording [14]. After

We divided the spectrum of EEG signals into six frequency bands: delta (1–4 Hz), theta (4–8 Hz), slow alpha (8–10 Hz), fast alpha (10–13.5 Hz), beta (13.5–30 Hz), and gamma (30–80 Hz). We obtained the power spectrum of the EEG data by short-time Fourier transform with 250-ms Hamming windows and a nonoverlap. After the short-time Fourier transform of each participant’s EEG data, we took the log of the frequency bands’ power, and these log values were divided by the max value of each frequency band to see the trend of each frequency band’s

Participants

A total of 10 healthy participants (five women, mean age of 23.6 ± 2.5 years) were recruited through an online advertisement in Seoul, South Korea. Participants had at least 14 years of education (16.6 ± 2.5 years). All participants were medication free and psychiatric illness free and did not take any medication on the day of the experiment. Experiment protocol

Each participant was seated on a comfortable chair and was fitted with tDCS and one-channel EEG equipment (Fig. 1a). After installation, we recorded resting state EEG with the eyes closed for 10 min. Next, we stimulated the brain by tDCS while simultaneously recording EEG for 10 min. Finally, we again recorded resting state EEG with the eyes closed for 10 min.

Fig. 1

(a)

(b) 1.3

tDCS

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Beta-frequency EEG activity increased during transcranial direct current stimulation.

Transcranial direct current stimulation (tDCS) is a technique for noninvasively stimulating specific cortical regions of the brain with small (...
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