Acta Psychologica 146 (2014) 1–6

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The influence of theta transcranial alternating current stimulation (tACS) on working memory storage and processing functions Norbert Jaušovec 1, Ksenija Jaušovec ⁎, Anja Pahor Univerza v Mariboru, Filozofska fakulteta, Koroška 160, 2000 Maribor, Slovenia

a r t i c l e

i n f o

Article history: Received 25 July 2013 Received in revised form 11 November 2013 Accepted 29 November 2013 Available online 18 December 2013 PsycINFO codes: 2343 Keywords: Working memory tACS Theta frequency Fronto-parietal network

a b s t r a c t The study aimed to explore the role of the fronto-parietal brain network in working memory function—in temporary storage and manipulation of information. In a single blind sham controlled experiment 36 respondents solved different working memory tasks after theta transcranial alternating current stimulation (tACS) was applied to left frontal, left parietal and right parietal areas. Both verum tACS protocols stimulating parietal brain areas (target electrodes positioned at location P3, or P4) had a positive effect on WM storage capacity as compared with sham tACS, whereas no such influence was observed for the stimulation of the left frontal area (target electrode positioned at location F3). A second finding was that left parietal theta tACS had a more pronounced influence on backward recall than on forward recall, which was not related to task content (spatial or verbal). The influence of theta tACS on WM executive processes was most pronounced for right parietal stimulation. The results are discussed in the broad theoretical framework of the multicomponent model of working memory. © 2013 Elsevier B.V. All rights reserved.

1. Introduction The psychological construct of working memory (WM) refers to a system that temporary holds or manipulates information we have just experienced, or retrieved from long-term memory (Cowan, 2001; Miyake & Shah, 1999). The majority of WM definitions encompass both, storage and processing components which are also integrated in the two most accepted models of WM —Baddeley's multiple-component system (Baddeley, Allen, & Hitch, 2011; Baddeley and Hitch, 1974), and Cowan's embedded processes model (Cowan, 2001, 2011). From the neuropsychological perspective, the fronto-parietal network has been associated with working memory tasks (e.g., Chein & Fiez, 2010; Jonides et al., 2008; Palva, Monto, Kulashekhar, & Palva, 2010; Posner, 1990). It has been further suggested that the central executive function of WM is linked to frontal lobes whereas the WM storage component is associated with parietal areas (Champod & Petrides, 2010; Collette & Van der Linden, 2002; Olson & Berryhill, 2009; Sauseng, Griesmayr, Freunberger, & Klimesch, 2010). Based on the evidence from several brain imaging studies (Cowan, 2011; Cowan et al., 2011; Majerus et al., 2006, 2010; Todd & Marois, 2004; Xu & Chun, 2006), the left intraparietal sulcus (LIS) has been identified as unique for amodal or multimodal storage of information. Support for a fronto-parietal distinction related to the WM functions of processing and storing of

⁎ Corresponding author. E-mail address: [email protected] (N. Jaušovec). 1 Fax: +386 2 258180. 0001-6918/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.actpsy.2013.11.011

information comes also from research employing neuroelectric brain imaging methods (Klimesch, 1999, 2012; Klimesch, Freunberger, Sauseng, & Gruber, 2008; Sauseng et al., 2010). These studies showed that theta oscillations relate to working memory processes and that theta synchronizes during WM processes as well as acts as a gating mechanism, providing optimal neural conditions for specific processing (Sauseng et al., 2010). An alternative perspective has suggested that the dorsolateral region of the prefrontal cortex (DLPFC) supports storage as well as processing of WM functions (Courtney, 2004; Leung, Seelig, & Gore, 2004; Pessoa, Gutierrez, Bandettini, & Ungerleider, 2002) and that short term storage and manipulation of information actually activate the same brain areas (Veltman, Rombouts, & Dolan, 2003). Several neuroimaging studies (Narayanan et al., 2005; Veltman et al., 2003; Zarahn, Rakitin, Abela, Flynn, & Stern, 2005) have supported this viewpoint. To date, it seems that neuroimaging studies cannot clarify the conflicting perspectives on the role of the frontal and parietal brain areas in WM function. The recent rediscovered noninvasive brain stimulation techniques for inducing reversible changes in brain activity have become a valuable tool to investigate the underlying mechanisms of human cognition (Kuo & Nitsche, 2012). Thus far, three main forms of low-intensity transcranial electrical stimulation have been used (for review, see Kuo & Nitsche, 2012; Utz, Dimova, Oppenländer, & Kerkhoff, 2010; Zaghi, Acar, Hultgren, Boggio, & Fregni, 2009): transcranial direct current stimulation (tDCS; a method in which low-intensity constant current is applied to the head), transcranial alternating current stimulation (tACS in which low-intensity alternating current is applied to the head), and transcranial random noise stimulation (tRNS in which electrical stimulation is

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applied within a broad frequency spectrum (0.1–640 Hz) with random noise distribution). Most of the transcranial stimulation studies investigating the effects on WM performance stimulated the left DLPFC (Boggio et al., 2006, 2008; Fregni et al., 2005; Mulquiney, Hoy, Daskalakis, & Fitzgerald, 2011; Utz et al., 2010; Zaehle, Sandmann, Thorne, Jäncke, & Herrmann, 2011). Stimulation increased WM performance on different storage-and-processing tasks (e.g., n-back speed of performance and accuracy; accuracy in a visual recognition and in a sequential-letter working memory task). In contrast, tRNS did not influence WM performance on an n-back task (Mulquiney et al., 2011). To our knowledge just one study (Fregni, Boggio, Nitsche, Rigonatti, & Pascual-Leone, 2006) investigated the influence of tDCS of the left DLPFC on WM storage capacity (digit span forward and backward), showing a significant increase in digit-span after tDCS. However, a generalization of this finding with regard to the relationship between the left DLPFC and WM storage capacity is difficult for two reasons. First, respondents who participated in the study were patients with depression, and second, the individuals were not exposed to verum and sham conditions. Much less research has been conducted into stimulating parietal brain areas. Jacobson, Ezra, Berger, and Lavidor (2012) used anodal tDCS over the left intraparietal sulcus which had a positive effect on a verbal recognition memory task. In a second study Polanía, Nitsche, Korman, Batsikadze, and Paulus (2012) could show that left frontoparietal coupling in the theta band (00 phase tACS) increased speed of performance on a delayed letter discrimination task as compared to a sham condition. In a repetitive transcranial magnetic stimulation (rTMS) study it was shown that disruptive rTMS had a more pronounced influence on WM storage capacity when applied to parietal areas than when applied to DLPFC (Postle et al., 2006). The aim of the present study is to further explore the relationship between working memory functions (e.g., storage capacity and executive processes like: inhibition of irrelevant items, monitoring of ongoing performance and updating representations in memory) and brain activity in frontal and parietal areas. For that purpose we analyzed the influence theta tACS (delivered to left/right parietal and left frontal brain areas) has on the performance of various tasks of WM storage capacity and executive processes. The nature of the study was exploratory. Our general hypothesis was that transcranial alternating current stimulation of different brain areas would be reflected in respondents' performance of WM tasks. 2. Method 2.1. Subjects The sample included 36 right-handed individuals (27 females; average age = 20 years and 5 months; SD = 4.25 months), recruited from

a group of students participating in a large scale resting eyes closed EEG study. They were divided into three groups—left frontal, left parietal and right parietal—receiving tACS with target electrodes placed over left frontal, left parietal or right parietal sites (see Fig. 1). The respondents of the three groups were equalized with respect to sex and performance on Wechsler (1981), digit span task administered prior to the experiment (left parietal group: M = 7.00; SD = 1.00; right parietal group: M = 6.88; SD = 0.93; left frontal group: M = 6.96; SD = 1.32). The respondents had a similar educational background, taking no medication and reporting no medical treatments or health problems. The experiment was undertaken with the understanding and written consent of each subject, following the recommendations of the ethics committee of the Slovene Psychological Association. 2.2. Design The study was a single blind sham controlled experiment. Dependent variables were the aggregated outcome measures from the different memory tasks used and were based on Baddeley's (Baddeley et al., 2011) multi-component WM model which represents a broad theoretical framework allowing for experimental testing. The analysis of data was hierarchical. Starting by testing the influence of the three tACS protocols on storage and executive processes represented in the multi-component model as the episodic buffer and central executive. In the second step we separately analyzed the storage and executive control functions: (1) the influence of tACS protocols on spatial/verbal, and forward/backward storage capacity, and (2) the influence of tACS protocols on executive control. 2.3. Tasks and procedure Respondents participated in 2 sessions—a sham and a verum tACS setting which were counterbalanced. The sham and verum settings were separated by 28 days. This time delay was needed to ensure that females on sham and verum settings were tested on the same day of their menstrual cycle. It was shown that the relative release of sexual hormones in different phases of the menstrual cycle affected cognitive responses of females (e.g., Amin, Epperson, Constable, & Canli, 2006; Berman et al., 1997). The duration of the menstrual cycle was determined with a questionnaire administered after the first tACS session. Most of the female participants had a regular 28 day menstrual cycle (M = 28.42 days; SD = 0.73 days). In each setting respondents were exposed to sham/verum tACS for 15 min, then answered a questionnaire about their sensations during stimulation, after which they solved the WM tasks. The order of task presentation was rotated between respondents, but was the same for each subject in the sham and verum setting. All tasks were presented

Fig. 1. Position of target electrodes (square) and return electrode (rectangle) for the three tACS protocols.

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on a computer monitor. The tasks used were: (1) the forward and backward Corsi block-tapping tasks, a measure of spatial WM capacity (Corsi, 1972). In this task nine blue squares were presented on a screen. On each trial the squares were lit up one at a time in sequence. The respondents had to click on each square in the same order they were given (forward) or in the reverse order (backward). (2) The forward and backward digit-span tasks, a measure of verbal WM capacity (Wechsler, 1981). The task consisted of a sequence of digits, which were presented one at a time. The subjects had to type the list of digits in exactly the same order as presented (forward), or in a reverse order (backward). (3) n-back tasks were the same as used by Jaeggi, Buschkuehl, Jonides, and Perrig (2008). In these tasks, participants saw two series of stimuli that were synchronously presented at the rate of 2000 ms per stimulus. One string of stimuli consisted of single letters (presented aurally), whereas the other was blue squares in different spatial locations. Respondents had to decide whether the current stimulus matched the one that was presented n items back in the series. We used 5 strings with 1-back, 2-back, and 3-back series consisting of 20 items per string. For each WM storage task (1–2) a WM memory span score was determined. For each series of the n-back tasks the number of correct responses (corrected for wrong responses) was determined. On average the time needed by respondents to complete the session was between 30 min–40 min.

2.4. Electrical stimulation tACS was applied via two sponge electrodes (approx. 5 × 7cm/ 35 cm2; Neuroconn, Ilmenau, Germany), attached to the head underneath an EEG recording cap (see Fig. 1). The target electrode was placed over the left parietal location (P3), the left frontal location (F3), or the right parietal location (P4), and the return electrode was placed above the right eyebrow. These specific brain areas were stimulated because research has shown that they play a key role in different WM processes (Andrews, Hoy, Enticott, Daskalakis, & Fitzgerald, 2011, Fregni et al., 2005, 2006; Polanía et al., 2012; Postle et al., 2006). The waveform of the stimulation was sinusoidal without DC offset and a 00 relative phase. The impedance was kept below 10 kΩ. We applied oscillating theta currents adjusted to the individual alpha peak frequency (IAF) of each participant. IAF was determined by averaging peak alpha frequencies of all 19 electrodes during eyes closed resting EEG recording (left parietal group: theta = IAF—5 Hz; M = 5.07; SD = 1.25; right parietal group: theta = IAF—5 Hz; M = 5.68; SD = .87; left frontal group: IAF—5 Hz; M = 4.69; SD = 0.69). tACS was delivered using a battery-operated stimulator system (DC-stimulator plus, Neuroconn, Ilmenau, Germany). In the verum condition tACS was applied for 15 min. The current was ramped up and down over the first and last 15 s of stimulation. In the sham condition, the procedure and stimulation characteristics (current magnitude and frequency) were the same as in the verum condition, except for the duration of stimulation which was applied for just 30 s and then turned off automatically. Because most subjects feel an itching sensation only initially during tACS, this procedure prevents awareness of the stimulation conditions (Gandiga, Hummel, & Cohen, 2006; Nitsche et al., 2008). The magnitude of the stimulating current was based on individually determined thresholds for skin sensations induced by tACS. To determine the thresholds we applied tACS at the individual theta frequency for 1 min (ramping up and down for 15 s) at a time and increased the amplitude stepwise by 250 μA starting with 1000 μA and reaching a maximum of 2250 μA. Participants were asked to keep their eyes closed and indicate the presence of a skin sensation or phosphenes. For the remaining experiment, stimulation intensity was kept 250 μA below the lower threshold for skin sensations (left and right parietal group: Modus = 1750 μA peak-to-peak; range = 1000 μA to 2000 μA; left frontal group: Modus = 1750 μA peak-to-peak; range = 1000 μA to 2250 μA).

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3. Results The questionnaire data about respondents' sensations during tACS was analyzed with a Wilcoxon Signed Ranks Test (sham/verum). The test showed no significant difference between respondents' sensations during sham and verum tACS settings (Z(35) = 0.31; pexact b 0.77). 3.1. Storage versus processing Differences between the three tACS protocols in relation to storage and executive processes were analyzed with a GLM for repeated measures with tACS (sham/verum) and WM FUNCTION (storage/process) as within-subjects variables, and GROUP (left parietal, right parietal and left frontal), as a between-subjects variable. The analysis was performed on aggregated measures of the WM span tasks (forward/backward digit span and Corsi block), and the n-back tasks (1-back, 2-back, and 3-back). Significant was the main effect of tACS (F(1,33) = 21.56; p b 0.00005; η2 = 0.40), the interaction effects between tACS and GROUP (F(1,33) = 3.76; p b 0.03; η2 = 0.19), and among tACS, GROUP and FUNCTION (F(2,33) = 3.79; p b 0.03; η2 = 0.19). The three tACS protocols significantly influenced WM storage capacity and executive processes. After verum tACS respondents' WM storage capacity and executive processes significantly increased as compared to sham stimulation. To get a deeper insight into between group differences of tACS influences on WM storage and executive processes a GLM for repeated measures with tACS (sham/verum) as within-subjects variables and GROUP (left parietal, right parietal and left frontal), as a between-subjects variable for each WM function was performed. The GLM for WM storage capacity showed a significant main effect of tACS (F(1,33) = 8.74; p b 0.006; η2 = 0.21). On the other hand, the interaction effect between tACS and GROUP was not significant (F(2,33) = .75; p b 0.48; η2 = 0.04). As can be seen in Table 1 subsequent paired-sample t tests (not Bonferroni corrected) between sham/verum tACS computed for each group separately, showed more pronounced influences of verum tACS when the target electrodes were placed over parietal areas. In contrast the influence was minimal when the target electrode was placed over the left frontal area. The GLM for WM executive processes showed a significant main effect of tACS (F(1,33) = 20.42; p b 0.00008; η2 = 0.38). Also significant was the interaction effect between tACS and GROUP (F(2,33) = 3.78; p b 0.03; η2 = 0.19). As can be seen in Table 1, subsequent pairedsample t tests (Bonferroni corrected) between sham/verum tACS computed for each group separately showed that the influence of verum tACS was most pronounced when the target electrode was placed over the right parietal brain area. 3.2. Storage capacity Differences between the three tACS protocols in relation to storage capacity were analyzed with a GLM for repeated measures with tACS (sham/verum), DIRECTION (forward/backward) and CONTENT (verbal/figural), as within-subjects variables, and GROUP (left parietal, right parietal and left frontal), as a between-subjects variable. The GLM, beside the influence of tACS on WM storage capacity (F(1,33) = 8.74; p b .006; η2 = .21), also showed a significant interaction effect among the factors tACS, DIRECTION and GROUP, (F(2,33) = 3.94; p b .03; η2 = .19). In contrast, there was no significant interaction effect among the factors tACS, CONTENT and GROUP (F(2,33) = 1.15; p b .34; η2 = .07). Subsequent paired-sample t tests (Bonferroni corrected) between sham/verum tACS computed for each group separately showed that the influence of verum tACS on backward memory span was most pronounced when the target electrode was placed over the left parietal area (see Table 2). Also observed was a positive influence of verum tACS on forward memory span in the right parietal group (significant paired-sample t test, not Bonferroni corrected).

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Table 1 Means, standard deviations and paired-sample t tests for sham/verum differences between aggregated scores for tests measuring working memory capacity and executive processing for the three tACS groups.Bold values represent significant differences. Process

Parietal—left

WM capacity Executive processing

Parietal—right

Frontal—left

Sham

Verum

df(11)

Sham

Verum

df(11)

Sham

Verum

df(11)

M = 6.52 SD = .79 M = 49.79 SD = 9.53

M = 6.95 SD = .81 M = 53.49 SD = 13.28

t = 2.39; p b .03 d = .69 t = 2.07; p b .06 d = .60

M = 6.33 SD = .58 M = 47.53 SD = 9.35

M = 6.64 SD = .76 M = 60.48 SD = 4.56

t = 2.14; p b .05 d = .66 t = 5.80; p b .0001 d = 1.68

M = 6.54 SD = 1.04 M = 51.94 SD = 11.71

M = 6.68 SD = 0.84 M = 56.18 SD = 8.72

t = .74; p b .48 d = .20 t = 1.17; p b .27 d = .34

several neuroimaging studies (Champod & Petrides, 2010; Collette & Van der Linden, 2002; Cowan, 2011; Cowan et al., 2011; Olson & Berryhill, 2009; Sauseng et al., 2010), as well as in a recent rTMS study (Postle et al., 2006). To our knowledge this is the first reported evidence for a causal relation between left parietal theta activity and WM storage capacity. A second finding was that left parietal theta tACS had a more pronounced influence on backward recall than on forward recall, which was not related to task content (spatial or verbal). This would suggest that different brain areas are involved in forward and backward recall of data. Given the relation of parietal brain areas with spatial orientation and navigation (Kolb & Whishaw, 2009), a more spatial coding strategy for backward recall could be supposed. As stressed by Rudel and Denckla (1974) forward recall involves some form of verbal coding, in contrast, backward recall requires the translation of a given serial order into left–right spatial coordinates. However, this explanation is questionable given that right parietal stimulation did not show a similar backward recall advantage, on the contrary a tendency for better forward recall was observed. It has been also suggested that successful performance on backward recall tasks requires central executive function due to the additional requirement of manipulation of information within temporary storage (Groeger, Field, & Hammond, 1999; Lezak, 1995). Our study does not support this hypothesis. tACS with the target electrode positioned over the left DLPFC had no notable influence on the backward recall tasks. Ambivalent are also the results of neuroimaging studies. In a near infrared spectroscopy study Hoshi et al. (2000) showed that the digit backward task activated the DLPFC of each hemisphere more than the forward digit span task. These results suggest that the backward recall task engaged the working memory system to a greater extent than the forward task, and that the backward recall task implicated visuospatial imagery as well as verbal representation. In contrast, a positron emission study by Gerton et al. (2004) did not

3.3. Executive process Differences between the three tACS protocols in relation to executive process were analyzed with a GLM for repeated measures with tACS (sham/verum) and n-BACK (1- ,2- and 3-back) as within-subjects variables, and GROUP (left parietal, right parietal and left frontal), as a between-subjects variable. The GLM showed a significant main effect of tACS (F(1,33) = 20.41; p b .00008; η2 = .38), an interaction effect between the factors tACS and GROUP (F(2,33) = 3.74; p b .03; η2 = .19), and an interaction effect among tACS, n-BACK and GROUP (F(4,66) = 3.86; p b .007; η2 = .19). As can be seen in Table 1, verum tACS had the most pronounced influence on n-back performance when the target electrode was placed over the right parietal site. This influence was also dependent on the magnitude of n-back and the placement of the target electrode as indicated by subsequent paired-sample t tests, FDR corrected with the classical one-stage method (Benjamini & Hochberg, 1995). When the target electrode was placed over the left parietal site the highest performance increases were observed for the 2-back tasks, when placed over the right parietal area the increases were most pronounced for the 1-back and 2-back tasks, and when placed over the left frontal area a moderate increase for the 1-back, could be observed (see Table 3). 4. Discussion The study investigated the role of frontal and parietal brain areas in WM temporary storage and manipulation of information. The central finding was that stimulation of parietal areas (target electrodes positioned at P3 or P4) had a positive effect on WM storage capacity, whereas no such influence was observed for the stimulation of the left frontal area. This supports the hypothesis that parietal brain areas play a central role for WM storage capacity. A finding that has been confirmed in

Table 2 Means, standard deviations and paired-sample t tests for sham/verum differences between aggregated scores for forward/backward memory span for the three tACS groups.Bold values represent significant differences. Memory span

Forward Backward

Parietal—left

Parietal—right

Frontal—left

Sham

Verum

df(11)

Sham

Verum

df(11)

Sham

Verum

df(11)

M = 6.73 SD = .72 M = 6.31 SD = .91

M = 6.79 SD = .78 M = 7.10 SD = .97

t = .26; p b .80 d = .07 t = 4.18; p b .002 d = 1.20

M = 6.29 SD = .66 M = 6.38 SD = .97

M = 6.77 SD = .76 M = 6.50 SD = .93

t = 2.26; p b .04 d = .64 t = .63; p b .54 d = .17

M = 6.54 SD = 1.09 M = 6.54 SD = 1.04

M = 6.60 SD = .72 M = 6.75 SD = 1.22

t = .26; p b .80 d = .07 t = .99; p b .34 d = .27

Table 3 Means, standard deviations and paired-sample t tests for sham/verum differences between correctly solved n-back tasks for the three tACS groups. Paired-sample t tests were FDR corrected with the classical one-stage method (Benjamini & Hochberg, 1995). Bold values represent significant differences. n-Back

1-Back 2-Back 3-Back

Parietal—left

Parietal—right

Frontal—left

Sham

Verum

df(11)

Sham

Verum

df(11)

Sham

Verum

df(11)

M = 83.72 SD = 16.41 M = 39.42 SD = 16.54 M = 26.22 SD = 3.73

M = 80.89 SD = 21.50 M = 48.69 SD = 21.50 M = 30.89 SD = 7.47

t = .81; p b .44 d = .23 t = 2.84; p b .01 d = .82 t = 1.59; p b .14 d = .46

M = 82.17 SD = 16.89 M = 35.61 SD = 14.88 M = 25.08 SD = 7.89

M = 95.58 SD = 3.34 M = 59.17 SD = 12.62 M = 26.69 SD = 6.92

t = 2.65; p b .02 d = .77 t = 8.00; p b .00001 d = 2.31 t = .54; p b .60 d = .15

M = 81.08 SD = 18.64 M = 42.27 SD = 17.16 M = 32.03 SD = 13.05

M = 87.83 SD = 14.14 M = 45.27 SD = 13.37 M = 35.44 SD = 10.67

t = 2.31; p b .04 d = .67 t = .46; p b .66 d = .13 t = .62; p b .55 d = .18

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replicate these findings. The digit forward and backward tasks relied upon a largely overlapping functional neural system associated with working memory. The ambiguity of the results obtained does not allow for a firm conclusion on the differences in brain activation related to forward and backward recalls. A tentative explanation based on the data obtained in our study could be that increased storage capacity generated by left parietal stimulation more efficiently supported a spatial recall strategy for the backward tasks. However, further research will be needed to clarify the diversity of obtained results. Another objective of the study was to explore the influence of theta tACS on processing components of WM (e.g., inhibition of irrelevant items, monitoring of ongoing performance, updating representations in memory and binding processes between spatial positions and temporal context). The obtained pattern of differences in performance on the n-back tasks induced by the three tACS protocols was not in line with the hypothesized expectations which were mainly based on previous neuroimaging evidence obtained in correlational studies showing that executive processes were related to the activity of frontal brain areas (Champod & Petrides, 2010; Collette & Van der Linden, 2002; Curtis & D'Esposito, 2003; Olson & Berryhill, 2009; Sauseng et al., 2010), as well as with experimental evidence employing tDCS (Andrews et al., 2011; Fregni et al., 2005, 2006; Zaehle et al., 2011). The most pronounced influence on n-back performance was observed for the right parietal tACS protocol having a major influence on the 2-back task and a minor on the 1-back task. The stimulation of the left parietal area showed a more diverse effect, being significant for the performance of the 2-back tasks, yet negative for the 1-back task. The stimulation of the left frontal area had a minor influence on the 1-back task. A vague explanation of the obtained pattern of performance enhancements on the n-back tasks in relation to the area of stimulation could be that for more complex tasks (higher level of n) WM storage capacity is crucial for task performance, whereas for easier tasks (lower level of n) attentional control is dominant. This explanation seems also plausible from the requirements of the n-back task used in the present study. The n-back tasks, beside the executive processes of inhibition, monitoring, and updating, also required the binding between spatial positions and temporal context. In Baddeley's multicomponent model of WM this integrative function is assigned to the episodic buffer (Baddeley et al., 2011). Its function is the temporary storage and binding of information streaming from the phonological loop (the aurally presented single letters), and the visuo-spatial sketchpad (blue squares in different spatial locations) into unitized episodes or chunks. On the other hand, following the logic of the explanation that with a higher level of n, storage capacity is essential for task solution, whereas with a lower level of n attentional control is important, it would be expect that parietal stimulation (especially left parietal) would have some influence also on the 3-back tasks. However, as can be seen in Table 3, just a trend indicating the expected increase could be observed. Left parietal stimulation compared to the other settings had the greatest impact on the solution of the 3-back tasks, although not statistically significant (p b .14). Another variable that might have also influenced the obtained tACS enhancement patterns on the n-back tasks is the content of stimulus material used. Left DLPFC stimulation showed the expected positive influence on n-back performance only when symbolic/verbal stimulus material was used (Fregni et al., 2005; Zaehle et al., 2011), whereas for figural stimuli less pronounced or no influence was reported (Mulquiney et al., 2011). Yet another possible explanation could be that the attentional component of WM is not reflected just in the theta frequency band but also in alpha band activity. According to Klimesch (2012) alpha-band oscillations have inhibitional and timing roles which are related to attentional functions of suppression and selection of information. Monitoring new information, for instance, elicits increase in the theta frequency band accompanied by alpha synchronization. On the other hand alpha-band activity can also act as an inhibitory filter that keeps target information activated (Klimesch, 2012). From this view point it could be speculated that stimulating

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the frontal areas in one of the alpha bands might have had a more pronounced influence on attention, the so called attentional buffer that keeps target information activated, and thus have had a more prominent effect on n-back performance. Therefore further research is needed to clarify the influence these variables have on the performance of the n-back tasks. In conclusion, the study confirmed the central role of parietal brain areas, in particular the left one, for working memory storage capacity. On the other hand, the study also opened several questions (e.g., the relation between backward recall, attentional control and storage capacity; the role of theta and alpha band oscillations in WM executive control) that should be addressed in future research. References Amin, Z., Epperson, C. N., Constable, R. T., & Canli, T. (2006). Effects of estrogen variation on neural correlates of emotional response inhibition. NeuroImage, 32, 457–464. Andrews, S.C., Hoy, K. E., Enticott, P. 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