Journal of Cognitive Enhancement (2018) 2:88–96 https://doi.org/10.1007/s41465-017-0059-7
ORIGINAL ARTICLE
Transcranial Direct Current Stimulation over the Posterior Parietal Cortex (PPC) Enhances Figural Fluency: Implications for Creative Cognition Elham Ghanavati 1,2 & Vahid Nejati 1,2,3 & Mohammad Ali Salehinejad 3,4 Received: 30 June 2017 / Accepted: 22 November 2017 / Published online: 8 December 2017 # Springer International Publishing AG, part of Springer Nature 2017
Abstract Creative cognition and figural fluency are two closely related concepts. Previous studies suggest different brain regions involved in figural fluency, creativity, and divergent thinking including frontal and parietal cortices. Furthermore, neural underpinning of the figural fluency is yet to be studied. This study aimes to investigate effects of modulation of cortical excitability in the right posterior parietal cortex (r-PPC) and left dorsolateral prefrontal cortex (l-DLPFC) on figural fluency using transcranial direct current stimulation (tDCS). Twenty neurologically unimpaired participants (mean age 27.55, SD = 5.11) received anodal r-PPC (P4), anodal l-DLPFC (F3), and sham tDCS (15 min, 1.5 mA) with 72-h interval between each stimulation condition. After 5 min of stimulation, participants underwent the Five-Point Test (FPT) which is a measure of figural fluency. Results showed that although participants produced more unique figures under both stimulation montages, they significantly produced more unique designs under anodal r-PPC tDCS compared to anodal l-DLPFC and sham tDCS. Findings imply that figural fluency is more dependent on the activation of the right posterior regions of parietal cortex, which is associated with spatial cognition, visual attention, cognitive flexibility, and creative cognition, but may partially benefit from activation of prefrontal regions too. tDCS has beneficial effects in enhancing figural fluency and potentially creative cognition as well as potential therapeutic effects in disorders suffering from impaired figural fluency. Keywords Figural fluency . Creative cognition . Divergent thinking . Transcranial direct current stimulation . Posterior parietal cortex . Dorsolateral prefrontal cortex
* Elham Ghanavati
[email protected] Vahid Nejati
[email protected] Mohammad Ali Salehinejad
[email protected] 1
Department of Psychology, Islamic Azad University, Science and Research Branch, Tehran, Iran
2
Department of Psychology and Educational Sciences, Shahid Behehsti University Tehran, Tehran, Iran
3
Institute for Cognitive and Brain Sciences, Shahid Beheshti University, Tehran, Iran
4
Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
Introduction Fluency is defined as the ability to maximize unique response production while at the same time avoiding or minimizing response repetition (Ruff et al. 1994) and is generally divided into verbal and nonverbal categories. While verbal fluency is referred to the ability to generate and express words compatible with required criteria (Wysokiński et al. 2010), nonverbal fluency concerns with generating unique nonverbal responses and is usually measured by figural or design fluency (Ruff et al. 1986). Figural fluency tests are related to divergent thinking (Runco 1991) and creative cognition (Fink et al. 2010; Forthmann et al. 2016). These tests are usually used in tests of creativity and divergent thinking (Forthmann et al. 2016; Shamay-Tsoory et al. 2011), but some studies suggest that all forms of fluency, including verbal and nonverbal
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fluency, are among executive functions (EFs) in general (Zalonis et al. 2017) or some specific EF domains such as cognitive flexibility (Ruff et al. 1987). Interestingly, other studies have shown that creativity and EFs are associated with each other. These findings raise the question of whether figural fluency is a domain of EFs, creative cognition, or both which is not well-studied. The relationship between figural fluency and EFs can be better understood by comparing the way verbal and figural fluency interact. Verbal fluency is a domain of EFs which is related to activation of the left dorsolateral prefrontal cortex (lDLPFC) (Cattaneo et al. 2011), and the l-DLPFC is the primary cortical region involved in executive functioning and cognitive control (Miller and Cohen 2001). Although figural fluency is regarded as the nonverbal analogue of verbal fluency, it is not correlated with verbal fluency (Ruff et al. 1987) and is dissociated with it in terms of underlying brain regions and cognitive functions (Foster et al. 2005). Lesion studies supported this by showing that left hemisphere lesions produce more severe deficits in verbal fluency than right-sided lesions whereas figural fluency is particularly sensitive to right-sided brain lesions (Goebel et al. 2009), specifically right frontal lobe dysfunction (Foster et al. 2005; Ruff et al. 1994). Therefore, whether figural fluency is a domain of executive functioning and related to lDLPFC activation or not is still an open question. On the other hand, successful performance on figural fluency tasks such as the Five-Point Test (FPT) (Regard et al. 1982) and Ruff Figural Fluency Test (RFFT) (Ruff et al. 1987) depends on other cognitive functions and their respective brain regions too (Lee et al. 1997). Figural fluency tasks require participants to produce as many unique and novel figures as possible and are thus related to cognitive flexibility (Ruff et al. 1987), divergent thinking (Runco 1991), and creative cognition (Fink et al. 2010; Forthmann et al. 2016). In addition, performance on figural fluency tasks is dependent on spatial cognition, visual attention, and selective attention too. For example, during the FPT task, participants should generate as many unique line drawings as possible across five dots while trying to avoid repetitions. The parietal regions specially right posterior areas are involved in visual attention, spatial representation/updating, and retrospective coding of visual space (which is specifically important in a task like FPT) all of which serve a crucial role in transforming sensory input into motor output and guiding action (Behrmann et al. 2004; Curtis 2006; Husain and Nachev 2007). Additionally, the parietal cortex is involved in creative thinking tasks (Zmigrod et al. 2015) and lesion to this region is associated with poor performance on fluency tasks (Abraham et al. 2012). These findings again raise the question of whether figural fluency is an EF domain, divergent thinking/creativity, ability, or both. One way to address this question is to modulate cortical excitability in the potential areas of interest and see how performance on figural fluency tasks is affected. Transcranial direct current stimulation (tDCS) is a noninvasive brain
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stimulation technique established as a simple, effective, and safe method to modulate cortical excitability (Nitsche et al. 2009) and cognitive functions (Wassermann and Grafman 2005; Nejati et al. 2017a). tDCS is proposed as a method of cognitive enhancement and cognitive rehabilitation in healthy subjects and patients, respectively (Ward 2015). tDCS uses a relatively weak electric currents involving the flow of electric current from a positive to a negative site leading to modulation of cortical excitability and activity (Nitsche et al. 2015). Anodal stimulation increases cortical excitability, while cathodal stimulation decreases it (Utz et al. 2010). Recent tDCS studies showed that modulation of cortical excitability in different brain regions improves cognitive functions including but not limited to different types of memory (Brunoni and Vanderhasselt 2014; Javadi and Walsh 2012; Salehinejad et al. 2017a), attention (Coffman et al. 2014; Gladwin et al. 2012), executive functions (Gill et al. 2015; Nejati et al. 2017a; Nejati et al. 2017b), inhibitory control (Hsu et al. 2011; Salehinejad et al. 2017b), social cognition (Nejati et al. 2017c), and language processing (Flöel et al. 2008; Monti et al. 2013) in both normal and abnormal populations. Recent studies showed improving effect of left prefrontal regions tDCS in verbal fluency too (Cattaneo et al. 2011); however, enhancing effects of tDCS on figural fluency is not studied yet. Using electrical brain stimulation, we can investigate how modulation of cortical activity in different brain regions (e.g., left prefrontal cortex, right posterior parietal cortex) influences figural fluency and possibly creative cognition. When it comes to creative cognition and divergent thinking, recent brain stimulation studies have shown mixed results about potentially involved brain regions. L-DLPFC has been one of the frequently targeted area in creativity research with controversial results. While some studies found that increasing activity of the l-DLPFC with anodal tDCS enhances creativity and divergent thinking (e.g., Cerruti and Schlaug 2009; Zmigrod et al. 2015), others found opposite and suggest that cathodal l-DLPFC tDCS improves creative cognition through inhibition of cognitive control exerted by the l-DLPFC (e.g., Chrysikou et al. 2013; Luft et al. 2017). In addition to DLPFC, the role of the right partial cortex has been shown in creativity (Fink et al. 2010; Forthmann et al. 2016) and recent tDCS studies show the mediating role of the posterior parietal cortex (PPC) in creative thinking and problem solving. Therefore, the l-DLPFC and r-PPC seem to be two potential areas of interest for exploring components of creativity using brain stimulation method (Zmigrod et al. 2015). Targeting these areas of course should be based on task modalities and characteristics. All tDCS studies mentioned above (i.e., Cerruti and Schlaug 2009; Chrysikou et al. 2013; Luft et al. 2017; Zmigrod et al. 2015) have used verbal tasks for measuring creative cognition and divergent thinking (e.g., Remote Associates Task, Alternative Uses Task) which might explain
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why they targeted l-DLPFC which is shown to be involved in verbal fluency (Cattaneo et al. 2011). The FPT task is, however, a visuospatial task which makes it likely to mostly benefit from the r-PPC rather than l-DLPFC tDCS which is not studied yet. The present study, therefore, aims to investigate how modulation of cortical excitability in the r-PPC (involved in spatial and creative cognition) and l-DLPFC (involved in executive functions) alters performance on the FPT task and possibly affects creative cognition. Specifically, here we want to compare the effect of anodal and sham tDCS over the r-PPC and lDLPFC within a group of healthy participants undergoing a figural fluency task. Considering the role of right hemisphere in figural fluency and based on findings about involvement of both prefrontal and parietal cortices in figural fluency, we hypothesized that anodal r-PPC tDCS enhances performance on the figural fluency task more than anodal l-DLPFC and sham tDCS. In other words, we expect subjects to generate more novel and unique figures under anodal r-PPC tDCS and have less perseverative errors. To our knowledge, this is the first study investigating effect of tDCS on figural fluency task measured by the FPT which can shed more light on the involved brain regions not only in figural and nonverbal fluency but also in creative cognition and divergent thinking. It would also allow us to see to what extent figural fluency and divergent thinking benefit from l-DLPFC executive control or rPPC visuo-spatial abilities and cognitive flexibility.
Methods Participants Twenty neurologically unimpaired individuals blind to study hypothesis took part in the experiment (9 males, Mean age 27.55 years, SD = 5.11). The inclusion criteria were as follows: (1) no previous history of brain surgery involving implants to the head, epilepsy, seizures, brain damage, head injury, or loss of consciousness; (2) no history of chronic or acute neurologic, psychiatric, or medical disease; (3) no history of drug addiction and no current use of tobacco consumption; and (4) no current pregnancy. The SCL-25 questionnaire (Veijola et al. 2003) that measures general psychological health was also employed to initially screen participants’ psychological state before the beginning of the study. All participants were native speakers, right-handed, nonsmoker, and had normal or corrected-to-normal vision. Written informed consent was obtained from all participants, and they were free to withdraw from the experiment at any stage. The experiment was approved by the ethical committee of the local university, and the study was conducted in accordance with the latest version of the Declaration of Helsinki.
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Materials Five-Point Test (FPT) The FPT is a valid and reliable test of figural fluency (Goebel et al. 2009) developed by Regard et al. (1982). The standardization of the application of the test procedure and the clear instructions for evaluation of test performances ensure a high level of objectivity (Tucha et al. 2012). We used the FPT because of its relative advantages over other figural fluency measures (e.g., RFFT) including brevity and simplicity. Studies reported practice effects for the RFFT while such effects have not been found in other figural fluency tests (van Eersel et al. 2015). Moreover, the RFFT uses five different dot matrices creating a potentially more complex task which require figure-ground separation (Ross et al. 2003). Performance on it may then be more dependent on executive resources rather than fluency ability. The FPT stimulus material consists of a page on which 40 identical squares are printed in eight rows and five columns, each square containing five symmetrically arranged dots (Fig. 1). Participants are asked to draw as many different unique figures as possible in 5 min by connecting two or more dots with straight lines. Participants were informed that not all the dots had to be used. Each participant was instructed not to repeat figures or draw lines which did not connect dots. At the start of the test, two sample solutions were drawn by the examiner. The test was administered using the standard oral instruction suggested by Regards et al. (1982). Scoring includes counting the total number of unique designs and the number of repeated designs (perseverative errors) drawn. Because the number of unique designs drawn by patients can influence the number of perseverative errors, the percentage of perseverative errors (i.e., perseverative errors + total unique figures × 100) was also calculated. The scoring procedure was done by a blind rater.
tDCS Protocol For brain stimulation, we used the BActivaDose II Iontophoresis^ Delivery Unit manufactured by Activa Tek, with a 9-V battery as current source. Electrical direct current of 1.5 mA generated by the stimulator was applied through a pair of saline-soaked sponge electrodes with a size of 35 cm2 (7 × 5) for 15 min (with 15-s ramp up and 15-s ramp down). Three tDCS conditions were applied in this study: (a) anodal rPPC tDCS, (b) anodal l-DLPFC tDCS, and (c) sham tDCS. Anodal electrode was positioned over P4 (r-PPC) and F3 (lDLPFC) according to the 10–20 EEG International System. The reference electrode was positioned over the contralateral shoulder. For sham stimulation, electrical current was ramped up for 30 s to generate the same sensation as the active condition and then turned off without the participants’ knowledge (Palm et al. 2013). This method of sham stimulation has been shown to be reliable (Gandiga et al. 2006). It is of note that the anode and cathode electrodes were marked by number on
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Fig. 1 Test material for the Five-Point Test. The test consists of a sheet paper with 40 dot matrices arranged in eight rows and five columns as above. Participants are asked to produce as many different figures as possible by connecting the dots within each rectangle. From Regards et al. (1982)
them (either 1 or 2), and the experimenter was not aware of the polarity of stimulation. All participants were blind to the type of stimulation they received. A side-effect survey was done after each tDCS session (Fig. 2).
Procedure Prior to the experiment, participants completed a brief questionnaire to evaluate their suitability for brain stimulation. All participants received 15 min of anodal r-PPC, anodal lDLPFC, and sham stimulation with at least 72-h interval between each stimulation session in order to prevent transfer and confounding effect of stimulation. Five minutes after stimulation during which participants sat at rest, they started performing the FPT lasting around 5 min while they received electrical brain stimulation (Fig. 2). Participants were orally instructed about each task before the beginning of the experiment. The polarity of stimulation was randomized across participants in order to control for Border effects,^ and participants were blind to the type of stimulation they received.
Statistical Analysis This study was a double-blind, within-subjects, single-factor design. Data analyses were conducted using the statistical package SPSS for Windows, version 24 (IBM, SPSS, Inc., Chicago, IL). The normality and homogeneity of variance of data collected from each stimulation condition were confirmed using Shapiro-Wilk and Levin tests, respectively. To Fig. 2 Procedure of tDCS conditions. tDCS transcranial direct current stimulation, PPC posterior parietal cortex, DLPFC dorsolateral prefrontal cortex, FPT Five-Point Test
estimate the effect of tDCS on performance of the FPT, repeated measures ANOVA was carried out on the number of unique designs and perseverative errors with tDCS conditions (anodal r-PPC, anodal l-DLPFC, sham) as the within-subject factor. Mauchly’s test was used to evaluate the sphericity of the data before performing the repeated measures ANOVA for each dependent variable. We also added an analysis of covariance (ANCOVA) with order as covariate to control for its potential confounding effect. A significance level of p < 0.05 was used for all statistical comparisons.
Results All participants tolerated tDCS well, and no adverse effects were reported except for a mild itching sensation under the electrodes during approximately the first 30 s of stimulation in each tDCS condition. Results of Mauchly’s test showed that the assumption of sphericity was not violated. Data overview shows that performance on the FPT was different under the respective tDCS conditions (Fig. 3). The mean and standard deviation of task performance parameters are presented in Table 2. Demographic variables (Table 1) were not significantly correlated with FPT performance and thus were not included as covariates in the analysis. To test any tDCS effects, a series of repeated measures ANOVA was performed on FPT parameters. ANOVA results showed that tDCS significantly increased the number of unique figures generated by participants (F(2, 38) = 28.63,
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Fig. 3 Number of unique figures and percentage of preseverative errors in Five-Point Test after tDCS conditions. r-PPC right posterior parietal cortex, lDLPFC left dorsolateral prefrontal cortex
p < 0.01, eta2 = 0.60) which is indicator of figural fluency productivity. The Bonferroni correction post hoc test further showed that anodal r-PPC tDCS (p < 0.01; mean = 30.75) significantly improved the number of produced unique figures compared to anodal l-DLPFC (mean = 26.40) and sham tDCS (mean = 23.13). Interestingly, anodal r-PPC tDCS was also significantly different with anodal l-DLPFC in the number of produced unique designs (Table 2). However, it is of note that participants also produced more unique and novel designs under anodal l-DLPFC tDCS compared to sham stimulation (24.60 vs. 23.85) which although was not significant but almost close to significant (p < 0.08). ANCOVA results showed that the order of stimulation did not have any significant effect on dependent variable (F = 0.01, p < 0.93). The effect of tDCS condition on the number and percentage of perseverative errors was also investigated. ANOVA results showed that tDCS did not significantly decreased the number of repetitive figures produced by participants (F(2, 2 38) = 0.56, p < 0.55, eta = 0.03) although the number of perseverative errors was lower under anodal r-PPC tDCS. Similarly, tDCS did not have any significant effect on the percentage of perseverative errors (F(2, 38) = 1.19, p < 0.31, eta2 = 0.06) although the percentage of perseverative error was again lower under anodal r-PPC tDCS (mean = 9.24, SD = 10.82) compared to anodal l-DLPFC (mean = 13.93, SD = 12.98) and sham tDCS (mean = 11.95, SD = 8.67) which
Table 1
Demographic information of participants
Variable Sample size (n) Gender Age Education Marital status
Group
Male (female) Mean (SD) Bachelor degree Masters degree Single (married)
20 9 (11) 27.55 (5.11) 11 9 14 (6)
is not surprising given that perseverative errors are usually observed in neurological patients. ANOVA results are summarized in Table 3.
Discussion Neural underpinnings of creative cognition and divergent thinking have attracted many researchers in recent years and previous studies suggested different and sometimes contradictory brain region involved in creative cognition. Figural fluency is associated with divergent thinking (Forthmann et al. 2016) as well as executive functions (Zalonis et al. 2017) but the extent to which it benefits from divergent thinking ability and executive functioning and their respective brain regions is not well-studied. The present study investigated effects of increasing cortical plasticity of the l-DLPFC and r-PPC with anodal tDCS, on figural fluency to see which brain regions and their potential respective cognitive functions are more important during performing a figural fluency task. Results showed that anodal r-PPC tDCS (compared to anodal lDLPFC and sham tDCS) significantly improved performance on the figural fluency task. In other words, increasing activity in the r-PPC led participants to generate significantly more unique and novel figures possibly through enhancing divergent thinking ability. Several studies have investigated effects of tDCS on creative cognition (Cerruti and Schlaug 2009; Chrysikou et al. 2013; Luft et al. 2017); however, to the best of our knowledge, this is the first study to investigate effects of tDCS on creative cognition/divergent thinking measured by figural fluency task. Before discussing results, we should note to the difference between creativity and divergent thinking and its implication for this study. Figural fluency tasks are usually regarded among tests of creativity and divergent thinking; however, they may not accurately measure creativity. BOriginality^ is an integral component of creativity which should be measured by creative cognition tasks. Although the FPT task instruction
J Cogn Enhanc (2018) 2:88–96 Table 2 Means and SDs of FivePoint Test output under tDCS conditions
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Task
Five-Point Test
tDCS condition Anodal r-PPC tDCS M (SD)
Anodal l-DLPFC tDCS M (SD)
Sham tDCS M (SD)
Uniqe figures Preseverative error
30.75 (5.63) 2.60 (2.18)
26.40 (6.82) 3.4 (3.06)
23.85 (6.46) 2.80 (2.01)
% of preseverative error
9.24 (10.82)
13.93 (12.98)
11.95 (8.67)
tDCS transcranial direct current stimulation, r-PPC right posterior parietal cortex, l-DLPFC left dorsolateral prefrontal cortex, M mean, SD standard deviation
explicitly asks subjects to produce novel and unique designs, originality may not be captured accurately with the figural fluency tasks such as the FPT because fluency tasks mainly represent productivity. Therefore, the FPT task is suggested to be regarded as a measure of divergent thinking and not direct measure of creativity given that these two concepts are not synonymous (Runco 2008). Nevertheless, divergent thinking is a usual way for assessing creativity (Silvia et al. 2008). What we found in this study seems to be initially in line with previous evidence about role of the right hemisphere rather than left hemisphere, in nonverbal fluency (Goebel et al. 2009; Lee et al. 1997; Ruff et al. 1994). However, our results also indicated that there is a tendency toward a significant role of the l-DLPFC in producing unique designs which need to be investigated in future studies especially by using both verbal and nonverbal divergent thinking tasks. Therefore, we cannot firmly support the notion of double association of right and left frontal lobe dysfunction in figural (i.e., nonverbal) and verbal fluency, respectively (Foster et al. 2005). To further support the notion of double dissociation of right and left frontal lobe, we need to show enhancing effect of anodal rDLPFC tDCS on figural fluency which was not a target region for stimulation in our experiment. This is also important as previous studies introduced r-DLPFC as one of the potentially involved brain region in creative cognition although results have been mixed with this respect. A novel aspect of this study was stimulating the r-PPC as the target area for modulating figural fluency and its significant involvement in the FPT performance and possibly creative cognition. Our findings are initially in accordance with
Table 3 Results of repeated measures ANOVA for effects of tDCS conditions (anodal r-PPC/ anodal l-DLPFC/sham) on figural fluency task
those studies suggesting that posterior parietal regions in the right hemisphere are involved in divergent thinking, creative cognition, and cognitive flexibility (Abraham et al. 2012; Acar and Runco 2017; Runco 1991). In addition, they support the notion that figural fluency is strongly dependent on the posterior regions of parietal cortex than left prefrontal regions. This implicates that for the figural fluency task, right posterior parietal regions are more important than left prefrontal areas which possibly has implications for underlying cognitive functions that support figural fluency performance. The PPC is involved in visual attention, spatial representation and updating, retrospective coding of visual space, and creative cognitions, all of which are required for good performance on figural fluency tests (Behrmann et al. 2004; Curtis 2006; Husain and Nachev 2007; Shamay-Tsoory et al. 2011). Nevertheless, based on our findings, we cannot rule out involvement of the prefrontal regions especially in the right hemisphere, in figural fluency. First of all, we did not stimulate r-DLPFC in our experiment while this region is suggested by lesion studies to be involved in figural fluency tasks (Ruff et al. 1986). Secondly, our results showed that anodal lDLPFC tDCS which is supposed to enhance cognitive control (Salehinejad et al. 2017a; Nejati et al. 2017a), did not enhanced figural fluency and divergent thinking as much as anodal r-PCC did. This is in line with recent tDCS studies that found performance on the tasks requiring cognitive flexibility and creative cognitions (e.g., flexible use generation task) benefits from a state of diminished cognitive control as a result of cathodal l-DLPFC tDCS (Chrysikou et al. 2013). Anodal lDLPFC tDCS in our study, however, facilitated cognitive
Task
Source
df
Mean square
F
p
eta2
Five-Point Test
Uniqe figures Preseverative error % of preseverative error
2, 38 2, 38 2, 38
243.45 3.46 111.12
28.63 0.56 1.19
0.01 0.55 0.31
0.60 0.03 0.06
Significant results are highlighted (p ≤ 0.05) in italics tDCS transcranial direct current stimulation, r-PPC right posterior parietal cortex, l-DLPFC left dorsolateral prefrontal cortex
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control which may explain why it did not benefit generating original and novel figures. Accordingly, anodal r-DLPFC tDCS is a potentially beneficial tDCS montage to enhance figural fluency which is an interesting research question for future studies. Another important thing to consider when interpreting our findings is the nature and modality of the task used in our study and previous tDCS studies on creative cognition. Our results should be interpreted based on task modality and task characteristics. Previous tDCS studies usually used verbal tasks for measuring creativity and divergent thinking (e.g., Remote Associates Task, Alternative Uses Task) which are based on verbal ability and verbal fluency, and these abilities are shown to be related to left and right DLPFC activation (Cerruti and Schlaug 2009; Chrysikou et al. 2013; Luft et al. 2017; Zmigrod et al. 2015). On the other hand, studies on nonverbal problem solving usually targeted other brain regions such as temporal regions (Chi and Snyder 2011) that are supposed to be responsible for task performance. The reason we targeted r-PPC and not r-DLPFC was based on the FPT task characteristics and its visuospatial modality. Therefore, our results implicate that cortical regions supporting divergent thinking and creative cognition are task-specific and depend on task modality. One more implication concerns with the relationship between creative cognition and executive functioning. Recent studies have shown that creativity is associated with at least some EF domains. For example, updating, a major component of executive functioning, is found to have significant role in creativity (Benedek et al. 2014). Similarly, executive switching is another proposed EF that mediates creative cognition (Nusbaum and Silvia 2011), but there are some other studies contending that creative cognition and executive functions (e.g., verbal fluency, shifting, inhibition) are not correlated (Benedek et al. 2014; Ruff et al. 1987). Our findings showed that figural fluency and divergent thinking measured by the FPT is not significantly dependent on executive functioning of the l-DLPFC and is rather associated with parietalsupported cognitive functions like visual attention, spatial representation and updating, retrospective coding of visual space, and creative cognitions. However, we found that activation of the l-DLPFC is at least partially involved in divergent thinking. Our results showed that participants produced more unique designs under anodal l-DLPFC tDCS compared to sham condition. Although the difference was not significant but was almost close to significant. Studying how performance on a verbal and visual divergent thinking tasks are affected under l-DLPFC activation can shed light on how lDLPFC benefit divergent thinking tasks in different modalities. A possible explanation for partial role of the l-DLPFC in figural fluency concerns with the increased inhibitory control (a major EF domain) as a result of l-DLPFC activation. The more participants perform the FPT, the more inhibition is
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required to prevent from repeated figures which can be enhanced by l-DLPFC activation. In sum, our study provided promising results about neural underpinnings of figural fluency and divergent thinking by showing differential role of the parietal and prefrontal cortices in figural fluency. Despite promising results, our experiment had several limitations: first of all, the low spatial resolution of tDCS which is an inherent limitation of this noninvasive brain stimulation technique should be considered. Therefore, involvement of adjacent areas such as r-DLPFC in stimulation effects cannot be ruled out completely. Similarly, facilitatory effects induced by anodal tDCS we reported may not entirely depend on stimulation of the r-PPC itself but also on spreading of activation along other regions in the right hemisphere including right frontal or temporal regions. Secondly, we did not target r-DLPFC as a potentially involved region in figural fluency. Although we targeted areas for stimulation based on literature and task modality, it would be ideal to investigate performance on the figural fluency task under anodal rDLPFC and anodal r-PPC stimulation at the same time. This is of course not feasible in tDCS studies due to minimum distance required between electrodes (Nitsche et al. 2007) but requires further investigation in future studies. Despite limitations, our study implies potential enhancing effects of tDCS on figural fluency and possibly divergent thinking considering task modalities. Additionally, it suggests therapeutic use of tDCS in disorders suffering from impaired nonverbal fluency such as brain injury, dementia, or psychiatric illness (Ruff 2011). Acknowledgements We appreciate participants for taking part in this study. The authors are grateful of the reviewers for their insightful comments. Compliance with Ethical Standards Conflict of Interest The authors declare that they have no conflict of interest.
References Abraham, A., Beudt, S., Ott, D. V. M., & Yves von Cramon, D. (2012). Creative cognition and the brain: Dissociations between frontal, parietal–temporal and basal ganglia groups. Brain Research, 1482, 55–70. https://doi.org/10.1016/j.brainres.2012.09.007. Acar, S., & Runco, M. A. (2017). Latency predicts category switch in divergent thinking. Psychology of Aesthetics, Creativity, and the Arts, 11, 43–51. https://doi.org/10.1037/aca0000091. Behrmann, M., Geng, J. J., & Shomstein, S. (2004). Parietal cortex and attention. Current Opinion in Neurobiology, 14, 212–217. https:// doi.org/10.1016/j.conb.2004.03.012. Benedek, M., Jauk, E., Sommer, M., Arendasy, M., & Neubauer, A. C. (2014). Intelligence, creativity, and cognitive control: The common and differential involvement of executive functions in intelligence
J Cogn Enhanc (2018) 2:88–96 and creativity. Intelligence, 46, 73–83. https://doi.org/10.1016/j. intell.2014.05.007. Brunoni, A. R., & Vanderhasselt, M.-A. (2014). Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: A systematic review and meta-analysis. Brain and Cognition, 86, 1–9. https://doi.org/10.1016/j.bandc.2014.01.008. Cattaneo, Z., Pisoni, A., & Papagno, C. (2011). Transcranial direct current stimulation over Broca’s region improves phonemic and semantic fluency in healthy individuals. Neuroscience, 183, 64–70. Cerruti, C., & Schlaug, G. (2009). Anodal transcranial direct current stimulation of the prefrontal cortex enhances complex verbal associative thought. Journal of Cognitive Neuroscience, 21, 1980–1987. https://doi.org/10.1162/jocn.2008.21143. Chi, R. P., & Snyder, A. W. (2011). Facilitate insight by non-invasive brain stimulation. PLoS One, 6, e16655. https://doi.org/10.1371/ journal.pone.0016655. Chrysikou, E. G., Hamilton, R. H., Coslett, H. B., Datta, A., Bikson, M., & Thompson-Schill, S. L. (2013). Noninvasive transcranial direct current stimulation over the left prefrontal cortex facilitates cognitive flexibility in tool use. Cognitive Neuroscience, 4, 81–89. Coffman, B. A., Clark, V. P., & Parasuraman, R. (2014). Battery powered thought: Enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation. NeuroImage, 85(Part 3), 895–908. https://doi.org/10.1016/j.neuroimage.2013. 07.083. Curtis, C. E. (2006). Prefrontal and parietal contributions to spatial working memory. Neuroscience, 139, 173–180. https://doi.org/10.1016/j. neuroscience.2005.04.070. Fink, A., Grabner, R. H., Gebauer, D., Reishofer, G., Koschutnig, K., & Ebner, F. (2010). Enhancing creativity by means of cognitive stimulation: Evidence from an fMRI study. NeuroImage, 52, 1687– 1695. https://doi.org/10.1016/j.neuroimage.2010.05.072. Flöel, A., Rösser, N., Michka, O., Knecht, S., & Breitenstein, C. (2008). Noninvasive brain stimulation improves language learning. Journal of Cognitive Neuroscience, 20, 1415–1422. https://doi.org/10.1162/ jocn.2008.20098. Forthmann B, Wilken A, Doebler P, Holling H (2016) Strategy induction enhances creativity in figural divergent thinking. The Journal of Creative Behavior. Foster, P. S., Williamson, J. B., & Harrison, D. W. (2005). The Ruff Figural Fluency Test: Heightened right frontal lobe delta activity as a function of performance. Archives of Clinical Neuropsychology, 20, 427–434. https://doi.org/10.1016/j.acn.2004.09.010. Gandiga, P. C., Hummel, F. C., & Cohen, L. G. (2006). Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation. Clinical Neurophysiology, 117, 845– 850. https://doi.org/10.1016/j.clinph.2005.12.003. Gill, J., Shah-Basak, P. P., & Hamilton, R. (2015). It’s the thought that counts: Examining the task-dependent effects of transcranial direct current stimulation on executive function. Brain Stimulation, 8, 253–259. https://doi.org/10.1016/j.brs.2014.10.018. Gladwin, T. E., den Uyl, T. E., Fregni, F. F., & Wiers, R. W. (2012). Enhancement of selective attention by tDCS: Interaction with interference in a Sternberg task. Neuroscience Letters, 512, 33–37. https://doi.org/10.1016/j.neulet.2012.01.056. Goebel, S., Fischer, R., Ferstl, R., & Mehdorn, H. M. (2009). Normative data and psychometric properties for qualitative and quantitative scorin g criteria o f the Five-point Test. The Clinical Neuropsychologist, 23, 675–690. Hsu, T.-Y., et al. (2011). Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. NeuroImage, 56, 2249–2257. https://doi.org/10.1016/j.neuroimage.2011.03.059. Husain, M., & Nachev, P. (2007). Space and the parietal cortex. Trends in Cognitive Sciences, 11, 30–36. https://doi.org/10.1016/j.tics.2006. 10.011.
95 Javadi, A. H., & Walsh, V. (2012). Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimulation, 5, 231–241. https://doi.org/10. 1016/j.brs.2011.06.007. Lee, G. P., Strauss, E., Loring, D. W., McCloskey, L., Haworth, J. M., & Lehman, R. A. (1997). Sensitivity of figural fluency on the fivepoint test to focal neurological dysfunction. The Clinical Neuropsychologist, 11, 59–68. Luft, C. D. B., Zioga, I., Banissy, M. J., & Bhattacharya, J. (2017). Relaxing learned constraints through cathodal tDCS on the left dorsolateral prefrontal cortex. Scientific Reports, 7, 2916. https://doi. org/10.1038/s41598-017-03022-2. Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202. Monti, A., Ferrucci, R., Fumagalli, M., Mameli, F., Cogiamanian, F., Ardolino, G., & Priori, A. (2013). Transcranial direct current stimulation (tDCS) and language. Journal of Neurology, Neurosurgery, and Psychiatry, 84, 832–842. Nejati, V., Salehinejad, M. A., & Nitsche, M. A. (2017a). Interaction of the left dorsolateral prefrontal cortex (l-DLPFC) and right orbitofrontal cortex (OFC) in hot and cold executive functions: Evidence from transcranial direct current stimulation (tDCS). Neuroscience. https://doi.org/10.1016/j.neuroscience.2017.10.042. Nejati, V., Salehinejad, M. A., Nitsche, M. A., Najian, A., & Javadi, A.-H. (2017b). Transcranial direct current stimulation improves executive dysfunctions in ADHD: Implications for inhibitory control, interference control, working memory, and cognitive flexibility. Journal of Attention Disorders. https://doi.org/10.1177/1087054717730611. Nejati, V., Salehinejad, M. A., Shahidi, N., & Abedin, A. (2017c). Psychological intervention combined with direct electrical brain stimulation (PIN-CODES) for treating major depression: A pre-test, post-test, follow-up pilot study. Neurology, Psychiatry and Brain Research, 25, 15–23. https://doi.org/10.1016/j.npbr.2017.05.003. Nitsche, M. A., Boggio, P. S., Fregni, F., & Pascual-Leone, A. (2009). Treatment of depression with transcranial direct current stimulation (tDCS): A review. Experimental Neurology, 219, 14–19. https://doi. org/10.1016/j.expneurol.2009.03.038. Nitsche, M. A., et al. (2007). Shaping the effects of transcranial direct current stimulation of the human motor cortex. Journal of Neurophysiology, 97, 3109–3117. https://doi.org/10.1152/jn. 01312.2006. Nitsche, M. A., Kuo, M.-F., Paulus, W., & Antal, A. (2015). Transcranial direct current stimulation: protocols and physiological mechanisms of action. In H. Knotkova & D. Rasche (Eds.), Textbook of neuromodulation: Principles, methods and clinical applications (pp. 101–111). New York: Springer New York. https://doi.org/10. 1007/978-1-4939-1408-1_9. Nusbaum, E. C., & Silvia, P. J. (2011). Are intelligence and creativity really so different? Intelligence, 39, 36–45. https://doi.org/10.1016/j. intell.2010.11.002. Palm, U., et al. (2013). Evaluation of sham transcranial direct current stimulation for randomized, placebo-controlled clinical trials. Brain Stimulation, 6, 690–695. https://doi.org/10.1016/j.brs.2013. 01.005. Regard, M., Strauss, E., & Knapp, P. (1982). Children’s production on verbal and non-verbal fluency tasks. Perceptual and Motor Skills, 55, 839–844. https://doi.org/10.2466/pms.1982.55.3.839. Ross, T. P., Lindsay Foard, E., Berry Hiott, F., & Vincent, A. (2003). The reliability of production strategy scores for the Ruff Figural Fluency Test. Archives of Clinical Neuropsychology, 18, 879–891. https:// doi.org/10.1016/S0887-6177(02)00163-4. Ruff, R. (2011). Design fluency test. In J. S. Kreutzer, J. DeLuca, & B. Caplan (Eds.), Encyclopedia of clinical neuropsychology (pp. 821– 822). New York: Springer New York. https://doi.org/10.1007/9780-387-79948-3_1426.
96 Ruff, R. M., Allen, C. C., Farrow, C. E., Niemann, H., & Wylie, T. (1994). Figural fluency: Differential impairment in patients with left versus right frontal lobe lesions. Archives of Clinical Neuropsychology, 9, 41–55. https://doi.org/10.1016/0887-6177(94)90013-2. Ruff, R. M., Light, R. H., & Evans, R. W. (1987). The ruff figural fluency t e st : A no r m a t i v e s t u d y w i t h a du l t s . D eve lopment al Neuropsychology, 3, 37–51. Ruff, R. M., Marshall, L. F., & Evans, R. (1986). Impaired verbal and figural fluency after head injury. Archives of Clinical Neuropsychology, 1, 87–101. https://doi.org/10.1016/08876177(86)90009-0. Runco MA (1991) Divergent thinking. Ablex Norwood, NJ. Runco, M. A. (2008). Commentary: Divergent thinking is not synonymous with creativity. Psychology of Aesthetics, Creativity, and the Arts, 2(2), 93–96. Salehinejad, M. A., Ghanavai, E., Rostami, R., & Nejati, V. (2017a). Cognitive control dysfunction in emotion dysregulation and psychopathology of major depression (MD): Evidence from transcranial brain stimulation of the dorsolateral prefrontal cortex (DLPFC). Journal of Affective Disorders, 210, 241–248. https://doi.org/10. 1016/j.jad.2016.12.036. Salehinejad, M. A., Nejati, V., & Derakhshan, M. (2017b). Neural correlates of trait resiliency: Evidence from electrical stimulation of the dorsolateral prefrontal cortex (dLPFC) and orbitofrontal cortex (OFC). Personality and Individual Differences, 106, 209–216. https://doi.org/10.1016/j.paid.2016.11.005. Shamay-Tsoory, S. G., Adler, N., Aharon-Peretz, J., Perry, D., & Mayseless, N. (2011). The origins of originality: The neural bases of creative thinking and originality. Neuropsychologia, 49, 178– 185. https://doi.org/10.1016/j.neuropsychologia.2010.11.020. Silvia, P. J., et al. (2008). Assessing creativity with divergent thinking tasks: Exploring the reliability and validity of new subjective scoring methods. Psychology of Aesthetics, Creativity, and the Arts, 2, 68. Tucha, L., Aschenbrenner, S., Koerts, J., & Lange, K. W. (2012). The Five-Point Test: Reliability, validity and normative data for children and adults. PLoS One, 7, e46080.
J Cogn Enhanc (2018) 2:88–96 Utz, K. S., Dimova, V., Oppenländer, K., & Kerkhoff, G. (2010). Electrified minds: Transcranial direct current stimulation (tDCS) and Galvanic Vestibular Stimulation (GVS) as methods of noninvasive brain stimulation in neuropsychology—A review of current data and future implications. Neuropsychologia, 48, 2789–2810. https://doi.org/10.1016/j.neuropsychologia.2010.06.002. van Eersel, M. E. A., Joosten, H., Koerts, J., Gansevoort, R. T., Slaets, J. P. J., & Izaks, G. J. (2015). Longitudinal study of performance on the ruff figural fluency test in persons aged 35 years or older. PLoS One, 10, e0121411. https://doi.org/10.1371/journal.pone.0121411. Veijola, J., Jokelainen, J., Läksy, K., Kantojärvi, L., Kokkonen, P., Järvelin, M. R., Joukamaa, M. (2003). The Hopkins Symptom Checklist-25 in screening DSM-III-R axis-I disorders. Nordic Journal of Psychiatry, 57(2), 119–123. Ward J (2015) The student’s guide to cognitive neuroscience. Psychology Press. Wassermann, E. M., & Grafman, J. (2005). Recharging cognition with DC brain polarization. Trends in Cognitive Sciences, 9, 503–505. https://doi.org/10.1016/j.tics.2005.09.001. Wysokiński, A., Zboralski, K., Orzechowska, A., Gałecki, P., Florkowski, A., & Talarowska, M. (2010). Normalization of the Verbal Fluency Test on the basis of results for healthy subjects, patients with schizophrenia, patients with organic lesions of the chronic nervous system and patients with type 1 and 2 diabetes. Archives of Medical Science : AMS, 6, 438–446. https://doi.org/10. 5114/aoms.2010.14268. Zalonis, I., et al. (2017). Verbal and figural fluency in temporal lobe epilepsy: Does hippocampal sclerosis affect performance? Cognitive and Behavioral Neurology, 30, 48–56. Zmigrod, S., Colzato, L. S., & Hommel, B. (2015). Stimulating creativity: Modulation of convergent and divergent thinking by transcranial direct current stimulation (tDCS). Creativity Research Journal, 27, 353–360. https://doi.org/10.1080/10400419.2015.1087280.