Author’s Accepted Manuscript Decreasing propensity to mind-wander with Transcranial direct current stimulation Shogo Kajimura, Michio Nomura
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S0028-3932(15)30098-1 http://dx.doi.org/10.1016/j.neuropsychologia.2015.07.013 NSY5666
To appear in: Neuropsychologia Received date: 16 March 2015 Revised date: 7 June 2015 Accepted date: 11 July 2015 Cite this article as: Shogo Kajimura and Michio Nomura, Decreasing propensity to mind-wander with Transcranial direct current stimulation, Neuropsychologia, http://dx.doi.org/10.1016/j.neuropsychologia.2015.07.013 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Title: Decreasing propensity to mind-wander with transcranial direct current stimulation Authors: Shogo Kajimura and Michio Nomura Affiliation: Department of Cognitive Psychology in Education, Graduate School of Education, Kyoto University, Kyoto, Japan Corresponding author: Shogo Kajimura Graduate School of Education, Kyoto University, Kyoto, Japan, 606-8501. E-mail address: [email protected] Tel and FAX: +81 75 753 3004 Abstract Mind wandering or task-unrelated thought (TUT) is associated with various impairments as well as with adaptive functions, indicating the importance of regulating this process. Although Axelrod and colleagues (2015) have shown that anodal/cathodal transcranial direct current stimulation (tDCS) of the left/right lateral prefrontal cortex (LPFC) could increase the propensity for mind wandering, it remains unclear whether a different tDCS protocol could have the reverse effect. The present study investigated whether and how simultaneous stimulation of the left LPFC and right inferior parietal lobule (IPL) could modulate TUTs. These areas may be crucial for regulating both TUTs and its neural underpinning (default mode network). We applied tDCS to the right IPL/left LPFC prior to a perceptually demanding flanker task and compared TUT propensity during the task among tDCS groups. We found that TUT propensity was reduced by anodal/cathodal tDCS of the right IPL/left LPFC compared with cathodal/anodal tDCS, and the results for the sham group were intermediate between these two groups. This is the first study to demonstrate that tDCS can decrease, as well as increase, TUT propensity. Keywords: Task-unrelated thoughts; transcranial direct current stimulation; default mode network; right inferior parietal lobule; perceptual load task
Article body Introduction Mind wandering is the spontaneous transition of internal attention mainly to self-generated thoughts and occupies up to half of our waking hours (Axelrod et al. 2015). Mind wandering is related to adaptive functions such as planning, creativity, and a coherent sense of self (Andrews-Hanna, Smallwood, and Spreng 2014). However, mind wandering, also referred to as task-unrelated thoughts (TUTs), causes intermittent shifts of attention from the task at hand and dampens sensory information 1
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processing (Baird et al. 2014; Barron et al. 2011), resulting in poor task performance (Kam, Dao, and Stanciulescu 2013; Kane and McVay 2012), accidents (He et al. 2011), and maladaptation (e.g., poor lesson comprehension; Smallwood, Fishman, and Schooler 2007). Thus, regulating mind wandering propensity is quite important. Transcranial direct current stimulation (tDCS) is a low-cost, portable, noninvasive neuromodulation technique that may be suited to external regulation of TUT propensity (Axelrod et al., 2015; Coffman et al., 2014). tDCS has been shown to enhance various cognitive functions such as attention, learning, and memory (Coffman et al., 2014) and the effects last up to 1 hour following a 20-min session (Nitsche et al., 2003). Surprisingly and intriguingly, Axelrod and colleagues recently succeeded in increasing TUT propensity using tDCS (Axelrod et al. 2015). They applied the anodal electrode (generally increases neuronal excitability) to the left lateral prefrontal cortex (LPFC), which has been shown to be activated during mind wandering (Christoff et al., 2009), and the cathode (generally decreases neuronal excitability) to the right supraorbital area as a reference electrode. Stimulation that was applied during the first half of an attention task caused a clear increase in TUT propensity throughout the task. However, it remains unknown whether tDCS could decrease TUT propensity under different conditions. We know of two possible methods for decreasing TUT propensity, which may be combinable. One is cathodal stimulation of the left LPFC (Coffman et al., 2014). The other is anodal stimulation of the right inferior parietal lobule (IPL). The IPL is a core region of the default mode network (DMN) (Buckner et al., 2008) that is strongly linked with mind wandering (Fox et al., 2015). Furthermore, the right IPL has been implicated as a crucial regulator of TUTs via its effect on the other regions of the DMN (Christoff et al. 2009; Di and Biswal 2014; Hasenkamp et al. 2012; Mason et al. 2007). For example, Hasenkamp and colleagues examined neural activity related to mental experiences during meditation and reported that the IPL activates when attention shifts from mind wandering to breathing (Hasenkamp et al. 2012). In addition, dynamic causal modeling analysis of resting-state data has indicated that the right IPL causally affects activities in other core regions of the DMN (Di and Biswal 2014). Collectively, the data suggest that the right IPL is important in regulating TUTs and thus tDCS of the right IPL/left LPFC, with IPL anodal, is an appropriate strategy for external downregulation of TUT propensity. The present study explored whether tDCS of the right IPL/left LPFC can decrease TUT propensity. We hypothesized that the cathodal/anodal tDCS of the right IPL/left LPFC, which reproduces the anodal stimulation of the left LPFC implemented by Axelrod et al. (2015), would replicate the reported increasing effect of tDCS on TUT propensity. On the other hand, tDCS of the right IPL/left LPFC, with IPL anodal, is predicted to induce the opposite effect: a decrease in mind wandering. Since the IPL is involved in distractor filtering (Weiss and Lavidor, 2012) and response 2
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conflict resolution (Wendelken et al., 2009) as well as in DMN operations, we also made exploratory measurements to determine the effects of tDCS on such attention-related functions using a multi-condition, attention-demanding task. Materials and Methods Participants Eighty healthy participants with no history of neurological or psychiatric disease were paid to participate in this study (34 females; mean age = 21.5 years, SD = 2.4; only 1 participant, in the sham group, was left-handed). Participants were randomly allocated to three stimulation groups with different brain stimulation configurations (anode, cathode, and sham [control group]). Before conducting the data analyses, we excluded seven participants from further analyses: five participants were suspected to have made insincere responses because they selected the same thought probe category (see below) throughout at least one block, and two participants had trouble with the task program or the tDCS equipment. Ultimately, we included 24 participants in the anode group (14 males, mean age = 21.4 ± 2.6 years), 24 in the sham group (13 males, mean age = 21.0 ± 1.9 years), and 25 in the cathode group (14 males, mean age = 21.9 ± 2.6 years). These sample sizes are more than two-fold greater than in previous between-subjects tDCS studies (Axelrod et al. 2015; Weiss and Lavidor 2012). Participants provided written, informed consent before taking part in the study. The study was approved by the local institutional review board committee. tDCS Direct current was transferred by a saline-soaked pair of surface sponge electrodes (7 × 5 cm) and delivered by a battery-driven, constant-current stimulator (DC-stimulator, NeuroConn GmbH, Germany). The target electrode was placed over P4 according to the 10–20 International system for electroencephalographic electrode placement (Okamoto et al. 2004). The reference electrode was placed around AF7 over the LPFC (Bolognini et al. 2015; Nitsche et al. 2008). In the anode group, the anode and cathode were placed on P4 and around the AF7, respectively; these placements were reversed for the cathode group. Half of the participants in the sham group had the same electrode placement as the anode group, and the other half matched that of the cathode group. A constant 1.5-mA current was applied for 20 min. Participants felt the current as an itching sensation at both electrode contact points at the beginning of the stimulation. For sham stimulation, the stimulator was turned off after 30 s. Therefore, all participants felt the initial itching sensation but the sham group received no current for the rest of the stimulation period. This procedure enabled us to keep participants blind to their stimulation group.
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Perceptual Load Task We used the perceptual load task (Lavie and Cox 1997) which is known to induce sufficient TUTs (Forster and Lavie, 2009). Participants searched for two possible target letters (N or X) among central nontarget letters (see examples in Fig. 1). Participants responded by pressing a key to indicate which target letter was included in the stimulus. The task consists of two conditions: perceptual load and congruency. In the low-perceptual load condition, the circle included the target letter with five Os (low-competition condition). In the high-perceptual load condition, the circle contained the target letter and five additional competing letters (H, K, M, W, and Z; high-competition condition). In addition to the perceptual load, a flanker appeared to the right or left of the circle with equal probability. The flanker, which the participant was instructed to ignore, was X or N and could be congruent with or not congruent with the target letter (congruent condition and incongruent condition, respectively). The task was administered using Hot Soup Processor version 3.3 software (ONION software, Japan) on a 19-inch computer monitor (P190S, 1280 × 1024 pixels, refresh rate 75 Hz; Dell, USA). The distance between the participant and the monitor was about 57 cm. A fixation letter was displayed in the center of the monitor in a white 25-point Miriam font. The central and flanker letters were white in 31- and 37-point fonts, respectively. All letters were uppercase. Circle letters subtended 0.9° vertically and 0.6° horizontally. The flanker subtended 1.1° vertically and 0.9° horizontally. The distances from fixation to the central letters and the flanker subtended 2.1° and 4.3°, respectively. Target position, target letter, and distractor congruency were counterbalanced. Trial presentation was randomized within each session. Each experiment consisted of 3 sessions of 192 trials (48 trials for 4 conditions). Each trial began with a 500-ms fixation period before the stimulus was presented for 100 ms. A blank response screen was then presented until the response occurred or for 2,000 ms. A response after 2,000 ms was encoded as a miss. A blank screen was then presented for the intertrial interval of 2,600 ms minus the response time (RT), or for an additional 600 ms in the case of a miss trial. Thought probes Thought probes that required the participants to classify the contents of their immediately preceding thoughts appeared during the perceptual load task. Participants responded based on their thought content just before the probe appeared. The thought probe categories were: “1. Task contents,” “2. Task performance,” “3. A memory from the past,” “4. Something in the future,” “5. Current state of being,” “6. Fantasy,” and “7. Other.” Subjects responded by pressing corresponding keys (clearly explained in the instructions). The first thought probe of each block was always presented after the twelfth trial, and thereafter every seventh to ninth trial. This ensured that each probe appeared every 22.4–28.8 s. Each session 4
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included 20 thought probes. For analysis, the first and second categories were coded as task-related thoughts. We coded category 3–7 responses as TUTs, and we focused our analyses on these thought categories. Procedure After completing a practice session (24 trials and 2 thought probes), participants underwent tDCS before the task. During the stimulation period, participants were instructed to remain calm without napping. Before and after stimulation, they completed the positive and negative affect scale (PANAS) (Watson, Clark, and Tellegen 1988) and a 6-point discomfort scale (included in the PANAS negative mood for analysis). For purposes of assessing the effect of stimulation on motivation and mood, which might affect TUT propensity (Eastwood et al. 2012; Smallwood et al. 2009), participants were instructed to consider their “current” feelings instead of those of “the past few hours.” After stimulation, the electrodes were removed, and the subjects performed the perceptual load task. Data analyses We analyzed z-transformed PANAS indices using a three-way repeated-measures analysis of variance (ANOVA) (3 tDCS groups [between subject; anode, sham, cathode] × 2 moods [within; positive, negative] × 2 timings [within; time1 = before stimulation, time2 = after stimulation]). Because mood differences between groups potentially distort the main results as a confounding factor (Eastwood et al. 2012; Smallwood et al. 2009), the main analyses controlled for mood scores as covariates if there were any differences among tDCS groups, as well as controlling for the post-tDCS motivation score of the PANAS. For the TUT index (ratio of TUTs), we conducted a one-way analysis of covariance (ANCOVA, 3 tDCS groups [between]). For the task performance (performance accuracy and correct RT), we conducted a three-way repeated measures ANCOVA (3 tDCS groups × 2 load conditions [within; low, high] × 2 congruency conditions [within; congruent, incongruent]). In addition, the flanker effect was analyzed using a two-way repeated measures ANCOVA (3 tDCS groups × 2 load conditions). The flanker effect was defined for accuracy
as
(congruent
–
incongruent)/congruent,
and
for
RT
as
(incongruent
–
congruent)/congruent. If compatible effects were found between the modulations of TUT index and task performance, mediation analyses were conducted to examine whether the modulation of task performance induced by tDCS was mediated by a modulation of TUT. Results The descriptive statistics for the PANAS, TUT index, accuracy, and RTs are summarized in 5
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Table 1. ANOVA and ANCOVA PANAS. The three-way ANOVA showed an interaction between stimulation and mood (F[2, 70] = 2.35, p < .004, ηp2 = .144). Post hoc Bonferroni tests revealed that negative mood was higher than positive mood in the cathode group (F[1, 70] = 4.60, p = .036, ηp2 = .062), but the reverse relationship was observed in the sham group (F[1, 70] = 6.65, p = .012, ηp2 = .087). Thus, we included the difference between positive and negative moods as well as the post-tDCS motivation as covariates in subsequent analyses (the Spearman correlations of these indices were low [r = .24]). TUT propensity. The one-way ANCOVA showed a main effect of tDCS group (F[2, 68] = 4.10, p = .021, ηp2 = .108). Importantly, post hoc Bonferroni tests revealed that TUT propensity was significantly decreased in the anode group compared with the cathode group (p = .017, Cohen’s d = 0.82). This result indicated that preceding tDCS modulated TUT propensity in the subsequent attention task in a polarity-specific manner (see Fig. 2). Task performance. A three-way ANCOVA for RT only showed a main effect of load (F[1, 68] = 96.05, p = .000, ηp2 = .585). On the other hand, the main effects on accuracy of load and congruency were significant (F[1, 68] = 116.75, p = .000, ηp2 = .632; F[1, 68] = 7.631, p = .007, ηp2 = .101). Accuracy rates were higher in the low-load or congruent condition than in the high-load or incongruent condition. A three-way interaction was also found (F[2, 68] = 4.901, p = .010, ηp2 = .126). Sub effect tests revealed an inverse pattern between the sham and anode or cathode groups. In the sham group, low-load accuracy was decreased in the incongruent condition compared to the congruent condition (F[1, 68] = 24.57, p = .000, ηp2 = .265), and there was no difference in the high-load condition (F[1, 68] = 0.092, p = .763, ηp2 = .001). This finding is compatible with those of previous studies (Lavie 2005). Contrarily and surprisingly, there were no accuracy differences in either the anode or cathode groups in the low-load condition (anode: F[1, 68] = 2.08, p = .154, ηp2 = .030; cathode: F[1, 68] = 2.77, p = .101, η p2 = .039), and accuracy in the high-load/incongruent condition was lower than that in the high-load/congruent condition (anode: F[1, 68] = 12.11, p = .001, ηp2 = .151; cathode: F[1, 68] = 7.01, p = .010, ηp2 = .093). Furthermore, a two-way ANCOVA to assess the flanker effect on accuracy showed an interaction (F[2, 68] = 4.81, p = .011, ηp2 = .124; Fig. 3). Sub effect tests revealed that compared to sham, the flanker effect on the anodal group was significantly smaller in the low-load condition (p = .039, d = 0.79) and marginally larger in the high-load condition (p = .095, d = 0.64). The flanker effect on the cathodal group was marginally smaller in the low-load condition compared to sham (p = .081, d = 0.73). These results reveal that both anode and cathode groups, which have different mechanisms, have the same pattern of modulation of interference resolution and distractor processing during a perceptual load task. Because no congruent modulation effect was found between 6
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TUT index and task performance, further analysis was not conducted. Discussion Our main purpose was to explore whether tDCS of the right IPL/left LPFC can decrease, as well as increase, TUT propensity. We identified a main finding and additional observations supporting a significant effect of tDCS: TUT propensity was reduced by anodal/cathodal tDCS of the right IPL/left LPFC compared to cathodal/anodal tDCS of the same sites, and the flanker effects in both high- and low-load conditions were modulated in both stimulation groups independently of TUT modulation. To the best of our knowledge, this is the first study demonstrating that TUT propensity can be externally decreased via tDCS. Because mind wandering has both costs and benefits, it is quite beneficial for an understanding of the neural mechanisms of mind wandering regulation that tDCS can modulate mind wandering propensity in both an increasing (Axelrod et al., 2015) and a decreasing direction. In addition to the increase in TUT propensity by cathodal/anodal tDCS of the right IPL/left LPFC, which corresponds to the results of Axelrod et al. (2015), there was significantly different TUT propensity between the non-sham tDCS groups. However, comparisons between each non-sham tDCS group and the corresponding sham tDCS group did not show significant differences. This could be due to how TUT propensity was assessed. The thought probe used in this study was almost identical to the method of Kane & McVay (2012); asking participants to choose the most appropriate item representing the contents of their thoughts immediately before the probe and indexing the proportion of TUTs to reflect the frequency. On the other hand, the probe used by Axelrod et al. (2015) originally asked participants to choose the most appropriate extent of TUT experience, which is similar to that of Christoff et al. (2009). Axelrod et al. (2015) employed a four-point Likert scale and used the mean scores as the original index of TUT propensity, which might reflect TUT engagement as well as TUT frequency. Such a method might enable more accurate measurement of the effects of tDCS on TUT-related processing because it includes more components than the method used here that could be affected by the tDCS protocol. Thus, using the same thought probes as Axelrod et al. (2015), we might have been able to find clearer tDCS effects on TUT propensity. Nevertheless, the present results establish that tDCS of the right IPL/left LPFC can modulate TUT propensity. Although the precise neural underpinnings of the present results were not revealed, the supporting evidence for the present hypotheses indicates that the modulation of TUT propensity is induced in part via modulation of DMN function (Di and Biswal 2014; Hasenkamp et al. 2012; Taylor et al. 2013). The right IPL has been implicated as a crucial regulator of the DMN regions (Christoff et al. 2009; Di and Biswal 2014; Hasenkamp et al. 2012; Mason et al. 2007) that is 7
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strongly linked to mind wandering in addition to the left LPFC (Fox et al., 2015). Moreover, studies show that tDCS of the left LPFC also alters functional connectivity within the DMN (Keeser et al. 2011; Peña-Gómez et al. 2012). Considered in light of the present results, these studies suggest that tDCS of the right IPL/left LPFC induces alteration of DMN function (anodal/cathodal, upregulation; cathodal/anodal, downregulation), resulting in modulation of TUT propensity. To clarify the precise neural underpinnings of these observations, further studies using functional magnetic resonance imaging (fMRI) are needed. The supplementary observations made here may be associated with the right IPL’s multiple attention-related roles such as filtering distractor stimuli under high-load conditions (Weiss and Lavidor, 2012) and resolving response conflicts (Wendelken et al., 2009). First, the change in TUT propensity did not relate to task performance modulation, replicating the result of Axelrod et al. (2015). Incidental modulation of the attention processes by tDCS of the right IPL/left LPFC may disturb detecting the influence of TUT modulation on task performance. Second, the flanker effects were modulated in a load condition-dependent way (low-load, decrease; high-load, increase). One possible explanation for these phenomena is that while the modulation of the right IPL by tDCS improves response conflict processing under low-load conditions, the effect is restricted by consumption of neural resource for distractor filtering in high-load. To make progress in elucidating these issues, the use of high-definition tDCS (HD-tDCS), a novel technique of higher spatial resolution than regular tDCS, would be useful in attempts to modulate TUT propensity, because of fewer side effects and an ability to investigate the relationships between specific regions within the IPL and TUT/attentional processes. It would also be worth investigating whether and how tDCS of the left IPL, which is also part of the DMN, affects mind wandering propensity. Unlike the right IPL, the left IPL is included in the language network (Catani, Jones, and Ffytche, 2005) and is seemingly more related to the generation of mind wandering (Fox et al., 2015; Taylor et al., 2013). Therefore, the hemisphere-reversed version of the present tDCS protocol, that is, stimulation of the left IPL/right LPFC, may induce modulation effects opposite to those observed in the present study. In addition, stimulation of right IPL/left IPL may further strengthen the modulation effects. In conclusion, our results revealed that tDCS applied to the right IPL/left LPFC can modulate mind wandering propensity to decrease it as well as to increase it. Future fMRI and HD-tDCS studies will further reveal the neural mechanisms of mind wandering and identify tDCS protocols that can modulate mind wandering more effectively.
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Acknowledgments The authors thank Prof. Yoshihiro Kadono, Ohmula hospital, for medical support. This work was supported by MEXT. KAKENHI (Grant Number: 24240041). The authors declare no conflict of interest.
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Tables Table 1. Means and standard deviations of the TUT index and PANAS scores TUT
PANAS Time 1
Time 2
Positive
Negative
Positive
Negative
0.170 (1.00)
0.012 (1.00)
-0.232 (1.03)
0.070 (0.99)
Anode
38.06 (22.15)
Sham
46.32 (24.55) -0.126 (0.93) -0.247 (1.12) -0.033 (1.10) -0.381 (0.99)
Cathode 51.67 (21.82) -0.118 (0.97)
0.226 (0.83)
0.109 (0.80)
-0.516 (1.00)
Table 2. Means and standard deviations of task performance Low-Load Congruent Acc Anode
.97 (.03)
Sham
.97 (.03)
Cathode
.97 (.02)
RT 589.6 (70.7) 577.2 (102.5) 612.5 (72.8)
High-Load Incongruent
Acc .96 (.03) .94 (.06) .96 (.02)
RT 613.5 (68.8) 593.3 (94.1) 635.8 (76.6)
Congruent Acc .80 (.09) .77 (.09) .77 (.08)
RT 971.7 (130.2) 955.9 (154.7) 1000.2 (125.0)
Incongruent Acc .75 (.10) .76 (.08) .74 (.10)
RT 979.8 (126.1) 961.1 (153.9) 1009.4 (136.0)
Acc: Accuracy. Figure Legends Fig. 1. Examples of the perceptual load task stimuli for each condition Fig. 2. TUT propensity for each stimulation condition (error bars are the standard error of the mean) Fig. 3. The flanker effect on accuracy calculated as (congruent – incongruent)/congruent for each load condition (error bars are the standard error of the mean) Figure 1
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Figure 2
Figure 3
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Highlights This study explore whether tDCS of the right IPL/left LPFC can decrease TUT. TUT is reduced by anodal/cathodal tDCS of the right IPL/left LPFC. The results indicate the TUT modulation is induced via modulation of DMN function.
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PII: DOI: Reference:
S0028-3932(15)30098-1 http://dx.doi.org/10.1016/j.neuropsychologia.2015.07.013 NSY5666
To appear in: Neuropsychologia Received date: 16 March 2015 Revised date: 7 June 2015 Accepted date: 11 July 2015 Cite this article as: Shogo Kajimura and Michio Nomura, Decreasing propensity to mind-wander with Transcranial direct current stimulation, Neuropsychologia, http://dx.doi.org/10.1016/j.neuropsychologia.2015.07.013 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Title: Decreasing propensity to mind-wander with transcranial direct current stimulation Authors: Shogo Kajimura and Michio Nomura Affiliation: Department of Cognitive Psychology in Education, Graduate School of Education, Kyoto University, Kyoto, Japan Corresponding author: Shogo Kajimura Graduate School of Education, Kyoto University, Kyoto, Japan, 606-8501. E-mail address: [email protected] Tel and FAX: +81 75 753 3004 Abstract Mind wandering or task-unrelated thought (TUT) is associated with various impairments as well as with adaptive functions, indicating the importance of regulating this process. Although Axelrod and colleagues (2015) have shown that anodal/cathodal transcranial direct current stimulation (tDCS) of the left/right lateral prefrontal cortex (LPFC) could increase the propensity for mind wandering, it remains unclear whether a different tDCS protocol could have the reverse effect. The present study investigated whether and how simultaneous stimulation of the left LPFC and right inferior parietal lobule (IPL) could modulate TUTs. These areas may be crucial for regulating both TUTs and its neural underpinning (default mode network). We applied tDCS to the right IPL/left LPFC prior to a perceptually demanding flanker task and compared TUT propensity during the task among tDCS groups. We found that TUT propensity was reduced by anodal/cathodal tDCS of the right IPL/left LPFC compared with cathodal/anodal tDCS, and the results for the sham group were intermediate between these two groups. This is the first study to demonstrate that tDCS can decrease, as well as increase, TUT propensity. Keywords: Task-unrelated thoughts; transcranial direct current stimulation; default mode network; right inferior parietal lobule; perceptual load task
Article body Introduction Mind wandering is the spontaneous transition of internal attention mainly to self-generated thoughts and occupies up to half of our waking hours (Axelrod et al. 2015). Mind wandering is related to adaptive functions such as planning, creativity, and a coherent sense of self (Andrews-Hanna, Smallwood, and Spreng 2014). However, mind wandering, also referred to as task-unrelated thoughts (TUTs), causes intermittent shifts of attention from the task at hand and dampens sensory information 1
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processing (Baird et al. 2014; Barron et al. 2011), resulting in poor task performance (Kam, Dao, and Stanciulescu 2013; Kane and McVay 2012), accidents (He et al. 2011), and maladaptation (e.g., poor lesson comprehension; Smallwood, Fishman, and Schooler 2007). Thus, regulating mind wandering propensity is quite important. Transcranial direct current stimulation (tDCS) is a low-cost, portable, noninvasive neuromodulation technique that may be suited to external regulation of TUT propensity (Axelrod et al., 2015; Coffman et al., 2014). tDCS has been shown to enhance various cognitive functions such as attention, learning, and memory (Coffman et al., 2014) and the effects last up to 1 hour following a 20-min session (Nitsche et al., 2003). Surprisingly and intriguingly, Axelrod and colleagues recently succeeded in increasing TUT propensity using tDCS (Axelrod et al. 2015). They applied the anodal electrode (generally increases neuronal excitability) to the left lateral prefrontal cortex (LPFC), which has been shown to be activated during mind wandering (Christoff et al., 2009), and the cathode (generally decreases neuronal excitability) to the right supraorbital area as a reference electrode. Stimulation that was applied during the first half of an attention task caused a clear increase in TUT propensity throughout the task. However, it remains unknown whether tDCS could decrease TUT propensity under different conditions. We know of two possible methods for decreasing TUT propensity, which may be combinable. One is cathodal stimulation of the left LPFC (Coffman et al., 2014). The other is anodal stimulation of the right inferior parietal lobule (IPL). The IPL is a core region of the default mode network (DMN) (Buckner et al., 2008) that is strongly linked with mind wandering (Fox et al., 2015). Furthermore, the right IPL has been implicated as a crucial regulator of TUTs via its effect on the other regions of the DMN (Christoff et al. 2009; Di and Biswal 2014; Hasenkamp et al. 2012; Mason et al. 2007). For example, Hasenkamp and colleagues examined neural activity related to mental experiences during meditation and reported that the IPL activates when attention shifts from mind wandering to breathing (Hasenkamp et al. 2012). In addition, dynamic causal modeling analysis of resting-state data has indicated that the right IPL causally affects activities in other core regions of the DMN (Di and Biswal 2014). Collectively, the data suggest that the right IPL is important in regulating TUTs and thus tDCS of the right IPL/left LPFC, with IPL anodal, is an appropriate strategy for external downregulation of TUT propensity. The present study explored whether tDCS of the right IPL/left LPFC can decrease TUT propensity. We hypothesized that the cathodal/anodal tDCS of the right IPL/left LPFC, which reproduces the anodal stimulation of the left LPFC implemented by Axelrod et al. (2015), would replicate the reported increasing effect of tDCS on TUT propensity. On the other hand, tDCS of the right IPL/left LPFC, with IPL anodal, is predicted to induce the opposite effect: a decrease in mind wandering. Since the IPL is involved in distractor filtering (Weiss and Lavidor, 2012) and response 2
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conflict resolution (Wendelken et al., 2009) as well as in DMN operations, we also made exploratory measurements to determine the effects of tDCS on such attention-related functions using a multi-condition, attention-demanding task. Materials and Methods Participants Eighty healthy participants with no history of neurological or psychiatric disease were paid to participate in this study (34 females; mean age = 21.5 years, SD = 2.4; only 1 participant, in the sham group, was left-handed). Participants were randomly allocated to three stimulation groups with different brain stimulation configurations (anode, cathode, and sham [control group]). Before conducting the data analyses, we excluded seven participants from further analyses: five participants were suspected to have made insincere responses because they selected the same thought probe category (see below) throughout at least one block, and two participants had trouble with the task program or the tDCS equipment. Ultimately, we included 24 participants in the anode group (14 males, mean age = 21.4 ± 2.6 years), 24 in the sham group (13 males, mean age = 21.0 ± 1.9 years), and 25 in the cathode group (14 males, mean age = 21.9 ± 2.6 years). These sample sizes are more than two-fold greater than in previous between-subjects tDCS studies (Axelrod et al. 2015; Weiss and Lavidor 2012). Participants provided written, informed consent before taking part in the study. The study was approved by the local institutional review board committee. tDCS Direct current was transferred by a saline-soaked pair of surface sponge electrodes (7 × 5 cm) and delivered by a battery-driven, constant-current stimulator (DC-stimulator, NeuroConn GmbH, Germany). The target electrode was placed over P4 according to the 10–20 International system for electroencephalographic electrode placement (Okamoto et al. 2004). The reference electrode was placed around AF7 over the LPFC (Bolognini et al. 2015; Nitsche et al. 2008). In the anode group, the anode and cathode were placed on P4 and around the AF7, respectively; these placements were reversed for the cathode group. Half of the participants in the sham group had the same electrode placement as the anode group, and the other half matched that of the cathode group. A constant 1.5-mA current was applied for 20 min. Participants felt the current as an itching sensation at both electrode contact points at the beginning of the stimulation. For sham stimulation, the stimulator was turned off after 30 s. Therefore, all participants felt the initial itching sensation but the sham group received no current for the rest of the stimulation period. This procedure enabled us to keep participants blind to their stimulation group.
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Perceptual Load Task We used the perceptual load task (Lavie and Cox 1997) which is known to induce sufficient TUTs (Forster and Lavie, 2009). Participants searched for two possible target letters (N or X) among central nontarget letters (see examples in Fig. 1). Participants responded by pressing a key to indicate which target letter was included in the stimulus. The task consists of two conditions: perceptual load and congruency. In the low-perceptual load condition, the circle included the target letter with five Os (low-competition condition). In the high-perceptual load condition, the circle contained the target letter and five additional competing letters (H, K, M, W, and Z; high-competition condition). In addition to the perceptual load, a flanker appeared to the right or left of the circle with equal probability. The flanker, which the participant was instructed to ignore, was X or N and could be congruent with or not congruent with the target letter (congruent condition and incongruent condition, respectively). The task was administered using Hot Soup Processor version 3.3 software (ONION software, Japan) on a 19-inch computer monitor (P190S, 1280 × 1024 pixels, refresh rate 75 Hz; Dell, USA). The distance between the participant and the monitor was about 57 cm. A fixation letter was displayed in the center of the monitor in a white 25-point Miriam font. The central and flanker letters were white in 31- and 37-point fonts, respectively. All letters were uppercase. Circle letters subtended 0.9° vertically and 0.6° horizontally. The flanker subtended 1.1° vertically and 0.9° horizontally. The distances from fixation to the central letters and the flanker subtended 2.1° and 4.3°, respectively. Target position, target letter, and distractor congruency were counterbalanced. Trial presentation was randomized within each session. Each experiment consisted of 3 sessions of 192 trials (48 trials for 4 conditions). Each trial began with a 500-ms fixation period before the stimulus was presented for 100 ms. A blank response screen was then presented until the response occurred or for 2,000 ms. A response after 2,000 ms was encoded as a miss. A blank screen was then presented for the intertrial interval of 2,600 ms minus the response time (RT), or for an additional 600 ms in the case of a miss trial. Thought probes Thought probes that required the participants to classify the contents of their immediately preceding thoughts appeared during the perceptual load task. Participants responded based on their thought content just before the probe appeared. The thought probe categories were: “1. Task contents,” “2. Task performance,” “3. A memory from the past,” “4. Something in the future,” “5. Current state of being,” “6. Fantasy,” and “7. Other.” Subjects responded by pressing corresponding keys (clearly explained in the instructions). The first thought probe of each block was always presented after the twelfth trial, and thereafter every seventh to ninth trial. This ensured that each probe appeared every 22.4–28.8 s. Each session 4
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included 20 thought probes. For analysis, the first and second categories were coded as task-related thoughts. We coded category 3–7 responses as TUTs, and we focused our analyses on these thought categories. Procedure After completing a practice session (24 trials and 2 thought probes), participants underwent tDCS before the task. During the stimulation period, participants were instructed to remain calm without napping. Before and after stimulation, they completed the positive and negative affect scale (PANAS) (Watson, Clark, and Tellegen 1988) and a 6-point discomfort scale (included in the PANAS negative mood for analysis). For purposes of assessing the effect of stimulation on motivation and mood, which might affect TUT propensity (Eastwood et al. 2012; Smallwood et al. 2009), participants were instructed to consider their “current” feelings instead of those of “the past few hours.” After stimulation, the electrodes were removed, and the subjects performed the perceptual load task. Data analyses We analyzed z-transformed PANAS indices using a three-way repeated-measures analysis of variance (ANOVA) (3 tDCS groups [between subject; anode, sham, cathode] × 2 moods [within; positive, negative] × 2 timings [within; time1 = before stimulation, time2 = after stimulation]). Because mood differences between groups potentially distort the main results as a confounding factor (Eastwood et al. 2012; Smallwood et al. 2009), the main analyses controlled for mood scores as covariates if there were any differences among tDCS groups, as well as controlling for the post-tDCS motivation score of the PANAS. For the TUT index (ratio of TUTs), we conducted a one-way analysis of covariance (ANCOVA, 3 tDCS groups [between]). For the task performance (performance accuracy and correct RT), we conducted a three-way repeated measures ANCOVA (3 tDCS groups × 2 load conditions [within; low, high] × 2 congruency conditions [within; congruent, incongruent]). In addition, the flanker effect was analyzed using a two-way repeated measures ANCOVA (3 tDCS groups × 2 load conditions). The flanker effect was defined for accuracy
as
(congruent
–
incongruent)/congruent,
and
for
RT
as
(incongruent
–
congruent)/congruent. If compatible effects were found between the modulations of TUT index and task performance, mediation analyses were conducted to examine whether the modulation of task performance induced by tDCS was mediated by a modulation of TUT. Results The descriptive statistics for the PANAS, TUT index, accuracy, and RTs are summarized in 5
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Table 1. ANOVA and ANCOVA PANAS. The three-way ANOVA showed an interaction between stimulation and mood (F[2, 70] = 2.35, p < .004, ηp2 = .144). Post hoc Bonferroni tests revealed that negative mood was higher than positive mood in the cathode group (F[1, 70] = 4.60, p = .036, ηp2 = .062), but the reverse relationship was observed in the sham group (F[1, 70] = 6.65, p = .012, ηp2 = .087). Thus, we included the difference between positive and negative moods as well as the post-tDCS motivation as covariates in subsequent analyses (the Spearman correlations of these indices were low [r = .24]). TUT propensity. The one-way ANCOVA showed a main effect of tDCS group (F[2, 68] = 4.10, p = .021, ηp2 = .108). Importantly, post hoc Bonferroni tests revealed that TUT propensity was significantly decreased in the anode group compared with the cathode group (p = .017, Cohen’s d = 0.82). This result indicated that preceding tDCS modulated TUT propensity in the subsequent attention task in a polarity-specific manner (see Fig. 2). Task performance. A three-way ANCOVA for RT only showed a main effect of load (F[1, 68] = 96.05, p = .000, ηp2 = .585). On the other hand, the main effects on accuracy of load and congruency were significant (F[1, 68] = 116.75, p = .000, ηp2 = .632; F[1, 68] = 7.631, p = .007, ηp2 = .101). Accuracy rates were higher in the low-load or congruent condition than in the high-load or incongruent condition. A three-way interaction was also found (F[2, 68] = 4.901, p = .010, ηp2 = .126). Sub effect tests revealed an inverse pattern between the sham and anode or cathode groups. In the sham group, low-load accuracy was decreased in the incongruent condition compared to the congruent condition (F[1, 68] = 24.57, p = .000, ηp2 = .265), and there was no difference in the high-load condition (F[1, 68] = 0.092, p = .763, ηp2 = .001). This finding is compatible with those of previous studies (Lavie 2005). Contrarily and surprisingly, there were no accuracy differences in either the anode or cathode groups in the low-load condition (anode: F[1, 68] = 2.08, p = .154, ηp2 = .030; cathode: F[1, 68] = 2.77, p = .101, η p2 = .039), and accuracy in the high-load/incongruent condition was lower than that in the high-load/congruent condition (anode: F[1, 68] = 12.11, p = .001, ηp2 = .151; cathode: F[1, 68] = 7.01, p = .010, ηp2 = .093). Furthermore, a two-way ANCOVA to assess the flanker effect on accuracy showed an interaction (F[2, 68] = 4.81, p = .011, ηp2 = .124; Fig. 3). Sub effect tests revealed that compared to sham, the flanker effect on the anodal group was significantly smaller in the low-load condition (p = .039, d = 0.79) and marginally larger in the high-load condition (p = .095, d = 0.64). The flanker effect on the cathodal group was marginally smaller in the low-load condition compared to sham (p = .081, d = 0.73). These results reveal that both anode and cathode groups, which have different mechanisms, have the same pattern of modulation of interference resolution and distractor processing during a perceptual load task. Because no congruent modulation effect was found between 6
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TUT index and task performance, further analysis was not conducted. Discussion Our main purpose was to explore whether tDCS of the right IPL/left LPFC can decrease, as well as increase, TUT propensity. We identified a main finding and additional observations supporting a significant effect of tDCS: TUT propensity was reduced by anodal/cathodal tDCS of the right IPL/left LPFC compared to cathodal/anodal tDCS of the same sites, and the flanker effects in both high- and low-load conditions were modulated in both stimulation groups independently of TUT modulation. To the best of our knowledge, this is the first study demonstrating that TUT propensity can be externally decreased via tDCS. Because mind wandering has both costs and benefits, it is quite beneficial for an understanding of the neural mechanisms of mind wandering regulation that tDCS can modulate mind wandering propensity in both an increasing (Axelrod et al., 2015) and a decreasing direction. In addition to the increase in TUT propensity by cathodal/anodal tDCS of the right IPL/left LPFC, which corresponds to the results of Axelrod et al. (2015), there was significantly different TUT propensity between the non-sham tDCS groups. However, comparisons between each non-sham tDCS group and the corresponding sham tDCS group did not show significant differences. This could be due to how TUT propensity was assessed. The thought probe used in this study was almost identical to the method of Kane & McVay (2012); asking participants to choose the most appropriate item representing the contents of their thoughts immediately before the probe and indexing the proportion of TUTs to reflect the frequency. On the other hand, the probe used by Axelrod et al. (2015) originally asked participants to choose the most appropriate extent of TUT experience, which is similar to that of Christoff et al. (2009). Axelrod et al. (2015) employed a four-point Likert scale and used the mean scores as the original index of TUT propensity, which might reflect TUT engagement as well as TUT frequency. Such a method might enable more accurate measurement of the effects of tDCS on TUT-related processing because it includes more components than the method used here that could be affected by the tDCS protocol. Thus, using the same thought probes as Axelrod et al. (2015), we might have been able to find clearer tDCS effects on TUT propensity. Nevertheless, the present results establish that tDCS of the right IPL/left LPFC can modulate TUT propensity. Although the precise neural underpinnings of the present results were not revealed, the supporting evidence for the present hypotheses indicates that the modulation of TUT propensity is induced in part via modulation of DMN function (Di and Biswal 2014; Hasenkamp et al. 2012; Taylor et al. 2013). The right IPL has been implicated as a crucial regulator of the DMN regions (Christoff et al. 2009; Di and Biswal 2014; Hasenkamp et al. 2012; Mason et al. 2007) that is 7
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strongly linked to mind wandering in addition to the left LPFC (Fox et al., 2015). Moreover, studies show that tDCS of the left LPFC also alters functional connectivity within the DMN (Keeser et al. 2011; Peña-Gómez et al. 2012). Considered in light of the present results, these studies suggest that tDCS of the right IPL/left LPFC induces alteration of DMN function (anodal/cathodal, upregulation; cathodal/anodal, downregulation), resulting in modulation of TUT propensity. To clarify the precise neural underpinnings of these observations, further studies using functional magnetic resonance imaging (fMRI) are needed. The supplementary observations made here may be associated with the right IPL’s multiple attention-related roles such as filtering distractor stimuli under high-load conditions (Weiss and Lavidor, 2012) and resolving response conflicts (Wendelken et al., 2009). First, the change in TUT propensity did not relate to task performance modulation, replicating the result of Axelrod et al. (2015). Incidental modulation of the attention processes by tDCS of the right IPL/left LPFC may disturb detecting the influence of TUT modulation on task performance. Second, the flanker effects were modulated in a load condition-dependent way (low-load, decrease; high-load, increase). One possible explanation for these phenomena is that while the modulation of the right IPL by tDCS improves response conflict processing under low-load conditions, the effect is restricted by consumption of neural resource for distractor filtering in high-load. To make progress in elucidating these issues, the use of high-definition tDCS (HD-tDCS), a novel technique of higher spatial resolution than regular tDCS, would be useful in attempts to modulate TUT propensity, because of fewer side effects and an ability to investigate the relationships between specific regions within the IPL and TUT/attentional processes. It would also be worth investigating whether and how tDCS of the left IPL, which is also part of the DMN, affects mind wandering propensity. Unlike the right IPL, the left IPL is included in the language network (Catani, Jones, and Ffytche, 2005) and is seemingly more related to the generation of mind wandering (Fox et al., 2015; Taylor et al., 2013). Therefore, the hemisphere-reversed version of the present tDCS protocol, that is, stimulation of the left IPL/right LPFC, may induce modulation effects opposite to those observed in the present study. In addition, stimulation of right IPL/left IPL may further strengthen the modulation effects. In conclusion, our results revealed that tDCS applied to the right IPL/left LPFC can modulate mind wandering propensity to decrease it as well as to increase it. Future fMRI and HD-tDCS studies will further reveal the neural mechanisms of mind wandering and identify tDCS protocols that can modulate mind wandering more effectively.
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Acknowledgments The authors thank Prof. Yoshihiro Kadono, Ohmula hospital, for medical support. This work was supported by MEXT. KAKENHI (Grant Number: 24240041). The authors declare no conflict of interest.
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Tables Table 1. Means and standard deviations of the TUT index and PANAS scores TUT
PANAS Time 1
Time 2
Positive
Negative
Positive
Negative
0.170 (1.00)
0.012 (1.00)
-0.232 (1.03)
0.070 (0.99)
Anode
38.06 (22.15)
Sham
46.32 (24.55) -0.126 (0.93) -0.247 (1.12) -0.033 (1.10) -0.381 (0.99)
Cathode 51.67 (21.82) -0.118 (0.97)
0.226 (0.83)
0.109 (0.80)
-0.516 (1.00)
Table 2. Means and standard deviations of task performance Low-Load Congruent Acc Anode
.97 (.03)
Sham
.97 (.03)
Cathode
.97 (.02)
RT 589.6 (70.7) 577.2 (102.5) 612.5 (72.8)
High-Load Incongruent
Acc .96 (.03) .94 (.06) .96 (.02)
RT 613.5 (68.8) 593.3 (94.1) 635.8 (76.6)
Congruent Acc .80 (.09) .77 (.09) .77 (.08)
RT 971.7 (130.2) 955.9 (154.7) 1000.2 (125.0)
Incongruent Acc .75 (.10) .76 (.08) .74 (.10)
RT 979.8 (126.1) 961.1 (153.9) 1009.4 (136.0)
Acc: Accuracy. Figure Legends Fig. 1. Examples of the perceptual load task stimuli for each condition Fig. 2. TUT propensity for each stimulation condition (error bars are the standard error of the mean) Fig. 3. The flanker effect on accuracy calculated as (congruent – incongruent)/congruent for each load condition (error bars are the standard error of the mean) Figure 1
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Kajimura S
Figure 2
Figure 3
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Kajimura S
Highlights This study explore whether tDCS of the right IPL/left LPFC can decrease TUT. TUT is reduced by anodal/cathodal tDCS of the right IPL/left LPFC. The results indicate the TUT modulation is induced via modulation of DMN function.
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