The effect of high-frequency rTMS of the left dorsolateral prefrontal cortex on the resolution of response, semantic and task conflict in the colour-word Stroop task Benjamin Parris, Michael Wadsley, Gizem Arabaci, Nabil Hasshim, Maria Augustinova, Ludovic Ferrand

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Benjamin Parris, Michael Wadsley, Gizem Arabaci, Nabil Hasshim, Maria Augustinova, et al.. The effect of high-frequency rTMS of the left dorsolateral prefrontal cortex on the resolution ofresponse, semantic and task conflict in the colour-word Stroop task. Brain Structure and Function, Springer Verlag, 2021, 226, pp.1241-1252. ￿10.1007/s00429-021-02237-4￿. ￿hal-03147527￿

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ORIGINAL ARTICLE

The efect of high‑frequency rTMS of the left dorsolateral prefrontal cortex on the resolution of response, semantic and task confict in the colour‑word Stroop task

Benjamin A. Parris1 · Michael G. Wadsley1 · Gizem Arabaci1 · Nabil Hasshim2 · Maria Augustinova3 · Ludovic Ferrand4

Received: 14 October 2020 / Accepted: 5 February 2021 © The Author(s) 2021

Abstract Previous work investigating the efect of rTMS of left Dorso-Lateral Prefrontal Cortex (DLPFC) on Stroop task performance reports no changes to the Stroop efect but reduced reaction times on both congruent and incongruent trials relative to sham stimulation; an efect attributed to an enhanced attentional (or task) set for colour classifcation. The present study tested this account by investigating whether, relative to vertex stimulation, rTMS of the left DLPFC modifes task confict, a form of confict that arises when task sets for colour classifcation and word reading compete, given that this particular type of confict would be reduced by an enhanced task set for colour classifcation. Furthermore, the present study included measures of other forms of confict present in the Stroop task (response and semantic confict), the potential efects on which would have been hidden in previous studies employing only incongruent and congruent stimuli. Our data showed that left DLPFC stimulation had no efect on the magnitude of task confict, nor did it afect response, semantic or overall confict (where the null is supported by sensitive Bayes Factors in most cases). However, consistent with previous research left DLPFC stimulation had the general efect of reducing reaction times. We, therefore, show for the frst time that relative to real vertex stimulation left DLPFC stimulation does not modify Stroop interference. Alternative accounts of the role of the left DLPFC in Stroop task performance in which it either modifes response thresholds or facilitates responding by keeping the correct response keys active in working are discussed.

Keywords TMS · Dorsolateral prefrontal cortex · Stroop · Cognitive control · Selective

Introduction in when the word spells out a diferent colour (i.e., incon- gruent trials- the word ‘red’ printed in green) compared to a Since its inception (Stroop 1935), the Stroop task has baseline compound stimulus (i.e., colour-neutral trials- the become an important clinical tool and has been referred to as word ‘top’/ string of xxx printed in red). It is often viewed as the gold-standard measure of selective attention (MacLeod a unitary phenomenon that results entirely from the single- 1992). The Stroop interference efect is the robust fnding stage of response competition that colour-incongruent trials that people are slower to name a colour that a word is printed produce (see e.g., MacLeod 1992 for a review). Yet, abundant research suggests that interference in the * Stroop task is potentially underpinned by confict at vari- Benjamin A. Parris ous points in the processing stream including at the level of [email protected] task set activation, semantic activation and response output 1 Department of , Bournemouth University, Talbot (Klein 1964; Monsell et al. 2001; see Parris et al. (under Campus, Fern Barrow, Poole, Dorset BH12 5BB, UK review)). In this view, task confict derives from the simul- 2 School of Applied Sciences, De Montfort University, taneous preparation of two task sets (word reading vs. colour Leicester, UK naming; Goldfarb and Henik 2007; Parris 2014) which cre- 3 Normandie Université, UNIROUEN, CRFDP, Rouen, France ates confict even before the identity of the Stroop stimulus 4 Université Clermont Auvergne, CNRS LAPSCO, has been revealed (Hershman and Henik 2019). Subsequent Clermont‑Ferrand, France processing of the meaning of the word results in semantic

Vol.:(0123456789)1 3 Brain Structure and Function confict when the irrelevant word dimension gives confict- contribution of a neural region to is ing information about which is the target stimulus (Augusti- through the use of transcranial magnetic stimulation (TMS). nova and Ferrand 2012, 2014; Augustinova et al. 2015,2018; White et al. 2016). Finally, when the irrelevant word is also Stimulation studies of the left DLPFC’s role in Stroop a possible response option (i.e., incongruent trials) it creates task performance confict at the response level (i.e., response confict, Hasshim and Parris 2018; Milham et al. 2001). TMS is a non-invasive tool for modulating cortical activ- ity (Wassermann et al. 2008). High frequency (≥ 5-Hz) The neural mechanisms of Stroop task performance repetitive TMS (rTMS) is typically considered to have an excitatory efect on underlying neurons, whereas the efects The specifc neural mechanisms involved in guiding our of low frequency (≤ 1-Hz) rTMS are considered inhibitory attention in the Stroop task still remain a source of debate. (Pell et al. 2011). Using rTMS to inhibit or facilitate brain The dorsolateral prefrontal cortex (DLPFC), along with the regions to be responsible for attentional control, one anterior cingulate cortex (ACC), has long been considered could observe the efect on performance across diferent trial central to the circuitry of attentional control (MacDonald types and consequently determine whether specifc regions et al. 2000). Popular models of selective attention posit are essential for resolving diferent types of confict. that the ACC is responsible for detecting the presence of The few studies that have previously employed this tech- response confict between competing representations and nique to target the left DLPFC during Stroop task perfor- consequently engages the DLPFC to impose cognitive con- mance have reported that left DLPFC stimulation does not trol (e.g., Banich 2009, 2019; Banich et al. 2019; Botvinick modify interference levels. Vanderhasselt et al. (2006) dem- et al. 2001; MacDonald et al. 2000). This theory is supported onstrated that, compared to a sham condition, one session of by studies that link selective attention in the high frequency (10-Hz) rTMS over the left DLPFC (loca- Stroop task to activity in these regions and in particular tion F3 on the international 10–20 EEG position system or the left hemisphere of the brain (e.g., Adleman et al. 2002; BA8) decreased reaction times (RTs) to both congruent and Bench et al. 1993; Coderre et al. 2008; Khorram-Sefat et al. incongruent trials. However, the stimulation did not modify 1996; Langenecker et al. 2004; Liu et al. 2004; Mead et al. the Stroop efect (incongruent – congruent trial RTs) and as 2002; Parris et al. 2019a, b; Peterson et al. 1999; Song and such they concluded that their data were consistent with the Hakoda 2015; van Veen and Carter 2005; van Veen et al. notion that the role of the left DLPFC was to implement top- 2001; Zysset et al. 2001). Whilst the role of both regions is down attentional control by imposing a task set for colour a matter of ongoing debate (for debate around the function classifcation. of the ACC see e.g. Aarts et al. 2008; Banich 2009, 2019; In a more recent study, Li et al. (2017) investigated Botvinick et al. 2001; Khorram-Sefat et al. 1996; MacDon- whether multiple sessions of rTMS of the left DLPFC (F3/ ald et al. 2000; Mead et al. 2002; Milham et al. 2001; Parris B8) could improve Stroop task performance and explored et al. 2019a, b; Roelofs Van Turennout and Coles 2006; Song the time course changes of cognitive processing after rTMS. and Hakoda 2015; van Veen and Carter 2005; van Veen et al. Consistent with Vanderhasselt et al. (2006) they showed that 2001; Zysset et al. 2001), here we focus on the role of the compared to sham stimulation, rTMS reduced RTs to con- left DLPFC. gruent and incongruent trials whilst making no diference A dissociation has been reported for the function of the to the Stroop interference efect indicating that left DLPFC DLPFC in a study considering the type of confict presented. plays no role in Stroop interference control; a fnding that is Van Veen and Carter (2005) reported that semantic confict also consistent with studies employing transcranial Direct activated dorso-lateral prefrontal cortex (DLPFC: BA8/9), Current Stimulation (Baumert et al. 2020; Fecteau et al. whereas response confict activated more inferior lateral 2007, 2013; Loftus et al. 2015, although see Frings et al. prefrontal cortex (BA9/44/45/46). In contrast, Milham and 2018). colleagues (Milham et al. 2001,2003) reported that both left In the most recent assay investigating the efect of rTMS and right PFC were activated by response confict, but only on Stroop task performance, Friehs et al. (2020) compared left PFC was activated by semantic confict. Consistently, the efect of stimulation of the left DLPFC and right DLPFC a recent study by Parris et al. (2019a, b) reported that the to sham stimulation over the vertex. They showed that whilst left PFC plays an important role in the processing of both right DLPFC stimulation resulted in the disruption of the response and semantic confict. However, since neuroimag- congruency sequence efect (reduced Stroop interference on ing work is correlational it does not aid in the identifcation incongruent trials that follow incongruent trials in the pres- of the causal role of diferent brain regions in processing entation sequence), the left DLPFC did not modify Stroop Stroop conficts. One way to directly investigate the causal interference nor the congruency sequence efect.

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All of the above studies reported no signifcant reduc- reported to be more precise and reliable than the 5.5 cm tions in Stroop interference following stimulation of the targeting method (Trapp et al. 2020). We initially aimed to left DLPFC, but all three studies had important limita- test 20 participants but with the objective of collecting data tions: (1) neither Vanderhasselt et al. (2006) and Li et al. until the Bayes Factor for the efect of stimulation on overall (2017) provided evidence for the null hypothesis of no Stroop interference was sensitive (either for or against the efect on Stroop interference; evidence that can be provided null hypothesis). by employing Bayes Factors (Dienes 2014, 2016; see for To attribute the contribution of each confict type to example Friehs et al. 2020); (2) neither Vanderhasselt et al. Stroop interference we ran a number of planned pairwise (2006) and Li et al. (2017) employed vertex stimulation as comparisons. For each comparison, we took a condition their baseline performance condition which better controls that permits the measurement of the relevant confict type for the potential infuence of somato-sensory efects on and compare this critical condition to a suitable baseline in performance (Boschin, Mars and Buckley 2017; Duecker which the relevant confict is assumed to be absent (Has- and Sack 2015; Hayward et al. 2004; Jung et al. 2016) and shim and Parris 2014, 2015, 2018; Parris et al. 2019a, b). Friehs et al. (2020) used sham vertex stimulation where the To index task confict, we employed non-word letter strings TMS paddle is directed 45 degrees to the saggital plane and (e.g., XXXX), which are thought to involve little to no con- thus also results in no actual stimulation sensation; (3) the fict and compared them to non-colour-related neutral words conclusions that can be drawn regarding the efect of left (e.g., Kalanthrof et al. 2015; Monsell et al. 2001; Stein- DLPFC stimulation on interference and/or confict are also hauser and Hübner 2009). Semantic-associative trials (e.g., limited due to the use of only incongruent and congruent TOMATO, GRASS) are compared to neutral word trials as trials. Although these trial types are commonly employed an index of semantic confict and response confict is iso- to measure Stroop interference, it confounds the interfering lated using an incongruent vs. non-response set comparison. efect of incongruent trials with facilitating efect of con- Finally, overall interference is measured by comparing the gruent items (MacLeod 1991; Parris et al. (under review)). incongruent condition against non-word letter strings condi- Also, and importantly, it does not allow for the potential tion. To maximise the distinction between confict types in diferential efect of left DLFPC stimulation on the difer- our experiment we employed a pure block trial type presen- ent components of Stroop interference—task, semantic and tation method (Hasshim and Parris 2018). response confict. Given previous accounts of the role of Since task confict results from a failure to fully engage the left DLPFC in Stroop task performance, task confict, in the attentional set (Kalanthrof et al. 2018; Parris 2014), the particular, should be modifed be left DLPFC stimulation. litmus test for whether DLPFC is involved in setting atten- tional set, as others have argued, is the efect it has on the The present study magnitude of task confict. If the role of the left DLPFC in attentional control is to implement a general attentional or The aim of the present study was to investigate whether and task set by keeping task-relevant information online (Bot- the extent to which rTMS stimulation of left DLPFC afects vinick et al. 2001; Li et al. 2017; Vanderhasselt et al. 2006), overall, task, semantic and response confict. Specifcally, then enhancing DLPFC function using rTMS would increase using a fully within-subjects design the present study set out the activation of the colour naming task set. Therefore, it to investigate whether facilitating left DLPFC region stimu- would enable it to win out more easily over the competing lated in previous studies (F3/BA8) diferentially afects the endogenously activated task set for word reading. In short, resolution of these conficts when compared to vertex stimu- enhancing DLPFC function using rTMS should reduce lation and to use Bayes Factors to establish evidence for the task confict. If task confict was indeed reduced, we would null hypothesis of no diference. Given neuronavigation was expect a reduction in RTs for all trials that involve this type unavailable we employed the Beam F3 approach to localisa- of confict (any trial with word stimuli: incongruent, non- tion (Beam et al. 2009).1 The Beam F3 method produces a response set, semantic associative and neutral word trials). reasonable approximation to neuronavigated localisation of Since repeated letter trials do not include irrelevant words, left DLPFC (Mir-Moghtadaei et al. 2015) and has also been there would be no task confict to reduce and hence this trial type would be unafected by stimulation. Moreover, since following task confict reduction, all trial types involving 1 The Beam F3 method was created as a way of reducing human words would have their RTs uniformly reduced, the difer- error and time consumption when localising F3. The numerous meas- ence between them would remain the same, and thus the urements normally required take time and are prone to error. Beam measures of other conficts will be unafected. F3 system involves taking only three skull measurements (distance In contrast, left DLPFC might play a role in resolv- from tragus to tragus, distance from nasion to inion, head circumfer- ence) which are inputted into the F3 locator program. The program ing just semantic confict (van Veen and Carter 2005) or then produces two values that are used to locate F3. resolving both response and semantic confict (Milham

1 3 Brain Structure and Function et al. 2001; Parris et al. 2019a, b). Finally, left DLPFC Procedure might play little to no role in modifying Stroop conficts, and thus there will be evidence for no efect on all confict Participants were frst provided with information about the types. use of TMS and were given the opportunity to ask ques- tions. After the procedure had been explained and informed consent had been obtained participants completed a com- puterised Stroop task administered using OpenSesame 3.2 Method software (Mathôt et al. 2012). Response latencies were recorded using a headset microphone and were measured Participants as the time point a participant started to speak. The experi- menter sat behind the participant and recorded errors includ- 22 participants (3 male, Mage = 21.86, SD = 4.04) recruited ing incorrect responses (reading the word instead of the col- from the Bournemouth University student population com- our), corrected responses (starting to read the word, then pleted the study. One participant withdrew from the study naming the colour) and noises preceding a response (e.g., after the frst session of DLPFC stimulation after report- coughing or fller words such as ‘um’). Participants were ing some discomfort. This participant was later replaced. sat approximately 65 cm from the screen which measured All participants were between 18 and 35 years old, fuent 24 inches diagonally. Before beginning the experimental tri- in English and had a normal or corrected-to-normal vision, als, the sensitivity of the microphone in detecting responses as well as normal colour vision. Participants were screened was checked in a series of practice trials. The practice trials for potential risk factors associated with rTMS according consisted of 16 colour patches (4 of each response colour: to published guidelines (Rossi et al. 2009). Each partici- red, blue, green and yellow) presented in a random order. pant was tested individually across two testing sessions and Participants were instructed to name the colours out loud, received course credits or £20 for participating. Written and each patch remained on the screen until a response had informed consent was obtained from all participants and been detected. the study was approved by the Bournemouth University After practice, 300 experimental trials were completed. Research Ethics Committee. Participants were instructed to respond as quickly and as accurately as possible to the colour of each stimulus whilst ignoring the meaning of the irrelevant word. The stimuli Design were presented in mini-blocks containing all and only the 12 stimuli for each trial type and the 12 stimuli were presented The study used a 2 × 2 × 5 (stimulation condition (DLPFC in random order. Once all 5 trial types had been presented in vs. Vertex) vs. pre/post-stimulation performance vs. trial their mini-blocks, participants would have completed a block type) single-blind within-subjects design. (therefore, 60 trials comprised a block). Within each block, each mini-block was presented in a random order. Each trial began with a white fxation dot for 300 ms. The stimuli were Stimuli then presented and remained on the screen until a response was made or until 3000 ms had elapsed. After a response had Twelve unique stimuli were used for each of the fve trial been made the stimulus was immediately replaced by a black types (single-letter string trials, neutral word trials, seman- screen for 1000 ms. After each block of 12 stimuli partici- tic-associative trials, non-response set trials and incongru- pants could take a break and pressed the spacebar to start the ent trials). Stimuli were presented individually in uppercase next block of trials. The task lasted approximately 15 min. Courier New font, size 42, on a black background. All items After the initial Stroop task block high-frequency rTMS were presented in the centre of the screen in one of four was performed. All stimulations were performed using a colours: red (RGB; 255; 0; 0), blue (RGB: 0; 32; 96), green DuoMAG XT stimulator (Rogue Resolutions Ltd, Cardif, (RGB: 0; 176; 80), and yellow (RGB: 255; 255; 0), with UK) with a fgure 8-shaped coil. The EMG was recorded all words with an association with colour (e.g. red, grass) using two pregelled Deymed Diagnostic 22 × 30 mm­ 2 always being presented in an incongruent colour. The trials Ag–AgCl disposable electrodes placed over the region of consisted of single letter strings: XXX, XXXX, XXXXX, the abductor pollicus brevis (APB) belly and associated XXXXXX, neutral non-colour words: TOP, CLUB, tendon of the right hand, and a Velcro wraparound Ground STAGE, CHIEF; colour-associated words: SKY, TOMATO, Electrode on the right wrist. The resting motor threshold LEMON, GRASS; colour words (non-response): PURPLE, (RMT) of each participant was determined before each GOLD, WHITE, GREY; incongruent colour words: RED, stimulation by establishing the lowest setting at which ≥ 5 BLUE, GREEN, YELLOW. out of 10 stimulations of the left motor cortex resulted in

1 3 Brain Structure and Function a minimum MEP amplitude of 50 μV elicited at a given RT reduction in incongruent trial RTs following DLPFC stimulation intensity. Stimulation intensity was set at 110% stimulation in Vanderhasselt et al. (2006). of the established RMT for each individual. The study used Bayes factors were also calculated for comparisons the parameters previously set by Vanderhasselt et al. (2006), of confict types between the vertex and DLPFC condi- with a stimulation frequency of 10Hz and intertrain interval tions. Predictions of the theory were represented as a of 26 s. Forty trains were applied in a ca. 20 min period half-normal scaled with an expected reduction of 55 ms (1,560 pulses per session), with each train lasting 3.9 s. The for the overall interference comparison, which represents left DLPFC was defned as the F3 location given by the the average signifcant interference (incongruent–neutral International 10–20 system (BA8/9; Herwig et al. 2003) and words) reduction after post-hypnotic suggestion, taken was identifed for each participant using the Beam F3 sys- from Augustinova and Ferrand (2012; Experiments 1 and tem (Beam et al. 2009). The vertex was identifed as the Cz 2) and Zahedi et al. (2019); both these studies, like the pre- location using the International 10–20 system (Herwig et al. sent study, employed vocal response Stroop tasks and had 2003). Immediately post-stimulation, participants completed an original interference value of ~ 100 ms. Inevitably the a further 300 trials of the Stroop task. expected reduction of the individual components of inter- The order of the two testing sessions was counterbalanced ference should not be as great and, therefore, we use 1/3 such that 11 participants received DLPFC stimulation and of the prior value for overall interference (which assumes 11 participants received vertex stimulation on the frst ses- all confict types contribute equally to interference). There- sion. During the second session, participants completed the fore, task, semantic and response confict are expected to be same procedure except that they were assigned to the oppo- reduced by 18.33 ms. site condition (DLPFC or vertex). The two testing sessions were separated by a delay of 1 week and participants were stimulated at the same time of the day. In total, participants Results completed 1200 trials across the two testing sessions. After completing the experiment participants were fully debriefed Analysis of reaction times and thanked for their time. Errors rates were low in our experiment and accounted for only 2.86% of all trials. Error trials were removed before Statistical analysis running the analyses. Reaction times of correct responses were analysed using a 2 × 2 × 5 (stimulation condition: Where necessary, we applied the Greenhouse–Geisser cor- vertex vs. LDLPFC vs. pre/post vs. trial type: response set rection to ensure the assumption of sphericity. The signif- incongruent vs. non-response set incongruent vs. semantic cance level was set at p ≤ 0.05 for all analyses. The data were associative incongruent vs. non-colour word neutrals vs. analysed using a repeated-measures analysis of variance repeated letter strings) repeated measures ANOVA. Laten- (ANOVA) and signifcant efects were investigated using cies of correct responses more than two standard deviations paired t-tests. away from each participant’s mean in each condition were Bayes factors (B) were used to assess the strength of removed as outliers (Vanderhasslet et al. 2006). This resulted evidence for 1-degree of freedom alternative hypotheses, in the exclusion of 4.85% of the trials. H1, over the null, H0 where results were non-signifcant. A The results of the ANOVA revealed a signifcant main B of above 3 indicates moderate evidence for H1 over H0 efect of trial type on reaction times [F(1.87,39.26) = 64.95, 2 and below 0.33 moderate evidence for the H0 over H1. All p < 0.001, ηp = 0.756]. No signifcant main efect of stimu- 2 Bayes factors, B, reported here represent the evidence for lation condition [F(1,21) = 2.58, p = 0.123, ηp = 0.110] or 2 H1 relative to H0; to fnd the evidence for H0 relative to H1, pre/post [F(1,21) = 2.64, p = 0.119, ηp = 0.112] was found. take 1/B. Bs between 3 and 0.33 indicate data insensitivity The interaction between stimulation condition and pre/ (see Dienes 2014). Here, BH(0, x) refers to a Bayes factor in post was shown to be signifcant [F(1,21) = 4.38, p = 0.049, 2 which the predictions of H1 were modelled as a half-normal ηp = 0.173] and resulted from an increase in RT from pre- distribution with an SD of x (see Dienes 2014, 2016); the to post-stimulation in the vertex condition. This fnding half-normal can be used when a theory makes a directional contrasts with those in previous studies in which a pre-to- prediction where x scales the size of the efect that could be post decrease in RTs in the DLPFC stimulation condition expected. All Bayes factors were calculated with an adjusted was reported (Li et al. 2017; Vanderhasselt et al. 2006). standard error where SE = SE × (1 + 20/df × df) due to the The interaction between stimulation condition and trial 2 sample size being less than 30 (Dienes 2014). Predictions of type [F(2.18,45.72) = 0.23, p = 0.811, ηp = 0.011] and the the theory were represented as a half-normal scaled with an interaction between pre/post and trial type [F(4,84) = 0.63, 2 expected reduction of 26 ms which represents the signifcant p = 0.644, ηp = 0.029] were non-signifcant. However, the

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Fig. 1 Mean reaction times 800 Vertex DLPFC per trial type for pre and post stimulation as a function of 780 stimulation type. Error bars represent SE. ‘LS’ refers to 760 letter strings. ‘NW’ refers to neutral words. ‘SA’ refers to 740 semantic associates. ‘NR’ refers s) 720 to non-response set. ‘I’ refers to (m incongruent 700 RT 680

Mean 660 640 620 600 LS NW SA NR ILSNWSANRI Pre Post

crucial three-way interaction between stimulation condition, − 2.27, p = 0.034, d = 0.40] all signifcantly increased after pre/post and trial type was signifcant [F(2.64,55.43) = 3.44, stimulation. The Bayes factors (two tailed) for non-response 2 p = 0.028, ηp = 0.141]. Mean reaction times for each condi- set trials BH(0,26) = 1.85 and incongruent trials BH(0,26) = 0.42 tion are displayed in Fig. 1. were both insensitive. For the DLPFC condition, there was This interaction effect was explored using follow-up no signifcant diference in RTs from pre to post and Bayes paired t tests. We frst compared the diference in base- factors for letter strings BH(0,26) = 0.24 and incongruent trials line (pre-stimulation) performance between the vertex and BH(0,26) = 0.22 indicate moderate evidence for H0. The Bayes DPLFC conditions for each trial type. Analysis showed that factors for neutral words BH(0,26) = 0.94, sematic associative performance on each trial type before stimulation was not BH(0,26) = 0.68, and non-response set trials BH(0,26) = 0.37, signifcantly diferent for the vertex and DLPFC conditions were all insensitive but favoured H0. (p > 0.261). Bayes factors (two-tailed) for letter string trials BH(0, 26) = 0.43, neutral word trials BH(0, 26) = 0.42, seman- tic associative trials BH(0, 26) = 0.51, non-response set trials Analysis of confict types BH(0, 26 = 0.42, and incongruent trials BH(0, 26) = 0.67, were all insensitive but favoured H0. The magnitude of each confict type was calculated for each A comparison of post-stimulation performance revealed participant using the planned comparisons outlined in the a signifcant reduction in RTs to letter strings [MD = 18.94, introduction. The results were analysed using a 2 × 2 × 4 SD = 37.90, t(21) = 2.34, p = 0.029, d = 0.23], neutral (stimulation condition vs. pre/post vs. confict type) repeated words [MD = 26.83, SD = 52.48, t(21) = 2.40, p = 0.026, measures ANOVA. d = 0.28] and semantic associates [MD = 33.01, SD = 54.23, The main efect of stimulation condition [F(1,21) = 4.08, 2 t(21) = 2.86, p = 0.009, d = 0.27] after DLPFC compared p = 0.056, ηp = 0.163] and pre/post [F(1,21) = 1.84, 2 to vertex stimulation. The RT reduction on nonresponse p = 0.190, ηp = 0.080] were both non-signifcant. How- set trials was non-significant [MD = 23.00, SD = 52.95, ever, there was a signifcant main efect of confict type 2 t(21) = 2.04, p = 0.054, d = 0.21] but the Bayes factor indi- [F(3,63) = 60.43, p < 0.001, ηp = 0.742]. The mean magni- cated evidence for H1, BH(0,26) = 3.82. For incongruent trials tude of each confict type for each condition is displayed in (9.12 ms) the Bayes factor was insensitive, BH(0, 26) = 0.86. Table 1. The performance change from pre to post was also com- The interaction between stimulation condition and pre/ 2 pared for each trial type in the DLPFC and vertex stimulation post [F(1,21) = 1.06, p = 0.314, ηp = 0.048], the inter- conditions. After vertex stimulation, it was found that RTs to action between stimulation condition and conflict type 2 the letter strings [MD = − 27.54,SD = 56.27, t(21) = -2.30, [F(2.11,44.48) = 0.61, p = 0.557, ηp = 0.028], and the inter- p = 0.032, d = 0.41], neutral words [MD = − 20.79, action between pre/post and confict type [F(3,63) = 0.54, 2 SD = 45.44, t(21) = − 2.15, p = 0.044, d = 0.28] and seman- p = 0.660, ηp = 0.025] were all non-signifcant. The three- tic associative trials [MD = − 34.51, SD = 71.30, t(21) = way interaction between stimulation condition, pre/post and

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Table 1 Mean magnitude of Confict type Pre Post confict types (ms) for each planned comparison in the pre Vertex DLPFC Vertex DLPFC and post conditions for vertex a vs. DLPFC stimulation Task confict (NW-LS) 20.61 (24.09) 32.94 (32.30) 29.44 (29.09) 34.09 (30.25) Semantic confict (SA-NW) 21.62 (41.07) 29.51 (35.45) 34.83 (44.39) 28.89 (36.14) Response confict (I-NRS) 41.60 (38.49) 34.62 (38.43) 27.60 (36.93) 45.44 (45.33)a Overall interference (I-LS) 101.09 (49.57) 104.10 (52.90)# 98.82 (43.88) 122.33 (70.55)a

‘SD’ is presented between parentheses. ‘LS’ refers to letter strings. ‘NW’ refers to neutral words. ‘SA’ refers to semantic associates. ‘NRS’ refers to non-response set. ‘I’ refers to incongruent All confict efects were signifcant in all conditions (p < .05) a Bayes Factor < 0.3 = Evidence for the null hypothesis of no diference between vertex and DLPFC stimula- tion confict type was also non-signifcant [F(2.34,49.19) = 2.27, (stimulation condition vs. pre/post vs. trial type) repeated 2 p = 0.106, ηp = 0.098]. measures ANOVA. Comparisons between the critical and baseline trial types The results of the ANOVA revealed a signifcant main (the confict efects) were signifcant (p < 0.05), providing effect of trial type [F(1.95,40.94) = 38.44, p < 0.001, 2 evidence for the task, semantic and response confict in ηp = 0.647] and pre/post [F(1,21) = 11.84, p = 0.002, 2 all conditions. Since no signifcant interaction efect was ηp = 0.360]. However, the main efect of the stimulation observed the mean diferences in the magnitude of confict condition was nonsignifcant [F(1,21) = 3.00, p = 0.098, 2 types between the vertex and DLPFC conditions were not ηp = 0.125]. analysed. However, Bayes factors were calculated for these The interaction between stimulation condition and comparisons to assess evidence for H1 vs. H0. For the pre- pre/post was shown be significant [F(1,21) = 5.68, 2 stimulation comparisons the Bayes factor (two-tailed) for p = 0.027, ηp = 0.213]. However, the interaction between overall interference provides evidence for no diference, stimulation condition and the trial type was nonsig- 2 BH(0,55) = 0.14. The Bayes factors (two-tailed) for task con- nificant [F(1.72,36.16) = 1.10, p = 0.336, ηp = 0.050], fict, BH(0,18.33) = 0.85, semantic confict, BH(0,18.33) = 0.60, as was the interaction between pre/post and trial type 2 and response confict BH(0,18.33) = 0.55, were all insensitive [F(2.56,53.77) = 2.64, p = 0.067, ηp = 0.112]. The three- but favoured H0. way interaction between stimulation condition, pre/post and For the post-stimulation comparison the Bayes fac- the trial type was also nonsignifcant [F(2.60,54.56) = 1.52, 2 tor for overall interference provides strong evidence for p = 0.224, ηp = 0.067]. Error rates for each condition are no efect of stimulation, BH(0,55) = 0.06. The Bayes factors displayed in Fig. 2. for task confict, BH(0,18.33) = 0.29, and response confict, BH(0,18.33) = 0.29, both suggest moderate evidence for H0. The Bayes factor for semantic confict, BH(0,18.33) = 0.76, Discussion was insensitive but favoured H0. Therefore, the results of the Bayesian analysis suggest that stimulation of the left The aim of the present study was to investigate the efect DLPFC does not reduce overall Stroop interference, task of left DLPFC stimulation on overall, task, semantic, and confict or response confict. Consistent with previous fnd- response confict in the Stroop task. Previous fMRI stud- ings then (Friehs et al. 2020; Li et al. 2017; Vanderhasselt ies and infuential neurocognitive models suggest that left et al. 2006) we found no evidence for an efect of stimula- DLPFC is involved in confict resolution (e.g., Banich 2009, tion of left DLPFC on interference control. In contrast to 2019; Banich et al. 2019; Botvinick et al. 2001; MacDon- previous studies, however, we provide Bayesian evidence ald et al. 2000). In contrast to these accounts, previous for no diference. work employing stimulation of the left DLPFC report no changes to the Stroop efect, but do report reductions in Analysis of errors reaction times on congruent and incongruent trials (Friehs et al. 2020; Li et al. 2017; Vanderhasselt et al. 2006). Whilst The total error rates for each trial type were, 0.74%, 1.53%, these studies concluded that enhancing left DLPFC has no 2.80%, 2.80%, and 6.42% for the letter strings, neutral words, efect on confict control two did not provide evidence for semantic associates, nonresponse set, and incongruent tri- the null (Li et al. 2017; Vanderhasselt et al. 2006), all three als, respectively. Error rates were subjected to a 2 × 2 × 5 employed only sham stimulation as a control condition, and

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Fig. 2 Mean error rates (%) 10 Vertex DLPFC per trial type for pre and post stimulation as a function of stimulation type. Error bars represent SE. ‘LS’ refers to 8 letter strings. ‘NW’ refers to neutral words. ‘SA’ refers to semantic associates. ‘NR’ refers 6 to non-response set. ‘I’ refers to incongruent 4 Mean error rate (%) 2

0 LS NW SA NR ILSNWSANRI Pre Post none addressed the efect of stimulation on the underlying and response confict are also unafected where evidence components of Stroop interference. for the null is provided for task and response confict. Our Consistent with previous stimulation fndings, the results results, therefore, replicate and extend those from previous of the present study show a clear efect of left DLPFC stimu- stimulation studies and, moreover, are inconsistent with lation on task performance; as evidenced by both reduced interpretations of neuroimaging data (Milham et al. 2001; RTs and reduced errors. However, the pattern in our data Parris et al. 2019a, b) and predictions from leading neuro- were diferent in that when comparing performance change cognitive models of selective attention and cognitive con- from pre to post stimulation in the DLPFC condition it was trol (Banich 2009, 2019; Botivnick et al. 2001; van Veen & shown that RTs on all trials were non-signifcantly diferent Carter, 2005). As noted recently by Baumert et al. (2020) whereas in the vertex condition, RTs on all trials increased the absence of confict modulation does not support the idea after stimulation. Therefore, a possible interpretation of our that the left DLPFC is causally involved in interference con- fndings is that vertex stimulation resulted in a reduction in trol. However, a caveat to this conclusion is the possibility performance rather than that DLPFC stimulation improved presented recently by Hartwigsen (2018) who argued that performance. However, the vertex condition is our baseline stimulation of a subcomponent region of a neural network condition and permits us to see what happens to RTs when might result in a temporary re-organisation and subsequent actual stimulation occurs in a putatively non-critical region compensation of function by another region of the network. of the cortex for cognitive control. It is precisely this soma- The process of temporary re-organisation would result in the tosensory efect that was missing in previous studies and absence of a modifcation of the specifc cognitive function thus one of the important contributions made by the present under test. study. Thus, looking at the baseline condition only, we can A more efective attentional set should result in reduced argue that rTMS stimulation to a non-critical region results competition between the target task set of colour naming in increased RTs. This we interpret to be due to the general and the exogenously activated task set of word reading; that efect of cortical stimulation. Since this increase does not is, it would reduce task confict. To support the hypothesis happen in the DLPFC stimulation condition, we interpret that stimulation of the left DLPFC reduces task confict by the relatively shorter post-stimulation RTs in this condition imposing an enhanced attentional set, it was necessary to compared to the post-stimulation vertex condition as rep- show that relative to our baseline letter string trials, RTs to resenting a decrease in RTs due to the DLPFC stimulation. neutral word trials were signifcantly reduced after stimu- This improved performance post-DLPFC stimulation was lation. However, comparisons of post-stimulation perfor- supported in our data by reduced errors. mance in the vertex and DLPFC conditions revealed that A further important contribution from the present work performance on both letter string and neutral word trials is that our data suggest that left DLPFC stimulation does were improved to the same extent resulting in no signifcant not modify the Stroop interference efect where the null is change in the magnitude of task confict. Thus, whilst previ- supported by sensitive Bayes Factors (see also Friehs et al. ous studies have concluded that a reduction in RTs is consist- 2020) and, moreover, further suggests that task, semantic ent with a role for the left DLPFC in setting an attentional

1 3 Brain Structure and Function set, it is not clear why a modifcation of the attentional set might indicate that facilitation of the left DLPFC leads to a would not also modify task confict. decrease in RTs except when response confict is high. If we One interpretation of the present data is that facilitation assume that the reduction in RTs on all other trials refects of DLPFC is merely setting a new response threshold; an the facilitation of an ‘attentional set’, and that this efect can efect similar perhaps to changes in response threshold on be negated on incongruent trials when response competition word naming times brought about by mixing high and low- is high, then our fndings remain somewhat consistent with frequency words (Lupker et al. 1997, 2003). In these stud- the role of the left DLPFC in implementing top-down atten- ies, Lupker and colleagues show that word reading response tional control supported in previous TMS studies (Li et al. times can be modifed by mixing words that are read quickly 2017; Vanderhasselt et al. 2006) and proposed by infuen- (e.g., high-frequency words) with words that are read slowly tial fndings and models of cognitive control (Banich 2009, (e.g., low-frequency words). In all cases, they showed that 2019; Botvinick et al. 2001; MacDonald et al. 2000). the more slowly named stimuli were named faster when It has previously been suggested that while the left mixed with word stimuli that had quicker naming times; an DLPFC is responsible for actively preparing for a specifc efect they attributed to the strategic use of a time-criterion task in the presence of a distracting task (Vanderhasselt et al. to guide responding. Such an account is not entirely incon- 2010), the right DLPFC is recruited after confict detection sistent with the attentional set account of reduced RTs fol- to subsequently minimize conflict (Vanderhasselt et al. lowing stimulation of the left DLPFC if one assumes that 2009; see Friehs et al. 2020 for a discussion of hemispheric the attentional set is not one that biases the target task of col- lateralisation of control in the Stroop task). According to our naming but instead is one that enhances attention to the Vanderhasselt et al. (2009) left DLPFC activation is related stimuli and modifes response thresholds. Indeed, the fnding to a preparatory and temporary increased attentional set, of reduced RTs to both incongruent and congruent stimuli in whereas the right DLPFC is related to large-scale cognitive previous studies (Li et al. 2017; Vanderhasselt et al. 2006) is control adjustments in a confict-driven context which ena- not consistent with an account based on enhanced attention bles us to build representations that bias behaviour towards to colour naming since this would reduce the input from an appropriate response. In an fMRI study employing neu- the word dimension which would decrease, not increase, tral, non-response set and incongruent trials Milham et al. facilitation on congruent trials (and thus increase and not (2001) reported that only response confict (indexed using an decrease RTs to congruent trials). Only a reduction in task incongruent–non-response set comparison) elicited activa- confict could explain reduced RTs to both incongruent and tion in the right PFC, whereas the left PFC was activated by congruent stimuli since a reduction in task confict would confict at the response and pre-response levels. This sug- decrease RTs to incongruent trials and permit facilitation to gests that while both hemispheres of the prefrontal cortex be more fully expressed on congruent trials (Goldfarb and are recruited by the cognitive demands of the Stroop task, Henik 2007). But as the present data suggest, task confict their involvement may difer depending on the type of con- is not reduced. Thus, our results suggest that left DLPFC fict that arises. However, these fndings are the subject of stimulation might play a role in setting response thresholds. continual debate (Chen et al. 2013; Song and Hakoda 2015; An alternative interpretation of speeding responses when van Veen and Carter 2005) and neither the present results correctly classifying the colour of presented words is that nor those from recent research using optimised measures the left DLPFC plays a role in the determination of work- of response and semantic confict are consistent with this ing memory capacity (Baumert et al. 2020). Baumert et al. notion (Parris et al. 2019a, b). argued that enhanced capacity would facil- An interesting direction for future research would be to itate responding in the Stroop task, independent of trial type examine the efect of right DLPFC stimulation on levels because the correct response keys are kept active in working of the various types of confict in the Stroop task given the memory (see also Frings et al. 2018). Such an account is potential for lateralisation of control raised by the work of not inconsistent with the aforementioned response threshold Milham et al. and recent research showing an efect of right account. DLPFC stimulation on congruency sequence efects (Fri- Our analysis revealed that RTs on incongruent trials were ehs et al. 2020). Given our use of blocked presentation of not signifcantly reduced after DLPFC stimulation. This trial types to optimise measurement of confict types (Has- fnding is somewhat surprising given that previous stud- shim and Parris 2018), we are unable to measure congru- ies employing similar parameters demonstrate a reduction ency sequence efects, but this potential lateralisation of the in RTs on incongruent trials (Li et al. 2017; Vanderhasslet function should be investigated further. Moreover, Friehs et al. 2006). Nevertheless, in contrast to these studies we et al. also employed online stimulation whilst the present maximised response confict in our experiment by employ- study and most previous studies used ofine stimulation; a ing a pure block design (Hasshim and Parris 2018) and a diference that could prove to be important in producing the vocal response (Augustinova et al. 2019). Thus, our data reported efects.

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We employed vertex stimulation as a control condition Bayes factor favoured the null). Importantly, we also show since numerous previous studies have suggested that this for the frst time that stimulation of the DLPFC enhances region is unrelated to task performance (e.g., Boschin et al. performance compared to an active stimulation control con- 2017; Hayward et al. 2004), and a recent fMRI study inves- dition (cf. Li et al. 2017; Vanderhasselt et al. 2006, 2007). tigating BOLD signal changes across the whole brain linked We have argued that the failure to observe a reduction in task to vertex stimulation, provides support for its use as a control confict is problematic for the previously profered atten- site (Jung et al. 2016). However, Jung et al. (2016) did show tional set account. Instead alternative accounts of the role of that low-frequency rTMS of the vertex resulted in the deac- the left DLPFC in Stroop task performance were suggested tivation of regions within the default mode network (DMN) according to which the left DLPFC either implements an suggesting that vertex stimulation is not entirely inert. attentional set that facilitates faster responses by modifying While we assume that vertex stimulation does not result in response thresholds or facilitates responding in the Stroop any functional changes that efect task performance, more task by keeping the correct response keys active in working research is needed to fully understand the impact of vertex memory (Baumert et al. 2020; Frings et al. 2018). How- stimulation at diferent TMS parameters. ever, in contrast to previous studies our data suggest that the While we employ vertex stimulation to better control for efect of left DLPFC stimulation may be limited to situations the somatosensory efects of TMS, the precise neural efects where response competition is small. In instances where the of such stimulation at diferent TMS parameters are rela- expectancy of response confict is high, the right DLPFC tively unknown. We assume that vertex stimulation produces may be recruited to a greater extent to implement permanent no neural efects that infuence task performance and as such macro-adjustments in cognitive control (Friehs et al. 2020; explain the signifcant diference between conditions at post- Kerns et al. 2004; Milham et al. 2001; Vanderhasselt et al. test as being due to a general worsening in performance due 2007, 2009). to stimulation which is counteracted by the benefcial efects of DLPFC stimulation. However, we are unable to conclu- sively rule out the possibility that vertex stimulation impairs Funding The writing of this manuscript was supported in part by ANR Grant ANR-19-CE28-0013 and RIN Tremplin Grant 19E00851 of Nor- performance as a result of cortical efects. Furthermore, in mandie Région, France. our experiment the Beam F32 and International 10–20 sys- tem were used to defne the left DLPFC (F3) and vertex Data availability The data and materials are available at https://osf.io/​ (Cz). Although this method provides an acceptably approxi- ehp84​/?view_only=8bdb2​43ca4​1e468​295be​dfefd​b0c88​15. mate localization method and has been shown to be bet- ter than the 5.5 cm method (Trapp et al. 2020), MRI-based Code availability Not applicable. neuronavigation is more accurate (Mir-Moghtadaei et al. 2015). Finally, it should be noted that whilst high frequency Compliance with ethical standards (≥ 5-Hz) repetitive TMS (rTMS) is typically considered to Conflict of interest The authors have no competing interests to declare. have an excitatory efect on underlying neurons (Pell et al. 2011), this is accurate for motor cortex stimulation, and can- Open Access This article is licensed under a Creative Commons Attri- not be assumed to be true for nonmotor regions (Bergmann bution 4.0 International License, which permits use, sharing, adapta- and Hartwigsen 2020). Neuroimaging is considered crucial tion, distribution and reproduction in any medium or format, as long to provide strong proof of target engagement. as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated Conclusion otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will In sum, our fndings suggest that left DLPFC has no causal need to obtain permission directly from the copyright holder. To view a role in modifying overall, task nor response confict (our copy of this licence, visit http://creativeco​ mmons​ .org/licen​ ses/by/4.0/​ . data were insensitive for semantic confict, although the

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