Brain and Behavioral Inhibitory Control of Kindergartners Facing Negative Emotions Tali Farbiash and Andrea Berger

Developmental Science (2015), pp 1–16 DOI: 10.1111/desc.12330

PAPER Brain and behavioral inhibitory control of kindergartners facing negative emotions Tali Farbiash and Andrea Berger

Department of Psychology, Ben-Gurion University of the Negev, Israel

Abstract

Inhibitory control (IC) – one of the most critical functions underlying a child’s ability to self-regulate – develops significantly throughout the kindergarten years. Experiencing negative emotions imposes challenges on executive functioning and may specifically affect IC. In this study, we examined kindergartners’ IC and its related brain activity during a negative emotional situation: 58 children (aged 5.5–6.5 years) performed an emotion-induction Go/NoGo task. During this task, we recorded children’s performance and brain activity, focusing on the fronto-central N2 component in the event-related potential (ERP) and the power of its underlying theta frequency. Compared to Go trials, inhibition of NoGo trials was associated with larger N2 amplitudes and theta power. The negative emotional experience resulted in better IC performance and, at the brain level, in larger theta power. Source localization of this effect showed that the brain activity related to IC during the negative emotional experience was principally generated in the posterior frontal regions. Furthermore, the band power measure was found to be a more sensitive index for children’s inhibitory processes than N2 amplitudes. This is the first study to focus on kindergartners’ IC while manipulating their emotional experience to induce negative emotions. Our findings suggest that a kindergartner’s experience of negative emotion can result in improved IC and increases in associated aspects of brain activity. Our results also suggest the utility of time-frequency analyses in the study of brain processes associated with response inhibition in young children.

Research highlights Introduction

• Inhibition of NoGo trials was associated with larger Inhibitory control (IC) is an executive function defined N2 amplitudes and theta power, compared to Go as the ability to deliberately suppress dominant, auto- trials. matic, or prepotent responses (Diamond, 2013; Roth- • The negative emotional experience resulted in better bart, Ahadi, Hershey & Fisher, 2001). It is also IC performance and an increase in the theta band frequently termed response inhibition (Miyake, Fried- power within the N2 time window. man, Emerson, Witzki, Howerter et al., 2000). IC • Compared with N2 amplitudes, theta band power implies the ability to exert top-down control and act was more strongly associated with children’s inhibi- voluntarily according to the requirements of a situation. tory processes during a negative emotional experi- At the brain level, the development of IC occurs in ence. parallel to the maturation and connectivity of the • Source localization analyses suggested that the dif- prefrontal cortex (PFC; Berger, 2011; Luna, Padmanab- ference in brain activity between Go and NoGo trials han & O’Hearn, 2010; Posner & Rothbart, 2000; Wolfe during the negative emotional experience was princi- & Bell, 2007). Furthermore, the process of overriding a pally generated in the cingulate gyrus and in the prepotent response usually elicits conflict between alter- medial frontal gyrus. native, incompatible responses (Braver, Barch, Gray,

Address for correspondence: T. Farbiash, Department of Psychology, Ben-Gurion University of the Negev, Beer Sheva, Israel 84501; e-mail: [email protected]

Molfese & Snyder, 2001), which is often evident in the For example, Leue, Lange and Beauducel (2012) inves- activity of the anterior cingulate cortex (ACC; Albert, tigated the effects that aversive reinforcements have on Lopez-Martin, Tapia, Montoya & Carretie, 2012; conflict monitoring during a Go/NoGo task and found Botvinick, Cohen & Carter, 2004; Braver et al., 2001; that subjects improved their performance during aversive Rueda, Posner & Rothbart, 2005; van Veen & Carter, conditions. Locke and Braver (2008) found that the 2002). reward/penalty manipulation altered subjects’ perfor- Throughout the kindergarten years, IC development is mance, resulting in improved performance for Go trials reflected in a child’s transition from infantile behavior – in the reward condition as well as improved performance which lacks self-regulation – toward greater maturity for NoGo trials in the penalty condition. In addition to and an increasing ability to self-regulate. Indeed, during these studies, it should be mentioned that some studies these years children are expected to be able to delay did not find behavioral effects on IC for the negative gratification, to work through difficulties, and to expe- emotional manipulation (Albert et al., 2010; Wang, rience frustration without losing control (Bronson, Yang, Yuan, Fu, Meng et al., 2011; Yuan, Xu, Yang, 2000). Accordingly, it has been shown that throughout Liu, Chen et al., 2011). the kindergarten years, children are better able to meet As far as we know, only two studies using emotion- the increasing expectations that the social environment induction manipulation have been conducted on children imposes on them, to internalize rules, and to follow (Lamm & Lewis, 2010; Lewis, Lamm, Segalowitz, Stieben directions (Kochanska, Murray & Coy, 1997; Rhoades, & Zelazo, 2006), and they were restricted to school-aged Greenberg & Domitrovich, 2009). Indeed, children’s children. These studies showed that the negative emotion inhibitory abilities, as demonstrated in various inhibitory condition resulted in decreased children’s IC perfor- and conflict tasks, increase throughout the kindergarten mance compared to the nonemotional conditions. The years (Carlson, 2005; Checa, Castellanos, Abundis- negative emotional manipulation was created in these Gutierrez & Rueda, 2014; Diamond & Taylor, 1996; studies by causing the children to lose points in a Go/ Garon, Bryson & Smith, 2008; Kochanska, Murray & NoGo task. We also used this type of manipulation to Harlan, 2000; Kochanska, Coy & Murray,2001; Rueda, investigate kindergartners’ IC during a negative emo- Fan, McCandliss, Halparin, Gruber et al., 2004; Zelazo, tional experience, thus creating an adaptation of the Muller,€ Frye & Marcovitch, 2003). emotion-induction Go/NoGo task developed by Lewis Experiencing negative emotions imposes challenges on et al. (2006). Because previous studies showed inconsis- executive functioning (Mitchell & Phillips, 2007) and tencies regarding the direction of the influence that may specifically affect IC (Calkins & Dedmon, 2000; negative emotions have on IC, in this study we proposed a Eysenck, Derakshan, Santos & Calvo, 2007). Previous bidirectional hypothesis, assuming that the children’sIC findings reveal an inconsistent pattern of results: several performance would differ during the negative emotional studies show that negative emotions impair executive condition compared to the nonemotional conditions. performance (De Houwer & Tibboel, 2010; Padmala, Electrophysiological brain processes can be investi- Bauer & Pessoa, 2011; Verbruggen & De Houwer, 2007), gated using event-related potentials (ERP) and time- whereas other studies show the converse (Ohman,€ Flykt frequency (T-F) analyses as different, although related, & Esteves, 2001; van Steenbergen, Band & Hommel, indicators of cortical brain activity. In children, ERP 2011). These studies used a brief presentation of emo- analysis is often used; however, considering that ERP tional stimuli (such as a short presentation of emotional components contain a mixture of overlapping T-F pictures or affective words), which had less intense components, T-F analyses can provide additional infor- influence on the subject’s emotional experience, com- mation regarding brain activity found in a specific range pared to longer lasting emotional manipulations (Albert, of frequencies. Lopez-Mart ın & Carretie, 2010). Considering that To investigate kindergartners’ related brain processes, motivation and emotion are closely linked (Pessoa, we used the electrophysiological measure of ERP. One of 2009), manipulations that contain motivational aspects the most studied ERP components in relation to IC (i.e. incentives and/or penalties) offer an opportunity to performance and conflict monitoring is the N2 compo- explore the effect that emotional experience has on nent (e.g. Donkers & van Boxtel, 2004; Lewis et al., executive functioning in general and on IC in particular. 2006; Nieuwenhuis, Yeung, van Den Wildenberg & The current study aims to investigate the influence of a Ridderinkhof, 2003). N2 is a negative amplitude negative emotional experience – evoked by motivational recorded approximately 200–400 ms following a manipulation – on kindergartners’ IC. stimulus; it usually appears at the electrodes located in Most of the studies that have employed motivational the fronto-central areas of the scalp (Falkenstein, manipulations have done so with an adult population. Hoormann & Hohnsbein, 1999; Jodo & Kayama,

1992). The ERP approach gives us information about the One recent study investigated theta activity during amplitude of the wave component, but not about response control in children and adolescents using the the frequencies embedded within this amplitude. Because emotion-induction Go/NoGo task (Liu et al., 2014). the brain activity shows oscillations at a variety of Findings from this study showed – only in adolescents – frequencies, time-frequency (T-F) analyses using wave- that theta power increased when the subjects needed to lets enable the examination of a specific frequency at a exert more effort to regain their lost points (after the specific point in time (Samar, 1999). At the frequency emotion-induction manipulation), compared to the theta level, theta EEG signals (4–8 Hz) are related to response power measured before any emotional manipulation was inhibition (Liu, Woltering & Lewis, 2014; Nigbur, conducted. However, in this study, theta power in the Ivanova & Sturmer,€ 2011) and conflict detection and emotional situation was not analyzed. monitoring (Nigbur, Cohen, Ridderinkhof & Sturmer,€ The integration of the electrophysiological findings 2012; Tzur & Berger, 2007). T-F analyses such as wavelets cited above indicates that both N2 amplitudes and theta indicate that the theta oscillations are reflected in the N2 power are usually larger when response inhibition and/or component (Balconi & Pozzoli, 2009; Harper, Malone & conflict processing are required. Hence, in this study we Bernat, 2013) and that the ACC brain area is the main predicted that the children’s IC performance, as common generator of both N2 (Nieuwenhuis et al., expressed in successful NoGo trials, would be associated 2003) and theta EEG signals (Harper et al., 2013). with larger N2 amplitudes and theta power, compared to Previous studies using the Go/NoGo task showed successful Go trials. Moreover, it appears that emotion- larger N2 amplitudes in successful NoGo trials com- ally arousing situations also elicit larger N2 amplitudes pared to Go trials in adults (Ciesielski, Harris & Cofer, and larger theta power. Therefore, in this study we 2004; Falkenstein et al., 1999; Jodo & Kayama, 1992; predicted that the children’s N2 amplitudes and theta Kirmizi-Alsan, Bayraktaroglu, Gurvit, Keskin, Emre power would be larger during the negative emotional et al., 2006) as well as in children (Johnstone, Pleffer, condition compared to the nonemotional conditions. Barry, Clarke & Smith, 2005; Todd, Lewis, Meusel & Previous neuroimaging and neurocognitive studies Zelazo, 2008). A recent study that investigated conflict have reported inconsistent findings regarding the brain monitoring in preschool and school-aged children areas associated with inhibitory processes in populations showed that N2 amplitudes were larger during conflict of children and adults (see detailed review in Berger, monitoring, but only for the children in the older age 2011). Adults’ brain activity during IC is usually group (Buss, Dennis, Brooker & Sippel, 2011). For the reported in the PFC and dorsolateral prefrontal cortex emotional experience, findings show that response inhi- (DLPFC) regions. Specifically, studies show middle bition evoked larger N2 amplitudes during a negative frontal gyrus activation (MFG; Booth, Burman, Meyer, emotion condition compared to nonemotion conditions Lei, Trommer et al., 2003; Durston, Thomas, Yang, (Lamm, White, McDermott & Fox, 2012; Lewis et al., Ulug, Zimmerman et al., 2002; Rubia, Overmeyer, 2006; Yuan et al., 2011). Furthermore, children’s reports Taylor, Brammer, Williams et al., 2000) as well as of their negative emotional experience were associated inferior frontal gyrus activation (IFG; Booth et al., with larger inhibitory N2 amplitudes during an emotion- 2003; Bunge, Dudukovic, Thomason, Vaidya & Gabrieli, induction manipulation (Lewis et al., 2006). These larger 2002; Rubia et al., 2000; Tamm, Menon & Reiss, 2002). N2 amplitudes were interpreted to reflect higher effortful Some researchers have reported right hemisphere activity brain activation when emotionally distressed (Lewis & in those regions (Booth et al., 2003; Bunge et al., 2002; Stieben, 2004). Durston et al., 2002), whereas others report activity in So far, most studies investigating IC performance with the left hemisphere (Rubia et al., 2000; Tamm et al., a T-F approach have been conducted only in adults. 2002) or bilateral activity (Casey, Trainor, Orendi, These studies indicate that theta power is larger during Schubert, Nystrom et al., 1997; Durston et al., 2002). successful NoGo trials compared to Go trials (Harper Cingulate cortex involvement was also activated in et al., 2013; Kirmizi-Alsan et al., 2006; Nigbur et al., studies of adults; however, some of the studies reported 2011) and that theta phase synchrony (which also a more anterior localization in the cingulate cortex indicates higher theta power) is larger during conflict (Casey et al., 1997; Tamm et al., 2002), whereas others processing (Nigbur et al., 2012). Theta oscillations are found more posterior localizations within it (Durston also seen in relation to emotional arousal and emotional et al., 2002; Rubia et al., 2000). regulation (Balconi & Pozzoli, 2009; Knyazev, 2007). For Inconsistencies in PFC and DLPFC activation during instance, Ertl, Hildebrandt, Ourina, Leicht and Mulert IC were also seen in some of the studies with children. (2013) found that theta power was larger during a For instance, Casey et al. (1997) reported bilateral demand for regulating negative emotions. activity of the middle frontal gyrus, whereas others

© 2015 John Wiley & Sons Ltd 4 Tali Farbiash and Andrea Berger reported only right activity in this region (Booth et al., Method 2003; Durston et al., 2002). Furthermore, several studies reported bilateral activity in the inferior frontal gyrus (Booth et al., 2003; Casey et al., 1997; Durston et al., Participants 2002), whereas Bunge et al. (2002) only found activity in The initial sample consisted of 65 kindergarten children; the left side of this brain region. Because left inferior however, seven children did not have complete data for frontal activity is related to language production and the Go/NoGo task: four of them did not agree to perform comprehension, this finding in children was interpreted the task at all, two of them dropped out at the beginning by the researchers to be an indication of children’s use of of the task, and one child was not able to play because of verbal aid to complete the inhibitory tasks. technical computer problems. It is important to state that As for the brain regions active during a negative none of the children dropped out of the game during the emotional experience, evidence is scarce. Lewis et al. emotion-induction block. Thus, the final sample for the (2006) investigated the sources of brain activity during a behavioral analyses consisted of 58 children (27 boys) negative emotional experience and showed that in aged 5.5–6.5 years (M = 5.79, SD = 0.27). The children school-aged children, a negative emotional experience who participated in the study were from Hebrew-speaking resulted in more posterior brain regions of the frontal families with normal or corrected-to-normal vision. and parietal lobes than is usually found in adults. These Normative development was ensured by recruiting results were attributed to less mature brain activity children from regular kindergartens and relying on the resulting from the negative emotional experience. The parents’ reports; the children were born full term and had process of frontalization was also evident in several no history of developmental delays or neurological previous studies (Bunge et al., 2002; Rubia et al., 2000). damage/head injury. In addition, the children’s level of In a later study in the Lewis group (Lamm & Lewis, intelligence was assessed (Raven, 1960; Raven, Raven & 2010), ventral PFC activation was reported during Court, 2003), and no univariate outliers were found (all negative emotional experiences; however, this study was z-scores were in the range of 2.58). Furthermore, interested in morphology-based regions of interest several background variables were collected and taken (ROI), which did not include the more posterior frontal into account in the analyses (background list and regions or parietal brain areas. descriptive statistics are presented in Table 1). The extant literature contains marked inconsistencies regarding the exact brain regions activated during IC, whether or not negative emotions are involved. These Measures discrepancies exist for adults and are even greater in children. To date, there are no data regarding brain The emotion-induction Go/NoGo task source localization related to IC of kindergarten chil- The emotion-induction Go/NoGo task was adapted dren, which is one of the goals of investigation in the from Lewis et al. (2006) to measure response inhibition present study. during a negative emotional situation. This task was developed and presented using the E-Prime software

The present study Table 1 Descriptive Statistics of the Background Variables Variable Mean SD The aim of this study was to investigate the neurocognitive correlates of children’s IC performance and the Mother effect that a negative emotional experience has on Age 35.49 3.77 Education 15.60 4.15 behavioral and brain inhibitory mechanisms of kinder- Raven score (% correct) 0.56 0.17 garten children. This study is the first to investigate Father kindergartners’ IC and related brain activity during a Age 37.95 4.15 Education 15.11 3.02 negative emotional manipulation. Moreover, the use of Child several methodological approaches (such as T-F Age 5.79 0.27 analysis and the analysis of the amplitude sizes) in Raven score (% correct) 0.55 0.11 Target duration (ms) children this young is innovative; these approaches, Block A 741.36 110.78 including the source localization analysis, can provide Block B 802.52 149.26 a comprehensive picture regarding kindergartners’ Block C 740.90 129.46 inhibitory brain processes while experiencing negative emotions. Note: Age and education in years.

(Psychological Software Tools Inc., Pittsburgh, PA). In To induce negative emotions, children were told they the Go/NoGo task, the children were asked to press a were competing against other children who had already response key as quickly as possible at the detection of a played the game. This was, in fact, an artificial compe- Go stimulus and to inhibit their response when they tition. The children were also told that if they won the detected a NoGo stimulus. Pressing was executed with game they would receive a prize. For every 20 trials, the the index finger of the child’s dominant hand. children received visual feedback in the form of a The task was divided into three blocks (A, B, and C). pyramid, detailing their performance and ranking in To increase children’s interest in the task, each block of the competition. In Block A, the feedback showed that the task included different pairs of Go and NoGo stimuli the child was in first/second place. During Block B, the (either flower–mushroom, apple–worm, or sheep–wolf, children’s ranking gradually decreased until it reached as Go and NoGo stimuli, respectively, see Figure 1). To last place. This artifically low ranking was used to induce avoid a situation where the images of stimuli pairs served negative emotions in response to the possible loss of the as a confound, their order was counterbalanced between prize. In the last block (C) the children’s ranking blocks. Blocks A and C contained 200 trials; 33% of gradually increased until it again reached first place, them were NoGo trials (66 NoGo trials and 134 Go ensuring that every child won a prize and finished the trials). Block B was shorter to limit children’s duration game with a positive feeling. In addition, after the task of frustration during the emotion-induction block and performance, children were given information regarding thus contained 160 trials; 28% were NoGo trials (45 the artificial feedback they received and were informally NoGo trials and 115 Go trials). NoGo trials were debriefed regarding their feelings during and at the end presented in a pseudorandom order without the presen- of the task. tation of consecutive NoGo trials. Go stimuli were presented for an initial duration of 1500 ms, which was Manipulation check adjusted with a dynamic-tracking method to maintain the level of task diffculty between children and to sustain The emotion-induction manipulation was checked using their engagement in the task. This dynamic method a subjective rating scale, which the children completed adjusted Go stimulus duration (50 ms increase/decrease after each block of the task. The rating scale included a after an incorrect/correct response, respectively), and no 6-point Likert scale (higher score reflected higher neg- minimum target duration was set. Thus, Go accuracy ative emotional experience) for three measures: Enjoy- rate was maintained at 50 10%. NoGo stimulus ment (reversed), Annoyance, and Subjective Success duration was 500 ms. The interstimulus interval (reversed). Significant positive correlations ranging from occurred randomly: 600, 800, or 1000 ms after a r = .33 to r = .69 were found between those three scales; response was made or after a NoGo stimulus disap- thus, they were averaged to create a single score. peared (when no response was made). Children were Moreover, although the children were instructed to sit given short breaks between blocks (approximately quietly while performing the task, when they did speak 3 minutes). During these breaks, children remained their vocalizations were written down and used as seated and electrode impedences were rechecked. additional evidence reflecting their emotional experience.

Intelligence estimation (Raven, 1960; Raven et al., 2003) Children and their mothers were tested with the Raven Colored Progressive and Standard Progressive Matrices (CPM and SPM, respectively).

Procedure The researchers contacted kindergartens in Beer Sheva and surrounding areas to recruit children between the ages of 5.5 and 6.5 years. Letters detailing the research topic and procedures were sent to parents by the kindergarten teachers; interested parents were contacted by phone to arrange a home visit. A 90-minute home Figure 1 The stimuli that were used in the task. visit was scheduled to give the parents a thorough

© 2015 John Wiley & Sons Ltd 6 Tali Farbiash and Andrea Berger explanation of the experimental procedure, including the To corroborate the behavioral results obtained using ERP method. To avoid a situation in which the children the averaged Go/NoGo score, an additional analysis was would be prepared in advance for the emotional manip- applied based on the Signal Detection Theory (SDT; ulation, the information regarding this process was given Stanislaw & Todorov, 1999). Specifically, this methdol- to the mothers only, at the lab, just before they gave their ogy yields a measure of sensitivity (dʹ) that reflects the consent for their child to be tested in the Go/NoGo ERP subjects’ ability to distinguish signals (i.e. Go stimuli) task. During the home visit the mother signed a consent from noise (i.e. NoGo stimuli) without the need to form regarding the behavioral procedures included in the composite an average score of Go and NoGo trials. In study. In addition, the child and his/her mother were addition, SDT yields a measure of response bias (c) that given an intelligence assessment. The home visit also reflects the extent to which the subjects favor one provided an initial opportunity for the child to meet the response over the other. experimenter. This facilitated the child’s feelings of comfort at the subsequent visit at the neuropsychological EEG and ERP recording and analysis lab. A 90-minute lab visit was scheduled within two weeks of the home visit. The children were accompanied ERP analysis. EEG was recorded from 128 scalp sites by their mothers to the lab. Before performing the Go/ using the EGI Net Station Geodesic Sensor net and NoGo task, the mother signed a consent form regarding system (Tucker, 1993). Electrode impedances were kept the ERP procedures and the child’s assent to participate below 40 KO, an acceptable level for this system (Ferree, was obtained. The electrode sensor net was then applied Luu, Russell & Tucker, 2001). All channels were refer- and the experimenter explained the task instructions. enced to the Cz channel. Data were collected using a 0.1– The Go/NoGo task was conducted in a quiet room using 100 Hz bandpass filter; signals were collected at 250 Hz a video camera, which allowed the experimenter to and digitized with a 24-bit A/D converter. monitor the child’s behavior during the experiment. Continuous EEG data were filtered with a 0.1 Hz high The study was approved by the Ethics Committee of pass and 30 Hz low pass filter (following Lewis et al., the Department of Psychology at Ben-Gurion University 2006). The data were segmented into trials time-locked to of the Negev and the scientific department of the the presentation of the Go/NoGo stimulus. Each seg- Ministry of Education. Furthermore, the ERP proce- ment contained 880 ms (the maximal segment length, dures were approved by the Helsinki Committee of without overlapping the next segment), with 200 ms as Soroka University Medical Center. baseline. The segmented data were categorized into Go and NoGo trials for each block and contained only succesful trials. In addition, the succesful Go trials were Analyses filtered to include trials with response times greater than 200 ms. The segmented data were subjected to automatic Statistical analyses of behavioral data artifact detection for bad channels and/or eyeblinks. Statistical analyses were conducted using STATISTICA- Segments with voltage deviations of more than 100 lv Windows version 9.2 (Statsoft, Tulsa, OK) software within eye channels were excluded as having an eye blink. package. The data obtained from the Go/NoGo task Channels with voltage deviations of more than 140 lv were analyzed using two methods: The first method, relative to baseline were marked as bad and segments following Lewis et al. (2006), took into consideration the having more than 20 bad channels were excluded from fact that perseverative nonresponse leads to high accu- analyses. Segments with more than 20 bad channels were racy percentages on NoGo trials versus Go trials and excluded, and bad channels were replaced with spherical vice versa. Again, following Lewis et al. (2006), the interpolation of the neighboring channels values. Eye statistical analyses averaged the Go and NoGo accuracy movements and verification of the automatic artifact percentages. Furthermore, to avoid analyzing automatic detection were also manually detected. Children with Go responses, and because target duration was not set to noisy ERP data, meaning less than 10 clean segments for a minimum time, trials in which the response time was NoGo and Go trials in each block, were excluded from below 200 ms were discarded. Moreover, Go response analyses. Thus, the electrophysiological N2 analyses times (rt) were directly influenced by the dynamic- included data from 40 children. After cleanup, the mean tracking method, and in accordance, by target duration. number of segments for all blocks was 30.92 (SD = Considering possible factors (such as fatigue, practice, 11.34). Table 2 presents the means and standard devia- etc.) that may have interfered with the response times tions for the number of Go and NoGo segments obtained, their interpretation seems problematic; thus, obtained in each block of the task. After averaging, response times were excluded from the analyses. each trial was re-referenced with the polar average

Table 2 Descriptive Statistics of Clean Segments was limited to the time window and the electrodes that were used for the N2 analysis. Theta power was calculated Variable Mean SD as the adaptive mean of 4–8 Hz frequency range. Block A Go 37.6 11.57 Source localization analysis. Each child’s ERP data NoGo 28.5 12.2 were analyzed using the standardized low-resolution Block B Go 35.72 10.12 brain electromagnetic tomography (sLoreta) algorithm NoGo 21.9 7.92 (Pascual-Marqui, 2002). sLoreta is a method that provides Block C a 3D solution for the EEG inverse problem and computes Go 33.42 13.01 NoGo 28.37 13.22 images of electric neuronal activity from EEG. Although, in general, solutions provided by EEG-based source localization algorithms should be interpretedwith caution reference effect (PARE) technique. Finally, baseline due to their potential error margins, this method can correction was applied. provide an estimation of the EEG neuronal origin. The Visual inspection of the grand average revealed an N2 relevant time window used for analyzing source localiza- negative peak around 325 ms after the NoGo stimulus. tion was 280–380 ms poststimulus. The differences Thus, statistical extraction was limited to 250–400 ms. A between the Go and NoGo conditions in each block were group of nine electrodes around FCz and Fz were analyzed using paired t-tests. The p-values were calculated selected for statistical extraction based on the literature with a bootstrap method based on 5000 iterations. regarding the N2 scalp topography (Falkenstein et al., Significance was obtained if p < .05. 1999; Jodo & Kayama, 1992; Lewis et al., 2006; see Figure 2). The N2 amplitude was calculated for each electrode as the adaptive mean within two samples Results around the minimum peak in the specified time window. All of the following analyses were conducted while Time-frequency analysis. Time-frequency analysis was controlling for correlated background variables, for all performed using the EGI Net Station Geodesic Sensor net levels of analyses (see Tables 3 and 4). The correlation and system (Tucker, 1993). To examine theta frequencies analyses involving the background variables suggested measured in the same time window of N2, the same some associations of the electrophysiological measures processes that were described in the ERP analysis were with child gender. However, these associations are not used in the T-F analysis, except for the data filtering. the focus of the current manuscript and will not be Because one of the children could not be included in the further discussed. It should be noted that the results wavelet analyses due to technical reasons, 39 children were presented below did not change significantly when the included in the T-Fanalyses. The wavelet analysis included ANOVA analyses were run without the covariates. 0.1 Hz high pass and a 50 Hz notch filter. No additional Because there were fewer NoGo segments in Block B, low pass filter was applied. Waveletswere created using the we repeated the tests for amplitude/theta power differ- Morlet function defined by the frequency scale factor of 7, ences by block, with the number of segments as a ranging from 1 to 40 Hz in 1 Hz steps. Statistial extraction covariate, revealing similar results.

Figure 2 Average waveforms showing N2 amplitude differences for Go and NoGo trials in Blocks A, B, and C (left); the montage of scalp locations for statistical analyses (right).

Table 3 Correlations with Background Variables

Mother’s Child’s Trial Mother’s Mother’s raven Father’s Father’s Child’s Child’s raven Block type age education score age education gender age score

Go/NoGo A .06 .22 .07 .00 .47** .21 .05 .12 Performance B .15 .13 .06 .03 .26† .14 .10 .09 C .27* .05 .00 .15 .31* .08 .26* .04 N2 A Go .01 .03 .12 .08 .15 .145 .03 .25 Amplitude NoGo .05 .04 .21 .03 .16 .35* .04 .04 B Go .00 .02 .09 .11 .22 .26† .01 .16 NoGo .17 .01 .11 .19 .09 .40* .05 .03 C Go .17 .25 .00 .13 .13 .29† .00 .07 NoGo .06 .03 .16 .08 .15 .52** .01 .07 Theta Power A Go .20 .22 .09 .16 .07 .56*** .10 .04 NoGo .20 .07 .32* .28 .17 .69*** .14 .09 BGo.21 .23 .10 .15 .11 .59*** .06 .01 NoGo .04 .01 .42** .14 .03 .63*** .21 .02 CGo.12 .11 .33* .20 .02 .52** .18 .08 NoGo .12 .03 .18 .16 .22 .59*** .16 .13

Note: Pearson correlations are presented for the continuous variables. Point biserial correlations are presented for the dichotomous child’s gender variable only. The significantly correlated background variables were statistically controlled as covariates in the research analyses. †p<.1.*p<.05. **p<.01.***p<.001.

Table 4 Correlations with Target Duration Table 5 Descriptive Statistics of the Emotional Scale

Target duration Block A Block B Block C

Block Block A Block B Block C Enjoyment 5.50 (1.24) 5.18 (1.59) 5.34 (1.33) Annoyance 5.51 (1.09) 5.12 (1.57) 5.21 (1.46) Go/NoGo A .10 Subjective success 5.50 (1.14) 4.46 (1.87) 5.60 (1.04) Performance B .39*** Total 5.51 (0.92) 4.92 (1.32) 5.38 (1.04) C .23† N2 Amplitude A Go .31† NoGo .07 Note: This table presents descriptive statistics of children’s subjective BGo .14 emotional scale in Blocks A, B, and C. Scoring ranges between 1-6. NoGo .14 CGo .12 NoGo .15 Theta Power A Go .18 and variations (see Table 5). Children’s averaged ratings NoGo .09 of their subjective emotional experience were analyzed BGo .15 using repeated-measures ANOVA. Results revealed that NoGo .21 CGo .18 children’s ratings were different between blocks (F(2, 108) = NoGo .24 7.85, p < .001, MSE = 2.34, g²q =.13). Planned comparisons revealed that the Block B rating was higher than the Note: Pearson correlations between the study variables and target ratings of Blocks A and C (F(1, 54) = 9.80, p < .01, MSE = duration are presented for each block. †p<.1.*p<.05. 1.04, g² = .15), indicating that the children did not enjoy ** < *** < q p .01. p .001. playing the block with the negative emotional induction as much as they enjoyed playing the other blocks. When General Linear Models (GLM) were used, Greenhouse-Geisser’s correction was applied if Mauch- Go/NoGo results ley’s test indicated that sphericity was violated. First, we calculated the descriptive statistics for the behavioral study measures, which provided an initial Behavioral results description of the children’s response time accuracy in terms of averages and variations (see Table 6). Second, Manipulation check an examination of the Go tracking method was First, we calculated the descriptive statistics for the conducted, which revealed that (as expected) Go manipulation check rating scales, in terms of averages accuracy percentages ranged between 47% and 52%.

Table 6 Descriptive Statistics of the Behavioral Data higher sensitivity in Block B compared to Blocks A and C(F(1, 40) = 25.30, p < .001, MSE = .07, g²q = .39). Block SDT differences were not found in children’s response bias (c): Response Averaged IC Sensitivity Response (F < 1, g²q = .02). times performance (dʹ) bias (c)

Mean SD Mean SD Mean SD Mean SD Electrophysiological Go/NoGo results Block A 474.4 79.5 0.58 0.06 0.51 0.38 0.28 0.30 Block B 465.1 76.1 0.63 0.06 0.76 0.43 0.32 0.32 First, we calculated the descriptive statistics for the Block C 455.7 71.7 0.58 0.06 0.52 0.40 0.32 0.28 electrophysiological measures, which provided an initial description of the N2 amplitudes and the theta power, in Note: This table presents descriptive statistics of children’sIC terms of averages and variations (see Table 7). Second, A 2 performance in Blocks A, B, and C (percent of accuracy ranged from 0- (trial type) 9 3 (block) GLM repeated-measures ANOVA 1). Additionally, this table presents SDT descriptive statistics: Sensitivity (d’) and response bias (c) are measured in standard deviation was conducted to analyze N2 effects. As expected, a main units. Sensitivity ranges from -1 to +1. Values of d’ =-1 indicates effect of trial type was found, showing larger N2 ampli- the subject’s repeated confusion between Go and NoGo stimuli; d’ =0 = ’ tudes for NoGo trials than for Go trials (F(1, 38) 50.35, indicates the subject s inability to distinguish a Go from a NoGo < = ² = stimulus, and d’ =+1 indicates perfect performance. Response bias p .001, MSE 13.01, g q .57). Findings did not 1 1 also ranges between - to + . Negative values signify a bias toward indicate block differences (F < 1, g²q = .003) or block-by- responding, and a positive value signifies a bias toward not responding trial type interaction (F < 1, g² = .002). Accordingly, the to the signal. q N2 difference waves (NoGo–Go) did not show any significant block differences (F < 1, g²q = .002; see NoGo accuracy percentages ranged between 68% and Figure 2). Another 2 (trial type) 9 3 (block) GLM 74%. repeated-measures ANOVA was conducted to analyze The analysis of whether children’s IC performance effects in theta power within the N2 window. As was differed between the emotion-induction block (B) and the hypothesized, results showed a main effect of trial type, other blocks (A and C) was conducted first, based on the indicating larger theta power for NoGo trials than for Go average score of Go and NoGo accuracy percentages. This trials (F(1, 36) = 15.03, p < .001, MSE = .20, g²q = .29). In analysis was conducted with GLM one-way repeated- addition, a block main effect was found, showing that measures ANOVA, with block (3 levels) as the within- theta power differed between blocks (F(2, 72) = 2.58, ’ subject factor. Results revealed that children s accuracy p < .05, MSE = .07, g²q = .07). As expected, planned differed between blocks (F(2, 78) = 3.04, p < .05, MSE = comparisons indicated that theta power in Block B was .001, g²q = .07). Planned comparisons indicated that significantly larger than theta power in Blocks A and C ’ children s IC performance was better in Block B com- (F(1, 36) = 5.63, p < .05, MSE = .08, g²q = .14). Further- = < = pared to Blocks A and C (F(1, 39) 37.00, p .001, MSE more, a block-by-trial type interaction was found (F(1.70, ² = .001, g q .49). Additional GLM repeated-measures 61.03) = 3.82, p < .05, ɛ = .85, MSE = .13, g²q = .10). ANOVAs were then conducted using SDT to measure Planned comparisons showed that theta power in Block B block differences in sensitivity and response bias. Results revealed that children’s sensitivity (dʹ) differed between blocks (F(2, 80) = 4.73, p < .05, MSE = .07, g²q = .11). Planned comparisons revealed that children showed

Table 7 Descriptive Statistics of the Electrophysiological Data

N2 amplitudes Theta power

Go NoGo Go NoGo

Measure Mean SD Mean SD Mean SD Mean SD

Block A 7.54 3.39 10.97 5.07 0.43 0.29 0.73 0.57 Block B 7.55 4.84 10.55 5.11 0.45 0.27 0.88 0.81 Block C 7.61 5.11 10.91 6.37 0.41 0.37 0.70 0.77 Figure 3 Theta power for NoGo trials (darker columns) and Note: This table presents N2 amplitudes (lv) and theta power (lv)2 of Go trials (lighter columns) in each block. The bars represent all of the blocks of the Go/NoGo task. standard errors.

sional scalp topographic maps, showing larger frontal power in NoGo trials compared to Go trials. To assess whether theta power contributed to N2 amplitudes during IC performance, multiple regression analyses were performed. These regression analyses included theta power and N2 amplitudes in NoGo trials separately for each block and controlled for background variables, which were entered first into the regression model. Consistent with the hypothesis, the results indicated that children’s theta power contributed to N2 amplitudes in all the task blocks (A-NoGo: b = .65, < = < = Figure 4 Two-dimensional scalp topographic maps p .01; B-NoGo: b .54, p .01; C-NoGo: b .70, < illustrating theta power (lV)² for NoGo trials (left) and Go trials p .001). (right) in the negative emotional block. Notice the brighter yellow color reﬂecting higher theta power in NoGo trials at the Source localization results frontal location (left topographic map), compared to the lower theta power in Go trials (right topographic map). The source localization results showed that during the emotion-induction block (B), children’s brain activity is different from Blocks A and C for NoGo trials (F(1, 36) = significantly differed between Go and NoGo trials in 4.60, p < .05, MSE = .16, g²q = .11), but not for Go trials several brain areas. Differences were found in several (F < 1, g²q = .01). Figure 3 presents a bar diagram for theta regions of the limbic lobe and, specifically, in the dorsal power in NoGo trials compared to Go trials for each area of the anterior cingulate gyrus. Additional Go/ block. Figure 4 illustrates the theta power in two-dimen- NoGo differences in brain activation were found in the

Figure 5 Loreta source localization differentiating children’s brain activity for Go versus NoGo trials in Block B. The upper image illustrates these differences as seen in the posterior cingulate and parahippocampal gyrus. The lower image illustrates these differences as seen in the medial frontal gyrus. The colored scale denotes the t-values for the difference between Go and NoGo trials.

© 2015 John Wiley & Sons Ltd Kindergartners’ brain and behavioral IC 11 prefrontal lobe and especially in the posterior medial irrelevant stimuli. However, these studies, conducted by frontal gyrus. Significant results were also found in the Yechiam and Hochman (2013a, 2013b) did not refer to anterior part of the parietal lobe. Figure 5 presents the emotional experience evoked by those losses. Pad- examples of the Go/NoGo differences, as seen in the mala et al. (2011) suggest that motivational aspects cingulate gyrus (320 ms poststimulus) and in the medial improve executive functions and that the possibility of frontal gyrus (368 ms poststimulus) during the negative receiving a reward increases motivation to perform emotional condition. better. However, this explanation is not enough to Brain activity differences between Go and NoGo trials explain the block differences found in our study, since were marginally seen in Block A in the medial frontal children could receive their prize only after completing gyrus. In Block C, these differences were marginal and all three blocks and not just after completing Block B of appeared bilaterally in the inferior frontal gyrus and in the task. It appears that as Sarter, Gehring and Kozak the middle frontal gyrus. (2006) have claimed, it is the possible loss of the reward that increases motivation, attentional effort, and performance, as was evident during Block B of the Go/NoGo Discussion task. The behavioral results found in this study are consis- The main interest of the present study was to investigate tent with most of the adult literature in this respect, as neurocognitive correlates of children’s IC, specifically detailed in the Introduction. However, they appear the effects that negative emotional experience may have different from the findings presented by Lewis et al. on the behavioral and brain inhibitory mechanisms of (2006) and Lamm and Lewis (2010), which showed that kindergarten children. All of the study’s hypotheses were children’s inhibitory performance was impaired during confirmed, indicating the expected behavioral and elec- the emotion-induction block. Lewis and colleagues trophysiological differences regarding the IC perfor- explained this performance impairment with the idea mance of kindergarten children during a negative that children recruit additional attentional resources to emotional experience. regulate the induced negative emotions. Assuming that The manipulation check indicated that the negative attentional resources are limited, the available remaining emotional manipulation worked, and children reported resources for task performance were reduced; thus experiencing more negative emotions in Block B com- executive performance was impaired. pare to Blocks A and C of the Go/NoGo task. This How can we interpret the difference in results between negative emotional experience was accompanied by Lewis’ studies and the present study? A plausible improved behavioral IC performance, compared to the explanation could be related to the differences in the non-negative emotional experience. Cohen and Henik tasks’ designs. For example, in Lewis’ design, children (2012) offer several interpretations for understanding the were asked to press a button for each stimulus presented impact that negative emotions can have on executive (e.g. x,y) but to refrain from pressing if the stimulus was functions. First, it may be that the negative emotional repeated a second time in succession. This means that the experience evoked children’s more focused, goal-oriented same stimulus was a Go trial in some instances and a attention to minimize their negative emotional experi- NoGo trial in others. In the present study, each stimulus ence and win the game (Inzlicht, Bartholow & Hirsh, kept its role as a Go or a NoGo stimulus during each 2015). Such an attentional narrowing was also evident in block. Lewis’ design creates a greater cognitive load previous studies, which showed that stress/threat because it requires switching and working memory improves selective attention (Chajut & Algom, 2003; abilities and not just inhibitory functions. Previous van Steenbergen et al., 2011). Second, improvement in findings have shown that when a task is highly IC performance may also be related to the relevance of resource-intensive and demands careful concentration, the negative emotional experience to the task (Kanske & negative emotions have a deleterious impact on executive Kotz, 2011; Kanske, 2012). Hence, it may be that functioning (Eysenck et al., 2007; Mitchell & Phillips, children’s negative emotional experience signaled a 2007). problematic situation that required recruiting more The electrophysiological results were fully consistent efficient and/or more attentional resources, and thus with the hypotheses. As expected, larger fronto-central children’s performance was accelerated (Inzlicht et al., N2 amplitudes were found during successful NoGo 2015). Consistent with these points of view, it was shown trials, compared to successful Go trials. This pattern of that losses improve cognitive performance since they results has been consistently replicated in adult studies enhance on-task attention. This increased attention leads (Ciesielski et al., 2004; Falkenstein et al., 1999; Jodo & to greater focusing, which enhances the ability to ignore Kayama, 1992; Kirmizi-Alsan et al., 2006), although for

© 2015 John Wiley & Sons Ltd 12 Tali Farbiash and Andrea Berger children the evidence was less consistent (Ciesielski case, it was surprising that the electrophysiological et al., 2004; Davis, Bruce, Snyder & Nelson, 2003; differences regarding children’s negative emotional expe- Johnstone et al., 2005; Lewis et al., 2006; Todd et al., rience were not evident at the level of N2 amplitudes. It 2008). In the present study, the difference between Go appears that the theta band power can be better at versus NoGo N2 amplitudes can also be interpreted in detecting children’s inhibitory processes during a nega- terms of conflict monitoring. High conflict accompanies tive emotional experience than N2 amplitudes. One the demand for withholding a prepotent response and, explanation for this difference may be methodological, indeed, previous studies have indicated that resolving meaning that the averaging process resulted in a flattened conflict between incompatible responses was associated averaged amplitude size, statistically reducing the chance with larger N2 amplitudes compared to nonconflict of finding a significant effect; this process does not occur conditions (Donkers & van Boxtel, 2004; Nieuwenhuis in the frequency analyses (Luck, 2005). Additional et al., 2003). explanation may be that other frequencies (besides the The electrophysiological results using a T-F approach theta frequency) play a role in children’s inhibitory provided the first evidence of its kind for IC performance processes, thus affecting the results obtained. in kindergarten children. Specifically, children’s larger The source localization analysis revealed clear local- fronto-central theta power was evident during NoGo ization of the differences between Go and NoGo trials compared to Go trials. Findings from the ERP conditions, although these differences were strong literature with adult participants suggest that larger theta enough to reach significance only in the negative power reflects higher demand for inhibiting the motor emotion block. It seems the negative emotional manip- preparation for executing a Go response (Harper et al., ulation evoked larger brain activity when inhibition was 2013; Kirmizi-Alsan et al., 2006; Nigbur et al., 2011). required. Such activity was seen in parts of the limbic Liu, Woltering and Lewis (2014) investigated theta power system, specifically in the dorsal ACC. ACC activity in school-aged children and suggested that theta power during response inhibition is firmly established in may reflect response inhibition as well as conflict neurocognitive research in Go/NoGo paradigms (Braver monitoring. Indeed, previous findings show that larger et al., 2001; Durston et al., 2002) as well as in other theta power is evident during conflict detection and executive tasks (i.e. Stroop, Flanker, etc.), which include conflict processing as well (Nigbur et al., 2011, 2012; an element of inhibition in addition to conflict moni- Tzur & Berger, 2007). toring (Carter & van Veen, 2007; van Veen & Carter, Our results also indicated that theta power was 2002). Botvinick et al. (2004) have suggested that the increased in the negative emotional Block B, compared dorsal ACC is involved in the detection of the conflict to the other two blocks. Moreover, this difference was as well as in triggering top-down control to minimize evident in NoGo trials but not in Go trials. There is a that conflict. Children’s brain activity during a negative paucity of research regarding the impact of emotional emotional experience was also shown in the medial experience on adults’ theta power during IC performance. frontal cortex (MFC). It is suggested that the posterior To date, one study revealed that frontal theta power was MFC (pMFC) is involved in the process of evaluating larger during emotional regulation, assuming that the performance as well as in exerting the relevant perfor- increase in theta oscillations was due to the emotional mance adjustments. In addition, pMFC activity is processing as well as to the attentional processes active related to reward-based association learning: When during cognitive reappraisal (Ertl et al., 2013). Moreover, negative feedback indicates that the probability of considering the links between theta power and conflict receiving a reward is reduced, performance needs to monitoring (Nigbur et al., 2011, 2012; Tzur & Berger, be changed and/or effort increased (Ridderinkhof, van 2007), it may well be that the negative emotional den Wildenberg, Segalowitz & Carter, 2004). This experience enhanced the conflict experienced by the suggestion is compatible with the behavioral findings children, thus resulting in larger theta power in the of this study, which showed that children’s performance emotional block (B). Liu et al. (2014) investigated theta was better when the negative emotional experience was power using Lewis’ previously reported emotional manip- induced; moreover, it is consistent with the electrophys- ulation; however, this study did not report theta power iological and source localization results, which show results from the emotion-induction block (B), leaving this that brain activity is larger while inhibiting responses piece of information unclear. during a negative emotional situation. Furthermore, the In this study, we showed that theta power strongly posterior regions found in the present study are contributes to N2 amplitudes during IC performance. consistent with Lewis et al. (2006), who suggested that These findings are in line with previous findings in adults younger children show more activation in central- (Balconi & Pozzoli, 2009; Harper et al., 2013). In this posterior areas during an inhibitory control task instead

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