Response inhibition difficulties in preterm children aged 9–12 years: Relations with emotion and...

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Child Neuropsychology: A Journal onNormal and Abnormal Development inChildhood and AdolescencePublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/ncny20

Response inhibition difficulties inpreterm children aged 9–12 years:Relations with emotion and behaviorMorgane Réveillona, Cristina Borradori Tolsab, Maryline Monnierc,Petra S. Hüppib & Koviljka Barisnikova

a Child Clinical Neuropsychology Unit, Department of Psychology,University of Geneva, Geneva, Switzerlandb Division of Development and Growth, Department of Pediatrics,University Hospital of Geneva, Geneva, Switzerlandc Follow-up Unit, Division of Neonatology, Department ofPediatrics, University Hospital of Lausanne, Lausanne, SwitzerlandPublished online: 08 Jan 2015.

To cite this article: Morgane Réveillon, Cristina Borradori Tolsa, Maryline Monnier, Petra S. Hüppi& Koviljka Barisnikov (2015): Response inhibition difficulties in preterm children aged 9–12 years:Relations with emotion and behavior, Child Neuropsychology: A Journal on Normal and AbnormalDevelopment in Childhood and Adolescence, DOI: 10.1080/09297049.2014.994486

To link to this article: http://dx.doi.org/10.1080/09297049.2014.994486

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Response inhibition difficulties in preterm children aged

9–12 years: Relations with emotion and behavior

Morgane Réveillon1, Cristina Borradori Tolsa2, Maryline Monnier3,Petra S. Hüppi2, and Koviljka Barisnikov1

1Child Clinical Neuropsychology Unit, Department of Psychology, University of Geneva,Geneva, Switzerland2Division of Development and Growth, Department of Pediatrics, University Hospital ofGeneva, Geneva, Switzerland3Follow-up Unit, Division of Neonatology, Department of Pediatrics, University Hospitalof Lausanne, Lausanne, Switzerland

Previous studies with children have demonstrated inhibition difficulties associated with prematurity,but the question of potentially catching up with a delay in inhibition processes before adolescence stillremains. Moreover, preterm adolescents are more at risk than their term-born peers for presentingbehavioral problems such as emotional difficulties and attention deficit/hyperactivity disorder. Inaddition to examining response inhibition, this study addressed, for the first time, the impact of anemotional context on response inhibition abilities and its relation to behavioral problems in lateschool-aged preterm children. Fifty-eight preterm children aged 9–12 years were compared with 61controls on two versions of a stop-signal task, the Delay Frustration Task, and the Strengths andDifficulties Questionnaire. Results showed general difficulties in inhibiting a response, rather than aspecific impact of emotional context in preterm children. Compared with controls, these childrenexhibited more and longer button presses in a delay situation, as well as faster go reaction timesassociated with lower probability of inhibition in the stop-signal tasks. These difficulties reflectedimpulsivity and were associated with higher hyperactivity/inattention and conduct problems.Additionally, intrauterine growth restriction was found to be an additional perinatal risk factor forhyperactivity/inattention symptoms. These findings suggest that remaining inhibition difficulties inthe preterm population at preadolescence could reveal increasing behavioral issues.

Keywords: Response inhibition; Prematurity; Behavior; Impulsivity; Children.

The funding sources had no involvement in this study and in the decision to submit the article forpublication. The authors declare that they have no conflict of interest. Professional English language and styleediting was provided by Barbara Every, ELS, of BioMedical Editor. The authors thank Sébastien Urben for hisconstructive suggestions and his help in designing the tasks, and Claudio Straccia for his help in revising themanuscript. We also thank all the children and their parents for participation.

This work was supported by the Swiss Confederation (grant number UN7528) and the Swiss NationalScience Foundation (grant number 32000B0-113632).

Address correspondence to M. Réveillon, Child Clinical Neuropsychology Unit, University of Geneva (UniMail – 6163), Bld. Du Pont-d’Arve 40, CH-1211 Geneva 4, Switzerland. E-mail: Morgane.Reveillon@unige.ch

Child Neuropsychology, 2015http://dx.doi.org/10.1080/09297049.2014.994486

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Being born preterm is a particular risk factor for presenting neurodevelopmental problemsand long-term cognitive difficulties (Soria-Pastor et al., 2009; Taylor & Jakobson, 2010).Among these difficulties, it has been well documented that preterm children are at highrisk for executive function deficits (Aarnoudse-Moens, Duivenvoorden, Weisglas-Kuperus, Van Goudoever, & Oosterlaan, 2012; Anderson & Doyle, 2004; Edgin et al.,2008; Mulder, Pitchford, Hagger, & Marlow, 2009; Pizzo et al., 2010). Moreover, execu-tive function difficulties in preterm children have been reported to underlie their schoolunderachievement (Anderson & Doyle, 2008; Arpino et al., 2010) as well as their laterbehavioral problems (Bhutta, Cleves, Casey, Cradock, & Anand, 2002; Hack et al., 2009)such as emotional, disorders, conduct disorders, and attention deficit/hyperactivity dis-order (ADHD). Specifically, the latter disorder was reported to be two to four times moreprevalent in the preterm than in the general population (Arpino et al., 2010; Bhutta et al.,2002; Johnson & Wolke, 2013). These difficulties appeared to be predictive of socialinteraction problems and seemed to persist through adolescence and adulthood.

The development of executive function has been linked to the maturation of thefrontal lobe and particularly the prefrontal cortex (PFC). With the essential maturationprocess of the frontal lobe occurring during the first year of life, any damage ordisturbance caused by perinatal factors, such as preterm birth, may impair executivefunctioning (Sun & Buys, 2012; Taylor, Donner, & Pang, 2012). Moreover, impairmentsin executive function performance in preterm children have been associated with theirneonatal white matter abnormalities (Edgin et al., 2008; Woodward, Clark, Pritchard,Anderson, & Inder, 2011). Inhibition is one of the core executive functions and has beenreported to be a particular issue in preterm children (e.g., Mulder, Pitchford, & Marlow,2011). Inhibition, which develops in the first few years of life, is critical to other executiveabilities (e.g., Anderson, 2002; Aron, Robbins, & Poldrack, 2004; Brocki & Bohlin, 2004)and consequently to social behavior (Luna & Sweeney, 2004). Children born pretermpresent lower inhibition performances compared with those of their term-born peers(Aarnoudse-Moens et al., 2012; Aarnoudse-Moens, Smidts, Oosterlaan, Duivenvoorden,& Weisglas-Kuperus, 2009; Anderson & Doyle, 2004; Baron, Kerns, Müller, Ahronovich,& Litman, 2012; Bayless & Stevenson, 2007; Böhm, Katz-Salamon, Smedler,Lagercrantz, & Forssberg, 2002). Inhibition has been assessed with many different tests,covering different processes (e.g., Aron, 2007), thus leading to disagreement regarding itsdevelopmental trends in premature populations (for a review, see Mulder et al., 2009).Although several recent neuropsychological studies appear to agree that a delay ininhibition processes seems to be caught up between 8 and 12 years old (Aarnoudse-Moens et al., 2012; Ritter, Nelle, Perrig, Steinlin, & Everts, 2013; Ritter, Perrig, Steinlin,& Everts, 2014), other studies have reported inhibition difficulties in late childhood(Mulder et al., 2011) and adulthood (Nosarti et al., 2007). Mulder et al. have also reportedthat, unlike other core executive functions such as working memory and shifting, responseinhibition difficulties in preterm children are not mediated by processing speed.Furthermore, functional magnetic resonance imaging studies with adolescents(Lawrence et al., 2009) and adults (Nosarti et al., 2006) have shown that, comparedwith healthy controls, very preterm participants demonstrate different brain activationrelated to successful response inhibition.

Response inhibition is a widely accepted inhibition process, defined as the ability toactively suppress, to interrupt, or to delay an action (Clark, 1996). The stop-signal task(Logan, 1994; Logan & Cowan, 1984) has proven to be a sensitive tool to study responseinhibition in both general and clinical populations (Nigg, 2000; Schachar et al., 2007). In

2 M. RÉVEILLON ET AL.

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this task, subjects perform a two-choice reaction task, responding differently to two typesof stimuli (go trials). On a small proportion of trials (stop trials), a stop signal appearsafter the go stimulus, requiring the subjects to inhibit their ongoing response. Because theassociation between stimuli and responses are inconsistent in this task, subjects arerequired to maintain effortful control processes in order to inhibit their responses(Verbruggen & Logan, 2008b). To the best of our knowledge, the stop signal has beenused in only two studies with preterm children. Aarnoudse-Moens et al. (2012) reported adecrease in group differences between very preterm and full-term children between 4 and12 years on the stop-signal reaction time (SSRT). Potharst et al. (2013) reported similarinhibition performances between very preterm and full-term children at age 5 years on apreschool version of this task. However, they also reported that a greater number of verypreterm children were not able to complete the task.

Inhibition has further been reported to interact with emotional and motivationalprocesses at both brain and behavior levels (Horn, Dolan, Elliott, Deakin, & Woodruff,2003; Padmala & Pessoa, 2010; Pessoa, 2008). At the brain level, the interaction betweenexecutive function and emotion is associated with more ventral and medial regions of thePFC, such as the orbitofrontal area (Zelazo, Qu, & Muller, 2005), which is stronglyconnected to limbic regions, including the amygdala (e.g., Ochsner, Bunge, Gross, &Gabrieli, 2002). The orbitofrontal region has been reported to be particularly vulnerable inpreterm children (Peterson et al., 2000, 2003). Structural studies have also shown altera-tion of the amygdala (Peterson et al., 2000) and the fusiform gyrus (Healy et al., 2013;Nosarti et al., 2008) in preterm samples, those regions being part of an emotionalprocessing brain network. At the behavioral level, several authors have used tasks thatmeasure response inhibition in which neutral stimuli were replaced with emotional stimuliand have reported that emotional context undermines response inhibition processes inadults (Hare, Tottenham, Davidson, Glover, & Casey, 2005; Schulz et al., 2007;Verbruggen & De Houwer, 2007) and in children (Tottenham, Hare, & Casey, 2011;Urben, Van Der Linden, & Barisnikov, 2012). In a more “motivational” way, other authorshave examined response inhibition in a context of frustration by using delay tasks withchildren and adolescents (Bitsakou, Psychogiou, Thompson, & Sonuga-Barke, 2009;Huijbregts, Warren, De Sonneville, & Swaab-Barneveld, 2008; Jahromi & Stifter, 2008;Prencipe et al., 2011; Solanto et al., 2001; Willoughby, Kupersmidt, Voegler-Lee, &Bryant, 2011). In these tasks, participants have to regulate their frustration in order toinhibit their ongoing response during delays (Bitsakou, Antrop, Wiersema, & Sonuga-Barke, 2006; Huijbregts et al., 2008). Delay tasks have been used particularly to study theADHD population, as these individuals are characterized by a response inhibition deficitand delay aversion or intolerance (Solanto et al., 2001; Sonuga-Barke, Taylor, Sembi, &Smith, 1992). Regarding preterm populations, studies investigating parents’ ratings ofpreterm children with the Strengths and Difficulties Questionnaire (SDQ) agree on thepresence of emotional and hyperactivity/inattention symptoms in these children (Bayless,Cate, & Stevenson, 2008; Gardner et al., 2004; Guellec et al., 2011; Hall & Wolke, 2012;Hayes & Sharif, 2009). However, very little data are available on the relation betweenresponse inhibition and emotion. Recently, one study assessed response inhibition in 24-month-old preterm children with both delay reward and Go/No-Go tasks and reportedlower global inhibition performances compared with those of their full-term peers (Voigt,Pietz, Pauen, Kliegel, & Reuner, 2012). Moreover, these authors reported that thecomposite score obtained by putting together all individual scores from the delay andGo/No-Go task explained the lower general cognitive performances of the participants.

INHIBITION DIFFICULTIES IN PRETERM CHILDREN 3

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Additionally, the severity of difficulties in preterm children seems to depend upongestational age (GA) and/or birth weight (e.g., Aarnoudse-Moens, Weisglas-Kuperus, VanGoudoever, & Oosterlaan, 2009; Burnett, Scratch, & Anderson, 2013; Gardner et al.,2004; Kerstjens et al., 2011). In their meta-analysis of outcomes in school-aged pretermchildren, Bhutta et al. reported that GA and birth weight were directly proportional tocognitive performances. However, very low birth weight can be associated either withvery low GA or with intrauterine growth restriction (IUGR)/small for gestational age(Gardner et al., 2004; Nosarti et al., 2007). IUGR, defined as small for gestational agewith abnormal umbilical artery blood flow prior to birth, has been considered as anadditional risk factor for executive function and behavioral difficulties (Geva, Eshel,Leitner, Valevski, & Harel, 2006; Guellec et al., 2011; Hall & Wolke, 2012; Morsing,Asard, Ley, Stjernqvist, & Marsal, 2011; Walker & Marlow, 2008).

In summary, preterm children seem to have response inhibition difficulties, but itremains unclear whether or not they catch up with these difficulties before adolescence.Moreover, as far as we know, despite their well-known risk for executive function andbehavioral and emotional problems, no study has yet examined response inhibition in anemotional context in school-aged preterm children. Finally, given that the dynamicintegration of both emotion regulation and executive function during development hasbeen shown to have an impact on social skills, peer relationships, and behavioral outcome(Calkins & Marcovitch, 2010), it seems of particular interest to examine relations betweenthose processes in preterm children. In this context, the present study aimed to do thefollowing:

(1) Evaluate response inhibition and how it is impacted by an emotional context inpreterm children aged 9–12 years old compared with full-term children by usingtwo versions of a stop-signal task and a delay-inducing frustration task. We hypothe-sized poorer inhibition performances in the preterm group, more particularly in anemotional context.

(2) Rate behavioral difficulties with the SDQ, recently shown to be a sensitive tool toscreen emotional disorders, ADHD, and conduct disorders in preterm children(Johnson, Hollis, Marlow, Simms, & Wolke, 2014) and then explore the relationsbetween those difficulties and response inhibition in preterm children. We expectedpoorer response inhibition to be associated with poorer emotion regulation andbehavioral difficulties.

(3) Finally, explore the impact of the degree of prematurity and IUGR on the significantlylower scores obtained by preterm children to see if their difficulties could beexplained by more specific perinatal risk factors.

METHODS

Participants

The group of preterm children (< 35 weeks GA) was part of a longitudinal cohort andthe children were recruited through the Division of Child Development and Growth at theUniversity Hospitals of Geneva and Lausanne. Between October 2011 and February 2013,all children from this cohort currently aged between 9 and 12 years and free of severedisabilities (cerebral palsy, blindness, hearing loss) were selected to participate. Of the 71

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families contacted, 12 declined assessment. One child was excluded because of nonverbalintelligence below the fifth percentile for his age. Fifty-eight children (27 girls and 31 boys)born preterm, with GA < 35 weeks, were included in the present study. Chronological ageof preterm children ranged between 8.82 and 11.81 years (M = 10.14, SD = 0.84). Allchildren were educated in mainstream schools. Eighteen children had been diagnosed withIUGR, which is defined as small for gestational age (i.e., birth weight below the 10thpercentile for GA and gender) and the presence of placental insufficiency defined asresistance to arterial umbilical blood flow at higher than the 95th percentile (Sonessonet al., 1993). Preterm group characteristics are reported in Table 1.

The control group was composed of 61 healthy children born full term (> 37weeks GA) recruited through local primary schools. The control group matched thepreterm group such that the two groups did not differ at assessment on chronologicalage (M = 10.42, SD = 0.89; range: 8.99–12.29), t(117) = 1.778, p = .087, d = .33, andgender distribution (30 girls and 31 boys), χ2(1) = 0.082, p = .774. The socioeconomicstatus (SES) was lower in the preterm group (M = 6.14, SD = 2.28) than in the controlgroup (M = 4.75, SD = 2.20), t(117) = −3.371, p = .001, d = ‒.63. The family’s SESwas calculated by using the index of Largo et al. (1989) computed on two 6-pointscales based on parental occupation and maternal education (1 = high education and/orliberal activity and 6 = no training and/or a position of employee). Scores from bothscales were added and ranged from 2 to 12. In order to assess nonverbal reasoningabilities, all participants performed the Coloured Progressive Matrices test (Raven,Court, & Raven, 1998). This task was performed to ensure that preterm and controlchildren did not differ on basic nonverbal intelligence. All participants included in thestudy had a percentile score that corresponded to their age and was above the fifthpercentile. Finally, there was no difference on the raw score between the preterm andthe control children, t(117) = 0.993, p = .323, d = .18.

Table 1 Preterm Population Characteristics.

Mean (± SD), range or number (percentage)

Preterm children (n = 58)

Neonatal characteristicsGestational age, weeks 28.89 (± 3.29), 23–35Gestational age < 28 weeks 36 (62%)Birth weight, g 1125.96 (± 434.78), 520–2170Birth weight < 1,000 g 23 (40%)Intrauterine growth restriction (IUGR) 18 (32%)Intraventricular hemorrhage Grades I and II 4 (0.7%)Intraventricular hemorrhage Grades III and IV 1 (0.2%)Periventricular leukomalacia (PLV) 0 (0%)Bronchopulmonary dysplasia 16 (28%)Asphyxia 2 (0.3%)General cognitive abilities at 5 yearsK-ABCMental Processing Composite score 97.36 (± 12.43), 72–133

Note. IUGR, birth weight below the 10th percentile for gestational age and gender and the presence ofplacental insufficiency defined as a resistance to arterial umbilical blood flow higher than the 95th percentile(Sonesson et al., 1993). The diffuse PVL diagnostic was based on magnetic resonance imaging. K-ABC =Kaufman Assessment Battery for Children (Kaufman & Kaufman, 1993).

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Procedure and Materials

All tasks were administered in a quiet room by a trained psychologist and regularbreaks were offered. Tasks were built and run with E-Prime software version 1.2(Psychology Software Tools) and were administered in a counterbalanced order acrossparticipants. Each task was preceded with practice trials, and participants were instructedto respond as quickly and as accurately as possible. This study was approved by themedical ethical review boards of the University Hospitals of Geneva and Lausanne andthe ethics committee of the Faculty of Psychology (University of Geneva). Writteninformed consent was obtained from parents. Participants gave their oral consent to takepart in the study and were free to withdraw from the procedure at any time.

The Speed Processing Color Test (Miller & Vernon, 1997) was used to verify thatthe expected differences between groups in the following tasks could not be attributed todifferences in speed of information processing (Mulder et al., 2011). The participant hadto indicate whether two shapes appearing in the center of the screen were the same coloror different colors. This task used four colors (red, green, blue, and yellow) and twoshapes (triangle and circle) and was 24 trials long. Median reaction times were computedand all reaction times (RTs) below 200 ms were considered anticipatory and were nottaken into consideration.

The stop-signal task (Logan, 1994; Logan & Cowan, 1984) was chosen to assessinhibition of a prepotent response. On the basis of a previous study (Urben et al., 2012),two versions of the stop signal were used, one with neutral stimuli (letters) and one withemotional stimuli (faces). The structure, timing parameters, and number of “go” and“stop” trials were the same in both versions.

The stop-signal task with neutral stimuli was a choice reaction task in whichparticipants had to discriminate between two stimuli (letters “X” and “O”—go stimuli)by pressing two response keys (buttons “c” and “m,” marked with different signs). Eachtrial began with a fixation cross during a random time comprising between 500 and1,000 ms, followed by the presentation of the stimulus, which ended with the participant’sresponse or after 1,500 ms. Participants were presented with six blocks of 48 trials, ofwhich 12 (25%) had a stop signal. The stop signal consisted of a red square appearingaround the letters after a delay, which was continuously adjusted according to the successof inhibiting the preceding stop trials, as suggested by Logan (1994). The stop-signaldelay was initially fixed at 250 ms and increased by 50 ms if the participant succeeded ininhibiting his or her response to the last stop trial, or decreased by 50 ms if the participantfailed to inhibit his or her response, in order to have a mean success rate for the stop trialsof about 50%. This adjustment allows a good estimation of the stop signal reaction time(SSRT; Band, Van Der Molen, & Logan, 2003). For go trials (execution of the response),the mean percentage of correct responses (Accuracy go) and the median go reaction time(MRT) for correct responses were computed. For each participant, anticipatory RT (below200 ms) and all RTs above 2.5 standard deviations from the original mean RT wereexcluded. For stop trials (inhibition process), the mean percentage of inhibited trials(Accuracy stop) and the SSRT were computed. On the basis of the horse-race model(see Logan, 1994), the SSRTwas calculated by rank-ordering RT distributions for go trialsin order to find the RT (centile) corresponding to the percentage of failed responseinhibition. The mean stop-signal delay was then subtracted from this centile RT.

The stop-signal task with emotional stimuli was constructed in the same way as thestop-signal task with neutral stimuli. However, the stimuli of this emotional version of the

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task consisted of happy and fearful facial expressions from 12 individuals (six females andsix males) selected from the Macbrain Face Stimulus Set available at www.macbrain.org.Those two facial expressions have been described as more readily discriminated than sadand angry expressions (Tottenham et al., 2011). Participants had to decide whether theface appearing on the screen was presenting a happy or a fearful expression by pressingone of two response keys (again, buttons “c” and “m,” marked with different signs). Thevariables computed were the same as for the stop-signal task with neutral stimuli. Inaddition, each variable was computed separately for happy and fearful facial expressions.

The Delay Frustration Task (DeFT; Bitsakou et al., 2006) comprised 55 very simplemath additions displayed on a computer screen, each math question presenting fourresponse choices. Participants were asked to select the correct answer by pressing oneof the four response keys (buttons “s,” “f,” “h,” and “k,” marked “1,” “2,” “3,” and “4”).On most trials, the next question was presented 1,000 ms after the participant’s responsewas recorded (no postresponse delay). However, on the 16 remaining trials, access to thenext trial was delayed either by 20 s (eight trials, postdelay condition) or by 3 to 10 s(eight distractor trials). There were no delay trials for the 10 first trials; the postresponsedelay trials were randomized across the 45 last trials. The participants were instructed thatthe computer had shown signs of malfunctioning but that they should not worry, becausetheir responses were going to be recorded anyway. This task was designed to create delay-related frustration, so that delay-aversive participants would avoid this situation bypressing response buttons to move on to the next question. Thus, refraining from pressingbuttons is indicative of inhibitory control (Huijbregts et al., 2008). For the eight 20-seconddelay periods, the mean number of presses per second (MN), the mean duration of pressesper second (MD), and their product (mean total duration; MTD) were recorded. The firstresponse in each delay (the response to the arithmetic question) was not taken intoaccount, as it is not a reaction to delay aversion.

The Strengths and Difficulties Questionnaire (SDQ; Goodman, 1997, 2001) is abehavioral screening questionnaire for children aged 4 to 16 years. The confirmed Frenchversion of the SDQ (d’Acremont & Van Der Linden, 2008) was used in the present study.This short questionnaire includes 25 items grouped on five dimensions. Four dimensionsassess problematic behaviors: (a) conduct problems (antisocial, aggressive, and opposi-tional behavior); (b) hyperactivity/inattention (impulsive behavior); (c) peer problems(poor relationships with others); and (d) emotional symptoms (anxiety and sadness).The four dimensions are summed to obtain an overall score. The fifth dimension evaluatesprosocial behavior (empathy and kindness). Responses are given on a 3-point scale: 0 (nottrue), 1 (somewhat true), and 2 (certainly true). Parents’ ratings were obtained for allparticipants, except for 2 children whose parents did not complete the questionnaire.Three subscales were of special interest for the present study: conduct problems, hyper-activity/inattention, and emotional symptoms.

Analyses

All data were analyzed by using SPSS Version 19. Between-group differences inspeed of processing were tested with independent sample t-tests. The scores on the stop-signal tasks (except for MRT and SSRT in both versions), the DeFT, and the SDQ werenot normally distributed. These scores were thus transformed into rank-ordered scores.Except for correlation analyses, all analyses were run on raw scores for the normallydistributed data and on the ranked dependent variables for the not normally distributed

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data (Conover & Iman, 1982). Because the control group had significantly higher SEScompared with the preterm group, all analyses of covariance (ANCOVAs) tested groupdifferences, controlling for SES. First, ANCOVAs were performed on each main scorefrom the stop-signal tasks (separated for happy and fearful faces for the emotionalversion), from the DeFT, and from the SDQ. Second, for scores related to the stop-signaltasks, two repeated-measures ANCOVAs were conducted in order to investigate the globaleffect of group, the influence of the type of material on performances, and their possibleinteraction, with one ANCOVA exploring the influence of the type of task (neutral vs.emotional) and the other testing the influence of the type of emotion (happy vs. fearful).For statistical comparisons, p-values of less than .05 were considered significant andp-values of less than .10 as marginally significant. Then, in order to explore the linksbetween scores showing a deficit in preterm children, we used Spearman correlations.Finally, since the prevalence of preterm children’s difficulties has been shown to increasewith decreasing GA and the presence of IUGR, univariate linear regression analyses wereconducted to assess which of these two variables predicted the scores of preterm children.We chose GA over birth weight, as birth weight can be associated either with low GA orwith higher GA and prenatal growth restriction (Gardner et al., 2004). Each score forwhich we obtained group differences in ANCOVAs was entered as the dependent vari-able, and GA and IUGR were entered simultaneously as independent variables, with thestatistical threshold set at .05.

RESULTS

Regarding cognitive evaluation, the 119 participants completed all tasks. The onlymissing data (1 participant from the control group) was in the stop-signal task withemotional stimuli and was due to a technical problem. Concerning the questionnaire,the parents of 2 participants from the control group did not complete it. The preterm(M = 518.79, SD = 70.51) and control (M = 526.29, SD = 67.18) groups did not differ inmedian speed of information processing, t(117) = 0.594, p = .554, d = .11, as assessedwith the Speed Processing Color Test.

Group Comparisons

Results and descriptive statistics concerning univariate ANCOVAs controlling forSES are reported in Table 2. On the neutral version of the stop-signal task, pretermchildren were significantly less accurate than controls regarding go trials and marginallyless accurate regarding stop trials. No significant group differences were found on MRTand SSRT. On the emotional version of the task, preterm children had significantly fasterMRT than did controls for both happy and fearful faces and were less accurate regardingstop trials in fearful conditions only. The two groups did not differ on accuracy for gotrials and SSRT. Preterm children performed significantly less well than controls regardingall measures of the DeFT. Group differences were also found on the total difficulties scorefrom the SDQ. More specifically, preterm children were screened as having higherconduct problems, higher hyperactivity/inattention, and marginally higher peer problems.The scores of the two groups did not differ on the emotional symptoms and prosocialbehavior scales. All of these results persisted after taking chronological age, gender, andnonverbal intelligence (raw scores from the Coloured Progressive Matrices) into accountas additional cofactors.

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le2AllScoresof

Control

andPreterm

Children.

meanscores

ANCOVAs

Effectsize

Preterm

F-value

p-value

Cohen’sd

Stop-signal

neutral

(13.1)

.2(13.6)

(10.7)

fearful

(15.0)

(10.0)

MRTneutral

845.8(186.2)

793.1(197.3)

(180.6)

934.1(169.7)

fearful

1041.7

(166.3)

966.7(170.1)

ACCstop

neutral

.3(9.3)

fearful

SSRTneutral

197.4(107.4)

213.6(118.6)

4.7(133.8)

309.4(132.9)

fearful

329.7(154.5)

338.5(142.6)

Frustration

(0.39)

(0.40)

80.23(119

104.74

62.14(150.41)

75.71(116

Strengthsan

dDifficultiesQuestion

Overallstress

(4.70)

11.14(6.79)

problems

(1.55)

(2.37)

Emotionalsymptom

(1.83)

(2.57)

Hyperactiv

ity/in

attention

(2.11)

(2.82)

Peerproblems

(1.28)

(1.54)

Prosocial

behavior

(1.36)

(1.67)

Notes.ANCOVAs=un

ivariate

analyses

ofcovariance

controlling

forsocioeconomic

status;df

=degreesof

freedo

m;Md=meandifference

betweencontrols

andpreterms;

=meannu

mberof

respon

sespersecond;MD

=meandu

respon

sespersecond;MTD

×MD;ACCgo

=meansuccessrate

for“go”

trials;MRT=median

reactio

efor“go”

trials;ACCstop

=meansuccessrate

for“stop”

trials;SSRT=stop-signalreactio

e.a Statisticscalculated

onrank-ordered

scores.bStatisticscalculated

onrawscores

asnorm

distributed.

p-Valuesof

.05arein

boldface;p

-valuesof

.10arein

boldface

anditalic.

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We performed follow-up 2 (Task Type: neutral vs. emotional) × 2 (Group: pretermsvs. controls) ANCOVAs on measures of the stop-signal tasks, while controlling for SES.Regarding the accuracy for go trials, there was no main effect of Group, F(1, 115) = 1.48,p = .227, η2 = .013. Results showed a main effect of Task Type, F(1, 115) = 8.76, p = .004,η2 = .071, but no interaction, F(1, 115) = 1.26, p = .265, η2 = .011. The percentage ofcorrect responses was lower in the emotional task compared with the neutral one. RegardingMRT, results showed a marginal effect of Group, F(1, 115) = 3.58, p = .061, η2 = .030, anda main effect of Task Type, F(1, 115) = 17, p < .001, η2 = .129, but no interaction, F(1,115) = 1.38, p = .243, η2 = .012. Preterm children were faster than controls and MRT washigher in the emotional task. Regarding the accuracy for stop trials, results showed a maineffect of Group, F(1, 115) = 4.71, p = .032, η2 = .039, and a marginal effect of Task Type,F(1, 115) = 3.70, p = .057, η2 = .031, but no interaction, F(1, 115) = 0.27, p = .605,η2 = .002. Preterm children were less accurate than controls, and the percentage of correctlyinhibited trials was higher in the emotional task. Finally, for SSRT, there was no main effectof Group, F(1, 115) = 0.00, p = .985, η2 = .000. Results showed a main effect of Task Type,F(1, 115) = 10.44, p = .002, η2 = .083, SSRT being higher in the emotional task but nointeraction, F(1, 115) = 0.57, p = .452, η2 = .005.

In order to investigate the effect of emotional valence, we conducted 2 (Emotion Type:happy vs. fearful) × 2 (Group: preterm vs. control) ANCOVAs on measures of the stop-signaltask with emotional stimuli, still adjusting for the SES. The analyses related to the accuracyfor go trials revealed no significant results. Results regarding MRT showed a main effect ofGroup, F(1, 115) = 6.05, p = .015, η2 = .050, a main effect of Emotion Type, F(1, 115) = 8.64,p = .004, η2 = .070, and a marginally significant interaction, F(1, 115) = 2.82, p = .096,η2 = .024. Preterm children were faster than controls, and all participants were faster in thehappy compared with the fearful condition. TheMRT difference between both conditions wasmore important in the preterm group. The analyses related to the accuracy for stop trialsshowed a marginally significant effect of Group, F(1, 115) = 3.52, p = .063, η2 = .030,no effect of Emotion Type, F(1, 115) = 0.24, p = .624, η2 = .002, and no interaction,F(1, 115) = 1.08, p = .301, η2 = .009. Preterm children were less accurate than controls.Finally, results showed a higher SSRT in the fearful condition, with a main effect of EmotionType, F(1, 115) = 8.80, p = .004, η2 = .071, no effect of Group, F(1, 115) = 0.11, p = .746,η2 = .001, and no interaction, F(1, 115) = 2.24, p = .138, η2 = .019.

Despite the fact that the stop-signal tasks had been built in order to have a meansuccess rate of about 50% (see “Methods” section), group differences in the percentage ofcorrectly inhibited trials were found, along with group differences in MRT. Therefore,extra analyses of variance were performed on the centile RT and the mean stop-signaldelay from the two tasks taken together. Compared with controls, preterm childrenshowed a lower centile RT, F(1, 117) = 4.287, p = .041, and a marginally lower delay,F(1, 117) = 3.404, p = .068.

Given that preterm children were faster than controls, we recalculated groupcomparisons regarding MRT and SSRT from both stop-signal tasks, including all reactiontimes less than 200 ms (anticipatory responses). All results presented above were main-tained and therefore only those results are presented.

Relations between Scores in Preterm Children

Spearman correlations conducted within the preterm group between the scores thatdiffered from the control group are presented in Table 3. All measures within each task

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le3Spearman

Correlatio

nsbetweenTasksandQuestionnaire

Scoresin

Preterm

Children.

Stop-signal

frustrationtask

Strengths

andDifficulties

Questionnaire

1ACCstop

neutral

.90***

.49***

.60***

−.10

−.08

−.10

−.29*

−.20

−.26

*c−.18

2ACCstop

−.05

−.04

−.11

−.16

−.03

−.30

ACCstop

fearful

..34**

**−.04

−.01

−.30*

−.20

−.45

−.17

4MRTneutral

..53***

.63***

−.07

−.05

−.06

−.34**

−.33

*−.22

−.23

5MRThapp

**−.07

−.02

−.05

−.24a

−.25

b−.18

−.27

MRTfearful

.−.04

−.03

−.04

−.21

a−.27

*−.16

−.27

..89***

.97***

..97***

−.06

−.01

−.04

10Overallstress

**.80*

**.60*

ctprob

**.29*

12Hyperactiv

ity/in

attention

13Peerprob

Notes.n=58

=meannu

mberof

respon

sespersecond

=meandu

respon

sespersecond

×MD;MRT=medianreactio

efor“go”

trials;

ACCstop

=meansuccessrate

for“stop”

trials.

a r=‒.30

afterpartialcorrelation,

controlling

forchronologicalage,

gender,andnonverbalintelligence.

br=‒.32

afterpartialcorrelation,

controlling

c r=‒.21

afterpartialcorrelationcontrolling

*p<.05.**

p<.01.**

*p<.001.

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correlated positively with each other, except inhibition accuracy in happy conditions,which did not correlate with inhibition accuracy in neutral and fearful conditions. In thestop-signal tasks, lower MRTs were associated with better inhibition accuracy. The scoresfrom the DeFT did not correlate with any score from the stop-signal tasks or the SDQ.Regarding the SDQ, higher conduct problems were associated with faster MRT in the stopsignal, while higher hyperactivity/inattention was related to lower inhibition accuracy inthe stop signal, except for happy conditions. Higher peer problems correlated with lowerinhibition accuracy in happy conditions and faster MRT in happy and fearful conditionsfrom the stop signal. Correlation analyses were then run a second time, partialing for theeffect of chronological age, gender, and nonverbal intelligence. The results did notchange, except that conduct problems correlated more strongly with MRT in happyconditions and hyperactivity/inattention did not correlate with inhibition accuracy in theneutral version of the task.

Degree of Prematurity and Intrauterine Growth Restriction as Risk

Factors

Regression analyses conducted within the preterm group for each score where groupdifferences were found are reported in Table 4. Concerning the stop-signal variables,lower GA was associated with lower MRT in the emotional task only, independent of thetype of emotion. IUGR did not predict any MRT score. Both IUGR and lower GA wererelated to poorer inhibition accuracy in the emotional version of the task, specifically inthe fearful condition. Results further showed that the two factors, GA and IUGR, did notpredict the scores on the DeFT. Regarding the SDQ scales, only IUGR was associatedwith a higher hyperactivity/inattention score, but neither of the two variables predictedtotal difficulties, conduct problems, or peer problems.

DISCUSSION

In the current study, we examined response inhibition in a population of childrenborn preterm compared with their full-term peers and explored the relations with emotionand behavior. We also investigated the impact of GA and IUGR as specific risk factors forpreterm children’s performances.

Response Inhibition

First, consistent with our hypotheses, results showed that preterm children hadlower inhibition accuracy (probability of inhibition) in the stop signal. However, thetwo groups did not differ regarding the stop-signal reaction time (SSRT), which was thevariable of interest, as it measures effortful control processes involved in stopping theresponse (Verbruggen & Logan, 2008a, 2008b). These results are in agreement with thoseof Aarnoudse-Moens et al. (2012), who reported that 4- to 12-year-old very pretermchildren had lower inhibition accuracy in the stop-signal task compared with controls, butthat group differences regarding the SSRT disappeared at middle-school age. Along withlower inhibition accuracy, our results revealed that preterm children tended to be fasterthan controls in responding to go stimuli (median reaction time; MRT) and that this groupdifference was mostly driven by the emotional condition. Given that faster responses werecorrelated with lower inhibition accuracy in preterm children in each type of stimuli

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Predictorsof

theScoresin

Preterm

Children.

Stop-signal

Predictor

variab

MRTneutral

otional

ACCstop

neutral

ACCstop

emotional

(−10.42to

23.53)

(1.83to

28.84)

(−0.30

to0.64)

(0.14to

−18.14

(−138.80

to102.51)

−0.04

−68.84

(−164.83

to27.15)

−0.20

−0.41

(−3.72

to2.91)

−0.04

−4.35

(−6.83

to−1.88)

−0.45

Stop-signal

withem

otional

Predictor

variab

MRThappy

MRTfearful

ACCstop

fearful

(2.01to

29.92)

*14.74

(0.61to

28.87)

(−0.07

to0.29)

(0.02to

−73.91

(−173.09

to25.27)

−0.20

−60.16

(−160.60

to40.28)

−0.17

−0.76

(−2.02

to0.50)

−.17

−2.08

(−3.38

to−0.79)

−0.42

Frustration

Predictor

variab

−1.13

(−3.01

to0.74)

−0.17

−1.71

(−4.37

to0.96)

−0.18

−1.83

(−4.50

to0.84)

−0.19

−3.95

(−17.30to

−0.08

−8.59

(−27.52to

10.34)

−0.13

−6.84

(−25.80to

12.11)

−0.10

Strengthsan

dDifficultiesQuestion

Predictor

variab

Overallstress

Conduct

problems

Hyperactiv

ity/in

attention

Peerproblems

−0.03

(−0.59

to0.52)

−0.02

−0.04

(−0.24

to0.17)

−0.05

−0.19

(−0.41

to0.04)

−0.22

−0.09

(−0.22

to0.04)

−0.19

(−0.26

to7.62)

(−0.56

to2.31)

(0.71to

**0.19

(−0.74

to1.12)

Notes.B

=unstandardized

ate;CI=confidence

interval;β=standardized

ates;GA

=gestationalage;IU

GR=intrauterine

threstriction;

MN=meannumberof

respon

sespersecond;MD

=meandu

respon

sespersecond;MTD

×MD;MRT=medianreactio

efor“go”

trials;ACCstop

=meansuccessrate

for“stop”

trials.

*p<.05.**

p<.01.**

*p<.001.

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(letters, happy and fearful faces), we suggest that they responded in an impulsive way.Consistent with our findings, a positive correlation between go RT and the probability ofinhibition in a stop-signal task has been found in children with ADHD (Solanto et al.,2001). In addition to these results, the complementary group differences concerning thecentile RT and the stop-signal delay suggested that the lack of group differences regardingthe SSRT could be attributable to the group differences in MRT. However, caution isneeded regarding this interpretation, as the few studies that have used a stop-signal taskwith preterm children have not reported MRT data (Aarnoudse-Moens et al., 2012;Potharst et al., 2013).

Impact of an Emotional Context on Response Inhibition

In agreement with recent literature (Tottenham et al., 2011; Urben et al., 2012;Verbruggen & De Houwer, 2007), the emotional context displayed a negative impact oneffortful response inhibition performances (SSRT) and MRT in all children. Consistentwith the idea that faces expressing negative emotions capture attention (e.g., Fenske &Eastwood, 2003), the negative impact was higher for fearful faces compared with happyfaces, and this was marginally more pronounced in preterm children. In addition, longergo RTs for negative emotions compared with positive emotions have been similarly foundin previous studies with adults (Hare et al., 2005; Schulz et al., 2007) and children (Lewis,Todd, & Honsberger, 2007; Urben et al., 2012). These results could be explained in lightof the “dual competition” model (Pessoa, 2009), which suggests that emotional informa-tion is processed first, as it automatically captures the attention, taking away part of theavailable resources to process the task. Thus, task-irrelevant emotional informationimpairs performance on the main task. Furthermore, the impact on performances dependson the level of threat of the emotional information, with higher threat informationrecruiting more effortful control. However, in the context of our study, emotional stimuli,specifically fearful faces, improved inhibition accuracy, suggesting that taking more timeto respond to go stimuli increases the chances of inhibiting the response. This supports ourprevious proposition that preterm children’s faster, or more impulsive, way of respondingcould explain their greater difficulty in inhibiting the response. Therefore, from the resultsconcerning both tasks, we can suggest that the differences between preterm and controlchildren could underlie a difference in the strategy used to perform the task. In the stopsignal, go and stop processes are competitive, and participants have to adjust betweenspeeds of reaction and caution (Logan & Cowan, 1984). As the slower MRT of controlchildren could be interpreted as much caution or a proactive strategy to increase thechances of inhibiting the response (Verbruggen & Logan, 2009), preterm children’s fasterMRT suggests impulsivity or lack of caution. Finally, emotional information had animpact on response inhibition performances, but the lack of interaction suggests thatthis impact was not different for preterm and control children.

Regarding the Delay Frustration Task (DeFT), during the delays, preterm childrenpressed the response buttons more times and for longer durations compared with controls,which reflects difficulties in inhibiting a response in a context of frustration. Following thetheory of Bitsakou et al. (2009), this implies that preterm children are more delayintolerant. According to these authors, delay-intolerant participants are particularly fru-strated by this type of imposed delay, as it represents an obstacle to the completion of thetask (i.e., mathematical question). Consequently, they keep pressing the response button inan attempt to reduce the perceived length of time in order to avoid this delay situation

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(Sonuga-Barke, Houlberg, & Hall, 1994). In agreement with previous studies withchildren of mothers who smoked during pregnancy (Huijbregts et al., 2008) and withchildren with ADHD (Solanto et al., 2001), preterm children’s performances on the DeFTdid not correlate with any measure of the stop signal, even in its emotional version. Thiscould be explained by the fact that the DeFT and the emotional version of the stop-signaltask imply different kinds of emotions. In contrast with those from the DeFT, emotionalstimuli from the stop signal are not seen as obstacles, as they do not get in the way of therealization of the task, and therefore do not involve the motivational aspect of escapingfrustration. Nevertheless, our results from the stop-signal tasks showed that pretermchildren did not behave in a different way from control children when emotional stimulireplaced neutral stimuli (i.e., lack of significant interaction). Therefore, our results seem toconvey a general difficulty in inhibiting a response displayed in both neutral and emo-tional contexts, rather than a specific impact of an emotional context on response inhibi-tion in preterm children. At a neuronal level, these findings favor a general vulnerabilityof the prefrontal cortex, including both dorsolateral and ventromedial regions, rather thana specific vulnerability of the orbitofrontal region in preterm children (Peterson et al.,2000). It has been established that the frontal lobe, particularly the PFC, is related tohigher cognitive skills such as executive function and thus has a prolonged maturationalcourse, which makes it more sensitive to developmental perturbations (Taylor et al., 2012)such as preterm birth. Finally, this general difficulty in inhibiting a response could beassociated with impulsivity, given that failure of response inhibition, rapid processing ofinformation, and inability to delay gratification have all been listed as components ofimpulsivity (Horn et al., 2003).

Behavioral Difficulties and Relations to Response Inhibition

Parent ratings on the SDQ revealed a higher global difficulties score for pretermchildren. Specifically, in agreement with our hypotheses, they had higher scores thancontrols on hyperactivity/inattention, conduct, and peer relationship problems (this lastscore being only marginally significant). Similar findings have been reported in a previousstudy with very low birth weight adolescents (Indredavik, Vik, Heyerdahl, Kulseng, &Brubakk, 2005). Higher hyperactivity and peer relationship difficulties have also beenreported by parents of teenagers with extremely low gestational age in a study byGardner et al. (2004). In addition, our correlation results indicated that preterm childrenwith faster MRT and lower inhibition accuracy in the stop signal with neutral and fearfulstimuli had higher conduct problems and hyperactivity/inattention symptoms, respectively.This could suggest that these behavioral difficulties hindered response inhibition in pretermchildren, with conduct problems being associated with their impulsive way of responding.In accordance with previous studies (e.g., Aarnoudse-Moens, Weisglas-Kuperus, et al.,2009), this could also inversely imply that difficulties associated with response inhibitionunderlie behavioral difficulties. However, no correlations were found between scores on theSDQ and measures on the DeFT. Regarding the hyperactivity/inattention score, this wasunexpected, given that the DeFT was built to test ADHD populations and that Sonuga-Barke et al. (1994) proposed considering inattention/overactivity and impulsivity as func-tional expressions of delay aversion (Solanto et al., 2001). However, in a study by Solantoet al, the inability or reluctance to delay a response in children with ADHD correlated withtheir teacher’s ratings of impulsivity, hyperactivity, and conduct problems but not with theirparent’s ratings. Therefore, teachers’ ratings could have been used as complementary ratings

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in the present study in order to stress a more complete profile of preterm children’sdifficulties, which would also be of clinical interest (Johnson et al., 2014).

Unlike the results of previous studies using the SDQ and contrary to our hypotheses(Gardner et al., 2004; Horn et al., 2003; Johnson et al., 2010), our preterm children werenot rated as having more emotional problems compared with controls. This inconsistencycould be attributed to population characteristics, such as different parental backgrounds,but also to perinatal factors. Although previous studies have examined very or extremelypreterm and/or very or extremely low birth weight children, our preterm group had a largegestational age (GA) range (23–35 weeks). Our regression analyses showed that intrau-terine growth restriction (IUGR) and lower GA were both related to lower inhibitionaccuracy in the emotional version of the stop-signal task only, specifically in fearfulconditions. Perinatal factors might therefore also explain our lack of correlation betweeninhibition accuracy in happy and fearful conditions, suggesting that preterm children withbetter inhibition performances in one emotional condition do not have better inhibitionperformances in the other emotional condition. This could also be the reason that norelation between performances in the stop signal and behavioral difficulties was observedin the happy conditions. Furthermore, in agreement with Guellec et al. (2011), ourregression analyses showed that IUGR was associated with more hyperactivity/inattentionsymptoms in the SDQ. Considering that IUGR predicted lower inhibition accuracy, butneither faster MRT in the stop signal, nor inhibition difficulties associated with delayintolerance, we suggest that IUGR is more related to inattention difficulties than toimpulsivity. Potharst et al. (2013) have shown that being born very small for gestationalage was associated with marked attention difficulties, a finding that is consistent withours. Moreover, a recent study has also shown that brain regions such as the parietallobules, precuneus, and medial frontal cortex, recruited by 6-year-old children bornpreterm with IUGR to perform a Go/No-Go task, suggest inefficient attentional control(Réveillon et al., 2013).

Limitations and Conclusions

Given the nature of the present study in putting these different concepts into relationin a preterm population, these results could be considered as exploratory. In fact, theinterpretation of our results from the stop-signal tasks and the DeFT is limited because ofthe lack of use of these tasks in preterm populations. Regarding the stop signal, wesuggest that the lack of group differences regarding the SSRT could mostly be attributableto the group differences in the MRT. However, we are limited in interpreting thosefindings given that the only studies that have used a stop-signal task with preterm childrenhave not reported MRT data (Aarnoudse-Moens et al., 2012; Potharst et al., 2013).Moreover, previous studies with healthy children of about the same age have reportedlower MRT compared with that of our control group (Solanto et al., 2001; Urben et al.,2012; Van Den Wildenberg & Van Der Molen, 2004; Williams, Ponesse, Schachar, Logan,& Tannock, 1999). Given that the stop-signal task has been described as a very good andwidely used tool to study response inhibition, validation and normative data would behelpful. Regarding the DeFT, preterm children have been reported to have more mathe-matical difficulties (for a review, see Aarnoudse-Moens, Weisglas-Kuperus, et al., 2009).Therefore, even if the math questions were simple and all children were capable of givinga correct response, it could have raised their anxiety level and amplified their delayintolerance. It would be interesting if further studies were to consider using a similar

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task but to perhaps propose different types of questions. The results of the present studytherefore need to be replicated in further research with a preterm population. An additionallimitation is the choice of the stop-signal tasks (one with letters and the second withemotional faces) and the interpretation of the impact of emotion. This choice was based onresults from a previous study that assessed 6- to 13-year-old children with three versionsof the stop-signal tasks (neutral material, neutral faces, and emotional faces) and did notfind differences between the two neutral versions, both of which differed from theemotional version (Urben et al., 2012). However, without a control version with neutralfaces, we cannot confirm that our results are generated by differences in emotion (emo-tional vs. neutral) rather than by stimulus type (faces vs. letters), as demonstrated in thestudy by Urben and colleagues. Further research with preterm children should use neutralfaces to confirm the present findings. Finally, considering the higher prevalence ofhyperactivity/inattention in preterm adolescents compared with their term-born peers(Arpino et al., 2010; Bhutta et al., 2002; Johnson & Wolke, 2013), a deeper examinationof the links between response inhibition and delay intolerance as impulsive responsesshould be examined in further studies. Questionnaires that dissociate measures of impul-sivity and hyperactivity, such as the Conner’s Questionnaire, would be of great interest.

In conclusion, the present study favors difficulties in inhibiting a response displayedin both neutral and emotional contexts, rather than a specific impact of an emotionalcontext on response inhibition in preterm children. More particularly, these difficultiesseem to reflect impulsivity rather than effortful cognitive control processes in 9- to 12-year-old preterm children, as expressed by more and longer button presses in an unpre-dictable imposed delay situation and faster go reaction times in the stop-signal tasksassociated with lower probability of inhibition but no difference in SSRT. The poorerperformances of preterm children on the stop signal were additionally related to theirhigher conduct and hyperactivity/inattention problems. Therefore, we propose that atpreadolescence, the remaining inhibition difficulties observed in preterm children couldbe associated with more automatic, attentional, or motivational processes and could reflectdeveloping behavioral problems.

Original manuscript received March 20, 2014Revised manuscript accepted November 29, 2014

First published online January 12, 2015

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Response inhibition difficulties in preterm children aged 9–12 years: Relations with emotion and...

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