Emotion, attention, and effortful control in 24-month-old very preterm and full-term children

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Emotion, attention, and effortful control in 24-month-old very preterm and full-term children

Fleur Lejeune, Cristina Borradori Tolsa, Myriam Bickle Graz, Petra S Hüppi et KoviljkaBarisnikov

L’Année psychologique / FirstView Article / February 2015, pp 1 - 24DOI: 10.4074/S0003503314000116, Published online: 18 February 2015

Link to this article: http://www.necplus.eu/abstract_S0003503314000116

How to cite this article:Fleur Lejeune, Cristina Borradori Tolsa, Myriam Bickle Graz, Petra S Hüppi et KoviljkaBarisnikov Emotion, attention, and effortful control in 24-month-old very preterm and full-term children. L’Année psychologique, Available on CJO 2015 doi:10.4074/S0003503314000116

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Emotion, attention, and effortful controlin 24-month-old very preterm

and full-term children

Fleur Lejeune1∗, Cristina Borradori Tolsa

2, Myriam Bickle Graz

3,

Petra S Hüppi2

and Koviljka Barisnikov1

1Child Clinical Neuropsychology Unit, Geneva, Switzerland2Division of Development and Growth, Department of Child and Adolescent, University

Hospital, Geneva, Switzerland3Follow-up Unit, Division of Neonatology, Department of Pediatrics, University Hospital,

Lausanne, Switzerland

ABSTRACTThe literature reports behavioral and socio-emotional problems in childrenborn preterm that persist throughout adolescence and early adulthood.However, no study has simultaneously investigated emotion, attention,and effortful control. In the present study, we compared these abilitiesbetween children born very preterm (<29 weeks of gestation) and full-termchildren at 24 months of age by parental questionnaire and experimentaldesign. Results on the questionnaire showed that very preterm childrenwere rated by parents as having a higher level of negative affect and lowersustained attention than full-term children. Results on the experimentaltasks revealed a distinct attention pattern between the two groups: Thefull-term children showed a peak of attention in the second trial whilepreterm children exhibited an unchanged level of attention throughout thetask. The preterm children also exhibited greater difficulties in maintaininginhibitory control compared with full-term children. Taken together, theresults observed in very preterm children clearly showed difficulties in keyabilities which allow a voluntary self-regulation behavior and consequently,they should be considered to improve early intervention strategies.

∗Corresponding author: Fleur Lejeune, Unité de psychologie clinique et neuropsychologie de l’enfant, Faculté dePsychologie et de Sciences de l’Éducation, Université de Genève - Bd du pont d’Arve, 40 - 1211 Genève – Suisse.E-mail: [email protected]. This research was supported by Leenaards Foundation Grant N◦ 2667 and Swiss NationalScience Foundation SNF 32-102127; 32-113632 (PSH). We thank the children and parents who participated in thestudy. We would like to extend our gratitude to the psychologists and pediatricians of the child development unitsat the University Hospital of Geneva and the University Hospital of Lausanne, as well as to Naomi Langerock.

L’année psychologique/Topics in Cognitive Psychology, 2015, 00, 1-24

2 Lejeune � Borradori Tolsa � Bickle Graz � Hüppi � Barisnikov

Émotion, attention et contrôle volontairechez des enfants prématurés et nés à terme âgés de 24 mois

RÉSUMÉLes enfants nés prématurément présentent plus des problèmes comportementaux etsocio-émotionnels qui persistent jusqu’à l’âge adulte. Cependant, aucune étude ne s’estintéressée simultanément à l’émotion, l’attention et au contrôle volontaire. Cette étudea pour objectif de comparer ces compétences entre des enfants très grands prématurés(<29 semaines de gestation) et nés à terme à l’âge de 24 mois, grâce à des questionnairesparentaux et à une évaluation comportementale. Les enfants prématurés sont évalués parleurs parents comme ayant un affect négatif plus élevé et une attention soutenue moindre.L’évaluation expérimentale met en évidence des patterns attentionnels distincts entre lesdeux groupes. Finalement, les enfants prématurés ont plus de difficultés à maintenir uncontrôle volontaire lors d’une tâche d’inhibition en comparaison aux enfants nés à terme.L’ensemble de ces résultats révèlent chez ces enfants prématurés des difficultés de certainescompétences clés permettant un comportement d’autorégulation volontaire.

1. INTRODUCTION

Children born prematurely are at increased risk for developmentaldisorders, including cognitive, behavioral (Bhutta, Cleves, Casey, Cradock,& Anand, 2002), motor (de Kieviet, Piek, Aarnoudse-Moens, & Oosterlaan,2009), attentional (Pizzo et al., 2010), executive (Aarnoudse-Moens,Smidts, Oosterlaan, Duivenvoorden, & Weisglas-Kuperus, 2009), andsocio-emotional problems (Treyvaud et al., 2012) that result in laterdifficulties in academic achievement. A high prevalence of behavioralproblems has notably been reported during adolescence and early adult-hood, in particular the inattentive subtype of attention deficit-hyperactivitydisorder, as well as anxiety and socio-emotional difficulties (Johnson &Marlow, 2011; Nosarti et al., 2012; Somhovd, Hansen, Brok, Esbjorn, &Greisen, 2012). These studies highlight the necessity of detecting as early aspossible specific dysfunctions that could predict later behavioral problems,in order to implement early intervention.

Socio-emotional and behavioral difficulties have been linked toattentional and inhibition problems in the general population (Allan &Lonigan, 2011; Kim, Nordling, Yoon, Boldt, & Kochanska, 2013; van deWeijer-Bergsma, Wijnroks, & Jongmans, 2008). Moreover, developmentalstudies revealed links between attention, effortful control, and emotionalabilities. Effortful control is defined as “the ability to voluntarily regulatebehavior and attention, as seen in the inhibition of a dominant responseand activation of a subdominant response” (Rothbart, Sheese, Rueda, &


Emotion, attention, effortful control in preterms 3

Posner, 2011, p. 207). Eight- to ten-month-old infants displaying longerand more intense focused attention showed better regulation of negativeemotions (Kochanska, Coy, Tjebkes, & Husarek, 1998). Greater effortfulcontrol correlated with better regulation of positive and negative emotionin children from 9 to 45 months (Aksan & Kochanska, 2004; Kochanska,Aksan, Penney, & Doobay, 2007; Kochanska, Murray, & Harlan, 2000;Putnam, Rothbart, & Gartstein, 2008). In 4- to 5-year-old children, anoptimal emotional regulation was related to a medium level of inhibitorycontrol (Carlson & Wang, 2007). Finally, low self-regulation in preschoolchildren has also been linked to later behavior problems and low academicachievement (Eisenberg et al., 2009; Kim et al., 2013). These resultshighlight the importance of considering attention, effortful control, andemotion in studies examining populations at risk for behavioral andsocio-emotional difficulties such as preterm children.

In order to detect these problems in children born prematurely,researchers have compared their performances to those of their term-bornpeers. Based on parental reports, 6- to 12-month-old very preterm infantswere described as being less adaptable and more active than their full-termcounterparts (Kerestes, 2005; Medoff-Cooper, 1986). Moreover, accordingto an experimental design, 8-month-old very preterm infants showed moredifficulties in inhibiting distraction than full-term infants did (Sun, Mohay,& O’Callaghan, 2009), and 12-month-old very preterm infants expressedhigher anger reactivity, lower fear reactivity, and a distinct attentionalpattern (Langerock et al., 2013). Preterm children thus already displayedemotional, attentional and inhibition difficulties during infancy.

At 24 months, very preterm children were rated by parents as havingmore internalizing problems and lower socio-emotional competences andas being more dysregulated (Spittle et al., 2009). In contrast, accordingto another parental questionnaire, no difference was found in negativeaffectivity (Voigt et al., 2013) and effortful control (Voigt, Pietz, Pauen,Kliegel, & Reuner, 2012) between 24-month-old very preterm and full-termchildren. However, if measured with experimental tasks, very pretermchildren displayed lower effortful control compared with full-term children(Voigt et al., 2012). During problem-solving tasks, 24-month-old verypreterm children produced less positive vocalizations (Evrard et al., 2011)and were characterized by poorer self-regulation and less persistencein different problem solving tasks, though no difference was revealedby parental report (Clark, Woodward, Horwood, & Moor, 2008). Inconclusion, the few studies investigating attention, effortful control, andemotion at 24 months, revealed differences between preterm and full-termchildren, but contradictory results were found.



The discrepancies between the results obtained by experimentaldesign and by parental questionnaire should not necessarily be seen ascontradictory; rather, they might turn out to be complementary. Theparental questionnaire informs about daily life in a variety of situations,but it also reflects parents’ subjective representation of their children,which could be different between the two groups, due to the anxietyeliciting NICU experience. Indeed, it has been reported that the parents’personality could influence the perception of their child. For example,parents displaying higher negative affectivity reported more fear for their6- to 12-month-old full-term children (Gartstein & Marmion, 2008).Experimental design refers to standardized procedures during which theenvironment can be controlled, minimizing external influences. However,these procedures represent a short evaluation realized at a particularmoment, limiting the generalization of the interpretation of the behaviorof children. Consequently, consideration of the findings from bothexperimental design and parental questionnaires allows a more completeand reliable view of the early behavior of preterm children. However, thereis a paucity of studies that have thoroughly examined the behavior ofpreterm children using both methods.

Furthermore, most studies focusing on early development in pretermchildren used the corrected age for prematurity (age since expected term).Although the literature converges to support the use of corrected ageuntil a minimum of 12 months, there is no clear consensus beyondthis age (Wilson & Cradock, 2004). Many studies revealed that severaldifferences between preterm and full-term children disappeared whenage was corrected for prematurity as compared with chronological age.However, this correction could lead to an overestimation of the pretermchildren’s early abilities and could in turn delay intervention services,especially for the more vulnerable infants born before 28 weeks (Wilson& Cradock, 2004). Moreover, in their review, van de Weijer-Bergsma,Wijnroks, and Jongmans (2008) noted that attentional problems seemedto become more apparent as preterm infants grew up. The same authorsmentioned that “the possibility that the trend of worsening outcome withage is confounded by an age-related change in correction for prematurityshould therefore not be discarded” (van de Weijer-Bergsma et al., 2008,p. 347). With the aim of detecting specific dysfunctions in preterm childrenas early as possible, we compared preterm children with full-term childrenat a chronological age of 24 months.

The above-mentioned studies revealed contradictory results concerningearly differences between preterm and full-term children, and no study hasbeen reported in which researchers simultaneously investigated attention,



effortful control, and emotion. In order to have a more complete overviewof their abilities and difficulties, we used both an experimental design(4 episodes of the Laboratory Temperament Assessment Battery, and 3episodes of the Effortful Control Battery) and parental report (EarlyChildhood Behavior Questionnaire), with a control for parental anxiety(State-Trait Anxiety Inventory). Similarly to Langerock et al. (2013), weanalyzed performances across time (trial after trial) for the experimentaldesign, in order to evaluate the dynamic tracking across trials. For thedifferences detected between the two groups, we examined the link betweenthese difficulties in very preterm children. On the basis of the literature,very preterm children were expected to have higher negative emotionality,lower positive emotionality, and lower attention and effortful control skillsthan their term-born peers. We also hypothesized that higher negativeemotionality in very preterm children would be related to lower attentionand effortful control skills.

2. METHOD

2.1. ParticipantsThe participants were 49 very preterm children (31 girls and 18 boys) born before29 weeks of gestational age. They were recruited in the University Hospitals ofGeneva and Lausanne, where they were offered developmental follow-up after theirpreterm birth. The behavioral evaluation took place in the follow-up units of thetwo hospitals. Very preterm children with congenital malformations were excludedfrom this study. An overall description of the preterm population is shown inTable 1.

The control group consisted of 27 full-term children (11 girls and 16 boys),recruited through day care centers in Geneva after the parents received aninformation letter and a consent form about the study. The behavioral evaluationtook place in the day care centers or in the evaluation room at the university. Verypreterm and full-term children were enrolled between June 2009 and February 2011and both groups were evaluated at the chronological age of 24 months (+ or - 2months). The study was approved by the local ethics committees and parents gavewritten informed consent for the participation of children in the experiment. Therewas no difference in sex ratio, χ2(1) = 3.572, p > .05, or age at testing, t(74) = .749,p > .05, between very preterm and full-term children. The family’s socioeconomicstatus (SES) was calculated using the Largo et al.(1989) 12-point scale based onparental occupation and maternal education (range from 2 - the highest SES - to12 - the lowest SES). The SES of the families of very preterm children (M = 5.56,SD = 3) was significantly lower than the SES of the families of full-term children(M = 3.6, SD = 2.4), t(74) = 2.923, p < .01.



Table 1. Population characteristics: Mean (standard deviation)or number (percentage)

Variables Very preterm children (N = 49)

Gestational age (weeks) 27.25 (1.16)Birth weight (g) 928.3 (221.9)

SGA 7 (14.3%)IVH grades III and IV 1 (2%)

PVL 1 (2%)MDI 88 (14.7)PDI 86.1 (15.7)

Note. SGA, small for gestational age (<10th percentile for birth weight as a function of GA andgender); IVH, intraventricular hemorrhage (Grade III: intraventricular with distension, Grade IV:hemorrhagic parenchymal infarction, according to Papile, Burstein, Burstein, & Koffler, 1978); PVL,periventricular leukomalacia (based on magnetic resonance imaging); MDI, Mental DevelopmentIndex of the Bayley Scales of Infant Development; PDI, Psychomotor Development Index of theBayley Scales of Infant Development, second edition (Bayley, 1993).

2.2. ProcedureThe study was conducted by using an experimental paradigm and parentalquestionnaires. Children were evaluated on four episodes of the LaboratoryTemperament Assessment Battery (Lab-TAB; Goldsmith & Rothbart, 1999) andthree episodes of the Effortful Control Battery (Kochanska et al., 2000). The fourselected episodes from the Lab-TAB were “Puppet Game,” “Attractive Toy PlacedBehind Barrier,” “Unpredictable Mechanical Toy,” and “Blocks.” These episodesevaluate joy, anger, fear, and sustained attention, respectively. The three episodesselected from the Effortful Control Battery were “Snack Delay,” “Wrapped Gift,”and “Tower.” These episodes evaluate two components of effortful control: delaying(waiting for a pleasant event) twice and suppressing or initiating activity to signal(taking turns), respectively. All children were evaluated in a quiet room with atleast one reference person present. Children were seated in front of a small tableon a small chair, or on the reference person’s lap. The episodes were presented in apseudo-random order, always starting with an episode to make the child feel moreat ease (Blocks or Puppet Game). All the evaluations were videotaped with parentalconsent for subsequent analysis. Three coders scored the episodes independentlyfor 15% of the sample (5 very preterm and 5 full-term children) after thoroughtraining on the scoring methods. Inter-rater reliability was calculated using Pearsoncorrelations on the means for each variable by episode. Correlations ranged from.59 to 1 with a mean r of .92.

To evaluate the child’s behavior, parents were requested to complete aFrench version of the Early Childhood Behavior Questionnaire (ECBQ) shortform (Putnam, Gartstein, & Rothbart, 2006; Putnam, Jacobs, Gartstein, &Rothbart, 2010) translated by Laurin, Gosselin, and Forman (see websitehttp://www.bowdoin.edu/~sputnam/rothbart-temperament-questionnaires/). The



State-Trait Anxiety Inventory (STAI; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs,1993) was completed by parents to assess their own anxiety.

2.3. Measures2.3.1. Laboratory Temperament Assessment Battery(Lab-TAB)Lab-TAB coding was performed in accordance with the LAB-TAB guidelines,which mainly involve facial, vocal, and bodily measures. For each episodemeasuring a specific emotion, most of the measures were rated on 4-point Likertscales according to the intensity of a specific behavior (0 = absent; 1 = small;2 = medium; 3 = intense). A higher score thus indicates more emotional reactivityduring a specific emotion-eliciting situation.

Puppet Game (joy). The experimenter performed a scripted humorous dialogue(60-90 s) using two friendly puppets during which the child was gentlytickled 3 times by the puppets. Scoring was performed in four equivalent timeintervals (introduction, first tickle, second tickle, third tickle) for smiling, positivevocalizations, and positive motor activity. Only positive vocalizations and positivemotor activity scores were significantly intercorrelated (r = .642, p < .001), and sothey were averaged to compute a composite score of joy (Cronbach’s α = .76). Thesmiling score was analyzed independently.

Attractive Toy Placed Behind Barrier (anger).The child was given an attractivetoy with which to play for approximately 15 s. The experimenter then gently tookthe toy from the child and placed it behind a plexiglass barrier for 30 s (two trials).Each trial of 30 s was split into six time intervals of 5 s. For each 5-s time interval,facial anger, distress vocalizations, and struggle were coded. All measures were thenaveraged across time intervals for each trial. All scores were intercorrelated (meanr = .30 for Trial 1; mean r = .34 for Trial 2), and they were averaged to obtaina composite measure of anger by trial (Cronbach’s α = .50 and .58, respectively).The scores from both trials were averaged to create a total anger score (Cronbach’sα = .86).

Unpredictable Mechanical Toy (fear). A mechanical robot (dog) was put on atable in front of the child. First, the dog moved toward the child (10 s), and thenit stopped and barked in front of the child (10 s), and finally, it moved back tothe initial position (10 s; two trials). For each time interval, facial fear, distressvocalizations, bodily fear, and intensity of escape were coded. All measures werethen averaged across time intervals for each trial. All scores were significantlyintercorrelated (mean r = .60 for Trial 1; mean r = .63 for Trial 2), and they wereaveraged to compute a composite score of fear by trial (Cronbach’s α = .85 and .87,respectively). The scores from both trials were averaged to create a total fear score(Cronbach’s α = .92).

Blocks (sustained attention). A wooden array of blocks was put in front ofthe child, who was left to observe and play with these blocks for 3 min. Theexperimenter and the reference person stayed at a distance so as not to disturb thechild. Each minute was divided into six time intervals of 10 s. Each time interval was



coded for intensity of facial interest, duration of observation (0 = absent; 1 = 1-4 s;2 = 5-8 s; 3 = 9-10 s), and duration of manipulation (0 = absent; 1 = 1-4 s; 2 = 5-8s; 3 = 9-10 s). All scores were significantly intercorrelated (mean r = .62 for Minute1; mean r = .76 for Minute 2; mean r = .69 for Minute 3), and they were averaged tocompute a composite score of sustained attention by minute (Cronbach’s α = .82,.90, and .85, respectively). The scores from each minute were averaged to create atotal sustained attention score (Cronbach’s α = .65).

2.3.2. Effortful Control BatterySnack Delay (delaying gratification). The child, with hands on a mat on the table,waited for the experimenter to ring the bell before retrieving a treat from undera transparent cup (four trials, with delays of 10, 20, 30, and 15 s, respectively). Inmid-delay, the experimenter lifted the bell but did not ring it. Coding reflected theability to delay (1 = eats candy before experimenter lifts bell; 4 = touches candyafter experimenter lifts bell; 7 = waits until bell rung). One point was added forkeeping hands on the mat only before or only after the experimenter lifted the bell,and 2 points were added for keeping hands on the mat during the entire time. Scoresacross the four trials were significantly intercorrelated (mean r = .54), and so theywere averaged to compute a composite score of inhibition (Cronbach’s α = .83).

Wrapped Gift (delaying gratification). The experimenter brought a gift for thechild, as well as gift wrap, and she asked the child to sit down with his or herback to the experimenter and not to peek while the gift was being wrapped (60s). The experimenter then put the gift on the table and, before leaving to get a bow,asked the child to stay on his or her chair and not to touch the gift until she cameback (180 s). Scoring during the wrapping time reflected the peek and turn score(1 = turns around and continues to peek, 3 = peeks over shoulder, 5 = does notpeek).Scoring during the waiting-for-bow time included the touch score (on a scaleranging from 1 = opens gift to 4 = does not touch) and the seat score (child ison the seat for a total time of 1 = less than 30 s; 2 = less than 1 min; 3 = lessthan 2 min; 4 = more than 2 min). The scores were not significantly intercorrelated(mean r = .16); consequently, no composite inhibition score was calculated for thisepisode.

Tower (suppressing activity to signal). The child and the experimenter took turnsbuilding a block tower (two trials) together, after which the experimenter explainedto the child what it meant “to take turns.” The total number of the placed blocks(multiplied by 10) was divided by the number of blocks placed by the child. Ifa child took turns with the experimenter every time, she or he placed as manyblocks as the experimenter (20 was the highest score). A penalty of -5 was givenfor intentionally knocking down the tower. As scores from both trials were notsignificantly intercorrelated (mean r = .29), no composite inhibition score wascalculated for this episode.

2.3.3. State-Trait Anxiety Inventory (STAI)The STAI is a self-report inventory and contains two subscales of 20 items assessingstate and trait anxiety. Cronbach’s alphas, averaged over both scales, were .90



(range = .65 to .96; Barnes, Harp, & Jung, 2002). The State Anxiety subscaleevaluates the intensity of current feelings at this moment (1 = not at all; 4 = verymuch so), and the Trait Anxiety subscale evaluates frequency of feelings in general(1 = almost never; 4 = almost always). Parents rated each item on a 4-point Likertscale.

2.3.4. Early Childhood Behavior Questionnaire (ECBQ)The ECBQ Short Form measures temperament in toddlers aged 1.5–3 years andcontains 107 items and 18 four- to eight-item scales. Cronbach’s alphas, averagedover all scales, were .74 (range from .65 to .83) for the Short Form, in comparisonto .80 (range from .67 to .90) for the Standard Form (Putnam et al., 2010). TheECBQ measures 18 discrete traits embedded within three higher-order factors:Negative Affect (discomfort, fear, frustration, motor activation, sadness, perceptualsensitivity, shyness, negatively loaded soothability), Surgency (impulsivity, activitylevel, high-intensity pleasure, sociability, positive anticipation), and EffortfulControl (inhibitory control, attention shifting, low-intensity pleasure, cuddliness,attentional focusing). Parents were asked to report on the frequency of specific childbehaviors to a concrete situation (e.g. “while at home, how often did your childshow fear at a loud sound (blender, vacuum cleaner, etc.)?”; “when a familiar childcame to your home, how often did your child seek out the company of the child?”)on a 7-point Likert scale (1 = never; 4 = about half the time; 7 = always).

2.4. Statistical AnalysisKolmogorov-Smirnov analyses revealed that the variables of the Lab-TAB (exceptfor the Puppet Game and the Blocks episodes) and the Effortful Control Batterywere not normally distributed. These scores were thus log-transformed. Becausethe SES of the very preterm children was significantly lower (2.1. participants’subsection), all of the analyses were performed to control for the effects ofbetween-group differences in SES, as suggested in a recent systematic review(Wong & Edwards, 2013). Analyses of covariance (ANCOVAs) were conductedon raw scores for the normally distributed data and on the log-transformeddependent variables for the not normally distributed data. These analyses wereperformed for each dependent variable with the group (full-term vs. preterm) asthe between-subjects factor. For the experimental tasks comprising more than onetrial, repeated-measures ANCOVAs were also conducted with the trial (or the timeinterval for the Blocks episode) as a within-subjects factor (Trial 1 vs. trial n) andthe group as a between-subjects factor (very preterm vs. full-term children), inorder to evaluate whether very preterm and full-term children presented differentpatterns according to the trials. As parental anxiety is known to influence parentalperceptions of their child (Gartstein & Marmion, 2008), data from the STAI werealso entered as a covariate in ANCOVAs for the ECBQ data. Spearman correlationswere used to investigate the link between the very preterm children’s difficulties.The significance threshold was .05.



2.5. Missing DataFor the experimental design, not all data were available for every child for manydifferent reasons: Some children did not want to perform some or any episodes;others were excluded a posteriori because of technical problems or becausechildren were too tired, stressed, or not interested in the episode. Consequently,42 very preterm and 24 full-term children were part of the experimental design(they performed at least one episode). Moreover, not all parents returned thequestionnaires (41% for the very preterm group and 12.5% for the full-termgroup), or they completed only one of them. Consequently, 21 questionnairescompleted by parents of full-term children were compared with 29 questionnairescompleted by parents of very preterm children. The sample size is specified for eachepisode in the 3.Results section.

3. RESULTS

3.1. Between-Groups AnalysesResults for each episode of the experiment are reported in Table 2, and thoseof the parental questionnaire are reported in Table 3.

Puppet Game (joy).One very preterm child did not perform this episode.The scores of 41 very preterm children and 24 full-term children were thuscompared. ANCOVAs indicated no significant difference between the twogroups.

Attractive Toy Placed Behind Barrier (anger). Two very preterm childrenand one full-term child did not perform this episode. The scores of 40 verypreterm children and 23 full-term children were analyzed. Five additionalvery preterm children did not perform the second trial. Thus, 35 verypreterm children and 23 full-term children were analyzed for this trial. Noscore differed significantly between the two populations.

Unpredictable Mechanical Toy (fear). Four very preterm children and onefull-term child did not perform this episode. Consequently, the scores of38 very preterm and 23 full-term children were compared. One additionalfull-term child did not perform the second trial. Thus, 38 very preterm and22 full-term children were analyzed for this trial. ANCOVAs did not showany significant difference between the two groups.

Blocks (sustained attention). Three very preterm children did notperform this episode. The scores of 39 very preterm and 24 full-termchildren were analyzed. Three additional very preterm children stoppedplaying with the blocks during the third minute, and so 36 very preterm



Table 2. Results of the Lab-TAB and the Effortful Control Battery byepisode and by variable

Very preterm Full-term

Episodes M (SD) M (SD) F p

Puppet GameJoy 1.35 (.9) 1.40 (.95) .464 .498Smiling .32 (.49) .19 (.41) .191 .664Toy Behind Barriera

Anger - Trial 1 .49 (.40) .37 (.34) .161 .690Anger – Trial 2 .57 (.61) .49 (.42) .052 .820Total anger .54 (.48) .43 (.37) .006 .936Unpredictable Toya

Fear – Trial 1 .59 (.56) .84 (.79) 2.040 .159Fear – Trial 2 .64 (.72) .94 (.95) 1.301 .259Total fear .61 (.63) .90 (.85) 2.000 .163BlocksSustained attention - Minute 1 1.87 (.48) 1.73 (.49) .171 .680Sustained attention - Minute 2 1.88 (.69) 1.99 (.61) 2.798 .100Sustained attention - Minute 3 1.92 (.61) 1.7 (.77) 1.564 .216Total sustained attention 1.87 (.46) 1.81 (.51) .017 .898Snack Delaya

Inhibition 1 6.58 (2.4) 6.83 (2.6) .133 .717Inhibition 2 5.87 (2.7) 6.17 (3.4) .141 .709Inhibition 3 4.57 (3.1) 6.39 (2.5) 2.544 .118Inhibition 4 5.08 (3.2) 6.89 (2.6) 2.698 .108Total inhibition 5.47 (2.3) 6.57 (2.5) .626 .433Wrapped Gifta

Peak and turn 1.37 (.85) 1.63 (.71) 2.361 .131Touch 2.45 (1.1) 2.63 (1.1) .211 .648Seat 2.19 (3.3) 3.33 (1.1) 7.760 .007Towera

Inhibition 1 15 (4.5) 15.5 (3.6) .124 .726Inhibition 2 14.2 (3.3) 16.1 (2.4) 4.222 .047

Note. Boldface entries indicate significant difference (p < .05); Lab-TAB, Laboratory Temperament AssessmentBattery; SES, socioeconomic status. aNormalized by log-transformation for ANCOVAs.

children and 24 full-term children were analyzed for this interval time.ANCOVAs indicated no significant difference between the two populations.

Snack Delay. Eleven very preterm and six full-term children did notperform this episode. Moreover, one additional very preterm child did notperform Trials 3 and 4, and five other preterm children did not performTrial 4. Consequently, 18 full-term children were compared with 31 verypreterm children for Trials 1 and 2, with 30 very preterm children for Trial



Table 3. Results of the ECBQ

Very preterm Full-term

Scales M (SD) M (SD) F a p

Effortful Control 4.39 (0.62) 4.68 (0.59) 2.418 .127Attentional focusing 4.21 (0.85) 4.82 (0.76) 5.466 .024Attentional shifting 4.45 (0.66) 4.71 (0.71) 1.244 .271Cuddliness 4.68 (0.98) 5.06 (0.61) 2.038 .160Inhibitory control 3.57 (1.08) 3.93 (1.06) .816 .371Low-intensity pleasure 5.04 (1.24) 4.9 (1.05) .016 .901Negative Affect 3.37 (0.64) 2.78 (0.48) 10.213 .003Discomfort 3.14 (0.97) 2.39 (0.74) 9.681 .003Fear 2.62 (1.04) 1.94 (0.68) 5.802 .020Motor activation 2.72 (0.76) 1.7 (0.5) 26.654 <.001Perceptual sensitivity 5.09 (1.21) 4.23 (1.07) 5.756 .021Sadness 2.69 (1.23) 2.31 (0.85) .454 .504Shyness 3.5 (1.27) 3.1 (1) 1.661 .204Soothability 4.81 (0.99) 4.92 (0.92) .005 .943Frustration 3.99 (1.26) 3.48 (0.75) 1.323 .256Surgency 4.8 (0.71) 4.87 (0.56) .372 .545Activity level/energy 4.8 (0.95) 4.58 (0.73) .223 .639High-intensity pleasure 4.39 (1.26) 4.37 (0.96) .000 .987Impulsivity 4.48 (1.17) 5 (1.12) 3.010 .090Positive anticipation 5.03 (1.03) 4.66 (1.1) 1.354 .251Sociability 5.29 (1.01) 5.72 (0.97) 3.058 .087

Note. Boldface entries indicate significant difference (p < .05); ECBQ, Early Childhood Behavior Questionnaire.aAdjusted for socioeconomic status and state and trait anxiety subscales from the State-Trait Anxiety Inventory.

3, and with 25 very preterm children for Trial 4. ANCOVAs indicated nosignificant difference between the two groups.

Wrapped Gift. Eleven very preterm children did not perform thisepisode. The scores of 31 very preterm children and 24 full-term childrenwere thus compared. ANCOVA revealed a significant difference only for theseat score, F(1,54) = 7.760, p < .05. During the waiting-for-bow time, thevery preterm children exhibited more difficulties staying on their chair thandid the full-term children.

Tower. Eighteen very preterm and three full-term children did notperform this episode. Four additional very preterm children did notperform the second trial. Therefore, 21 full-term children were comparedwith 24 very preterm children for the first trial and with 20 very pretermchildren for the second trial. ANCOVA showed that very preterm childrendisplayed a significantly lower inhibition score compared with that offull-term children only during the second trial, F(1,40) = 4.222, p < .05.



STAI. Twenty-one questionnaires completed by parents of full-termchildren were compared with 29 questionnaires completed by parents ofvery preterm children. The state and trait anxiety scales did not differsignificantly between very preterm (M = 38.3, SD = 11; M = 41.4,SD = 8.7, respectively) and full-term parents (M = 36.6, SD = 9.6; M = 40,SD = 7.3, respectively).

ECBQ. Twenty-one full-term and 29 very preterm children werecompared. First, very preterm children displayed significantly lowerattentional focusing than full-term children did. Second, a significantlyhigher level of negative affect was reported in very preterm children withmore discomfort, fear, motor activation, and perceptual sensitivity.

3.2. Repeated-measures analysesTo verify the potential influence of the sample size discrepancy, we reranthe analyses by excluding the children who did not perform all of the trials.The results remained unchanged. The following analyses include only thosechildren who completed all trials.

In order to evaluate whether very preterm and full-term childrenpresented different patterns according to the trials, repeated-measureANCOVAs were conducted with the trial (or the time interval for theBlocks episode) as a within-subjects factor (Trial 1 vs. trial n) and thegroup as a between-subjects factor (very preterm vs. full-term children).For the anger and fear scores, as well as for the Tower, ANCOVAs showedno significant group or trial effect, nor was there a significant trial ×group interaction. For the sustained attention score, ANCOVA revealed asignificant time interval × group interaction, F(2,114) = 3.382, p < .05:Full-term children displayed an increased level of attention in the middle ofthe episode, whereas the attention level of very preterm children remainedunchanged (Figure 1). For the Snack Delay, no significant effect of thegroup and the trial was found. Results indicated a significant trial × groupinteraction, F(3,120) = 3.129, p < .05: Inhibition difficulties emerged forthe very preterm children from the third trial and persisted during thefourth trial (Figure 2).

3.3. Link Between the Difficultiesof Very Preterm ChildrenThe difficulties of very preterm children were defined as the scores fromthe Lab-TAB, the Effortful Control Battery, and the ECBQ, which differedfrom those of the full-term children. To investigate the link between these



Figure 1. Sustained attention scores (adjusted for socioeconomic status) from theBlocks episode of the Laboratory Temperament Assessment Battery.

Figure 2. Inhibition scores (adjusted for socioeconomic status) from the Snack Delayepisode of the Effortful Control Battery.

difficulties, we performed Spearman’s correlations only for these scoresin the very preterm children (Table 4). Inhibition 3 and Inhibition 4from the Snack Delay were significantly and positively correlated witheach other and with Inhibition 2 from the Tower. However, the seatscore from the Wrapped Gift was unrelated to these three scores, but wassignificantly and positively related to Sustained Attention 2 from the Blocks.All of these scores from the experimental paradigm were not significantly



correlated to those from the parental reports. Regarding the results of theECBQ, three subscales (Discomfort, Fear, Motor Activation) correlatedsignificantly and positively with their higher-order factor, Negative Affect.Furthermore, the very preterm children rated by their parents as morefearful were those who were also rated with more discomfort and motoractivation and with less attentional focusing. Moreover, a higher level ofdiscomfort in very preterm children was positively correlated to a higherlevel of perceptual sensitivity. Finally, the very preterm children witha lower level of attentional focusing displayed a higher level of motoractivation.

Among the parents of the 42 very preterm children who participatedin the study, only 22 questionnaires were returned. To control for possibledifferences between very preterm children with and without completedquestionnaires, we used student t tests for each measure of the experimentaldesign, and no significant difference was found between the two groups (allps > .10). The generalization of these correlations to the whole very pretermgroup is thus allowed.

4. DISCUSSION

The aim of this research was to compare emotional, attentional, andeffortful control abilities of very preterm and full-term children at 24months of age with two methods of evaluation. The major study findingsare discussed below.

4.1. EmotionDuring the joy-eliciting episode of the Lab-TAB, no difference was observedbetween the two populations, unlike the results reported by Langerocket al. (2013), who indicated higher levels of positive motor activity in12-month-old very preterm children using the same task. At 24 months,preterm children seem to better regulate their level of excitement inresponse to positive stimulation. Moreover, Evrard et al. (2011) foundless positive vocalizations in 12- and 24-month-old very preterm children,although the problem-solving tasks in the study did not directly assess joy.The episodes of the Lab-TAB assessing negative emotion (fear and anger),revealed no difference between very preterm and full-term children. This



Tab

le4.

Spea

rman

’sco

rrel

atio

nan

alys

esin

very

pre

term

child

ren

Blo

cks-

Sust

ain

edat

ten

tion

2

Snac

kD

elay

–In

hibi

tion

3

Snac

kD

elay

–In

hibi

tion

4W

rapp

edG

ift

-Se

at

Tow

er-

Inhi

biti

on2

EC

BQ

-A

tten

tion

alFo

cusi

ng

EC

BQ

-D

isco

mfo

rtE

CB

Q-

Fear

EC

BQ

-M

otor

Act

ivat

ion

EC

BQ

–Pe

rcep

tual

Sen

siti

vity

Snac

kD

elay

--.

187

Inh

ibit

ion

329

Snac

kD

elay

--.

249

0.84

0∗∗

Inh

ibit

ion

424

25W

rapp

edG

ift

-0.

370∗

.080

.027

Seat

2826

23To

wer

-In

hib

itio

n2

-.33

70.

496∗

0.60

4∗-.

056

1917

1516

EC

BQ

-A

tten

tion

al.0

48-.

325

-.21

2.0

02-.

040

Focu

sin

g22

2018

1812

EC

BQ

-D

isco

mfo

rt-.

113

.262

.347

.288

.316

-.12

422

2018

1812

29E

CB

Q-

Fear

-.04

6.1

74.2

65.0

03.0

83-0

.374

∗0.

546∗

∗22

2018

1812

2929

EC

BQ

-M

otor

.121

.111

.046

-.14

2-.

150

-0.5

17∗∗

0.32

00.

440∗

Act

ivat

ion

2220

1818

1229

2929

EC

BQ

-Pe

rcep

tual

.011

.084

-.02

5-.

023

.309

-.05

90.

429∗

-.01

7-.

097

Sen

siti

vity

2220

1818

1229

2929

29E

CB

Q-

Neg

ativ

e.0

90.0

12.0

57.0

89.0

65-0

.351

0.76

6∗∗

0.69

0∗∗

0.53

4∗∗

0.32

2A

ffec

t22

2018

1812

2929

2929

29

Not

e.T

he

sam

ple

size

isin

dica

ted

un

der

the

coef

fici

ent

ofco

rrel

atio

n.

∗∗p

<.0

1.∗ p

<.0

5.



result is in accordance with other studies using an experimental paradigmat 24 months of age (Clark et al., 2008). We found, however, that verypreterm children were rated by their parents as having more negativeemotion. More precisely, the parents described very preterm children ashaving more negative affect related to more discomfort (sensory qualitiesof stimulation), fear (unease, worry, or nervousness related to anticipatedpain or distress or potentially threatening situations), motor activation(repetitive small-motor movements), and perceptual sensitivity (thresholdto detect slight, low intensity stimuli from the external environment). Thediscrepancies between the results obtained by experimental design andby parental questionnaire are in accordance with the literature showinginconsistent results between the two methods of evaluation. Furthermore,increased negative emotionality and sensory sensitivity (dysregulationdomain) was also found in 24-month-old very preterm children comparedwith a full-term group, according to parental questionnaire (Spittle et al.,2009). In contrast to our findings, Voigt et al. (2013) used the ECBQ andfound no difference on the negative affect factor and on its respectivesubscales. Nevertheless, it should be noted that the present study usedchronological age, the short form of the ECBQ, and a very preterm sampleborn before 29 weeks of gestational age, whereas Voigt et al. (2013) usedthe corrected age, the standard form of the ECBQ, and a very pretermsample born before 32 weeks of gestational age. These differences couldexplain the discrepancy between the results. Notwithstanding, preterminfants have been described as less fearful at 12 months of age, as measuredby parental questionnaire (Kerestes, 2005), as well as by experimentaldesign (Langerock et al., 2013), suggesting a different developmentaltrajectory of fear reactivity between very preterm and full-term childrenduring the first 2 years. Moreover, a study using an early interventionprogram for preterm children revealed the importance of consideringnegative affect: The low birth weight preterm children with a higher level ofnegative affect were those who benefited most from the intervention (Blair,2002).

Correlation analyses revealed that the most fearful very pretermchildren were those who displayed more discomfort and motor activation.Moreover, very preterm children with a higher level of discomfort alsoshowed a higher level of perceptual sensitivity. In sum, 24-month-old verypreterm children displayed an anxious and hypersensitive profile. Thisprofile was previously described in 12-month-old preterm children, as wellas during adolescence, and it is related to their later internalizing problems(Guedeney, Marchand-Martin, Cote, & Larroque, 2012; Somhovd et al.,2012).



4.2. AttentionFurthermore, results of the parental questionnaire showed that verypreterm had a lower sustained duration of orienting on an object andwere less resistant to distraction (attentional focusing). In addition,correlations showed that the very preterm children with a lower levelof focused attention were those who displayed a higher level of motoractivation and fear. During 3-minutes-free play with blocks, very pretermand full-term children had a similar total sustained attention score;however, different attentional patterns across time appeared. Indeed, thelevel of attention increased during the second minute for the full-termchildren, whereas the attention level of very preterm children remainedunchanged. The repeated-measures analysis allowed us to observe that verypreterm and full-term children seem to organize their attention toward theblocks differently throughout the episode. The unchanged attentional levelobserved in very preterm children could reflect an immature pattern ofsustained attention, with, for example, some difficulties in disengagement.Ruff, Lawson, Parrinello, and Weissberg (1990) observed that very pretermchildren were more attentive but less active at 24 months of age duringfree play, after controlling for the Bayley Mental Development Index. Thisbehavior could explain the unchanged pattern of attention that we observedin very preterm children. It could be informative to extend the duration ofthe Blocks episode in order to observe the evolution of these attentionalpatterns across time in the two populations, for example. Moreover,different attentional patterns between 12-month-old preterm and full-termchildren were previously observed during the same task (Langerock et al.,2013). However, the patterns observed at 12 and 24 months are different,showing different developmental trajectories of sustained attention duringfree play between very preterm and full-term children. The questionnaireand the experimental paradigm support other findings showing attentiondifficulties in preschool and school-aged preterm children compared tofull-term children (Pizzo et al., 2010; van de Weijer-Bergsma et al., 2008).Early sustained attention problems have been shown to be predictive of laterattentional, cognitive, and behavioral dysfunction in preterm children (vande Weijer-Bergsma et al., 2008).

4.3. Effortful ControlAttentional focusing was the only subscale from the higher-order factorEffortful Control of the parental questionnaire showing differences betweenthe two groups. In contrast, differences were observed during the three



experimental tasks assessing effortful control. It is interesting to note thatinhibition difficulties emerged only from the middle of the episodes. Forthe Snack Delay episode, very preterm children manifested lower scoreson delaying gratification from the third trial, which persisted during thefourth trial. Moreover, they exhibited more difficulties in taking turnsbuilding a tower only during the second trial. During the second halfof the Wrapped Gift episode, the preterm children stayed on their chairfor less time than full-term children did. These results demonstrate thatthis population experiences greater difficulties in maintaining inhibitorycontrol than full-term children do. Since effortful control is related topersistence (Zentner & Bates, 2008), our results are consistent with theliterature showing that very preterm children are less persistent at 12months (Medoff-Cooper, 1986) and at 24 months (Clark et al., 2008).Similarly, Voigt et al. (2012) reported lower effortful control compositescores (average of three tasks) in 24-month-old very preterm children.In addition, it is important to note that the number of preterm childrenwho did not perform all the trials during the experimental tasks washigher compared to full-term children, especially for effortful control tasks.These tasks were particularly difficult, as children had to follow complexinstructions involving attention, inhibition and emotional abilities. Thisobservation, together with lower scores for these tasks in very pretermchildren, clearly demonstrates difficulties in the key abilities that allow avoluntary self-regulatory behavior.

The correlation analyses indicated that very preterm children withlower inhibition scores for the Snack Delay were also those who hadlower inhibition scores for the Tower, whereas no link was found withthe Wrapped Gift episode. However, the very preterm children who satfor less time during the Wrapped Gift episode were those who had lowersustained attention scores during the Blocks episode. These differencescould be related to the context required for each task. The Snack Delay andTower episodes involved active participation of the experimenter, but theWrapped Gift (the second part) and Blocks episodes required the autonomyof the children. It is possible that these two different situations led totwo different susceptibilities among very preterm children. However, theseinterpretations remain speculative and require further investigation.

A large body of literature shows that children’s effortful control skillsare important correlates of early disruptive behavior, social relationships,school readiness, and academic performance (Blair & Razza, 2007;Eisenberg et al., 2009; Kochanska et al., 2000). Recent studies distinguished“hot” effortful control tasks from “cool” tasks (Zelazo & Carlson, 2012).Hot tasks include an emotional component (e.g., a reward), whereas cool



tasks do not. This distinction revealed that early effortful control abilitiesdifferentially predicted later behavior problems and academic achievement(Kim et al., 2013). Casey et al. (2011) reported that in 4-year-old children,delay of gratification, the most typical hot task, was related to performanceon a go-nogo task years later: Children who were less able to delaygratification had more difficulty in suppressing a response to a happy face40 years later. Moreover, using functional magnetic resonance imaging,these researchers found that the inferior frontal gyrus was less recruitedand the ventral striatum was exaggeratedly recruited in low delayers (forno-go relative to go trials). These findings suggest that delay gratificationin young children is a strong predictor of later inhibition abilities, which issupported on a neurostructural basis. Thus, inhibition difficulties observedduring the Snack Delay episode in the 24-month-old very preterm childrencould be a reliable predictor of later behavioral and social problems.Future longitudinal research should investigate this hypothesis in largersamples. As interventions focused on improvements in effortful controlare related to better academic achievement in full-term children (Ursache,Blair, & Raver, 2012), such interventions need to be considered in pretermchildren.

4.4. LimitationsLimitations to the generalizability of our findings should be acknowledged.First, we minimized the influence of the SES on emotion, attention, andeffortful control abilities between our two populations by using ANCOVAs,but caution should be used when generalizing these findings. Indeed, theSES is a complex cofounding variable (Wong & Edwards, 2013), and itsinfluence on these abilities could be investigated by comparing preterm andfull-term children with an equivalent SES, for example. Second, the samplesize was relatively modest, especially as there were many missing data,and it is therefore possible that it has resulted in non-significant results,particularly for the correlation analyses. To address these methodologicalissues, we performed additional statistical analyses. For the experimentaldesign, the analyses were rerun, excluding the children who did notperform all of the trials of an episode, and the results remained unchanged,Moreover, analyses were performed to control for the possible differencesbetween very preterm children with and without questionnaires, and theydid not reveal any significant differences between the two groups. However,future studies are needed with larger number of participants, in order toconfirm our findings.



4.5. ConclusionsIn conclusion, the results obtained from the parental reports and theexperimental tests, permit to add new information about specific attention,emotion and inhibition difficulties in 24-month-old very preterm childrencompared with full-term children. The present study also reinforces theimportance of considering both methods when evaluating young pretermchildren, in order to provide a more complete overview of their abilitiesand difficulties. Parental reports indicated the persistence of a higher levelof negative affect (discomfort, fear, motor activation, perceptual sensitivity)in very preterm children. This anxious and hypersensitive profile could berelated to later internalizing problems, given that very preterm children areat greater risk for developing such problems (Johnson & Marlow, 2011).The questionnaire also highlighted lower sustained attention abilities.Furthermore, the results on the experimental tasks, using analyses acrosstrials, were particularly informative, providing dynamic information aboutspecific dysfunctions in the very preterm group. A distinct attention patternbetween the two groups was observed: The full-term children showed apeak of attention in the second trial while preterm children exhibited anunchanged level of attention throughout the task. This pattern could reflectimmature sustained attention abilities, with difficulties of disengagementthat may be predictive of later attention and behavior problems amongpreterm children. Greater difficulties in maintaining inhibitory controlduring the second half of effortful control tasks were also observed invery preterm children. This atypical pattern of performances and thelower scores of attention, inhibition and emotion abilities observed invery preterm children clearly showed difficulties in key abilities whichallow a voluntary self-regulation behavior. This result, in line with thatreported in the recent literature, points out that inhibition control abilities,measured with a delay of gratification task, seem to be a strong predictor oflater behavioral problems in very preterm children. However, longitudinalfollow-up with a larger sample is necessary to strengthen these findingsby detecting longitudinal stability in these problems. Indeed, a differentdevelopmental trajectory of these abilities in the very preterm populationand their relations to later behavioral and socio-emotional difficulties couldbe identified. Their early detection could lead to adapted interventionstrategies to reduce the long-term negative impact of these impairments.

Received June 24, 2014.Revision accepted September 27, 2014.



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Emotion, attention, and effortful control in 24-month-old very preterm and full-term children

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