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Cognitive and behavioral aspects ofexecutive functions in children bornvery pretermBarbara Catherine Ritter a c , Walter Perrig b c , Maja Steinlin a c &Regula Everts a ca Children's University Hospital, Division of Neuropaediatrics,Development and Rehabilitation, Bern, Switzerlandb Institute of Psychology, University of Bern, Switzerlandc Center for Cognition, Learning and Memory, University of Bern,SwitzerlandVersion of record first published: 04 Mar 2013.

To cite this article: Barbara Catherine Ritter , Walter Perrig , Maja Steinlin & Regula Everts (2013):Cognitive and behavioral aspects of executive functions in children born very preterm, ChildNeuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence,DOI:10.1080/09297049.2013.773968

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Child Neuropsychology, 2013http://dx.doi.org/10.1080/09297049.2013.773968

Cognitive and behavioral aspects of executive functions

in children born very preterm

Barbara Catherine Ritter1,3 , Walter Perrig2,3 , Maja Steinlin1,3 ,and Regula Everts1,3

1Children’s University Hospital, Division of Neuropaediatrics, Development andRehabilitation, Bern, Switzerland2Institute of Psychology, University of Bern, Switzerland3Center for Cognition, Learning and Memory, University of Bern, Switzerland

This study investigated whether children aged between 8 and 12 years born very preterm (VPT)and/or at very low birth weight (VLBW) performed lower than same-aged term-born controls incognitive and behavioral aspects of three executive functions: inhibition, working memory, andshifting. Special attention was given to sex differences. Fifty-two VPT/VLBW children (26 girls,50%) born in the cohort of 1998–2003 and 36 same-aged term-born children (18 girls, 50%) wererecruited. As cognitive measures, children completed tasks of inhibition (Color-Word InterferenceTest, D-KEFS; Delis, Kaplan, & Kramer, 2001), working memory (digit span backwards, HAWIK-IV;Petermann & Petermann, 2008), and shifting (Trail Making Test, number-letter-switching, D-KEFS;Delis et al., 2001). As behavioral measures, mothers completed the Behavior Rating Inventory ofExecutive Function (BRIEF; Gioia, Isquith, Guy, & Kenworthy, 2000). Scales of interest were inhibit,working memory, and shift. Analyses of the cognitive aspects of executive functions revealed thatVPT/VLBW children performed significantly lower than controls in the shifting task but not in theworking memory and inhibition tasks. Analyses of behavioral aspects of executive functions revealedthat VPT/VLBW children displayed more problems than the controls in working memory in every-day life but not in inhibition and shifting. No sex differences could be detected either in cognitive orbehavioral aspects of executive functions. To conclude, cognitive and behavioral measures of execu-tive functions were not congruent in VPT/VLBW children. In clinical practice, the combination ofcognitive and behavioral instruments is required to disclose children’s executive difficulties.

Keywords: Children born very preterm; Executive functions; Inhibition; Working memory; Shifting;Behavior Rating Inventory of Executive Function.

Executive functions (EF) refer to multiple cognitive processes that contribute to humanhigher order abilities, such as purposeful and future-orientated behavior (Lezak, 1995).Miyake and colleagues (2000) described three core executive processes in young adults,

We thank the Swiss National Neonatal Follow Up Group for their collaboration. The research was fundedby the Swiss National Science Foundation (PZ00P1_126309).

This manuscript has not been published or simultaneously submitted elsewhere. The submission forpublication has been approved by all of the authors and by the institution where the work was carried out.

Address correspondence to Barbara Ritter, Children’s University Hospital, Division of Neuropaediatrics,Development and Rehabilitation, Inselspital, 3010 Bern, Switzerland. E-mail: barbara.ritter@insel.ch

© 2013 Taylor & Francis

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namely inhibition, working memory (WM), and shifting, which were correlated butstill dissociable and contributed to the execution of more complex executive skills,such as reasoning and problem solving. Some studies provide evidence of Miyake’sframework in normally developing children (Hughes, 1998; Lehto, Juujärvi, Kooistra,& Pulkkinen, 2003). Between the ages of 8 to 12 years, inhibition, WM, and shiftingdemonstrate a spurt of development, each reaching an adult-like level of performanceaccording to different timetables (Brocki & Bohlin, 2004; Lehto et al., 2003). Inhibitionseems to be the first function to level off, whereas WM and shifting mature intoadolescence (Lehto et al., 2003). Some theoretical frameworks assume that adequateinhibition is a precondition for other cognitive functions to emerge (Diamond, 1991).Furthermore, shifting is considered to be the last function to mature because it relieson both inhibition skills and WM capacity (Best & Miller, 2010). When performing ashifting task, the child has to inhibit the irrelevant set and to monitor simultaneouslywhether or not the shifting rules are being observed. Impairments in inhibition, WM,and shifting in school-aged children are associated with lower academic performancesin mathematics (Bull & Scerif, 2001) and reading and writing skills (Altemeier, Jones,Abbott, & Berninger, 2006). Some studies reported that typically developing girls aged8 to 12 years outperformed their male peers in inhibition, WM, or shifting (Overman,2004; Vuontela et al., 2003), whereas other studies did not establish sex differences(Brocki & Bohlin, 2004). In general, sex differences in EF tests are commonly small(Röthlisberger, Neuenschwander, Michel, & Roebers, 2010) and seem to be more evi-dent in children below the age of 8 years compared to older children (Vuontela et al.,2003).

The emergence of executive skills has been linked to the maturation of the prefrontalcortex (Casey, Giedd, & Thomas, 2000). A peak in grey matter maturation in the prefrontalcortex occurs at the age of 11 in girls and 12 in boys (Giedd et al., 1999), followed by aplateau of growth after puberty and a decline throughout adolescence (Thompson et al.,2000). In contrast, white matter volume increases steadily (Sowell et al., 1999). Together,both grey and white matter maturation parallels the increase of functional specialization ofEF during this phase of development (P. Anderson, 2002).

Children born very preterm (<32 weeks of gestation; VPT) and/or at very low birthweight (<1500 g birth weight; VLBW) usually perform lower in tests of inhibition, WM,and shifting than same-aged term-born controls (Aarnoudse-Moens, Smidts, Oosterlaan,Duivenvoorden, & Weisglas-Kuperus, 2009; P. J. Anderson & Doyle, 2004). Impairmentsof EF in VPT/VLBW children are related to severe neonatal complications (e.g., hemor-rhage, periventricular leukomalacia), with children having many complications being moreimpaired (Katz et al., 1996; Woodward, Edgin, Thompson, & Inder, 2005). In the age rangeof 8 to 12 years, some studies reported that preterm-born boys display more executive prob-lems than preterm-born girls (Aarnoudse-Moens, Duivenvoorden, Weisglas-Kuperus, VanGoudoever, & Oosterlaan, 2011), whereas other studies did not find any sex differences(Aarnoudse-Moens et al., 2009).

However, it is questionable if cognitive measures of executive skills fully representthe children’s behavioral difficulties in inhibition, WM, and shifting in daily situations(i.e., ecological validity). Ecological validity is defined as the relation between the cog-nitive performance in neuropsychological tests and the respective behavioral performancein the real-world context (Sbordone, 1996). Cognitive aspects of EF are regularly mea-sured by standardized neuropsychological tests, which are typically administered in aone-to-one setting while sitting in a quiet room, with the examiner regulating the child’s

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EF IN CHILDREN BORN VERY PRETERM 3

attention and responses. The standardization of the neuropsychological testing ensures thatthe conditions of administration are equivalent for each child, thereby enhancing the reli-ability and the internal validity of the test results. Yet, standardizing testing conditionsmay create an “artificial environment,” which might reduce the ecological validity of theperformed tests (Gioia & Isquith, 2004). In contrast to neuropsychological tests, every-day situations are often characterized by the attendance of several people, the presence ofmultiple distractive stimuli, and the demand of affective regulation, therefore possibly set-ting different executive demands for the child compared to laboratory settings. On the onehand, cognitive measures of EF may underestimate the child’s executive problems in real-world situations due to the quiet and structured setting of assessment. On the other hand,cognitive measures of EF may overestimate the child’s executive difficulties in daily lifebecause they neglect that the child may have developed compensatory strategies (Gioia& Isquith, 2004). The Behavior Rating Inventory of Executive Function (BRIEF; Gioiaet al., 2000) was developed to assess behavioral aspects of EF in children and adolescentsand has been demonstrated to sensitively detect executive difficulties occurring in every-day situations (e.g., V. A. Anderson, Anderson, Northam, Jacobs, & Mikiewicz, 2002).Recently, the BRIEF was translated and normed for German-speaking children (Drechsler& Steinhausen, in press). German-speaking term-born girls displayed better everyday exec-utive performance than boys in inhibition and shifting, but not in WM, with the sexdifferences declining with increasing age (Drechsler & Steinhausen, in press). Literaturereveals that VPT/VLBW girls and boys display greater problems in the behavioral aspectsof inhibition, WM, and shifting assessed by the BRIEF than same-aged control children (P.Anderson et al., 2011; P. J. Anderson & Doyle, 2004). However, the cognitive aspects ofEF do not necessarily correspond to the behavioral aspects of EF in everyday life (Gioia,Isquith, Retzlaff, & Espy, 2002). For example, children with traumatic brain injury candisplay average EF performance in the test situation and, according to their parents, stillexhibit deficits in everyday EF performance (Vriezen & Pigott, 2002).

The present study investigated whether there were differences between cognitiveand behavioral aspects of inhibition, WM, and shifting in VPT/VLBW children aged 8 to12 years compared with same-aged term-born controls. Special attention was given to sexdifferences. Based on the literature (e.g., Aarnoudse-Moens et al., 2009; P. J. Anderson &Doyle, 2004), it was hypothesized that VPT/VLBW children performed lower in all cogni-tive and behavioral aspects of EF than controls, with girls performing better than their malepeers. Furthermore, it was analyzed whether cognitive and behavioral aspects of EF relatedto each other and loaded on a common factor. The hypotheses were tested on a sample ofVPT/VLBW children with no or mild neonatal cerebral lesions and no or mild neurode-velopmental impairment, as these children represent the majority of the very preterm-bornpopulation (70%; Rüegger, Hegglin, Adams, & Bucher, 2012).

METHODS

This study reports on a subset of data from the NEMO (NEuropsychology andmeMOry) research project at the Children’s University Hospital in Bern, Switzerland.The NEMO project examines cognitive development in VPT/VLBW children. The studyprotocol was approved by the ethics committee of the Children’s University Hospital inBern. All children and caregivers provided informed written consent prior to participation,consistent with the Code of Ethics of the World Medical Association (Declaration ofHelsinki).

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Participants

Preterm Sample. The medical records of all surviving VPT/VLBW children(<32 weeks gestational age and/or <1500 g birth weight) born in the cohort of 1998 to2003 at the Children’s University Hospital in Bern, Switzerland, were reviewed. Inclusioncriteria were (a) aged between 8 and 12 years, (b) no or mild neonatal cerebral lesions(maximal hemorrhage grade II), (c) no or mild periventricular leukomalacia (maximalgrade II), (d) no chronic illness potentially influencing development (e.g., birth deformity,congenital heart defect, cerebral palsy, or epilepsy), (e) no postnatal occurring medicalproblems potentially influencing development (e.g., meningitis, encephalopathy, or trau-matic brain injury), (f) no pervasive developmental disorders (e.g., autism), (g) IQ > 85 inthe neuropsychological assessment, and (h) normal or corrected-to-normal vision and hear-ing. According to their available medical records, 247 children (92.5% of the screenedsample) fulfilled the inclusion criteria. They were contacted by a letter that included aninformation booklet for parents and children. Seventy-five children (29.1%) agreed toenter the study and completed the neuropsychological assessment, but 3 children had tobe excluded because of an IQ < 85 (n = 2; 2.7%) or refusal during assessment (n = 1;1.3%). Out of the remaining 72 children, a sample of girls and a sample of boys wererandomly selected as being comparable for age at assessment, maternal socioeconomicstatus (SES), IQ, gestational age (GA), and birth weight. Finally, 26 girls and 26 boys wereincluded in the analyses.

Control Sample. Healthy term-born children (>37 weeks of gestational age and>2500 g birth weight) were recruited with announcements on notice boards in the hospitaland local schools. Inclusion criteria were (a) aged between 8 and 12 years, (b) no chronicillness potentially influencing development (e.g., birth deformity, congenital heart defect,cerebral palsy, or epilepsy), (c) no medical problems potentially influencing development(e.g., meningitis, encephalopathy, or traumatic brain injury), (c) no pervasive develop-mental disorders (e.g., autism), and (d) normal or corrected-to-normal vision and hearing.Fifty-three children completed the neuropsychological assessment, but 3 (5.7%) had to beexcluded owing to attention deficit/hyperactivity disorder (n = 2; 3.8%) and refusal duringassessment (n = 1; 1.9%). Out of the remaining 50 children, a sample of girls and a sampleof boys were randomly selected as being comparable for age at assessment, maternal SES,and IQ. Finally, 18 girls and 18 boys were included in the analyses.

Instruments

To assess the cognitive aspects of inhibition, WM, and shifting, commonly usedand standardized clinical neuropsychological instruments were used. The performance wasexpressed as scaled score, with a high score indicating good EF performance. Impairmentwas defined as scaled score <7.

Inhibition was assessed using the first (color-naming task) and third conditions(interference task) of the D-KEFS’ Color-Word Interference Test (Delis-Kaplan ExecutiveFunction System, D-KEFS; Delis et al., 2001). In the color-naming task, the child wasasked to name color patches as fast as possible. In this condition, there is no inhibitory load.In the interference task, the child had to name the ink colors of words that are printed in anincongruent ink. This condition exhibits a high inhibitory load. The measure of inhibitionwas calculated by means of the difference between the color-naming and interference tasks.

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EF IN CHILDREN BORN VERY PRETERM 5

Working memory was measured using the digit span backward task of the Germanversion of the Wechsler intelligence scale for children (HAWIK-IV; Petermann &Petermann, 2008). The variable of interest was the maximum backward span attained.

Shifting was assessed using the fourth condition of the D-KEFS’ Trail Making Test(number-letter-switching; D-KEFS; Delis et al., 2001). The child was asked to connectnumbers (1 to 16) and letters (A to P) by switching between connecting numbers andletters in the correct order as fast as possible (i.e., 1-A-2-B-3-C, etc.). To control forbasic processing speed, condition two of the Trail Making Test (number sequencing) wasadministered.

General intelligence was measured using the short form of the German version ofthe Wechsler intelligence scale for children (HAWIK-IV; Petermann & Petermann, 2008;short form: Crawford, Anderson, Rankin, & MacDonald, 2010). Full-scale IQ and indexscores, such as verbal comprehension, were calculated from seven subtests of the originalHAWIK-IV (block design, similarities, digit span, coding, vocabulary, matrix reasoning,and symbol search; Crawford et al., 2010).

Socioeconomic status (SES) was defined as the mother’s education level at the timeof the neuropsychological assessment (no graduation = 1, college = 2, college of highereducation = 3, university degree = 4).

Information about the gestational age (GA) was collected from the children’s neona-tal medical records. It was measured in weeks and days based on the date of the lastmenstrual period and a prenatal ultrasound scan.

To assess the behavioral aspects of EF in everyday life, mothers completed theGerman parent version of the Behavior Rating Inventory of Executive Function (BRIEF;Drechsler & Steinhausen, in press), sitting alone in a quiet environment, while theneuropsychological assessment of the child took place. Variables of interest were the threescales inhibit, WM, and shift, because these scales are the behavioral counterparts of thecognitive tests. Raw scores were transformed into age-corrected T-scores (Drechsler &Steinhausen, in press), with a high score indicating poor EF performance in everyday life.Impairment was defined as a T-score > 60.

Procedure

After obtaining written consent from the caregivers, the participants were contactedby telephone to set a date for the neuropsychological assessment. Children were testedindividually by a trained neuropsychologist (R. E. and B. R.). Regular breaks were offered.

Statistical Analyses

In order to investigate whether or not the control sample and the VPT/VLBWsample were comparable by age at assessment, IQ, and maternal SES, two-tailed non-paired t-tests were calculated. Likewise, the comparability of girls and boys in the controland in the VPT/VLBW sample, in regard to age at assessment, IQ, maternal SES, and,in the VPT/VLBW sample, GA and birth weight, was tested using two-tailed nonpairedt-tests. Aiming to detect differences in cognitive and behavioral EF performance betweenVPT/VLBW children and controls (factor: group) and between girls and boys (factor: sex),two-way analyses of variance (ANOVA; Group x Sex) were conducted for cognitive andbehavioral measures of EF. The effect sizes of the mean differences were calculated usingCohen’s d with pooled standard deviation (Cohen, 1988). Pearson’s chi-squared tests were

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conducted to discover if frequencies of impairment in cognitive and behavioral aspectsof EF were different in VPT/VLBW children and controls. To establish the relationshipsbetween the cognitive measures and the behavioral measures of EF, one-tailed Pearson’scorrelations were calculated. To explore the factor structure of both cognitive and behav-ioral measures of EF, the standardized (z-transformed) dependent variables were enteredinto a factor analysis using principal component analysis with Varimax rotation. All sta-tistical analyses were performed using the Statistical Package for Social Sciences softwarefor Windows, version 17 (SPSS, Chicago, Illinois).

RESULTS

Descriptive Data

Table 1 shows the descriptive data of the control sample and the VPT/VLBWsample. Controls and the VPT/VLBW sample had an IQ mean within the normal range.Statistical analyses revealed that controls and VPT/VLBW children were comparable byage at assessment, t(86) = 0.09, p = .92, but not in terms of maternal SES, t(86) = 4.12,p < .01, and IQ, t(86) = 4.20, p < .01, with controls having a significant higher IQ meanand better educated mothers than VPT/VLBW children.

Table 2 reports the descriptive data of the girls and boys in the control and theVPT/VLBW sample. In the control sample, girls and boys were equal with respect toage at assessment, t(34) = −0.30, p = .77, maternal SES, t(34) = 0.01, p = .99, andIQ, t(34) = 1.39, p = .17. In the VPT/VLBW sample, girls and boys were equivalentin terms of age at assessment, t(50) = −1.05, p = .30, maternal SES, t(50) = 0.44,p = .66, IQ, t(50) = 0.82, p = .42, gestational age, t(50) = 1.01, p = .31, and birth weight,t(50) = −0.97, p = .34.

Cognitive Aspects of Executive Functions

Table 3 shows the results of the two-way ANOVAs (Group x Sex) of the cogni-tive measures of EF. Controls and the VPT/VLBW sample had mean test performanceswithin the normal range. Regarding inhibition performance, there was no effect of group,F(1, 82) = 1.35, MSE = 5.55, p = .25, or sex, F(1, 82) = 0.20, MSE = 5.55, p = .66, and nointeraction, F(1, 82) = 1.24, MSE = 5.55, p = .27. Results indicate that term- and preterm-born girls and boys performed similarly in the inhibition task. Pearson’s chi-squared test

Table 1 Descriptive Statistics of the Control Sample and the VPT/VLBW Sample.

Control sample (n = 36) VPT/VLBW sample (n = 52) Statistics

Variable M SD SE Min Max M SD SE Min Max T df p

Age at assessment 10.09 1.38 0.23 8.12 12.90 10.05 1.41 0.20 8.03 12.97 0.09 86 .92Maternal SES1 3.03 0.89 0.15 2 4 2.39 0.62 0.09 2 4 4.12 86 .00∗∗IQ2 109.28 7.77 1.29 92 125 101.17 10.34 1.43 85 122 4.20 86 .00∗∗

1Scale of SES: 1 = no graduation, 2 = college, 3 = college of higher education, 4 = university degree.2HAWIK-IV, short form (M = 100, SD = 15). M = Mean; SD = Standard Deviation; SE = Standard Error of

the mean; T = value of t test for independent groups; df = degrees of freedom; p = level of significance.∗∗p < .01.

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EF IN CHILDREN BORN VERY PRETERM 7

Table 2 Descriptive Statistics of Male and Female VPT/VLBW Children and Controls.

Girls Boys Statistics

Variable M SD SE M SD SE T df p

Control sample Age at assessment 10.02 1.30 0.31 10.15 1.50 0.35 −0.30 34 .77Maternal SES1 3.06 0.94 0.22 3.06 .88 0.21 0.01 34 .99IQ2 111.06 6.50 1.53 107.50 8.67 2.04 1.39 34 .17

VPT/VLBW sample Age at assessment 9.86 1.26 0.25 10.26 1.54 0.30 −1.05 50 .30Maternal SES1 2.39 0.63 0.13 2.31 .62 0.12 0.44 50 .66IQ2 102.35 10.83 2.12 100.00 9.98 1.94 0.82 50 .42Gestational Age3 30.13 2.15 0.42 29.51 2.24 0.44 1.01 50 .31Birth weight4 1179.04 277.99 54.52 1272.88 409.89 80.39 −0.97 50 .34

Note. The girls and boys of the control sample are comparable with respect to age at assessment, maternalSES, and IQ . The girls and boys in the VPT/VLBW sample are comparable with respect to age at assessment,maternal SES, IQ, gestational age, and birth weight.

1Scale of SES: 1 = no graduation, 2 = college, 3 = college of higher education, 4 = university degree.2HAWIK-IV, short form (M = 100, SD = 15).3Gestational age is reported in weeks and days.4Birth weight is reported in gram. M = Mean; SD = Standard Deviation; SE = Standard Error of the mean;

T = t value of t-test for independent groups; df = degrees of freedom; p = level of significance.

Table 3 Cognitive Aspects of Executive Functions.

Analysis ofVariance Effect Size

Variable Effect Category M SD F value p MD Cohen’s d

Inhibition Group Control 10.00 2.07Preterm 9.41 2.52 1.35 .25 0.59 .26

Sex Girls 9.82 2.15Boys 9.48 2.57 0.20 .66 0.34 .14

Group x Sex 1.24 .27

Working Memory Group Control 10.21 1.48Preterm 9.79 1.19 2.62 .12 0.42 .31

Sex Girls 10.05 1.42Boys 9.86 1.48 0.44 .51 0.19 .31

Group x Sex 0.08 .78

Shifting Group Control 11.23 2.20Preterm 8.75 3.50 13.64 .00∗∗ 2.48 .85

Sex Girls 9.89 3.32Boys 9.62 3.24 0.45 .50 0.27 .08

Group x Sex 2.38 .13

Note. Analyses of two-way ANOVAs and the Effect sizes (Cohen’s d) of the neuropsychological tasks arereported. M = Mean; SD = Standard Deviation; F value = test statistic of the ANOVA; MD = Mean differ-ence between controls and preterms / girls and boys; Cohen’s d = Effect size with pooled standard deviations.∗∗ p < .01.

was not significant, χ2 = 2.23, p = .14, demonstrating that there were similar frequenciesof cognitive inhibition impairment in VPT/VLBW children (n = 6, 11.4%) and controls(n = 1, 2.8%). Regarding WM performance, there was no effect of group, F(1, 82) = 2.62,MSE = 6.39, p = .12, or sex, F(1, 82) = 0.44, MSE = 6.39, p = .51, and no interaction,

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F(1, 82) = 0.08, MSE = 6.39, p = .78. Results reveal that term- and preterm-born girls andboys displayed equal WM performance. None of the VPT/VLBW children had a scaledscore < 7; therefore, no Pearson’s chi-squared test was conducted. Regarding shifting per-formance, there was a significant effect of group, F(1, 82) = 13.64, MSE = 9.18, p < .01,but there was no effect of sex, F(1, 82) = 0.45, MSE = 9.18, p = .50, and no interac-tion, F(1, 82) = 2.38, MSE = 9.18, p = .13. The group difference remained significantwhen controlled for processing speed, F(1, 82) = 6.22, MSE = 5.71, p < .05, maternalSES, F(1, 82) = 8.69, MSE = 9.22, p < .01, and verbal comprehension, F(1, 82) = 5.66,MSE = 9.17, p < .05, indicating that VPT/VLBW children performed lower than controlsin the shifting task, independent of processing speed, maternal SES, and verbal comprehen-sion. Cohen’s d revealed that the mean difference between the control and the VPT/VLBWsample in the shifting task was large (d = 0.85). Pearson’s chi-squared test was significant,χ2 = 3.92, p < .05, demonstrating that there were higher frequencies of cognitive shift-ing impairment in VPT/VLBW children (n = 11, 20.9%) than in controls (n = 2, 5.6%).To summarize, VPT/VLBW children performed significantly lower in the shifting task andhad significantly higher frequencies of shifting impairment than controls, with Cohen’s dindicating that the mean difference was substantial. No differences between VPT/VLBWchildren and controls were found in inhibition and WM.

Behavioral Aspects of Executive Functions

Table 4 reports the results of the two-way ANOVAs (Group x Sex) of the behavioralmeasures of EF. Controls and the VPT/VLBW sample had T-score means within the nor-mal range. Regarding the inhibition scale, there was no effect of group, F(1, 82) = 3.70,MSE = 77.15, p = .06, or sex, F(1, 82) = 0.38, MSE = 77.15, p = .54, and no interaction,

Table 4 Behavioral Aspects of Executive Functions.

Analysis ofVariance Effect Size

Scale Effect Category M SD F value p MD Cohen’s d

Inhibit Group Control 44.97 6.96Preterm 48.63 9.89 3.70 .06 −3.66 −0.43

Sex Girls 46.32 9.03Boys 47.95 8.89 0.38 .54 −1.63 −0.18

Group x Sex 1.81 .18

Working Memory Group Control 49.06 7.03Preterm 52.15 10.38 9.41 .00∗∗ −3.09 −0.35

Sex Girls 48.34 9.55Boys 50.98 9.57 1.65 .20 −2.64 −0.28

Group x Sex 0.05 .82

Shift Group Control 49.33 7.83Preterm 51.06 12.75 3.84 .05 −1.73 −0.16

Sex Girls 48.70 11.42Boys 49.55 11.09 0.06 .80 −0.85 −0.08

Group x Sex 0.28 .60

Note. Analyses of two-way ANOVAs and the Effect sizes (Cohen’s d) of the BRIEF scales are reported.M = Mean; SD = Standard Deviation; F value = test statistic of the ANOVA; MD = Mean difference betweencontrols and preterm / girls and boys; Cohen’s d = Effect size with pooled standard deviations. ∗∗p < .01.

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F(1, 82)= 1.81, MSE = 77.15, p = .18. Results point out that term- and preterm-born girlsand boys displayed equal inhibition skills in everyday life. Pearson’s chi-squared test wasnot significant, χ2 = 0.074, p = .79, demonstrating that there were similar frequenciesof behavioral inhibition impairment in VPT/VLBW children (n = 2, 3.8%) and controls(n = 1, 2.8%). Regarding the WM scale, there was a significant effect of group,F(1, 82) = 9.41, MSE = 84.12, p < .01, but there was no effect of sex, F(1, 82) = 1.65,MSE = 84.12, p = .20, and no interaction, F(1, 82) = 0.05, MSE = 84.12, p = .82.Results indicate that VPT/VLBW children displayed worse behavioral WM performancein everyday life than controls. The group difference remained significant when controlledfor maternal SES, F(1, 82) = 4.96, MSE = 123.42, p < .05, and verbal comprehension,F(1, 82) = 4.89, MSE = 82.70, p < .05, indicating that VPT/VLBW children displayedworse WM performance in everyday life independent of maternal SES and verbal com-prehension. Cohen’s d revealed that the mean difference between the control and theVPT/VLBW sample in the WM task was small (d = −0.35). Pearson’s chi-squared testwas significant, χ2 = 6.10, p < .05, demonstrating that there were higher frequencies ofbehavioral WM impairment in VPT/VLBW children (n = 11, 20.9%) than in controls(n = 1, 2.8%). Regarding the shift scale, there was no effect of group, F(1, 82) = 3.84,MSE = 123.60, p = .05, or sex, F(1, 82) = 0.06, MSE = 123.60, p = .80, and no interac-tion, F(1, 82) = 0.28, MSE = 123.60, p = .60. Pearson’s chi-squared test was significant,χ2 = 4.44, p < .05, demonstrating that there were higher frequencies of behavioral shiftingimpairment in VPT/VLBW children (n = 11, 20.9%) than in controls (n = 2, 5.6%).

Of all VPT/VLB children with an impairment in WM and/or shifting (T-score >

60), 3 children (15.8%) had impairments in both WM and shifting; the remaining childrenhad impairments in either WM (n = 8, 42.1%) or shifting (n = 8, 42.1%). To summa-rize, parents reported more problems in VPT/VLBW children than controls in workingmemory in everyday life, but not in inhibition and shifting, with Cohen’s d indicating thatthe mean difference was small. However, there were higher frequencies of impairment inVPT/VLBW children than in controls in WM and shifting, but not in inhibition.

Pearson’s Correlation and Factor Analysis

Table 5 presents Pearson’s correlation coefficients between the cognitive and behav-ioral aspects of EF of all children (n = 88). The cognitive measure of inhibition did not

Table 5 Pearson’s Correlation Between Cognitive and Behavioral Aspects of Executive Functions with allChildren.

Cognitive Measures

Behavioral measures Inhibition2 Working Memory3 Shifting4

Inhibit1 .11 −.03 −.03Working Memory1 −.08 −.29∗∗ −.34∗∗Shift1 .12 −.06 −.14

Note. One-tailed Pearson’s correlation coefficients are presented.1Scale of the BRIEF.2Color-Word Interference Test, D-KEFS.3maximum digit span backwards, HAWIK-IV.4Trail Making Test, number-letter-sequencing, D-KEFS.**p < .01.

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correlate with behavioral measures of EF (inhibit: r = .11, p = .16; WM: r = −.08, p = .23;shift: r = .12, p = .13). The cognitive measure of WM did not correlate with the behav-ioral measure of inhibition, r = −.03, p = .40, and the behavioral measure of shifting,r = −.06, p = .31, but displayed a significant association with the behavioral measureof WM, r = −.29, p < .01, indicating that children with higher cognitive WM capacitydisplayed better behavioral WM performance in everyday life. The cognitive measure ofshifting did not correlate with the behavioral measure of inhibition, r = −.03, p = .40,and the behavioral measure of shifting, r = −.14, p = .11, but revealed a significantassociation with the behavioral measure of WM, r = −.34, p < .01, indicating that chil-dren with better cognitive shifting skills displayed better behavioral WM performance ineveryday life.

In the factor analysis of all six variables (cognitive and behavioral), three factorswere extracted (Eigenvalues 2.11, 1.20, and 1.10, total variance 73%). The cognitive mea-sures WM and shifting loaded on one factor (WM: h2 = 0.77, loading = 0.59; shifting:h2 = 0.62, loading = 0.77), whereas the cognitive inhibition measure loaded on a separatefactor, h2 = 0.77, loading = 0.83. All behavioral measures of EF loaded on a third factor(Inhibit: h2 = 0.77, loading = 0.87; WM: h2 = 0.75, loading = 0.83; shift: h2 = 0.70,loading = 0.61).

DISCUSSION

The present study investigated whether there were differences between cognitive andbehavioral aspects of EF in VPT/VLBW children aged 8 to 12 years compared with same-aged term-born controls. It was hypothesized that VPT/VLBW children performed lowerin all cognitive and behavioral aspects of EF than controls, with girls performing better thantheir male peers. Furthermore, it was analyzed whether cognitive and behavioral aspects ofEF related to each other and loaded on a common factor.

Analyses of cognitive aspects of EF revealed that VPT/VLBW children performedsignificantly lower in the shifting task than the same-aged controls, independent of globalprocessing speed, maternal SES, and verbal comprehension, but not in the inhibition andWM tasks. Frequencies of impairment were significantly higher in VPT/VLBW childrenthan in controls for shifting, but not for inhibition and WM. These findings were contraryto the literature reporting that VPT/VLBW children aged 8 to 12 years display difficul-ties across all three EFs compared with controls (e.g., Aarnoudse-Moens et al., 2009). Yet,low performance in EF tasks is often related to severe neonatal complications (Katz et al.,1996; Woodward et al., 2005), making comparisons among studies on VPT/VLBW pop-ulations difficult. However, shifting is thought to be the most complex function amongthe three core executive skills, presumably because successful shifting taps both inhibitionand WM resources (Best & Miller, 2010), and to display the most prolonged timetableof maturation among the three EFs, reaching adult-like performance not until adolescence(Davidson, Amso, Anderson, & Diamond, 2006). The results of the present study indicatethat VPT/VLBW children in the age range of 8 to 12 years only performed lower thancontrols in the most complex and latest maturing EF, namely shifting. This possibly pointstowards either a deficiency of VPT/VLBW children in EF as a function of complexityor towards a delay of EF maturation in VPT/VLBW children. In the factor analysis ofcognitive and behavioral aspects, the WM and shifting tasks loaded on a common factor,whereas the inhibition task loaded on a separate one. This separation might be the result ofthe different timetables of maturation, with inhibition already being more mature than WM

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and shifting. Contrary to our hypotheses, no sex differences and no interactions betweengroup and sex were evident, indicating that preterm- and term-born girls and boys per-formed similarly in all cognitive aspects of EF. According to the literature, sex differencesin executive tasks are more apparent in younger children (6–8 years) than in older children(11–13 years; Vuontela et al., 2003) and are, if observable, commonly small (Röthlisbergeret al., 2010). In relation to the present study, it might be that the 8- to 12-year-old preterm-and term-born girls and boys displayed equal task performance because the time windowin which girls may surpass boys has already passed. However, future studies should inves-tigate the influence of gender on cognitive EF performances with larger samples and largerage ranges.

Analyses of behavioral aspects of EF revealed that, according to their mothers,VPT/VLBW children displayed significantly worse performance in WM in everyday lifethan the controls, independent of maternal SES, and verbal comprehension, but not in inhi-bition and shifting. In contrast, the frequencies of impairment were significantly higher inVPT/VLBW children than in controls for both WM and shifting but not for inhibition.Analyses revealed that 15.8% of all VPT/VLBW children with scores exceeding the nor-mal range had impairments in both behavioral WM and shifting performance, whereasthe others had impairment in either WM (42.1%) or shifting (42.1%). This result indicatesthat VPT/VLBW children had “specific” impairment rather than “global” impairment. Thepresent finding is in line with the current literature, reporting that VPT/VLBW childrenperform lower in WM and display higher frequencies of impairment in both WM andshifting (P. Anderson et al., 2011; P. J. Anderson & Doyle, 2004). Regarding the inhibitionscale, VPT/VLBW children are reported in some studies to display more inhibition prob-lems than their term-born counterparts in everyday life (P. Anderson et al., 2011), whereasthey were rated similar to controls in other studies (e.g., P. J. Anderson & Doyle, 2004).In relation to the present findings, it seems that inhibition was not the major problem in theVPT/VLBW children’s daily life. Overall, no sex differences and no interactions betweengroup and sex were detected in the behavioral aspects of EF. This finding contradicts theliterature, where girls performed better in everyday life than boys at least in inhibition andshifting (Drechsler & Steinhausen, in press). However, because sex differences in behav-ioral aspects of EF are most evident in younger children (Drechsler & Steinhausen, inpress), the reported sample of children between 8 and 12 years might lie beyond the agewindow where performance differences between girls and boys predominate.

In the present study, there were differences between cognitive and behavioral aspectsof EF (Vriezen & Pigott, 2002). VPT/VLBW children displayed significantly worsecognitive shifting performance and worse behavioral WM performance than controls.Accordingly, shifting problems became more evident in the neuropsychological assess-ment, whereas WM problems were more clearly observed by mothers in everyday life.The incongruity between cognitive and behavioral aspects of EF may arise from differ-ent sources (V. A. Anderson et al., 2002; Gioia & Isquith, 2004). On the one hand, theincongruity might reflect the difference in the measurement of EF, performance-basedversus parent’s report. It is unclear if the cognitive tasks of EF and the questions forparents about the behavioral manifestation of EF in everyday life are able to assess theexact same function (i.e., content validity) (Franzen & Wilhelm, 1996). In general, thetests should mirror the executive demands of everyday situations. Relating to the presentstudy, one can consider that, for example, the digit-span-backwards task did not tap thesame aspect as the BRIEF items about everyday WM performance. Yet, the cognitive WM

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12 B. C. RITTER ET AL.

scale correlated exclusively with the behavioral WM scale, indicating that higher cogni-tive WM performance was associated with better behavioral WM performance. This resultindicates that, the cognitive and behavioral measures of WM shared common variance,which provides an indication of ecological validity.

On the other hand, the incongruity between cognitive and behavioral aspects of EFmight arise from everyday situations setting different executive demands for the childcompared to laboratory settings. Everyday situations often require emotional regulation,social decision making and hold more sensory load to distract the child, probably makingexecutive problems more evident in everyday settings than in test situations. Concordantly,the frequency of impairment of VPT/VLBW children was higher in the behavioral perfor-mance of EF (WM and shifting) than in the cognitive performance of EF (only shifting).Another aspect is that mastering the executive demands of real-world situations is sug-gested to require the coordination of inhibition, WM, and shifting rather than the isolatedfunctions (Rabbitt, 1997). In the factor analysis of cognitive and behavioral aspects,the three BRIEF scales—inhibit, WM, and shift—loaded on a single factor. This resultcan either illustrate the interplay of executive skills in everyday situations or the globalapproach of the BRIEF to assess the everyday executive skills, therefore reducing thepossibility of identifying isolated EF domains (Gioia et al., 2002). One could argue thatquestionnaires are less suited to assessing executive domains separately than cognitivetests. However, in the present study, VPT/VLBW children had specific rather than globalimpairment in WM and shifting, which points to a distinctness of the BRIEF scales.

Finally, the discrepancy between cognitive and behavioral measures of EF couldbe interpreted as the difference between “cold” and “hot” aspects of EF (Zelazo, Qu, &Muller, 2004). Cold EF are described as a purely cognitive processes that are requiredin abstract and decontextualized situations, such as in standardized neuropsychologicalassessments. In contrast, hot EF are considered to tap situations where emotional controlor affective decision making are needed, such as in the activities of daily living. Childrenwith poor hot EF are likely to act rather impulsively, chaotically, or apathetically. They maybe easily distracted, lose the plot while talking or listening and have difficulties organizing,planning, and monitoring activities, which may lead to poor interpersonal skills and diffi-culties in observing social rules (P. J. Anderson, 2008). One can speculate that, accordingto the present findings, VPT/VLBW children seemed to have more problems with the hotaspects of EF than the cold aspects of EF, given that they displayed higher frequencies ofimpairment in the behavioral measures than in the cognitive measures. Neurobiologically,there is evidence that cold and hot EF may have different neural underpinnings. Cold EFare suggested to relate to the dorsolateral prefrontal cortex, whereas hot EF are thought torely on orbitofrontal and ventral prefrontal regions, which are more closely wired to thelimbic system (Stuss & Anderson, 2004).

The generalizability of the present findings is limited in several respects. First, thecurrent article focused only on inhibition, WM, and shifting and not on all supposableexecutive domains (P. Anderson, 2002). Second, the controls had higher IQ mean andbetter educated mothers, therefore reflecting a high-functioning control group. However,the mean IQ of the control group was still within the normal range. Given the nonindepen-dence between EF and IQ due to construct overlap, it was not appropriate to control thegroup differences between VPT/VLBW children and controls in cognitive and behavioralEF for IQ (Dennis et al., 2009). Differences in IQ between preterm- and term-born childrenare often reported in the literature. For example, a meta-analysis by Bhutta, Cleves, Casey,

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Cradock, and Anand (2002) revealed that the average difference in IQ between preterm-and term-born school-aged children was 10.9 IQ points, with both populations usuallyhaving a mean IQ in the normal range. A third aspect relies on the cognitive assessmentof the EF. Inhibition, WM, and shifting were measured by means of a single assessmenttask instead of a variety of tasks. To establish differential relationships between the cogni-tive and behavioral aspects of EF, it is desirable to operationalize executive domains withseveral tasks in future studies. In terms of the BRIEF, only the mothers completed the ques-tionnaire. Because mothers and fathers may have different perceptions of their child (Gioiaet al., 2000), both parents should complete the questionnaire. Finally, the VPT/VLBWsample consisted only of children with no or minimal brain lesions and no or minimalneurodevelopmental impairment. The current findings are not comparable with those ofstudies on preterm-born children with higher frequencies of neonatal complications, whichare thought to have higher rates of cognitive dysfunction (Woodward et al., 2005). Yet,children with low frequencies of neonatal complications, such as the children reportedhere, represent the major subgroup of 70% of the Swiss VPT/VLBW population (Rüeggeret al., 2012).

In conclusion, cognitive and behavioral measures of executive functions were notcongruent in VPT/VLBW children. Overall, the cognitive aspects of EF revealed shiftingproblems in VPT/VLBW children, whereas the behavioral aspects revealed WM and shift-ing deficiencies in everyday life. No sex differences were evident. Given the importanceof inhibition, WM, and shifting for academic performance, the combination of cognitiveand behavioral instruments is required to disclose the VPT/VLBW children’s executivedifficulties in the clinical context (Gioia et al., 2000).

Original manuscript received September 4, 2012Revised manuscript accepted February 2, 2013

First published online March 4, 2013

REFERENCES

Aarnoudse-Moens, C. S., Duivenvoorden, H. J., Weisglas-Kuperus, N., Van Goudoever, J. B., &Oosterlaan, J. (2011). The profile of executive function in very preterm children at 4 to 12 years.Developmental Science & Child Neurology, 54, 247–253. doi: 10.1111/j.1469–8749.2011.04150.x

Aarnoudse-Moens, C. S., Smidts, D. P., Oosterlaan, J., Duivenvoorden, H. J., & Weisglas-Kuperus,N. (2009). Executive function in very preterm children at early school age. Journal of AbnormalChild Psychology, 37, 981–993. doi: 10.1007/s10802–009–9327-z

Altemeier, L., Jones, J., Abbott, R. D., & Berninger, V. W. (2006). Executive functions in becomingwriting readers and reading writers: Note taking and report writing in third and fifth graders.Developmental Neuropsychology, 29, 161–173. doi: 10.1207/s15326942dn2901_8

Anderson, P. (2002). Assessment and development of executive function (EF) during childhood.Child Neuropsychology, 8, 71–82. doi: 10.1076/chin.8.2.71.8724

Anderson, P. J. (2008). Towards a developmental model of executive function. In: V. Anderson, R.Jacobs, & P. J. Anderson (Eds.), Executive functions and the frontal lobes: A lifespan perspective(pp. 3–22). New York, NY: Psychology Press, Taylor & Francis.

Anderson, P., De Luca, C. R., Hutchinson, E., Spencer-Smith, M. M., Roberts, G., &Doyle, L. W. (2011). Attention problems in a representative sample of extremelypreterm/extremely low birth weight children. Developmental Neuropsychology, 36, 57–73. doi:10.1080/87565641.2011.540538

Dow

nloa

ded

by [

Uni

vers

itäts

bibl

ioth

ek B

ern]

, [B

arba

ra R

itter

] at

03:

24 2

6 M

arch

201

3

14 B. C. RITTER ET AL.

Anderson, P. J., & Doyle, L. W. (2004). Executive functioning in school-aged children who wereborn very preterm or with extremely low birth weights in the 1990s. Pediatrics, 114, 50–57.doi: 10.1542/peds.114.1.50

Anderson, V. A., Anderson, P., Northam, E., Jacobs, R., & Mikiewicz, O. (2002). Relationshipsbetween cognitive and behavioral measures of executive function in children with brain disease.Child Neuropsychology, 8, 231–240. doi: 10.1076/chin.8.4.231.13509

Best, J. R., & Miller P. H. (2010). A developmental perspective on executive function. ChildDevelopment, 81, 1641–1660. doi: 10.1111/j.1467–8624.2010.01499.x

Bhutta, A. T., Cleves, M. A., Casey, P. H., Cradock, M. M., & Anand, K. J. (2002). Cognitiveand behavioural outcomes of school-aged children who were born preterm: A meta-analysis.Journal of the American Medical Association, 14, 728–737. doi: 10.1001/jama.288.6.728

Brocki, K. C., & Bohlin, G. (2004). Executive functions in children aged 6 to 13: A dimensionaland developmental study. Developmental Neuropsychology, 26, 571–593. doi: 10.1207/

s15326942dn2602_3Bull, R., & Scerif, G. (2001). Executive functioning as a predictor of children’s mathematics ability:

Inhibition, switching, and working memory. Developmental Neuropsychology, 19, 273–293.doi: 10.1207/S15326942DN1903_3

Casey, B. J., Giedd, J. N., & Thomas, K. M. (2000). Structural and functional brain developmentand its relation to cognitive development. Biological Psychology, 54, 241–257. doi: 10.1016/

S0301–0511(00)00058–2Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ:

Lawrence Erlbaum.Crawford, J. R., Anderson, V., Rankin, P. M., & MacDonald, J. (2010). An index-based short-form

of the HAWIK-IV with accompanying analysis of the reliability and abnormality of differences.British Journal of Clinical Psychology, 49, 235–258. doi: 10.1348/014466509X455470

Davidson, M. C., Amso, D., Anderson, L. C., & Diamond, A. (2006). Development ofcognitive control and executive functions from 4 to 13 years: Evidence from manipula-tions of memory, inhibition, and task switching. Neuropsychologia, 44, 2037–2078. doi:10.1016/j.neuropsychologia.2006.02.006

Delis, D. C., Kaplan, E., & Kramer, J. (2001). Delis Kaplan executive function system. San Antonio,TX: The Psychological Corporation.

Dennis, M., Francis, D. J., Cirino, P. T., Schachar, R., Barnes, M. A., & Fletcher, J. M. (2009).Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of theInternational Neuropsychological Society, 15, 331–343. doi: 10.1017/S1355617709090481

Diamond, A. (1991). Frontal lobe involvement in cognitive changes during the first year of life.In K. R. Gibson & A. C. Petersen (Eds.), Brain maturation and cognitive development:Comparative and cross-cultural perspectives (pp. 127–180). New York, NY: de Gruyter.

Drechsler, R., & Steinhausen, H. C. (in press). BRIEF. Verhaltensinventar zur Beurteilung exekutiverFunktionen. Manual [BRIEF. A behavioral inventory to assess executive functions. Manual.].Bern, Switzerland: Huber.

Franzen, M. D., & Wilhelm, K. L. (1996). Conceptual foundations of ecological validity inneuropsychological assessment. In R. J. Sbordone & C. J. Long (Eds.), Ecological validity ofneuropsychological testing (pp. 91–11). Boca Raton, FL: St. Lucie.

Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., . . . Rapoport,J. L. (1999). Brain development during childhood and adolescence: A longitudinal MRI study.Nature Neuroscience, 2, 861–863. doi: 10.1038/13158

Gioia, G. A., & Isquith, P. K. (2004). Ecological assessment of executive function in traumatic braininjury. Developmental Neuropsychology, 25, 135–158. doi: 10.1207/s15326942dn2501&2_8

Gioia, G. A., Isquith, P. K., Guy, S. C., & Kenworthy, L. (2000). Behavior rating of executivefunction. Lutz, FL: Psychological Assessment Resources.

Gioia, G. A., Isquith, P. K., Retzlaff, P. D., & Espy, K. A. (2002). Confirmatory factor analysisof the Behavior Rating Inventory of Executive Function (BRIEF) in a clinical sample. ChildNeuropsychology, 8, 249–257. doi: 10.1076/chin.8.4.249.13513

Dow

nloa

ded

by [

Uni

vers

itäts

bibl

ioth

ek B

ern]

, [B

arba

ra R

itter

] at

03:

24 2

6 M

arch

201

3

EF IN CHILDREN BORN VERY PRETERM 15

Hughes, C. (1998). Executive function in preschoolers: Links with theory of mind and verbal ability.British Journal of Developmental Psychology, 16, 233–253. doi: 10.1111/j.2044–835X.1998.tb00921.x

Katz, K. S., Dubowitz, L. M. S., Henderson, S., Jongmans, M., Kay, G. G., Nolte, C. A. & deVries, L. (1996). Effect of cerebral lesions on continuous performance test responses of schoolage children born prematurely. Journal of Pediatric Psychology, 21, 841–855. doi: 10.1093/

jpepsy/21.6.841Lehto, J. E., Juujärvi, P., Kooistra, L., & Pulkkinen, L. (2003). Dimensions of executive function-

ing: Evidence from children. British Journal of Developmental Psychology, 21, 59–80. doi: 10.1348/026151003321164627

Lezak, M. (1995). Neuropsychological assessment (3rd ed.). New York, NY: Oxford UniversityPress.

Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., & Wager, T. D. (2000).The unity and diversity of executive functions and their contributions to complex “Frontal Lobe”tasks: A latent variable analysis. Cognitive Psychology, 41, 49–100. doi: 10.1006/cogp.1999.0734

Overman, W. H. (2004). Sex differences in early childhood, adolescence, and adulthood on cognitivetasks that rely on orbital prefrontal cortex. Brain and Cognition, 55, 134–147. doi: 10.1016/

S0278–2626(03)00279–3Petermann, F., & Petermann, U. (2008). Hamburg-Wechsler-Intelligenztest für Kinder - IV

(HAWIK-IV) [Hamburg-Wechsler intelligence scale for children, 4th edition.]. Bern,Switzerland: Huber.

Rabbitt, P. (1997). Introduction: Methodologies and models in the study of executive function.In P. Rabbitt (Ed.), Methodology of frontal executive function (pp. 1–38). East Sussex, UK:Psychology Press.

Röthlisberger, M., Neuenschwander, R., Michel, E., & Roebers, C. M. (2010). Exekutive Funktionen:Zugrundeliegende kognitive Prozesse und deren Korrelate bei Kindern im späten Vorschulalter[Executive functions: Underlying cognitive processes and their correlates in preschool children].Zeitschrift für Entwicklungspsychologie und Pädagogische Psychologie, 42, 99–110. doi:10.1026/0049–8637/a000010

Rüegger, C., Hegglin, M., Adams, M., & Bucher, U. (2012). Population based trends in mortality,morbidity and treatment for very preterm and very low birth weight infants over 12 years. BMCPediatrics, 12, 17. doi: 10.1186/1471–2431–12–17

Sbordone, R. J. (1996). Ecological validity: Some critical issues for the neuropsychologist. In R. J.Sbordone & C. J. Long (Eds.), Ecological validity of neuropsychological testing (pp. 91–112).Boca Raton, FL: St. Lucie.

Sowell, E. R., Thompson, P. M., Holmes, C. J., Batth, R., Jernigan, T. L., & Toga, A. W. (1999).Localizing age-related changes in brain structure between childhood and adolescence usingstatistical parametric mapping. NeuroImage, 6, 587–597. doi: 10.1006/nimg.1999.0436

Stuss, D., & Anderson, V. (2004). The frontal lobes and theory of mind: Developmental con-cepts from adult focal lesion research. Brain and Cognition, 55, 69–83. doi: 10.1016/

S0278–2626(03)00271–9Thompson, P. M., Giedd, J. N., Woods, R. P., MacDonald, D., Evans, A. C., & Toga, A. W. (2000).

Growth patterns in the developing brain detected by using continuum mechanical tensor maps.Nature, 404, 190–193. doi: 10.1038/35004593

Vriezen, E. R., & Pigott, S. E. (2002). The relationship between parental report on the BRIEFand performance-based measures of executive function in children with moderate to severetraumatic brain injury. Child Neuropsychology, 8, 296–303. doi: 10.1076/chin.8.4.296.13505

Vuontela, V., Steenari, M. R., Carlson, S., Koivisto, J., Fjallberg, M., & Aronen, E. T. (2003).Audiospatial and visuospatial working memory in 6–13 year old school children. Learning &Memory, 10, 74–81. doi: 10.1101/lm.53503

Dow

nloa

ded

by [

Uni

vers

itäts

bibl

ioth

ek B

ern]

, [B

arba

ra R

itter

] at

03:

24 2

6 M

arch

201

3

16 B. C. RITTER ET AL.

Woodward, L. J., Edgin, J. O., Thompson, D., & Inder, T. E. (2005). Object working memory deficitspredicted by early brain injury and development in the preterm infant. Brain, 128, 2578–2587.doi: 10.1093/brain/awh618

Zelazo, P. D., Qu, L., & Muller, U. (2004). Hot and cool aspects of executive function: Relationsin early development. In W. Schneider, R. Schumann-Hengsteler, & B. Sodian (Eds.), Youngchildren’s cognitive development: Interrelationships among executive functioning, workingmemory, verbal ability, and theory of mind (pp. 71–93). Mahwah, NJ: Lawrence Erlbaum.

Dow

nloa

ded

by [

Uni

vers

itäts

bibl

ioth

ek B

ern]

, [B

arba

ra R

itter

] at

03:

24 2

6 M

arch

201

3