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

Emerging executive skills in verypreterm children at 2 years correctedage: A composite assessmentTiziana Pozzettia, Alessandra Omettoa, Silvana Gangia, OdoardoPicciolinia, Gisella Presezzia, Laura Gardona, Silvia Pisonia, FabioMoscaa & Gian Marco Marzocchiba NICU, Fondazione IRCCS Ca’ Granda - Ospedale MaggiorePoliclinico, Università degli Studi di Milano, Milan, Italyb Department of Psychology, University of Milan-Bicocca, Milan,ItalyPublished online: 29 Jan 2013.

To cite this article: Tiziana Pozzetti, Alessandra Ometto, Silvana Gangi, Odoardo Picciolini,Gisella Presezzi, Laura Gardon, Silvia Pisoni, Fabio Mosca & Gian Marco Marzocchi (2014) Emergingexecutive skills in very preterm children at 2 years corrected age: A composite assessment, ChildNeuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence,20:2, 145-161, DOI: 10.1080/09297049.2012.762759

To link to this article: http://dx.doi.org/10.1080/09297049.2012.762759

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Child Neuropsychology, 2014Vol. 20, No. 2, 145–161, http://dx.doi.org/10.1080/09297049.2012.762759

Emerging executive skills in very preterm children

at 2 years corrected age: A composite assessment

Tiziana Pozzetti1 , Alessandra Ometto1, Silvana Gangi1,Odoardo Picciolini1 , Gisella Presezzi1, Laura Gardon1,Silvia Pisoni1, Fabio Mosca1, and Gian Marco Marzocchi2

1NICU, Fondazione IRCCS Ca’ Granda - Ospedale Maggiore Policlinico, Università degliStudi di Milano, Milan, Italy2Department of Psychology, University of Milan-Bicocca, Milan, Italy

Executive Function (EF) deficits have previously been identified in preterm children. However, onlyrecently have emerging executive functions been studied in preschool children who were born pretermwithout major brain damage. Our study provides a broad assessment of EFs in 72 extremely pretermbirths (gestational age < 34 weeks and birth weight < 2500 g) and 73 full-term children, born between2006 and 2008, at 24 months of corrected age. Three factors were extracted from the EF administeredmeasures: working memory, cognitive flexibility, and impulsivity control. Only cognitive flexibilitywas found to discriminate preterm children from controls.

Keywords: Executive function; Premature; Low birth weight; Cognitive flexibility; Working memory.

Advances in neonatal care have yielded dramatic increases in the survival of preterm chil-dren over the past few decades. Infants born preterm are at risk for cognitive and motordifficulties. Previous studies have shown that these difficulties are evident early in tod-dlers (Rose, Feldman, & Jankowski, 2004), can persist throughout childhood (Böhm &Katz-Salamon, 2003) and are associated, even in the absence of major neurological dis-abilities, with an increased incidence of language delay (Byrne, Elsworth, Bowering, &Vincer, 1993; Grunau, Kearney, & Whitfield, 1990) and learning and behavioral problemsat school age (Anderson & Doyle, 2004; Hack, Friedman, & Fanaroff, 1996).

Despite the wide interest in this topic, investigations have focused mostly on globalmeasures of intelligence or general cognitive abilities (Bhutta, Cleves, Casey, Cradock,& Anand, 2002; Breslau, Johnson, & Lucia, 2001). However, most recent studies ofcognitive development in preterm infants suggest that executive function (EF) could playan important role in the etiology of early difficulties and could be predictive of subsequent

Address correspondence to Gian Marco Marzocchi, Department of Psychology, University of Milan-Bicocca, Piazza Ateneo Nuovo, 1, Milano, 20126 Italy. E-mail: gianmarco.marzocchi@unimib.it

© 2013 Taylor & Francis

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146 T. POZZETTI ET AL.

academic outcomes (Bayless & Stevenson, 2007; Böhm, Smedler, & Forssberg, 2004;Espy et al., 2002; Hughes & Ensor, 2008; Sastre-Riba, 2009; Sun, Mohay, & O’Callaghan,2009). In light of these findings, an increasing number of studies have focused on spe-cific early executive skills such as working memory (Luciana, Lindeke, Georgieff, Mills,& Nelson, 1999), response delay (Nosarti et al., 2006), and planning (Sun et al., 2009).

Although these studies provide strong evidence that children born extremely pretermare characterized by EF difficulties during middle childhood and early adolescence, theextent of these difficulties in early childhood is less clear (Lowe, Erickson, Maclean, &Duvall, 2009; Reed, Pien, & Rothbart, 1984; Vicari, Caravale, Carlesimo, Casadei, &Allemand, 2004).

It is also evident that the risk of these impairments increases as gestational age andbirth weight decrease (Taylor, Klein, Schatschneider, & Hack, 1998). Moreover, perfor-mance degrades in the presence of evident brain damage (Edgin et al., 2008; Nosarti et al.,2008; Stewart et al., 1999; Woodward, Edgin, Thompson, & Inder, 2005). Many authorsalso suggest that even preterm infants without major brain damage may exhibit subtle cog-nitive deficits (Caravale, Tozzi, Albino, & Vicari, 2005; De Haan, Bauer, Georgieff, &Nelson, 2000; Majnemer, Brownstein, Kadanoff, & Shevell, 1992; Torrioli et al., 2000;Vicari, et al., 2004).

The objective of this study was to utilize measures that are appropriate for children18–36 months of age (Espy, Kaufmann, Glisky, & McDiarmid, 2001) and to parse specificneuropsychological deficits that may result from subtle perinatal insults (Bhutta & Anand,2001).

The current study provides an EF profile of children born preterm without majorbrain damage at 2 years of corrected age. In accord with Anderson and Dewey (2011), weconsidered it more appropriate to use corrected age because this adjustment reflects moreaccurately both in-utero and post-utero brain development. Other studies that examinedthe outcomes of older children preferred to use chronological age. Previous studies havesuggested that correcting for gestational age at birth until 8.6 years in extremely pretermchildren is preferable because the scores have greater predictive utility (Edgine et al., 2008;Rickards, Kitchen, Doyle, & Kelly, 1989).

A control group of full-term children matched for age, gender, and socioeconomicstatus was selected.

An EF profile was obtained by administering an experimental battery that includedfour EF tasks chosen on the basis of previous studies: the Spin the Pots task (Hughes& Ensor, 2005), which assesses working memory; the Snack Delay task (Kochanska,Murray, Jacques, Koenig, & Vandegeest, 1996; Kochanska, Murray, & Harlan, 2000),which assesses response delay; the Reverse Categorization task (Carlson, Mandell, &Williams, 2004), which assesses the inhibition of predominant responses and shifting;and the Multi-Location Multi-Step Task (Zelazo, Reznick, & Spinazzola, 1998), whichsimultaneously assesses many EF components (working memory, inhibition, and cognitiveflexibility).

The relations between EF performance and medical factors such as severity of illnessat birth, birth weight, gestational age, and sociodemographic factors were also explored(Hunt, Bruce, Cooper, & Tooley, 1988). Our hypothesis was that preterm children wouldperform more poorly than full-term children on all EF tests. Moreover, we were interestedin understanding which component of EF is particularly impaired in premature childrenwithout major cerebral lesions.

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EF IN PREMATURE CHILDREN AT 24 MONTHS 147

METHOD

Participants

Two groups of children were included in this study. The total sample included72 preterm children and 73 control children born at term.

The group of preterm children (33 males, 39 females) included infants admit-ted between 2006 and 2008 to the Follow-up Clinic of the Neonatal Intensive CareUnit, Policlinico Regina Elena, Mangiagalli Foundation, Milan. All preterm infants wererecruited between September 1, 2008 and July 31, 2010. The inclusion criteria were asfollows: (a) born at less than 34 weeks gestational age and weighing < 2500 g; (b) no con-genital infections or deformities; (c) no retinopathy of prematurity greater than Grade IIplus; (d) no major lesions detected by ultrasound during the perinatal period or by con-ventional magnetic resonance imaging (MRI) at 40 ± 4 weeks of corrected age suchas intraventricular hemorrhage Grade III–IV, hydrocephalus, periventricular leucomala-cia Grade III–IV, arterial infarctus, and sinus thrombosis, abscess and infections; (e) nocerebral palsy, blindness, deafness, or cognitive delay assessed at 2 years corrected age(children with a Mental Development Index [MDI] < 84 on the Bayley Scales II wereexcluded); and (f) both parents Italian speaking.

The initial sample included 140 children. Of these, 40 infants were excluded from thestudy because they did not show all inclusion criteria. Another 28 infants did not participatein the study for the following reasons: (a) we were not able to contact their parents (5 chil-dren); (b) they were not observed within the assessment window (24 months ± 2 weeks)(7 children); or (c) illness or family circumstances (16 children) did not allow the familyto participate in the study.

The 72 remaining preterm children (33 males, 39 females) were born at a gestationalage of between 25 and 33 weeks (M = 30.14; SD = 2.22) and had a birth weight rangingfrom 500 to 2290 g (M = 1285.83; SD = 414.39); 25 premature children had a gestationalage (GA) of ≤ 29 weeks and 47 had a GA between 30 and 33 weeks.

The average corrected age at testing was 24.42 months (SD = 0.34).Details pertaining to each child’s neonatal medical history were collected on the

Neocare database. Specific maternal and neonatal medical problems included the preg-nancy being medically induced (pregnancy was induced in cases of assisted reproductiontechniques such as in vitro fertilization or intracytoplasmic sperm injection), prenatalsteroid administration (for hyaline membrane disease prophylaxis), single or multiple preg-nancy, mode of delivery, caesarean delivery, intrauterine growth restriction (defined as birthweight < tenth percentile, according to Fenton, 2003), Apgar index (at 1 and 5 minutes),and need for reanimation in the delivery room, number of preterm children placed onmechanical ventilation and duration of ventilation while in the Neonatal Intensive CareUnit (NICU) as an indicator of severity of distress, presence of a medical complica-tion such as bronchopulmonary dysplasia, necrotizing enterocolitis requiring intervention,and hemodynamically significant patent ductus arteriosus (defined by echocardiographiccriteria).

The sample medical characteristics for the preterm group are provided in Table 1.Additionally, a control group of 73 (36 males, 37 females) full-term children was recruitedat the outpatient pediatric clinic in Bergamo (a city near Milan): They were born between2006 and 2008, had a birth weight ≥ 2500 g (range 2500–4300 g), and a gestational age ≥37 weeks (range 37–42 weeks); they experienced no complications in the perinatal periodand had an MDI ≥ 84 on the MDI Bayley Scale of Infant Development II at 24 months (±

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148 T. POZZETTI ET AL.

Table 1 Subject Characteristics by Gestational Age.

Variables Total Preterm Group (n = 72) Full-Term Group (n = 73)

Gestational age, (weeks) M ± SD (range) 30.14 ± 2.22 (25–33) (37–42)Birth weight, (g) M ± SD (range) 1285.83 ± 414.39 (500–2290) (2500–4300)Age at testing, (months) M ± SD 24.42 ± 0.34 24.43 ± 0.33Males, n (%) 33 (45.83%) 36 (49.31%)Multiple gestation, n (%) 28 (38.88%) 0 (0%)Pregnancy medically induced, n (%) 24 (33.33%) −Prenatal steroid administration, n (%) 57∗ (79.16%) −Intrauterine growth restriction, n (%) 14 (19.44%) −Caesarean delivery, n (%) 64 (88.88%) −Apgar 1, M ± SD (range) 6.52 ± 1.95 (0–9) −Apgar 5, M ± SD (range) 8.27 ± 1.25 (3–10) −Resuscitation in delivery room, n (%) 32 (44.44%) −Ventilation during NICU, n [%] 62 (86.11%) −Ventilation during NICU, (days) M ± SD 11.06 ± 13.88 −Bronchopulmonary dysplasia, n (%) 6 (8.33%) −Necrotizing enterocolitis, n (%) 5 (6.94%) −Patent ductus arteriosus, n (%) 38 (52.77%) −

∗15/57 IVF/ET = In Vitro Fertilization and Embryo Transfer.

2 weeks). None of them suffered hearing loss or vision problems. The average age at thetime of testing was 24.43 months (SD = 0.33).

The initial sample included 81 children. Four infants were excluded from the studybecause they did not exhibit all of the inclusion criteria: Two twins had a gestational ageof less than 37 weeks; two twins were excluded because their score on the MDI BayleyScale of Infant Development II was less than 84. Another 4 infants did not participate inthe study for the following reasons: (a) 3 children because of errors in the administrationprocedure and (b) 1 child because of lack of parental permission.

Control children were matched with preterm children for age, gender, mother’seducational level, father’s occupational status, cognitive level (assessed by the BayleyScales of Infant Development; Bayley, 1993), and language skills. Language skills wereassessed by the Italian short version of the MacArthur-Bates Communicative DevelopmentInventory (Caselli, Pasqualetti, & Stefanini, 2007). The questionnaire was completed byboth parents.

Group comparisons by socioeconomic status, cognitive level, and language skills arereported in Table 2.

Materials and Measures

All infants recruited for this study were tested at 24 months ± 2 weeks, usinga combination of measures that assessed executive function and cognitive and psy-chomotor function. Parents’ questionnaires and the children’s medical records were alsoincluded. For the sample of preterm infants, age at testing was adjusted for gestational age.Participation was voluntary and informed consent was obtained from both parents of eachchild.

To assess EFs, four tests were administered to each child participant and both parentscompleted a questionnaire.

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EF IN PREMATURE CHILDREN AT 24 MONTHS 149

Tabl

e2

Gro

upC

ompa

riso

nby

Soci

oeco

nom

icSt

atus

,Cog

nitiv

eL

evel

,and

Lan

guag

eSk

ills.

Pret

erm

Infa

nts

(N=

72)

Full-

Term

Infa

nts

(N=

73)

Stat

istic

s

Var

iabl

esn

(%)

n(%

)X

2te

stp

Mot

her’

sE

duca

tion

prop

orti

on(%

)M

iddl

eSc

hool

8(1

3.6%

)7

(10.

4%)

X2(2

)=

0.37

p=.

832

Hig

hSc

hool

26(4

4.1%

)29

(43.

3%)

Uni

vers

ity

25(4

2.4%

)31

(46.

3%)

Fat

her’

sE

mpl

oym

ent(

%)

Bus

ines

sM

anag

er(i

nclu

des

high

-lev

elpr

ofes

sion

als

and

man

ager

sof

larg

een

terp

rise

s,co

rpor

ate

exec

utiv

es,o

wne

rsof

med

ium

-siz

edbu

sine

sses

and

min

orpr

ofes

sion

als)

13(2

2.03

%)

21(3

1.81

%)

X2(2

)=

5.97

.308

Adm

inis

trat

ive

(inc

lude

sad

min

istr

ativ

est

aff,

empl

oyee

s,sm

all

busi

ness

owne

rs,e

ngin

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ners

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hops

)29

(49.

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)30

(45.

45%

)

Wor

ker

(inc

lude

sm

anua

llab

orer

san

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ree

tem

pora

rily

unem

ploy

edin

the

pret

erm

grou

p)17

(28.

81%

)15

(27.

72%

)

Mea

n(r

ange

)SD

Mea

n(r

ange

)SD

t-te

stp

Men

talS

cale

–M

DI

(Bay

ley-

II)

105.

72(8

4–12

6)12

.52

108.

64(8

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6)11

.58

t=1.

45.1

50M

otor

Scal

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PD

I(B

ayle

y-II

)10

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(77–

121)

9.91

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70(8

0–15

2)11

.65

t=1.

05.2

71N

umbe

rof

wor

ds(m

othe

r)C

DI

47.5

0(6

–98)

26.5

255

.44

(4–9

8)22

.81

t=1.

72.0

89N

umbe

rof

wor

ds(f

athe

r)C

DI

48.6

2(4

–100

)27

.62

55.2

1(4

–100

)26

.33

t=1.

09.2

77

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150 T. POZZETTI ET AL.

The tasks are described in the order in which they were presented to the children.

Spin the Pots. In this task, adapted from Hughes and Ensor (2005) and used toassess working memory, children were presented with six visually distinct pots (the colorsof the six pots were yellow, red, green, black, silver, and white with flowers; each pot hada distinct width and height). The original eight-pot version was too difficult for children asyoung as 2 years old, as shown in our pilot study and, for this reason, an easier version ofthe task was created using only six pots.

The six pots were arranged on a rectangular tray placed 40 cm in front of the child.First, the child was invited to help the examiner (the first author) put tokens into four ofthe six pots. The red and green pots always remained empty. Before each trial, the traywas covered with a cloth and spun around, the cloth was then removed and the child wasinvited to choose a pot that contained a token. The choice was recorded and the child wasencouraged to continue. The chosen pot was returned to its place on the tray before movingon to the next trial. The task ended when all four tokens were found or after 12 trials. Fourmeasures were considered for this task. First was the total score, obtained by subtractingthe total number of errors from the total number of trials (12). A higher score indicateda better performance. Additionally, three types of perseverative errors were considered:(a) consecutive perseverative errors (the child chose the same pot in at least two consecu-tive trials); (b) position perseverative errors (the child chose a different pot but pointed tothe same position at least twice); (c) alternating pot-place perseverative errors (the childalternately chose the same two pots).

Snack Delay. This task, adapted from Kochanska et al. (1996, 2000), was selectedto assess the children’s capacity to delay a reward and their inhibitory control of a pre-potent or automatic response. The examiner placed a reward (a piece of candy) under aninverted cup and asked the child to wait for a bell to ring before taking the hidden reward.The task consisted of three trials (delays of 10, 15, and 20 seconds, respectively). In themiddle of each trial delay, the bell was raised but not rung. The examiner restated therule before each trial. The dependent measure was related to the child’s capacity to waitfor the bell to ring before taking the candy. The score was calculated as follows: fourpoints if the child was able to wait the total time without touching the cup; three pointsif the child touched the cup before the bell rang but after it was raised; two points if thechild touched the cup before the bell rang and before it was raised; one point if the childtook the reward before the bell rang but after it was raised; zero points if the child tookthe reward before the bell rang and before it was raised. The score range was between0 and 12.

Reverse Categorization. This task assessed complex response inhibition, cogni-tive flexibility, and shifting. In the preswitch condition of this task (adapted from Carlson,Mandell, and Williams, 2004), children were required to learn a simple rule to sort largeand small blocks according to their size into large and small buckets. The examiner demon-strated six preswitch trials (three of each size), reiterating the rule before each trial, andthen asked the child to sort the remaining six blocks.

When the child finished, the examiner removed the buckets from the child’s sightand introduced the postswitch condition: The empty buckets were again placed in frontof the child, as in the preswitch phase and the examiner asked him or her to reverse the

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EF IN PREMATURE CHILDREN AT 24 MONTHS 151

previous categorization scheme so that the large blocks would go into the small buckets andvice versa. The examiner demonstrated four postswitch trials (two for each size), emptiedthe buckets again and asked the child to sort all of the blocks by him or herself with-out offering any feedback. Three dependent measures were calculated: (a) the postswitchscore, based on the number of correctly sorted blocks in the postswitch phase and rangingfrom 0 to 12 points; (b) errors because of rule perseverations (the child continued to sortblocks according to the preswitch condition); and (c) errors because of motor responseperseverations (the child persisted in the same movement and put all the blocks into thesame bucket).

Multi-Location Multi-Step. This task is a modified A-not-B task developed byZelazo et al. (1998). Its correct execution involves all executive functions of 2-year-oldchildren: working memory, cognitive flexibility, and inhibitory control.

The hiding apparatus consisted of a wooden box that contained three different col-ored objects (a green circle, a blue square, and a yellow triangle); another object (a reddiamond) was used for the training phase. Each object was connected by a string to a trans-parent plastic bag. For more information about the hiding apparatus, readers are referredto previous papers that describe this task in detail (Zelazo et al., 1998; Woodward et al.,2005).

The testing procedure consisted of three phases. During the training phase, only oneobject (the red diamond) was used to allow the child to become familiar with the twosteps for retrieving a reward. The examiner showed each step to the children and thenasked them to retrieve the reward individually. The training phase finished when the childindependently executed the retrieval sequence without assistance.

During the preswitch phase, the examiner placed the three objects (a green circle,a blue square, and a yellow triangle) into the hiding box while the child was watching.While the child was looking carefully at the examiner, he or she placed a piece of candy(the reward) in the transparent bag at Position A (in the green circle on the left side). Thechildren were asked to find the candy as shown to them during the training phase. Thepreswitch phase ended when the child reached for the candy three consecutive times. Thepreswitch phase was interrupted if the child failed to respond repeatedly (> 2 times) orif the criterion (the child reached for the candy three consecutive times) was not obtainedwithin eight trials.

Children who learned how to retrieve the candy in the preswitch phase were pre-sented with the stimuli of the postswitch phase. The postswitch phase was almost identicalto the preswitch phase except that now the examiner explicitly hid the candy in Position B(the yellow triangle on the right side). The postswitch phase ended when the child foundthe reward, failed for three consecutive trials, lost interest or did not meet the criterionwithin five trials.

Two categorical measures were recorded: (a) achievement of the preswitch criterion(yes or no); and (b) achievement of the postswitch criterion (yes or no). Five continu-ous dependent variables were also calculated: (a) perseverative errors in the preswitchphase; (b) nonperseverative errors in the preswitch phase; (c) number of trials to reachthe postswitch criterion (range: 0–8); (d) perseverative errors in the postswitch phase; and(e) nonperseverative errors in the postswitch phase. Additionally, an error analysis of thefirst search location during the postswitch was conducted.

A summary of the tasks used in this study is reported in Table 3.

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152 T. POZZETTI ET AL.

Tabl

e3

Des

crip

tion

ofE

xecu

tive

Func

tion

Task

Adm

inis

tere

d.

Task

Des

crip

tion

Dep

ende

ntV

aria

ble

Exe

cutiv

eFu

nctio

nTa

skad

apte

dfr

om

Spin

the

Pots

Obj

ects

wer

ehi

dden

unde

rpo

ts.C

hild

ren

wer

ein

vite

dto

choo

sea

pott

hatc

onta

ined

ato

ken

and

toav

oid

goin

gba

ckto

one

that

had

prev

ious

lybe

enun

cove

red.

Pots

wer

esp

unaf

ter

ever

ych

oice

.

(a)

Tota

lsco

re(h

ighe

rsc

ores

corr

espo

nded

tobe

tter

perf

orm

ance

s:R

ange

:0–1

2);

(b)

thre

ety

pes

ofpe

rsev

erat

ive

erro

rs(h

ighe

rsc

ores

corr

espo

nded

tow

orse

perf

orm

ance

s):

−N

umbe

rof

cons

ecut

ive

pers

ever

ativ

eer

rors

(the

child

chos

eth

esa

me

potf

orat

leas

ttw

oco

nsec

utiv

etr

ials

;Ran

ge:0

–11)

;−

Num

ber

ofpo

sitio

npe

rsev

erat

ive

erro

rs(t

hech

ildch

ose

adi

ffer

entp

otbu

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nted

toth

esa

me

posi

tion

atle

astt

wic

e;R

ange

:0–1

1);

−N

umbe

rof

alte

rnat

ing

pot-

plac

epe

rsev

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ive

erro

rs(t

hech

ildal

tern

atel

ych

ose

the

sam

etw

opo

ts;R

ange

:0–1

0)

Wor

king

mem

ory

Hug

hes

&E

nsor

(200

5)

Rev

erse

Cat

egor

izat

ion

Dur

ing

pres

witc

h,ch

ildre

nso

rted

larg

ebl

ocks

into

ala

rge

buck

etan

dsm

allb

lock

sin

toa

smal

lbuc

ket.

Dur

ing

post

switc

h,ch

ildre

nha

dto

reve

rse

the

prev

ious

cate

gori

zatio

nsc

hem

e.

(a)

Post

switc

hsc

ore

(hig

her

scor

esco

rres

pond

edto

bette

rpe

rfor

man

ces;

Ran

ge:0

–12)

;(b

)Tw

oty

pes

ofpe

rsev

erat

ive

erro

rs(h

ighe

rsc

ores

corr

espo

nded

tow

orse

perf

orm

ance

s):

−N

umbe

rof

erro

rsbe

caus

eof

rule

pers

ever

atio

ns(t

hech

ildco

ntin

ued

toso

rtbl

ocks

acco

rdin

gto

the

pres

witc

hco

nditi

on;

Ran

ge:0

–12)

;−

Num

ber

ofer

rors

beca

use

ofm

otor

resp

onse

pers

ever

atio

ns(t

hech

ildpe

rsis

ted

inth

esa

me

mov

emen

tand

puta

llth

ebl

ocks

into

the

sam

ebu

cket

;Ran

ge:0

–11)

Com

plex

resp

onse

inhi

bitio

n,co

gniti

vefle

xibi

lity

and

shif

ting

Car

lson

,Man

dell,

&W

illia

ms

(200

4)

Mul

ti-L

ocat

ion

Mul

ti-St

epV

aria

tion

onA

-not

-B.D

urin

gpr

esw

itch,

anob

ject

was

hidd

enin

one

ofth

ree

loca

tions

;th

ech

ildre

nw

ere

aske

dto

find

the

cand

yth

ree

cons

ecut

ive

times

.Dur

ing

post

switc

h,th

eob

ject

was

visi

bly

switc

hed

toan

othe

rhi

ding

plac

ean

dch

ildre

nha

dto

find

iton

etim

e.

(a)

Ach

ieve

men

tof

the

pres

witc

hcr

iteri

on(y

esor

no);

Wor

king

mem

ory,

cogn

itive

flexi

bilit

yan

din

hibi

tory

cont

rol.

Zel

azo,

Rez

nick

,&Sp

inaz

zola

(199

8)

(Con

tinu

ed)

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EF IN PREMATURE CHILDREN AT 24 MONTHS 153

Tabl

e3

(Con

tinue

d).

Task

Des

crip

tion

Dep

ende

ntV

aria

ble

Exe

cutiv

eFu

nctio

nTa

skad

apte

dfr

om

(b)

Ach

ieve

men

tof

the

post

switc

hcr

iteri

on(y

esor

no).

Inth

efo

llow

ing

vari

able

s,hi

gher

scor

esco

rres

pond

edto

wor

sepe

rfor

man

ces;

Ran

ge0–

5):

(c)

Num

ber

ofpe

rsev

erat

ive

erro

rsin

the

pres

witc

hph

ase;

(d)

Num

ber

ofno

nper

seve

rativ

eer

rors

inth

epr

esw

itch

phas

e;(e

)N

umbe

rof

tria

lsto

reac

hth

epo

stsw

itch

crite

rion

;(f

)N

umbe

rof

pers

ever

ativ

eer

rors

inth

epo

stsw

itch

phas

e;(g

)N

umbe

rof

nonp

erse

vera

tive

erro

rsin

the

post

switc

hph

ase.

Snac

kD

elay

Chi

ldm

ustd

elay

agr

atifi

catio

n(t

akin

gth

ehi

dden

rew

ard)

until

the

bell

ring

s(t

rial

sof

diff

eren

tdur

atio

ns).

Chi

ld’s

capa

city

tow

aitu

ntil

the

bell

ring

sbe

fore

taki

ngth

eca

ndy

(hig

her

scor

esco

rres

pond

edto

bette

rpe

rfor

man

ces)

.Fo

rea

chof

the

thre

etr

ials

,the

follo

win

gsc

ores

wer

eas

sign

ed:4

poin

tsif

the

child

was

able

tow

aitt

heto

talt

ime

with

out

touc

hing

the

cup;

3po

ints

ifth

ech

ildto

uche

dth

ecu

pbe

fore

the

bell

rang

buta

fter

itw

asra

ised

;2po

ints

ifth

ech

ildto

uche

dth

ecu

pbe

fore

the

bell

rang

and

befo

reit

was

rais

ed;

1po

inti

fth

ech

ildto

okth

ere

war

dbe

fore

the

bell

rang

buta

fter

itw

asra

ised

;and

0po

ints

ifth

ech

ildto

okth

ere

war

dbe

fore

the

bell

rang

and

befo

reit

was

rais

ed(R

ange

:0–1

2).

Del

ayan

din

hibi

tory

cont

rol.

Koc

hans

ka,M

urra

y,Ja

cque

s,K

oeni

g,&

Van

dege

est(

1996

);K

ocha

nska

,M

urra

y,&

Har

lan

(200

0)

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154 T. POZZETTI ET AL.

Procedure

The neurocognitive assessment applied in this study was administered after thefollow-up routine health check of each preterm child conducted in the Follow Up Clinic,which included a neurofunctional assessment and auxological examination performed bythe two authors (O. Picciolini and S. Gangi).

The battery of EF tasks was administered in a single session of 15 minutes by twotrained psychology students and a trained psychologist (the first author). Next, the BayleyII scale was applied to the children for approximately 40 minutes. One parent, usually themother, was present during the testing session. The examiners did not know the child’sprevious medical history. All tests were videotaped (with the consent of both parents) tohave the possibility to reward and reclassify tests if necessary.

During all sessions, parents were instructed to keep the child’s attention on the tasks.The McArthur-CDI (Communicative Development Inventories) questionnaire was admin-istered to the parents at the end of the sessions.A written report on the child’s performanceon the tasks was presented to each family.

Statistical Analysis

A two-step Explorative Factor Analysis (EFA) was conducted on the13 neuropsychological continuous measures of the EF battery (see below for detailsof the 13 measures) to identify latent dimensions of neurocognitive functioning and toclarify the relations among the tasks. Considering only the control group of children bornat term, principal axis extraction, and varimax rotation with Kaiser normalization wereused to extract factors with eigenvalues greater than 1.

The first step of the EFA was performed to reduce the number of continuous vari-ables of each task: four measures of the Spin the Pots task (total score, consecutiveperseveration errors, alternating perseveration errors, and position perseveration errors);three variables of the Reverse Categorization task (postswitch score, rule perseverativeerrors, and motor perseverative errors), five measures of the Multi-Location Multi-Steptask (preswitch perseverative errors, preswitch nonperseverative errors, number of trials toreach postswitch criterion, postswitch perseverative errors, and postswitch nonpersevera-tive errors). For the Snack Delay task, an EFA was not necessary because there was onlyone dependent measure (total score).

A second order Exploratory Factor Analysis was performed on the seven factors(transformed into z scores) derived from the first order EFA (performed to reduce the num-ber of dependent variables, see Table 4). The final factors were considered the ExecutiveFunction latent domains. On these latent domains of the EF, a multivariate analysis of vari-ance (MANOVA) was performed to compare the performance of the premature children tothe full-term children.

RESULTS

To reduce the number of variables for each task, three Exploratory Factor Analyses(Principal Components, Varimax rotation, Eigenvalue > 1) were applied to each EF task toextract the main factors for each test and to extrapolate a general structure of EF processesin 24-month-old children.

Two factors were extracted from the four variables of the Spin the Pots task:Total score, position perseverative errors, alternating pot-place perseverative errors, and

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Table 4 Explorative Factor Analysis on the Seven Measures of the EF Battery.

Measures

Factor 1:CognitiveFlexibility

Factor 2:Inhibition

Factor 3:WorkingMemory

Reverse Categorization – Perseverative Errors 0.724MLMS Multi-Location Multi-Step – Perseverations Postswitch 0.667Spin the Pots – Consecutive errors 0.649Reverse Categorization – Motor errors 0.674Snack Delay 0.572Spin the Pots – Total score 0.543MLMS Multi-Location Multi-Step – Non perseverative errors −0.850% variance 19.18 16.92 15.76

consecutive perseverative errors, explaining 70.06% of the variance. Factor 1 includedthree variables: total score (saturation score = .939), position perseverative errors (satura-tion score = .531), and alternating pot-place perseverative errors (saturation score = .648).Factor 2 included only one variable: Consecutive perseverative errors (saturation score =.945), explaining 28.76% of the variance. Factor 1 included variables describing workingmemory functioning, whereas Factor 2 included only the measure of inhibition becausethis variable describes the immediate repetitive pointing of children to the same pot. Thetwo extracted factors were transformed into z scores and then entered into the second stepof the EFA.

For the Reverse Categorization task, three measures (postswitch score, errors due torule perseverations, and errors due to motor response perseveration) were reduced to twofactors, explaining 99.71% of the variance. Factor 1 included the postswitch score (satura-tion score = .952) and errors due to rule perseverations (saturation score = - .986). Factor 2included errors due to motor response perseveration (saturation score = .991). Factor 1is related to the ability to apply cognitive flexibility (shift), whereas Factor 2 representsinhibitory difficulties because children continued to sort the objects in the same mannerwithout applying any rule. For Spin the Pots, the two factors of the Reverse Categorizationtasks have been transformed into z scores and then entered into the second step of theExploratory Factor Analysis (EFA).

Finally, considering the Multi-Location Multi-Step task, a factor analysis of the fiveinitial variables (number of trials to reach the postswitch criterion, perseverative errors inthe postswitch phase, perseverative errors in the preswitch phase, nonperseverative errors inthe preswitch phase, and nonperseverative errors in the postswitch phase) allowed extrac-tion of two factors explaining 62.68% of the variance. Factor 1 included the number oftrials to reach the postswitch criterion (saturation score = .972) and perseverative errors inthe postswitch phase (saturation score = .972). Factor 2 included perseverative errors in thepreswitch phase (saturation score = .676), nonperseverative errors in the preswitch phase(saturation score = .508), and nonperseverative errors in the postswitch phase (saturationscore = .718). Factor 1 is related to the children’s ability to apply cognitive flexibilityto avoid perseverative errors in the postswitch phase; Factor 2 is related to the workingmemory of children because their errors are not due to perseverative behaviors but totheir difficulty in remembering the position of the three objects. The two factors of theMulti-Location Multi-Step task were transformed to z scores and entered into the secondstep of the EFA.

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Table 5 Comparison between Preterm and Full-Term Children on the Three EF Factors.

Difference Between Pre-Term and Full-TermsChildren (z scores)

Mean SD t-test p

Working Memory 0.29 1.06 1.71 .09Cognitive Flexibility 0.36 0.90 2.26 .02Inhibition 0.05 1.07 0.31 .76

The second step of the Exploratory Factor Analysis was conducted to discover latentdimensions of the Executive Function domain: seven standardized variables (z scores) wereused to conduct the second EFA, with varimax rotation (eigenvalue > 1): six factors wereextracted from the three tasks described above (Spin the Pots, Reverse Categorization, andMulti-Location Multi-Step); the seventh z score was computed from the Snack Delay task.

Three final EF factors were extracted from the seven preliminary factors and trans-formed into z scores. The three factors explained 51.86% of the variance. As reportedin Table 4, Factor 1 included two standardized factors derived from the initial measures:perseverative errors in the Reverse Categorization (Factor 1 of the Reverse Categorizationtask) and perseverative errors in the postswitch phase of the Multi-Location Multi-Step (Factor 1 of the Multi-Location Multi-Step); this factor could represent CognitiveFlexibility. Factor 2 included three measures: consecutive errors in the Spin the Pots (Factor2 of the Spin the Pots task), motor errors in the Reverse Categorization (Factor 2 of theReverse Categorization task), and the z score of the Snack Delay task. This second factorcould represent inhibitory behaviors. Finally, Factor 3 included two measures: total scoreof Spin the Pots (Factor 1 of the Spin the Pots task) and nonperseverative errors in theMulti-Location Multi-Step (Factor 2 of the Multi-Location Multi-Step). This third factor isrelated to Working Memory. Saturation scores of the three factors are reported in Table 4.

Because the group of premature children presented a wide range of gestational ages,a comparison between premature babies with extremely low birth weights (500–1000 g;N = 22) and those with low birth weights (1500–2500 g; N = 18) on EF test performancewas conducted. No significant difference between subgroups was identified; therefore, wedid not split the premature sample into subgroups according to gestational age. Moreover, acorrelational analysis between the performance of children on EF tasks and gestational agewas conducted, and there was no significant correlation between the parameters (p > .15).

A final comparison between the two groups was conducted using the three latentdomains of the EF battery: Cognitive Flexibility, Inhibition, and Working Memory.As reported in Table 5, premature children were significantly impaired in CognitiveFlexibility and a trend of significant difference between the two groups on WorkingMemory was identified. No inhibitory deficit was identified in the preterm children.

DISCUSSION

The present study provides a broad assessment of Executive Functions (EFs) in2-year-old preterm children without major brain damage, compared with a matched controlgroup.

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The scientific interest in the neuropsychological profile of emerging strengths anddifficulties in specific aspects of executive functions is recent (Woodward et al., 2011) andit is extremely important to extend our knowledge in this direction regarding early-agepreterm infants.

The present study is of particular interest for two reasons: First, because it examinesExecutive Functioning using a multivariate approach; second, it extends our knowledge ofEFs’ key components in the first years of life.

Consistent with previous studies (Hughes & Ensor, 2008; Lowe et al., 2009;Woodward et al., 2005), we found that 2-year-old preterm infants with average intelligenceand without major abnormalities on neurological examination or major cerebral lesions onan MRI at their term-equivalent age generally showed greater difficulties in tasks assessingEFs.

The two-step Explorative Factor Analysis (EFA) allowed us to extract only threeEF factors from the 13 initial variables: Working Memory, Cognitive Flexibility, andInhibition. According to the literature (Garon, Bryson, & Smith, 2008; Miyake et al., 2000;Woodward et al., 2011), we hypothesized that these three factors may represent differentexecutive processes necessary to successfully perform the required tasks.

Among these three factors, we found that only Cognitive Flexibility discriminatedbetween premature children and controls.

Cognitive Flexibility is one of the least studied components of EF because it repre-sents the most complex EF skill and there is no pure Flexibility task, most likely becauseCognitive Flexibility builds upon the other EF components (such as Inhibition and WorkingMemory; Garon et al., 2008). Because of this close correlation between different EF com-ponents, our findings highlight the need to simultaneously use a wide range of tasks toextract the underlying constructs.

Other authors who have examined Cognitive Flexibility reported conflicting results.Many of these studies are not comparable to ours because their focus was on school-agechildren. Aarnoudse-Moens, Smidts, Oosterlaan, Duivenvoorden, and Weisglas-Kuperus(2009) identified cognitive flexibility impairment in preterm children aged 6 years old.

Bayless and Stevenson (2007) analyzed preterm children aged from 6 to 12 yearsusing a multivariate analysis. They identified significant difficulties in the Shifting andInhibition components of EFs, although covariate analysis revealed that only Shifting wasindependent of IQ.

On the other hand, in preschool children, Espy et al. (2002), using a preliminarysample of 29 children between the ages of 2 and 3 years, identified in the preterm groupa specific deficit in the Delayed Alternation task, which evaluates Working Memory, not,however, in the Spatial Reversal task, which evaluates Cognitive Flexibility: This findingsuggests a specific weakness in Working Memory processes. However, Spatial Reversal isa task quite similar to our Multi-Location Multi-Step. As we have previously described,these tasks place a demand on working memory (learning an arbitrary stimulus-responseassociation [S-R] in the preswitch phase and subsequently a simple S-R remapping duringpostswitch). Although this working memory demand is minimal, it might have influencedthe negative results identified by a single-task analysis.

Edgine et al. (2008) concluded that children aged four years, extremely preterm, andwith white matter abnormalities (white matter signal abnormality [shortening T1-weightedimaging], reduction in white matter volume, cystic abnormality, lateral ventricular size andthinning of the corpus callosum, and delayed myelination) appeared to be able to inhibit a

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158 T. POZZETTI ET AL.

prepotent response but lacked cognitive inflexibility. However, in this case, differences inthe tasks’ individual variables were examined rather than their underlying common factors.

Our study, taking into account a combination of different variables, confirmed thepresence of cognitive inflexibility in the preterm group.

In summary, our belief is that cognitive flexibility could be a precursor of deficitwhen children are younger (preschool); however, it could become more evident when chil-dren attend primary school, when this function is more developed and the requests becomemore complex.

Regarding Working Memory and other research, we identified no significant differ-ence between the two groups.

Recent studies have shown that Working Memory is an area of weakness in pretermpreschoolers (Beauchamp et al., 2008; Vicari et al., 2004; Woodward et al., 2005), duringschool age (Luciana et al., 1999), and in adolescence (Bhutta et al., 2002).

Woodward et al. identified that difficulties in Working Memory, assessed at 2 yearswith the Multi-Location Multi-Step task in extremely preterm children, correlate witha reduction in total tissue volume of the dorsolateral prefrontal cortex, sensori-motor,parieto-occipital, and premotor on MRI scans at 40-weeks-term equivalent age. In addi-tion, Beauchamp et al. (2008) have identified that difficulties in Working Memory, assessedat 2 years by the Delayed Alternation task in extremely preterm infants, correlated with areduction in the hippocampal volumes on MRIs at term-equivalent age.

Vicari et al. (2004), using the “memory for location” task, identified that preterm chil-dren demonstrated more problems than controls did if the delay interval in each trial wasincreased. The authors argued that preterm children stored the spatial configuration patternnormally; however, their poor performance following the delay suggests that mechanismsresponsible for rehearsing the spatial representation to prevent its decay from memory weredeficient. Consequently, spatial memory span is reduced (Vicari et al., 2004).

Zelazo et al. (1998) have assessed 2-year-old full-term children using several mod-ified versions of the Multi-Location Multi-Step task and they identified that perseverativeerrors on postswitch are typical at this age, and that to commit them, an active responseis required during the preswitch phase. The authors suggest that children’s behavioris affected by having learned and consolidated a certain type of motor response onpreswitch, which must be inhibited to successfully pass the postswitch condition. Thistype of operation, however, seems to involve not only working memory but also cognitiveflexibility.

In fact, many tasks (such as Multi-Location Multi-Step) used in the literature to mea-sure working memory are not “pure” but require different steps involving multiple aspectsof executive functions, hence the need to extract the factors underlying them.

Although our study increases our knowledge about a poorly investigated area using acomprehensive assessment of EF at an early age, several limitations should be noted. Firstis the lack of standardized tasks to measure cognitive abilities, which therefore necessitatesthe use of tasks with limited psychometric validity and reliability.

Second, the pediatric outpatient clinic that has cooperated with us has selected forthis study children with no complications during the prenatal, perinatal, and postnatalcourses; however, the precise perinatal characteristics of these children are not availablefor publication.

Nonetheless, the present study highlights the benefit of using multivariate assess-ments of executive skills to better understand the specific cognitive weaknesses associated

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with preterm birth rather than focusing on a single EF component or on a general cognitiveoutcome alone.

In summary, the preterm children without major brain injury in this study showedappropriate levels of cognitive development and exhibited some weaknesses in higher cog-nitive functions, namely Cognitive Flexibility, of the EF domain. EF difficulties may alsobe the basis of more severe academic and behavioral problems during development, whenthe demands of the external environment increase and the EFs play an increasingly impor-tant role in accomplishing developmental tasks. A detailed understanding of EF difficultiescould pave the way for new types of interventions with the goals of improving academicperformance, preventing behavioral problems, and improving the quality of life of thesechildren.

Original manuscript received April 23, 2012Revised manuscript accepted December 23, 2012

First published online January 29, 2013

REFERENCES

Aarnoudse-Moens, C. S. H., Smidts, D. P., Oosterlaan, J., Duivenvoorden, H. J., & Weisglas-Kuperus, N. (2009). Executive function in very preterm children at early school age. Journalof Abnormal Child Psychology, 37, 981–993.

Anderson, P. J., & Doyle, L. W. (2004). Executive functioning in school-aged children who wereborn very preterm or with extremely low birthweights in the 1990s. Pediatrics, 114, 50–58.

Anderson, P. J., & Dewey, D. (2011). The consequences of being born very early or very small.Developmental Neuropsychology, 36(1), 1–4.

Bayless, S., & Stevenson, J. (2007). Executive functions in school-age children born very prema-turely. Early Human Development, 83, 247–254.

Bayley, N. (1993). Bayley Scales of Infant Development-II. San Antonio, TX: PsychologicalCorporation.

Beauchamp, M. H., Thompson, D. K., Howard, K., Doyle, L. W., Egan, G. F., Inder, T. E., et al.(2008). Preterm infant hippocampal volumes correlate with later working memory deficits.Brain, 131, 2986–2994.

Bhutta, A. T., & Anand, K. J. S. (2001). Abnormal cognition and behavior in preterm neonates linkedto smaller brain volumes. Trends in Neuroscience, 24, 129–132.

Bhutta, A. T., Cleves, M. A., Casey, P. H., Cradock, M. M., & Anand, K. J. S. (2002). Cognitiveand behavioral outcomes of school-aged children who were born preterm. Journal of AmericanMedical Association, 288, 728–737.

Böhm, B., & Katz-Salamon, M. (2003). Cognitive development at 5.5 years of children with chroniclung disease of prematurity. Archives of Disease in Childhood: Fetal and Neonatal Edition, 88,F101–F105.

Böhm, B., Smedler, A. C., & Forssberg, H. (2004). Impulse control, working memory and otherexecutive functions in preterm children when starting school. Acta Paediatrica, 93, 1363–1371.

Breslau, N., Johnson, E. O., & Lucia, V. C. (2001). Academic achievement of low birth weightchildren at age 11: The role of cognitive abilities at school entry. Journal of Abnormal ChildPsychology, 29, 273–279.

Byrne, J., Elsworth, C., Bowering, E., & Vincer, M. (1993). Language development in low birthweight infants: The first two years of life. Journal of Developmental and Behavioral Pediatrics,14, 208–209.

Caravale, B., Tozzi, C., Albino, G., & Vicari, S. (2005). Cognitive development in low risk preterminfants at 3–4 years of life. Archives of Disease in childhood: Fetal and Neonatal Edition, 90(6),F474–F479.

Dow

nloa

ded

by [

Uni

vers

ity o

f N

ewca

stle

(A

ustr

alia

)] a

t 01:

28 0

3 O

ctob

er 2

014

160 T. POZZETTI ET AL.

Carlson, S. M., Mandell, D. J., & Williams, L. (2004). Executive function and theory of mind:Stability and prediction from ages 2 to 3. Developmental Psychology, 40, 1105–1122.

Caselli, M. C., Pasqualetti, P., & Stefanini, S. (2007). Parole e frasi nel “primo vocabolario delbambino”. Nuovi dati normativi tra 18 e 36 mesi e forma breve del questionario [Words andsentences in “First vocabulary of children” New normative data between 18 and 36 months -short version of the questionnaire]. Milano, Italy: Franco Angeli.

De Haan, M., Bauer, P. J., Georgieff, M. K., & Nelson, C. A. (2000). Explicit memory in low-riskinfants aged 19 months born between 27 and 42 week of gestation. Developmental Medicineand Child Neurology, 42, 304–312.

Edgin, J. O., Inder, T. E., Anderson, P. J., Hood, K. M., Clark, C. A. C., & Woodward, L. J. (2008).Executive functioning in preschool children born very preterm: Relationship with early whitematter pathology. Journal of the International Neuropsychological Society, 14, 90–101.

Espy, K. A., Kaufmann, P. M., Glisky, M. L., & McDiarmid, M. D. (2001). New procedures to assessexecutive functions in preschool children. The Clinical Neuropsychologist, 15, 46–58.

Espy, K. A., Stalets, M. M., McDiarmid, M. M., Senn, T. E., Cwik, M. F., & Hamby, A. (2002).Executive functions in preschool children born preterm: Application of cognitive neuroscienceparadigms. Child Neuropsychology, 8, 83–92.

Fenton, T. (2003). A new growth chart for preterm babies: Babson and Benda’s chart updated withrecent data and new format. BMC Pediatrics, 16, 3–13.

Garon, N., Bryson, S. E. B., & Smith, I. M. (2008). Executive Function in preschoolers: A reviewusing an integrative framework. Psychological Bulletin, 134, 31–60.

Grunau, R. V., Kearney, S., & Whitfield, M. F. (1990). Language development at 3 years in pretermchildren of birth weight below 1000 g. British Journal of Disorder of Communication, 25,173–182.

Hack, M., Friedman, H., & Fanaroff, A. A. (1996). Outcomes of extremely low birthweight infants.Pediatrics, 98, 931–937.

Hughes, C., & Ensor, R. (2005). Executive function and Theory of Mind in 2 years olds: A familyaffair? Developmental Neuropsychology, 28, 645–668.

Hughes, C., & Ensor, R. (2008). Does executive function matter for preschoolers’ problembehaviors? Journal of Abnormal Child Psychology, 36, 1–14.

Hunt, J., Bruce, A., Cooper, B., & Tooley, W. (1988). Very low birth weight infants at 8 and 11 yearsof age: Role of neonatal illness and family status. Pediatrics, 82, 596–603.

Kochanska, G., Murray, K. T., & Harlan, E. T. (2000). Effortful control in early childhood: Continuityand change, antecedents, and implications for social development. Developmental Psychology,36, 220–232.

Kochanska, G., Murray, K. T., Jacques, T. Y., Koenig, A. L., & Vandegeest, K. A. (1996). Inhibitorycontrol in young children and its role in emerging internalization. Child Development, 67,490–507.

Lowe, J., Erickson, S. J., Maclean, P., & Duvall, S. W. (2009). Early working memory and maternalcommunication in toddlers born very low birth weight. Acta Paediatrica, 98, 660–663.

Luciana, M., Lindeke, L., Georgieff, M., Mills, M., & Nelson, C. (1999). Neurobehavioral evi-dence for working-memory deficits in school-aged children with histories of prematurity.Developmental Medicine & Child Neurology, 41, 521–533.

Majnemer, A., Brownstein, A., Kadanoff, R., & Shevell M. I. (1992). A comparison ofneurobehavioral performances of healthy term and low-risk preterm infants at term.Developmental Medicine & Child Neurology, 34, 417–424.

Miyake, A., Friedman, N., Emerson, M., Witzki, A., Howerter, A., & Wager, T. D. (2000). The unityand diversity of executive functions and their contributions to complex “frontal lobe” tasks: Alatent variable analysis. Cognitive Psychology, 41, 49–100.

Nosarti, C., Giouroukou, E., Healy, E., Rifkin, L., Walshe, M., Reichenberg, A., et al. (2008). Matterdistribution in very preterm adolescents mediates neurodevelopmental outcome. Brain, 131,205–217.

Dow

nloa

ded

by [

Uni

vers

ity o

f N

ewca

stle

(A

ustr

alia

)] a

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EF IN PREMATURE CHILDREN AT 24 MONTHS 161

Nosarti, C., Rubia, K., Smith, A. B., Frearson, S., Williams, S-C., Rikkin, L., et al. (2006). Alteredfunctional neuroanatomy of response inhibition in adolescent males who were born verypreterm. Developmental Medicine & Child Neurology, 48, 265–271.

Reed, M. A., Pien, D. L., & Rothbart, M. K. (1984). Inhibitory self-control in preschool children.Merrill-Palmer Quarterly, 30, 131–147.

Rickards, A. L., Kitchen, W. H., Doyle, L. W., & Kelly, E. A. (1989). Correction of developmentaland intelligence test scores for premature birth. Australian Journal of Paediatrics, 25, 127–129.

Rose, S. A., Feldman, J. F., & Jankowski, J. J. (2004). Dimensions of cognition in infancy.Intelligence, 32, 245–262.

Sastre-Riba, S. (2009). Prematurity: Longitudinal analysis of executive functions. Revista deNeurologia, 27(48 Suppl 2), S113–S118.

Stewart, A. L., Rifkin, L., Amess, P. N., Kirkbride, V., Townsend, J. P., Miller, D. H., et al. (1999).Brain structure and neurocognitive and behavioural function in adolescents who were born verypreterm. Lancet, 353, 1653–1657.

Sun, J., Mohay, H., & O’Callaghan, M. (2009). A comparison of executive function in very pretermand term infants at 8 months corrected age. Early Human Development, 85, 225–230.

Taylor, H. G., Klein, N., Schatschneider, C., & Hack, M. (1998). Predictors of early school ageoutcomes in very low birth weight children. Developmental Behavioral Pediatrics, 19, 235–243.

Torrioli, M. G., Frisone, M. F., Bovini, L., Luciano, R., Pascaa, M. G., Leporia, R., & Tortorolo,G. (2000). Perceptual motor, visual and cognitive ability in VLBW children without ultrasoundabnormalities. Brain Development, 22, 163–168.

Vicari, S., Caravale, B., Carlesimo, G. A., Casadei, A. M., & Allemand, F. (2004). Spatial work-ing memory deficits in children at ages 3–4 who were low birth weight, preterm infants.Neuropsychology, 18, 673–678.

Woodward, L. J., Clark, C. A. C., Pritchard, V. E., Anderson, P. J., & Inder, T. E. (2011). Neonatalwhite matter abnormalities predict global executive function impairment in children born verypreterm. Developmental Neuropsychology, 36, 22–41.

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.

Zelazo, P. D., Reznick, J. S., & Spinazzola, J. (1998). Representational flexibility and responsecontrol in a Multi-Location Multi-Step search task. Developmental Psychology, 34, 203–214.

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