Child Neuropsychology

A Journal on Normal and Abnormal Development in Childhood and

Adolescence

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/ncny20

Phasic and tonic alertness in preterm 5-year-old

healthy children

Dominique A. Jaeger, Nina Gawehn, Dominik T. Schneider & Boris Suchan

To cite this article: Dominique A. Jaeger, Nina Gawehn, Dominik T. Schneider & Boris Suchan
(2021) Phasic and tonic alertness in preterm 5-year-old healthy children, Child Neuropsychology,
27:8, 1073-1087, DOI: 10.1080/09297049.2021.1919297

To link to this article: https://doi.org/10.1080/09297049.2021.1919297

Published online: 26 Apr 2021.

Submit your article to this journal

Article views: 150

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

https://www.tandfonline.com/action/journalInformation?journalCode=ncny20
CHILD NEUROPSYCHOLOGY
2021, VOL. 27, NO. 8, 1073–1087
https://doi.org/10.1080/09297049.2021.1919297

Phasic and tonic alertness in preterm 5-year-old healthy

children
Dominique A. Jaegera, Nina Gawehnb, Dominik T. Schneiderc and Boris Suchand
a
Outpatients´ Department for Developmental Neuropsychology, Department of Social Paediatrics and
Neuropediatrics, Clinic of Pediatrics, Municipal Hospital Dortmund, Dortmund, Germany; bUniversity of
Health Sciences, Bochum, Germany; cClinic of Pediatrics, Municipal Hospital Dortmund, Dortmund,
Germany; dClinical Neuropsychology, Neuropsychological Therapy Centre, Ruhr University Bochum,
Bochum, Germany

ABSTRACT ARTICLE HISTORY

Preterm delivery may interrupt the intrauterine brain development Received 10 June 2020
and implies a risk factor for the developing brain. In the long term, Accepted 15 April 2021
most frequently particular forms of attention deficits are described KEYWORDS
which refer to the basic aspects of attention i.e., arousal or tonic Preterm birth; attention
alertness. As this reflects top-down processes, the current study functioning; phasic alertness;
focuses on bottom-up processed phasic alertness in preschool tonic alertness; bottom-up;
aged preterm children. Additionally, we made a division of top-down
response times into decision and movement time to quantify
more exactly the contribution of cognitive and motor performance
to reaction times. We investigated basic aspects of attention func­
tioning and contrasted phasic and tonic alertness in 31 low-risk
healthy preterm (28–36 weeks of gestation) and 22 term children of
five to 6 years of age by using a self-designed computerized test.
Preterm children exhibited delayed decision and reaction time in
the tonic non-cued alertness condition but not in the phasic cued
alertness condition compared to term children. Current results
suggest that preterm birth, even when clinically relevant symptoms
are absent, may have long-term consequences on basic aspects of
attention functioning. Results further suggest that preterm children
may profit from auditory cues to overcome these deviations, which
yield evidence for a clear distinction between impaired top-down
and intact bottom-up controlled processes. These findings might
provide a promising groundwork for the development of therapeu­
tical interventions and prevention strategies, whose use and impact
to support preterm children should be addressed in further
investigations.

Alertness represents the basis of attention functioning and for more complex cognitive
abilities. In the child`s development, alertness is highly relevant and affects the educa­
tional process. Alertness can be further subdivided into tonic and phasic alertness. Tonic
alertness reflects the intrinsic and more long-term control of the arousal level which is
defined as the internal cognitive control of wakefulness and arousal (Posner et al., 1978).

CONTACT Dominique A. Jaeger N.Jaeger@gmx.de Outpatients´ Department for Developmental

Neuropsychology, Department of Social Paediatrics and Neuropediatrics, Clinic of Pediatrics, Municipal Hospital
Dortmund, Klinikum Dortmund gGmbH, Beurhausstr. 40, Dortmund 44137
© 2021 Informa UK Limited, trading as Taylor & Francis Group
1074 D. A. JAEGER ET AL.

In everyday life, alertness is needed when reacting on an obstacle while cycling a bike,
following lessons, reading a book, writing or solving mathematical problems. The second
domain of alertness is described as phasic or exogenous alertness (Posner et al., 1978).
Phasic alertness allows the organism to activate resources promptly when they are actual
needed. It denotes the brief adaptive increase of the arousal subsequent to an upcoming
external warning stimulus (Posner, 2008; Sturm & Willmes, 2001). In everyday life phasic
alertness is required when waiting for the green lights following yellow lights at the traffic
lights, when the teacher asks to pay particular attention to the following, when someone
knocks on the door while waiting for a visitor, or when the telephone rings while waiting
for a call.
According to the Attentional Network Theory originally published by Posner and
Petersen (1990) and reviewed later by Petersen and Posner (2012), tonic alertness refers
to the anterior alerting system depending on the right frontal and parietal lobes and the
locus coeruleus. More detailed, modulations of tonic (intrinsic) alertness are mediated by
a right-hemispheric network in which frontal regions exert top-down control, via
thalamic nuclei, by activating noradrenergic nuclei of the ponto-mesencephalic part of
the brainstem (Petersen & Posner, 2012; Sturm & Willmes, 2001). Functional brain
imaging studies consistently found this tonic alertness network and have shown
a substantial overlap with the cerebral network underlying phasic alertness (Sturm
et al., 1999, 2006; Sturm & Willmes, 2001). However, differences in activation and
effective connectivity of the alertness network were found when comparing phasic and
tonic condition (Périn et al., 2010). Additionally, while tonic alertness activates
a predominantly top-down controlled system, phasic alertness based on a more bottom-
up, stimulus-driven attentional system (Périn et al., 2010) that leads to a more global
stimulation including the right and the left hemisphere (Finke et al., 2012). A possible
neuroanatomical structure representing this bottom-up controlled process is the ascend­
ing reticular activating system (ARAS; Finke et al., 2012; Jones, 2003). The ARAS is
a complex network of various nuclei in the brainstem which are associated to arousal and
of which the noradrenergic locus coeruleus is strongly related to the warning signal in an
alertness task (Aston-Jones & Cohen, 2005). The top-down control of the alerting system
is mainly exerted by higher cognitive control areas associated with frontal lobe structures,
which develop later in the ontogenesis of the brain. The ARAS, however, is a structure
that develops earlier in the ontogenesis of the brain.
As the brain develops from the bottom to the top, it is obvious that ontogenetic
younger brain structures are especially vulnerable to exogenous distortions. One sig­
nificant influencing factor for the early brain development may be the specific experience
of prematurity. Prematurity interrupts the prenatal brain development that goes through
substantial formative changes between 20 and 40 weeks of gestation including an
exponential volume increase of the cortical plate and surface, neuronal migration, glia
cell proliferation, synaptogenesis, wiring and reorganization, and myelination (Vasung
et al., 2019; Volpe, 2009). Additionally, the preterm brain may be exposed to multiple
risks in the neonatal period including infections, medication administration, and respira­
tory complications, nutritional compromise, sedation, the abnormal environment of the
neonatal intensive care unit (NICU), procedural pain, and stress (Bennet et al., 2013;
Dean et al., 2014). Consequently, the structural and functional brain development and
thus the complex spatial and temporal sequence of the brain development and the regular
 CHILD NEUROPSYCHOLOGY 1075

brain maturation is affected (Allin et al., 2011; Bennet et al., 2013; Nagy et al., 2011;
Nosarti et al., 2008). Reported deviations of the preterm brain include perturbation of the
trajectory of cerebral development with disturbed maturation of white and gray matter
microstructure (Murray et al., 2016; Zhou et al., 2018), alterations of cortical thickening
(Rimol et al., 2016, 2019) and general volume reduction of subcortical structures
(Brumbaugh et al., 2016; Chau et al., 2019). Additionally, there is evidence of long-
lasting changes in neural connectivity such as reduced thalamocortical connectivity
(Bennet et al., 2013; Kapellou et al., 2006; Zubiaurre-Elorza et al., 2014). As structural
brain alterations are associated with a complex combination of motor, cognitive and
behavioral concerns (Allin et al., 2011; Bennet et al., 2013; Murray et al., 2016; Schneider
& Miller, 2019) the likelihood of negative long-term outcomes after preterm birth
increases, whereas the prevalence of deviant outcomes is inversely related to the gesta­
tional age (Stoll et al., 2010). Well-known long-term outcomes may include neurosensory
deficits, cognitive disadvantages (Marret et al., 2013; Zubiaurre-Elorza et al., 2014),
neuropsychological deficits (Zubiaurre-Elorza et al., 2014), and psychiatric disorders
(James et al., 2020; Johnson et al., 2010). Most frequently, particular forms of attention
deficits are described (Breeman et al., 2016; James et al., 2020; Johnson & Marlow, 2011;
Murray et al., 2016). These deficits seem to differ in phenomenology and pathogenesis
from the combined presentation of an Attention-Deficit/Hyperactivity Disorder
(ADHD) as defined in the Diagnostic and Statistical Manual for Mental disorders, fifth
edition (DSM-V; American Psychiatric Association, 2013) in cohorts born at term
(Indredavik et al., 2004; Johnson & Marlow, 2011). Therefore, they apparently reflect
the specific experience of prematurity and its consequences for the early brain develop­
ment. The pathogenesis of the attention deficits following prematurity seems to have
a predominantly biological etiology as these deficits are associated to the known neuro­
logical consequences of preterm birth as described above. According to the phenomen­
ology of the attention deficits following prematurity clinical symptoms of hyperactivity,
impulsivity or behavioral problems often are absent on the behavioral level (Indredavik
et al., 2004; Johnson et al., 2010; Johnson & Marlow, 2011). In that sense Johnson (2007)
suggests the term “purer” form of attention deficits. In a neuropsychological oriented
attention task Gawehn (2009), Strang-Karlsson et al. (2010), and de Kieviet et al. (2012)
found slower reaction times in preterm children compared to term children in a tonic
alertness task. These results suggest reduced top-down controlled processes in preterm
children. Additionally, Jaeger et al. (2019) found EEG alterations in preschool aged
healthy preterm children and suggest a general arousal deficit on the neurophysiological
basis. These findings suggest that attention deficits following prematurity seem to
particularly include deficits in basic aspects of attention regulation i.e., alertness. As
mentioned above alertness is indispensable in everyday life and also for learning at
school. According to the school performance deficits in alertness or attention regulation
may be associated with lower learning outcomes and might cause poorer educational
achievement of preterm children compared to their term peers (Brogan et al., 2014).
Therefore, children at risk should be identified at the earliest possible date in order to
enable specific support.
On the behavioral level, alertness is typically assessed by measuring reaction times
(RTs) in the presence (phasic) or absence (tonic) of a preceding warning signal (Sturm
et al., 1999). The difference between tonic and phasic triggered reaction time is usually
1076 D. A. JAEGER ET AL.

expressed in an increase in response speed in the phasic reaction time as they profit from
the warning of the external cue (Périn et al., 2010). Additionally, Sprengelmeyer et al.
(1995) suggested a division of response time into decision and movement time to
quantify more exactly the contribution of cognitive and motor performance to reaction
times. This is realized by recording the time until subject release a pressed home button,
which is defined as decision time. Movement time is assessed by measuring the time after
releasing the home button and pressing the target button.
The current study aimed to extend the understanding of attention functioning follow­
ing prematurity in preschool aged, healthy preterm children compared to term children.
Therefore, we modified and expanded the subtest (tonic) Alertness of the computerized
test of attentional performance for children, (KITAP; Zimmermann et al., 2002) to
investigate phasic alertness and tonic alertness which rely differentially on top-down
and bottom-up controlled process, independently. To the best of our knowledge, this
study is the first that investigated phasic alertness additionally to tonic alertness in this
specific cohort. Furthermore, the paradigm includes the division of reaction time into
decision and movement time, to quantify more exactly the relative contributions of
cognitive and motor performance in a reaction time task.

Methods
The study was approved by the local ethics committee of the Psychological Faculty of the
Ruhr University Bochum and adhered strictly to the requirements according to the
Declaration of Helsinki and its subsequent amendments.

Sample
We recruited 53 preschool children, aged between 60 and 79 months from Dortmund
and the surrounding areas. Children of the preterm group were born in the Municipal
Hospital Dortmund and were participating in an overall monocentric clinical follow-up
study belonging to the same age cohort. Neonatal data were available from the hospital
database. Information on the child’s biological and medical data, the psychosocial
environment, the parental academic background, and place of residence were acquired
using a questionnaire. Voluntary testing took place in the Municipal Hospital in
Dortmund and included two 45 minute sessions. Assent was obtained from all partici­
pants, whereby parents gave written informed consent for their children. After testing,
parents were informed about the test results in written and oral form. All children were
attending the last year before school enrollment at the age of 6. Children were in a public
kindergarten. To the best of our knowledge, no standardized educational curricula was
given in kindergarten, so that systematic differences in educational contexts between the
preterm and term-born groups may not be assumed.
To guarantee high group homogeneity and to minimize confounding factors on
attention functioning and therefore on the study results, we excluded children from
the data analysis when one of the following criteria was met: (1) gestational age < 28 as
these children have the highest risks for deviant outcomes (2) IQ score < 85, (3) ADHD
symptoms with clinical relevance, (4) significant conduct problems, (5) living in a high-
risk psychosocial environment >3 risks. Mean IQ score was assessed using the German
 CHILD NEUROPSYCHOLOGY 1077

version of the Wechsler Preschool and Primary Scale of Intelligence III (WPPSI-III;
Petermann et al., 2009). Presence of ADHD was diagnosed according to the criteria of the
DSM-V with a German parent questionnaire (Fremdbeurteilungsbogen für
Vorschulkinder mit Aufmerksamkeitsdefizit-/Hyperaktivitätsstörungen (FBB-ADHS-V;
Breuer & Döpfner, 2008). Conduct problems were revealed using the total difficulties
score of the Strengths and Difficulties Questionnaire (SDQ; Goodman, 1997). The
psychosocial environment was assessed using the Family Adversity Index (FAI; Rutter
& Quinton, 1977). A FAI score of three or more indicates a high-risk psychosocial
environment. Parental education was coded as no degree, lower secondary education,
secondary education, or high school or university degree.
After exclusion, the group of preterm children included 31 children (13 females, 18
males, Mage = 68, SDage = 6). Mean gestational age was 32 weeks (SD = 2.8; range, 28–36),
see Figure 1) and mean birth weight was 1701 gram (SD = 646; range, 600–3590). Preterm
children stayed in hospital on average for 40 days after birth (SD = 24; range, 5–104).
Among the preterm children three (9.7%) were too small for their gestational age and 20
(65%) had some kind of respiratory distress after birth, requiring assisted ventilation or
respiratory support. No further medical risks such as PeriVentricular Leukomalacia
(PVL), Intraventricular Hemorrhage (IVH), neonatal asphyxia, congenital malforma­
tions or neurosensory deficits were reported.
The group of term children was recruited via postings in kindergartens and included
22 children (11 females, 11 males, Mage = 68, SDage = 7). Mean gestational age was
41 weeks (SD = 2.8; range, 37–41), (see Figure 1) with a mean birth weight of 3662 gram
(SD = 500; range, 2870–4700). No pre-, peri-, or postnatal complications were reported,

Figure 1. Distribution of the sample according to the gestational age.

1078 D. A. JAEGER ET AL.

Table 1. Mean (and SD) of biological, medical, and social variables in term children and
preterm children.
Term Preterm
(n = 22) (n = 31)
Biological and medical variables
Age at time of testing(month) 68 (7) 68 (6)
Birth weight (gram) 3662 (500) 1701 (646) 0.89a
Gestational age (weeks) 41 (7.5) 32 (2.8) 0.000a
Hospitalization length after birth (days) 3 (1) 40 (24) 0.000a
Child’s gender, % female 50 0.000a
Maternal age at birth, years 30.5 (4.8) 0.41
Social variables
Parental academic background, Mdn 4.5 4 0.37 c
Family adversity index, Mdn 0 1 0.3
Data are given as mean (standard deviation) unless stated otherwise. Parental education was coded as 1
(no degree), 2 (lower secondary education), 3 (secondary education), 4 (high school diploma or
university degree). A FAI score of 3 or more indicates a high risk psychosocial environment.
a
Two-tailed significance based on a t test.
b
Two-tailed significance based on a χ2 test.
c
Two-tailed significance based on a Mann-Whitney U test.

and no developmental disorders were known. Mean time in hospital after birth was three
days (SD = 1; range, 1–7), (see Table 1).

Experimental procedure
For the present study, we used a task with low cognitive demands to assess basic
attentional processes by designing a modified alertness task derived from the standar­
dized computerized test of attentional performance for children (KITAP; Zimmermann
et al., 2002). The paradigm allowed for measuring two different states of alertness where
responses are obtained in conditions with and without a preceding cue. Conditions
without a cue intended to reflect participants’ intrinsic alertness referring to the tonic
aspects of this basic attentional function that maintains a sufficient level of arousal to
respond to an event at any given point in time (Tonic Alertness (TA) condition).
Responses with a preceding cue are thought to reflect the participants’ externally trig­
gered responsiveness to a salient event at any given time point (Phasic Alertness (PA)
condition) (Fan et al., 2005; Sturm & Willmes, 2001). Furthermore, the version of this
alertness task allows the segregation of decision and movement times as introduced by
Sprengelmeyer et al. (1995) to quantify more exactly the relative contributions of
cognitive and motor skills to performance of the reaction time task. In the TA condition,
the visual target stimulus (a witch), was presented at random time intervals on
a computer screen. In the PA condition, a short auditory warning signal of 1,000 Hz
preceded the visual stimulus. The Inter Trial Intervals (ITI) were in intervals of 750 ms,
1000 ms, 1500 ms, and 2000 ms before the appearance of the target to avoid rhythmic
appearance. Presentation of the target had a response-dependent abortion. For PA trials,
duration of the warning tone was fixed at a length of 500 ms followed by the same ITIs as
used in the TA condition. The paradigm was a 64-trial RT paradigm, consisting of 4
blocks of 16 trials. Blocks were arranged in the following order: TA(1) – PA(1) – PA(2) –
TA(2). All participants were trained before data were recorded to ensure, that they had
understood the task.
 CHILD NEUROPSYCHOLOGY 1079

During both conditions, participants were seated in a light and sound attenuated room
fixating a computer screen and were asked to attentively look at it all the time.
Participants were instructed to hold the home key (key 1) pressed with the preferred
hand until the witch appears. As soon as the witch appeared, they were instructed to
release the home key and press the response key (key 2) with the same hand. By pressing
the response key the witch disappears. Response time and acuity were recorded to control
for the performance level. For the overall reaction time we measured the entire response
time from stimulus onset until pressing the response key. The decision time was defined
as the response time from stimulus onset until releasing the home key. The movement
time was defined as the response time from releasing the home key to press the response
key. In this paper we report the comparisons between the tonic and phasic alertness
condition for RT, DT, and MT (see Figure 2).

Statistical analysis
Data were analyzed using SPSS Statistics Version 23 (https://www.ibm.com/de-de/analy
tics/spss-statistics-software). Independent samples t-tests were used for group compar­
isons of biological and medical variables. Sex was compared between groups using a chi-
squared analysis and social variables were compared using a Mann–Whitney U test.
Mean response time was calculated for both conditions (tonic alertness and phasic
alertness) and each variable (RT, DT, MT). Group differences on the computerized
measures were analyzed using Multivariate Analysis of Variance (MANOVA) with
group as between-subject factor. Afterward, paired samples t-tests were used to probe
significant effects within groups and between conditions (tonic alertness and phasic
alertness) for each variable of the computerized measures (reaction time, decision time,

Figure 2. Schematic illustration of the experimental procedure. The participants were asked to fixate
the computer screen and were instructed to keep the home key (key 1) pressed until the stimulus
onset. After stimulus onset they had to release the home key and press the response key (key 2) as
soon as possible. Decision Time (DT) was defined as the interval between stimulus onset and releasing
the home key, while Movement Time (MT) was defined as the interval between releasing the home
key and pressing the response key. The overall Reaction Time (RT) was defined as the time interval
between stimulus onset and pressing the response key. For the phasic alertness condition, a warning
signal precedes the stimulus onset.
1080 D. A. JAEGER ET AL.

movement time). Finally, independent samples t-tests were used to examine differences
for each variable (reaction time, decision time, movement time) for both conditions
(tonic alertness and phasic alertness) between the groups. An alpha of 0.05 was defined as
the threshold for statistically significant difference. Effect sizes were given as the propor­
tion of variance accounted for (partial η2).

Results
Sample characteristics
Groups were compared regarding age at time of testing, birth weight, gestational age,
lengths of stay in hospital, gender, maternal age at birth, parental academic background,
and family adversities. Groups did not differ with respect to age at time of testing
(t = 0.141, p = 0.89), gender distribution (χ2 = 0.67, p = 0.41), maternal age at birth
(t = −1.2, p = 0.24), parental academic background (U = 195, p = 0.37) and family
adversities (U = 289.5, p = 0.3). As expected, groups differed concerning the gestational
age (t = 12.23, p = 0.000), the birth weight (t = 11.91, p = 0.000), and the lengths of time in
hospital after birth (t = −7.12, p = 0.000), (see Table 1).

Alertness testing
Group differences on the computerized measures were tested using Multivariate Analysis
of Variance (MANOVA) with group (term children, preterm children) as the indepen­
dent variable and condition (phasic alertness, tonic alertness) for reaction time, decision
time, and movement time as dependent variables. Preterm children differed significantly
from term children in the tonic reaction time (F(1, 52) = 6.496, p = 0.01; η2 = 0.11), the
tonic decision time (F(1, 52) = 4.08, p = 0.049; η2 = 0.74) and in the tonic movement time
(F(1, 52) = 4.624, p = 0.036; η2 = 0.083). In the phasic condition, movement time yielded
evidence for significant difference (F(1, 52) = 5.077, p = 0.029; η2 = 0.091). No effects for
the phasic reaction time (F(1, 52) = 3.828, p = 0.056) and phasic decision time were found
(F(1, 52) = 0.285; p = 0.596), (see Table 2). We then used independent samples t-tests to
probe significant differences for the three response times (RT, DT, MT) in both condi­
tions between the groups (Figure 2). In the tonic condition, term children responded
faster, they had a shorter reaction time (MRT = 766, SDRT = 132, p = 0.014), a shorter

Table 2. Descriptive statistic of the computerized assessment. Results of the MANOVA for group
differences between term children and preterm children with regard to the computerized assessment.
Only for significant effects the effect sizes are given as the proportion of variance accounted for
(partial η2).
Term Preterm
(n = 22) (n = 31) F(1,52) p partial η2
Tonic Reaction time 766 (132) 877 (172) 6.496 0.014* 0.113
Decision time 491 (47) 529 (78) 4.08 0.049* 0.074
Movement time 275 (114) 348 (128) 4.624 0.036* 0.083
Phasic Reaction time 727 (156) 813 (158) 3.828 0.056 0.091
Decision time 455 (58) 465 (73) 0.285 0.596
Movement time 272 (122) 348 (119) 5.077 0.029*
Data are given as mean of the response time median (standard deviation). Mean is in msec. * stands for p < 0.05.
 CHILD NEUROPSYCHOLOGY 1081

Figure 3. Mean responses plotted for preterm children (solid line) and term children (dashed line) for
the mean reaction time (left column), mean decision time (middle column), and mean movement time
(right column). Delayed reaction time and delayed decision time in the tonic alertness condition but
not in the phasic alertness condition can be observed in preterm children compared to term children.
Furthermore, we found delayed motor responses in both conditions in preterm children. Both groups
showed the expected increase in response speed in the phasic condition for reaction time and
decision time. * stands for p< 0.05; ** p< 0.01; ***p< 0.001.

decision time (MDT = 491, SDDT = 47, p = 0.049) and a shorter movement time (MMR
= 275, SDMR = 114, p = 0.036) than preterm children (MRT = 877, SDRT = 172; MDT = 529,
SDDT = 78; MMR = 348, SDMR = 128). In the phasic condition, term children had a shorter
movement time (MMR = 272, SDMR = 122, p = 0.03) than preterm children (MMR = 348,
SDMR = 119). Taken together, preterm children showed prolonged reaction and pro­
longed decision time in the tonic alertness condition but not in the phasic alertness
condition. Motor responses were prolonged in both conditions in the preterm group.
In addition, we analyzed possible differences between these conditions within the
groups using paired t-tests separately for each group. As expected, preterm and term
children showed an increase in response speed in the phasic condition compared to the
tonic condition regarding the overall reaction time (preterm children: p = 0.007; term
children: p = 0.000). Interestingly, this increase in response speech in the phasic condi­
tion was also found regarding the decision time in both groups (preterm children:
p = 0.002; term children: p = 0.000) but not regarding the movement time (see Figure 3).

Discussion
This study investigated basic aspects of top-down and bottom-up-based attention func­
tioning following prematurity using a computerized test of phasic and tonic alertness in
preschool aged low risk healthy children. Furthermore, the paradigm includes the
division of reaction time into decision and movement time, to quantify more exactly
the relative contributions of cognitive and motor skills to performance of the reaction
time task. Findings yielded evidence for long-term deviations in the regulation of tonic
but not phasic alertness in healthy preterm children compared to term children in
preschool age. Current results suggest that the deviations are mainly due to delayed
decision-making processes and not only to motor performance. Results further suggest
that preterm children benefit from external triggers to overcome the deviations of
alertness regulation, which yield evidence for intact bottom-up controlled attention
process.
1082 D. A. JAEGER ET AL.

Comparing the overall reaction time in the phasic and tonic condition we found the
expected effect i.e., a characteristic increase in response speed in the phasic condition
(Périn et al., 2010) in both groups. This effect was also found for the decision times but
not for the movement times. Hence, motor response in both groups seems to be
unaffected by the warning cue. When comparing the groups, we found longer reaction
times, longer decision times, and longer movement times in the tonic alertness condition
in preterm children compared to term children. In contrast, in the phasic condition only
longer movement times in the preterm children compared to the term children were
found. Differences in the reaction and decision times were not longer found. Due to the
fact that the overall reaction time is the sum of the decision and the movement time and
that the differences in the phasic condition are no longer found in the overall reaction
and in the decision time but in the movement time, the current findings suggest that the
observed differences in the overall reaction time in the tonic alertness condition in
preterm children compared to the term children can be best explained by the longer
decision times and not only by the motor performance. Moreover, due to the fact that the
differences in the phasic condition in the overall reaction and decision time are no longer
found between the groups, findings suggest that the external trigger in the phasic
alertness task (warning cue) helps the preterm children to overcome their differences
in the alertness regulation, which yield evidence for an intact bottom-up controlled
attention process. Hence, we suggest a clear distinction between impaired top-down
(tonic alertness) and intact bottom-up (phasic alertness) processes. We conclude that
preterm children benefit from auditory cues to increase their alertness function, which
might provide a promising groundwork for the development of effective prevention
strategies or even therapeutical interventions (Jamieson et al., 2014; Pijnenborg et al.,
2007; Wilson et al., 1997). It may be speculated that this effect is based on consequences
of prematurity in the development of the underlying anatomical structures. As tonic
alertness is thought to be mediated in a predominantly top-down mode in self-initiated
preparation by a right-hemispheric network in combination with frontal lobe structures
and thalamic nuclei, phasic alertness is thought to be mediated mainly by exogenous
stimulation in a bottom-up mode by the ARAS (Jones, 2003). The ARAS receives direct
sensory input (warning cue) and is a structure that develops earlier in the ontogenesis of
the brain. Unfortunately, this study has some limitations that need to be taken into
account. This is a monocentric clinical study with all participants belonging to the same
age cohort. As a consequence, group sizes were relatively small. However, the strict in-
and exclusion criteria for this study precluded possible confounding factors such as
respiratory distress after birth or the long-lasting hospital stays.
Given the precautions and limitations, we are confident that our study has important
implications. This study showed that alterations in the preterm brain, even when severe
impairments are absent, seem to interfere with the tonic alerting system and that the
regulation of tonic alertness is altered in preterm children. These alterations fall below
diagnostic threshold on a symptom-based level and therefore seem to be subtle, but still
are significant. First, alertness represents a basic and core ability for successful perfor­
mance in everyday life and especially at school age as it is an important prerequisite for
learning (Jaekel et al., 2016). Children with deficits in their alertness functioning are
described as dreamy and lethargic at times, they often react delayed, and need multiple
addresses and stronger stimuli to respond (Jacobs & Petermann, 2007; Sturm, 2009; van
 CHILD NEUROPSYCHOLOGY 1083

Zomeren & Brouwer, 1994). Second, current literature reports that initially subtle
dysfunctions become more apparent when children get older (Aylward, 2005) and that
difficulties in preterm children become increasingly apparent at higher levels in school
(Smith & Knight-Jones, 1990). It may be speculated that the subclinical deviations found
in the preschool age become clinical relevant later on. Third, even when the deviations
fall below diagnostic threshold, they may cause specific learning disabilities and poor
academic attainment (Brogan et al., 2014) as current literature shows that preterm
children without severe disabilities or/with normal intellectual potential have problems
in later academic achievement, and show behavioral and learning difficulties and further
difficulties in everyday life (Aylward, 2002, 2005; Ornstein et al., 1991; Reuner et al., 2011;
Walther et al., 2000). These attention deviations are rarely identified in the preschool
period, as they usually pose no problem for the child during preschool activities. This
may change during school period when higher demands have to be met.
Unfortunately, no estimation of the school performance of the children participating
in this study has been made. Therefore, a follow-up study to assess the academic
development and to investigate whether the observed deviations are permanent or
temporary is needed. Furthermore, this study cannot give any conclusion on neural
correlates for the observed deviations. Therefore further research is essential.
Additionally, multi centric follow-up studies with nationwide cohorts might add the
neuropsychological assessment of attention function to their study design.
Taken into account that it may be challenging to encounter the subtle preterm
educational needs without over-pathologizing them, our results support every effort to
have a closer look at preterm children´s neuropsychological development in preschool
age. Even though clinically symptoms initially fall below diagnostic threshold they may
become clinical relevant later. Additionally, detecting subclinical levels in children is
nevertheless relevant for learning and essential to reliable predict academic achievement
(Breeman et al., 2016; Jaekel et al., 2016). If children receive appropriate support early at
preschool age or school accompanying services, a later negative development cascade on
learning may be prevented (Fry & Hale, 1996). Therefore, the results highlight the need
for keeping a low threshold for providing support to this particular at-risk group and
early identification is essential for effective prevention strategies. Specific educational
strategies to raise alertness functioning may be helpful to support preterm children.
Promising interventions could be adapted to the prosthetic technology already used for
people with memory impairments such as the NeuroPage system (Jamieson et al., 2014;
Pijnenborg et al., 2007; Wilson et al., 1997). As a consequence, diagnosis, measures and
interventions must be adapted for these children. In addition, psychoeducation and
advice for parents have to emerge. Moreover, we suggest investigation of the effects of
visual or tactile triggers/warning cues in a tonic alertness task. Additionally, we suggest
that future research should focus on the role of executive functions such as decision-
making processes as a possible explanation for the observed deviations.

Disclosure statement
No potential conflict of interest was reported by the author(s).
1084 D. A. JAEGER ET AL.

References
Allin, M. P. G., Kontis, D., Walshe, M., Wyatt, J., Barker, G. J., Kanaan, R. A. A., McGuire, P.,
Rifkin, L., Murray, R. M., & Nosarti, C. (2011). White matter and cognition in adults who were
born preterm. PLoS One, 6(10), e24525. https://doi.org/10.1371/journal.pone.0024525
American Psychiatric Association. (2013). DSM library. American Psychiatric Publishing, Inc.
https://doi.org/10.1176/appi.books.9780890425596
Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine
function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403–450.
https://doi.org/10.1146/annurev.neuro.28.061604.135709
Aylward, G. P. (2002). Cognitive and neuropsychological outcomes: More than IQ scores. Mental
Retardation and Developmental Disabilities Research Reviews, 8(4), 234–240. https://doi.org/10.
1002/mrdd.10043
Aylward, G. P. (2005). Neurodevelopmental outcomes of infants born prematurely. Journal of
Developmental and Behavioral Pediatrics, 26(6), 427–440. https://doi.org/10.1097/00004703-
200512000-00008
Bennet, L., van den Heuij, L., Dean, J. M., Drury, P., Wassink, G., & Gunn, A. J. (2013). Neural
plasticity and the Kennard principle: Does it work for the preterm brain? Clinical and
Experimental Pharmacology & Physiology, 40(11), 774–784. https://doi.org/10.1111/1440-
1681.12135
Breeman, L. D., Jaekel, J., Baumann, N., Bartmann, P., & Wolke, D. (2016). Attention problems in
very preterm children from childhood to adulthood: The Bavarian longitudinal study. Journal of
Child Psychology and Psychiatry, 57(2), 132–140. https://doi.org/10.1111/jcpp.12456
Breuer, D., & Döpfner, M. (2008). Entwicklung eines Fragebogens zur Erfassung von
Aufmerksamkeitsdefizit-/Hyperaktivitätsstörungen (ADHS) bei Vorschulkindern im Eltern-
und im Erziehungsurteil. Zeitschrift Für Entwicklungspsychologie Und Pädagogische
Psychologie, 40(1), 40–48. https://doi.org/10.1026/0049-8637.40.1.40
Brogan, E., Cragg, L., Gilmore, C., Marlow, N., Simms, V., & Johnson, S. (2014). Inattention in
very preterm children: Implications for screening and detection. Archives of Disease in
Childhood, 99(9), 834–839. https://doi.org/10.1136/archdischild-2013-305532
Brumbaugh, J. E., Conrad, A. L., Lee, J. K., DeVolder, I. J., Zimmerman, M. B., Magnotta, V. A.,
Axelson, E. D., & Nopoulos, P. C. (2016). Altered brain function, structure, and developmental
trajectory in children born late preterm. Pediatric Research, 80(2), 197–203. https://doi.org/10.
1038/pr.2016.82
Chau, C. M. Y., Ranger, M., Bichin, M., Park, M. T. M., Amaral, R. S. C., Chakravarty, M.,
Poskitt, K., Synnes, A. R., Miller, S. P., & Grunau, R. E. (2019). Hippocampus, amygdala, and
thalamus volumes in very preterm children at 8 years: Neonatal pain and genetic variation.
Frontiers in Behavioral Neuroscience, 13, 51. https://doi.org/10.3389/fnbeh.2019.00051
de Kieviet, J. F., van Elburg, R. M., Lafeber, H. N., & Oosterlaan, J. (2012). Attention problems of
very preterm children compared with age-matched term controls at school-age. The Journal of
Pediatrics, 161(5), 824–829.e1. https://doi.org/10.1016/j.jpeds.2012.05.010
Dean, J. M., Bennet, L., Back, S. A., McClendon, E., Riddle, A., & Gunn, A. J. (2014). What brakes
the preterm brain? An arresting story. Pediatric Research, 75(1–2), 227–233. https://doi.org/10.
1038/pr.2013.189
Fan, J., McCandliss, B. D., Fossella, J., Flombaum, J. I., & Posner, M. I. (2005). The activation of
attentional networks. NeuroImage, 26(2), 471–479. https://doi.org/10.1016/j.neuroimage.2005.
02.004
Finke, K., Matthias, E., Keller, I., Müller, H. J., Schneider, W. X., & Bublak, P. (2012). How does
phasic alerting improve performance in patients with unilateral neglect? A systematic analysis of
attentional processing capacity and spatial weighting mechanisms. Neuropsychologia, 50(6),
1178–1189. https://doi.org/10.1016/j.neuropsychologia.2012.02.008
Fry, A. F., & Hale, S. (1996). Processing speed, working memory, and fluid intelligence: Evidence
for a developmental cascade. Psychological Science, 7(4), 237–241. https://doi.org/10.1111/j.
1467-9280.1996.tb00366.x
 CHILD NEUROPSYCHOLOGY 1085

Gawehn, N. (2009). Die Entwicklung ehemaliger frühgeborener Kinder: Aufmerksamkeitsleistungen

ehemaliger Frühgeborener im Schul-und Vorschulalter. Kovač.
Goodman, R. (1997). The strengths and difficulties questionnaire: A research note. Journal of Child
Psychology and Psychiatry, 38(5), 581–586. https://doi.org/10.1111/j.1469-7610.1997.tb01545.x
Indredavik, M. S., Vik, T., Heyerdahl, S., Kulseng, S., Fayers, P., & Brubakk, A. M. (2004).
Psychiatric symptoms and disorders in adolescents with low birth weight. Archives of Disease
in Childhood - Fetal and Neonatal Edition, 89(5), F445–50. https://doi.org/10.1136/adc.2003.
038943
Jacobs, C., & Petermann, F. (2007). Aufmerksamkeitsstörungen bei Kindern: Langzeiteffekte des
neuropsychologischen Gruppenprogrammes ATTENTIONER. Kindheit Und Entwicklung, 16
(1), 40–49. https://doi.org/10.1026/0942-5403.16.1.40
Jaeger, D. A., Gawehn, N., Schölmerich, A., Schneider, D. T., & Suchan, B. (2019). Reduction of the
event-related potential P3 in preterm born 5-year-old healthy children. Clinical
Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology,
130(5), 675–682. https://doi.org/10.1016/j.clinph.2019.02.003
Jaekel, J., Eryigit-Madzwamuse, S., & Wolke, D. (2016). Preterm Toddlers’ inhibitory control
abilities predict attention regulation and academic achievement at age 8 years. The Journal of
Pediatrics, 169, 87–92.e1. https://doi.org/10.1016/j.jpeds.2015.10.029
James, S. N., Rommel, A. S., Rijsdijk, F., Michelini, G., McLoughlin, G., Brandeis, D.,
Banaschewski, T., Asherson, P., & Kuntsi, J. (2020). Is association of preterm birth with
cognitive-neurophysiological impairments and ADHD symptoms consistent with a causal
inference or due to familial confounds? Psychological Medicine, 50(8), 1278–1284. https://doi.
org/10.1017/S0033291719001211
Jamieson, M., Cullen, B., McGee-Lennon, M., Brewster, S., & Evans, J. J. (2014). The efficacy of
cognitive prosthetic technology for people with memory impairments: A systematic review and
meta-analysis. Neuropsychological Rehabilitation, 24(3–4), 419–444. https://doi.org/10.1080/
09602011.2013.825632
Johnson, S. (2007). Cognitive and behavioural outcomes following very preterm birth. Seminars in
Fetal & Neonatal Medicine, 12(5), 363–373. https://doi.org/10.1016/j.siny.2007.05.004
Johnson, S., Hollis, C., Kochhar, P., Hennessy, E., Wolke, D., & Marlow, N. (2010). Psychiatric
disorders in extremely preterm children: Longitudinal finding at age 11 years in the EPICure
study. Journal of the American Academy of Child and Adolescent Psychiatry, 49(5), 453–463.e1.
https://doi.org/10.1016/j.jaac.2010.02.002
Johnson, S., & Marlow, N. (2011). Preterm birth and childhood psychiatric disorders. Pediatric
Research, 69(5 Part 2), 11R–18R. https://doi.org/10.1203/PDR.0b013e318212faa0
Jones, B. E. (2003). Arousal systems. Frontiers in Bioscience: A Journal and Virtual Library, 8, s438–
51. https://doi.org/10.2741/1074
Kapellou, O., Counsell, S. J., Kennea, N., Dyet, L., Saeed, N., Stark, J., Maalouf, E., Duggan, P.,
Ajayi-Obe, M., Hajnal, J., Allsop, J. M., Boardman, J., Rutherford, M. A., Cowan, F., &
Edwards, A. D. (2006). Abnormal cortical development after premature birth shown by altered
allometric scaling of brain growth. PLoS Medicine, 3(8), e265. https://doi.org/10.1371/journal.
pmed.0030265
Marret, S., Marchand-Martin, L., Picaud, J. C., Hascoët, J. M., Arnaud, C., Rozé, J. C., Truffert, P.,
Larroque, B., Kaminski, M., & Ancel, P. Y., & for the, Epipage Study Group. (2013). Brain injury
in very preterm children and neurosensory and cognitive disabilities during childhood: The
EPIPAGE cohort study. PLoS One, 8(5), e62683. https://doi.org/10.1371/journal.pone.0062683
Murray, A. L., Thompson, D. K., Pascoe, L., Leemans, A., Inder, T. E., Doyle, L. W.,
Anderson, J. F. I., & Anderson, P. J. (2016). White matter abnormalities and impaired attention
abilities in children born very preterm. NeuroImage, 124(Part A), 75–84. https://doi.org/10.
1016/j.neuroimage.2015.08.044
Nagy, Z., Lagercrantz, H., & Hutton, C. (2011). Effects of preterm birth on cortical thickness
measured in adolescence. Cerebral Cortex, 21(2), 300–306. https://doi.org/10.1093/cercor/
bhq095
1086 D. A. JAEGER ET AL.

Nosarti, C., Giouroukou, E., Healy, E., Rifkin, L., Walshe, M., Reichenberg, A., Chitnis, X.,
Williams, S. C. R., & Murray, R. M. (2008). Grey and white matter distribution in very preterm
adolescents mediates neurodevelopmental outcome. Brain, 131(1), 205–217. https://doi.org/10.
1093/brain/awm282
Ornstein, M., Ohlsson, A., Edmonds, J., & Asztalos, E. (1991). Neonatal follow-up of very low
birthweight/extremely low birthweight infants to school age: A critical overview. Acta Paediatrica
Scandinavica, 80(8–9), 741–748. https://doi.org/10.1111/j.1651–2227.1991.tb11943.x
Périn, B., Godefroy, O., Fall, S., & Marco, G. D. (2010). Alertness in young healthy subjects: An
fMRI study of brain region interactivity enhanced by a warning signal. Brain and Cognition, 72
(2), 271–281. https://doi.org/10.1016/j.bandc.2009.09.010
Petermann, F., Ricken, F., Fritz, A., Schuck, K. D., & Preuß, U. (2009). Wechsler preschool and
primary scale of intelligence (3rd ed.). Frankfurt: Pearson.
Petersen, S. E., & Posner, M. I. (2012). The attention system of the human brain: 20 years after. Annual
Review of Neuroscience, 35, 73–89. https://doi.org/10.1146/annurev-neuro-062111-150525
Pijnenborg, G. H. M., Withaar, F. K., Evans, J. J., van den Bosch, R. J., & Brouwer, W. H. (2007).
SMS text messages as a prosthetic aid in the cognitive rehabilitation of schizophrenia.
Rehabilitation Psychology, 52(2), 236–240. https://doi.org/10.1037/0090-5550.52.2.236
Posner, M. I. (2008). Measuring alertness. Annals of the New York Academy of Sciences, 1129(1),
193–199. https://doi.org/10.1196/annals.1417.011
Posner, M. I., Nissen, M. J., & Ogden, W. C. (1978). Attended and unattended processing modes: The
role of set for spatial location. Modes of Perceiving and Processing Information, 137(158), 2.
Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of
Neuroscience, 13(1), 25–42. https://doi.org/10.1146/annurev.ne.13.030190.000325
Reuner, G., Hassenpflug, A., & Pietz, J. (2011). Langzeitentwicklung von Späten Frühgeborenen:
Schullaufbahnen und therapeutische Förderung. Frühförderung Interdisziplinär, 30(3),
144–150. https://doi.org/10.2378/fi2011.art12d
Rimol, L. M., Bjuland, K. J., Løhaugen, G. C. C., Martinussen, M., Evensen, K. A. I.,
Indredavik, M. S., Brubakk, A. M., Eikenes, L., Håberg, A. K., & Skranes, J. (2016). Cortical
trajectories during adolescence in preterm born teenagers with very low birthweight. Cortex, 75,
120–131. https://doi.org/10.1016/j.cortex.2015.12.001
Rimol, L. M., Botellero, V. L., Bjuland, K. J., Løhaugen, G. C. C., Lydersen, S., Evensen, K. A. I.,
Brubakk, A. M., Eikenes, L., Indredavik, M. S., Martinussen, M., Yendiki, A., Håberg, A. K., &
Skranes, J. (2019). Reduced white matter fractional anisotropy mediates cortical thickening in
adults born preterm with very low birthweight. NeuroImage, 188, 217–227. https://doi.org/10.
1016/j.neuroimage.2018.11.050
Rutter, M. & Quinton, D.(1977). Psychiatric disorder - ecological factors and concepts of causa­
tion. In M. McGurk (Ed.), Ecological factors in human development (pp. 173–187). Amsterdam:
Noord-Holland.
Schneider, J., & Miller, S. P. (2019). Chapter 7 - Preterm brain injury: White matter injury. In
L. S. de Vries & H. C. Glass (Eds.), Handbook of clinical neurology: Neonatal neurology (Vol. 162,
pp. 155–172). Elsevier. https://doi.org/10.1016/B978-0-444-64029-1.00007-2
Smith, A. E. A., & Knight-Jones, E. B. (1990). The abilities of very low-birthweight children and
their classroom controls. Developmental Medicine and Child Neurology, 32(7), 590–601. https://
doi.org/10.1111/j.1469-8749.1990.tb08543.x
Sprengelmeyer, R., Canavan, A. G. M., Lange, H. W., & Hömberg, V. (1995). Associative learning
in degenerative neostriatal disorders: Contrasts in explicit and implicit remembering between
Parkinson’s and huntington’s diseases. Movement Disorders, 10(1), 51–65. https://doi.org/10.
1002/mds.870100110
Stoll, B. J., Hansen, N. I., Bell, E. F., Shankaran, S., Laptook, A. R., Walsh, M. C., Hale, E. C.,
Newman, N. S., Schibler, K., Carlo, W. A., Kennedy, K. A., Poindexter, B. B., Finer, N. N.,
Ehrenkranz, R. A., Duara, S., Sánchez, P. J., O’Shea, T. M., Goldberg, R. N., van Meurs, K. P.,
& Higgins, R. D. (2010). Neonatal outcomes of extremely preterm infants from the NICHD
neonatal research network. Pediatrics, 126(3), 443–456. https://doi.org/10.1542/peds.2009-
2959
 CHILD NEUROPSYCHOLOGY 1087

Strang-Karlsson, S., Andersson, S., Paile-Hyvärinen, M., Darby, D., Hovi, P., Räikkönen, K.,
Pesonen, A. K., Heinonen, K., Järvenpää, A. L., & Eriksson, J. G. (2010). Slower reaction
times and impaired learning in young adults with birth weight< 1500 g. Pediatrics, 125(1),
e74–e82. https://doi.org/10.1542/peds.2009-1297
Sturm, W. (Ed.). (2009). Lehrbuch der klinischen Neuropsychologie: Grundlagen, Methoden,
Diagnostik, Therapie (2. Aufl.). Spektrum. http://deposit.d-nb.de/cgi-bin/dokserv?id=
2992285&prov=M&dok_var=1&dok_ext=htm
Sturm, W., Simone, A. D., Krause, B. J., Specht, K., Hesselmann, V., Radermacher, I., Herzog, H.,
Tellmann, L., Müller-Gärtner, H. W., & Willmes, K. (1999). Functional anatomy of intrinsic
alertness: Evidencefor a fronto-parietal-thalamic-brainstem network in theright hemisphere.
Neuropsychologia, 37(7), 797–805. https://doi.org/10.1016/S0028-3932(98)00141-9
Sturm, W., Thimm, M., Küst, J., Karbe, H., & Fink, G. R. (2006). Alertness-training in neglect:
Behavioral and imaging results. Restorative Neurology and Neuroscience, 24(4–6), 371–384.
Sturm, W., & Willmes, K. (2001). On the functional neuroanatomy of intrinsic and phasic
alertness. NeuroImage, 14(1), S76–S84. https://doi.org/10.1006/nimg.2001.0839
van Zomeren, A. H., & Brouwer, W. H. (1994). Clinical neuropsychology of attention. Oxford
University Press.
Vasung, L., Abaci Turk, E., Ferradal, S. L., Sutin, J., Stout, J. N., Ahtam, B., Lin, P. Y., & Grant, P. E.
(2019). Exploring early human brain development with structural and physiological
neuroimaging. NeuroImage, 187, 226–254. https://doi.org/10.1016/j.neuroimage.2018.07.041
Volpe, J. J. (2009). Brain injury in premature infants: A complex amalgam of destructive and
developmental disturbances. The Lancet Neurology, 8(1), 110–124. https://doi.org/10.1016/
S1474-4422(08)70294-1
Walther, F. J., den Ouden, A. L., & Verloove-Vanhorick, S. P. (2000). Looking back in time:
Outcome of a national cohort of very preterm infants born in The Netherlands in 1983. Early
Human Development, 59(3), 175–191. https://doi.org/10.1016/S0378-3782(00)00094-3
Wilson, B. A., Evans, J. J., Emslie, H., & Malinek, V. (1997). Evaluation of NeuroPage: A new
memory aid. Journal of Neurology, Neurosurgery, and Psychiatry, 63(1), 113–115. https://doi.
org/10.1136/jnnp.63.1.113
Zhou, L., Zhao, Y., Liu, X., Kuang, W., Zhu, H., Dai, J., He, M., Lui, S., Kemp, G. J., & Gong, Q.
(2018). Brain gray and white matter abnormalities in preterm-born adolescents: A
meta-analysis of voxel-based morphometry studies. PLoS One, 13(10), e0203498. https://doi.
org/10.1371/journal.pone.0203498
Zimmermann, P., Gondan, M., & Fimm, B. (2002). Testbatterie zur Aufmerksamkeitsprüfung für
Kinder (KITAP). Herzogenrath: Psytest.
Zubiaurre-Elorza, L., Soria, S., & Junqué, C. (2014). Neuropsychological impairment and brain
damage in children and adolescents associated with preterm birth. Anuario De Psicología/The
UB Journal of Psychology, 43(3), 285–295.