Journal of Clinical and Experimental Neuropsychology, 2015

Vol. 37, No. 10, 1036–1051, http://dx.doi.org/10.1080/13803395.2015.1076380

Neuropsychological assessment of children with

epilepsy and average intelligence using NEPSY II
Tiziana Zilli1, Sergio Zanini1, Stefania Conte2, Renato Borgatti3, and Cosimo Urgesi1,4
1
Scientific Institute Eugenio Medea, San Vito al Tagliamento (Pordenone), Italy
2
Department of Psychology, University of Milano-Bicocca, Milan, Italy
3
Scientific Institute Eugenio Medea, Bosisio Parini (Lecco), Italy
4
Department of Human Sciences, University of Udine, Udine, Italy

(Received 13 October 2014; accepted 20 July 2015)

Introduction: Many studies have shown altered neuropsychological functioning of children with epilepsy even in
the absence of intellectual disability, with notable concerns for both patients and their families. Although studies
have described the cognitive profiles associated with specific epilepsy syndromes, there is incomplete agreement on
the relation between spared and impaired abilities in different cognitive domains and on how deficits in one
neuropsychological ability can secondarily affect performance in other cognitive domains. The aim of this study
was to investigate the neuropsychological profile and vulnerabilities of children with epilepsy without intellectual
disability or borderline intellectual functioning. Method: 23 children aged 7–15 years, with a diagnosis of epilepsy
of genetic or unknown cause and average intellectual functioning (IQ >85), were administered all age-appropriate
tests of the Italian-language version (Urgesi, Campanella, & Fabbro, 2011) of a comprehensive neuropsycholo-
gical battery (NEPSY–II: A Developmental Neuropsychological Assessment, Second Edition; Korkman, Kirk, &
Kemp, 2007). Their performance was compared with that of a control group matched for gender, age, handedness
and education. Results: Children with epilepsy showed significant impairments as compared to the control group
in tests of attention and executive functions and sensorimotor skills. Notably, particular difficulties were observed
also in social perception tasks that require affect recognition, an ability that has been so far poorly considered in
children with epilepsy. Conclusions: The results highlight the importance of performing extensive evaluation of
cognitive functions, including social cognition processes, in children with epilepsy with average intelligence in
order to design appropriate interventions aimed at minimizing long-term consequences on educational and
behavioral outcome.

Keywords: Epilepsy; NEPSY; Social perception; Emotion; Neuropsychological assessment.

The specific effects of childhood epilepsy on neu-
rocognitive development are not clearly under-
stood, and further studies are needed. Previous
studies have reported that intellectual functioning
is within the average range in most children with
epilepsy of genetic or unknown cause (Berg
et al., 2008a; Camfield et al., 1984; Hauser &
Hesdorffer, 1990), albeit altered cognitive devel-
opment is often observed (Dodson, 1993; Nolan
et al., 2003; Sherman, Brooks, Fay-Mcclymont,
& MacAllister, 2012). In fact, even when children
with intellectual disability are excluded, children

The authors wish to thank Valentina Soriano and Elisa Conforto for their help in data collection. The authors are also thankful to
Sergio Imelio, Antonino Romeo, Monica Morbi, and all staff of the “Centro Regionale per l’Epilessia Infantile e Neurologia
Pediatrica” at the “Azienda Ospedaliera Fatebenefratelli e Oftalmico” (Milan, Italy) and of the Neurological Institute Carlo Besta
(Milan, Italy) for kind help in patient recruitment.
This work was supported by the Italian Ministry of Health under grant Ricerca Corrente 2013 Scientific Institute (IRCCS) Eugenio
Medea.
The authors declare no personal or institutional conflict of interests.
Address correspondence to: Tiziana Zilli or Cosimo Urgesi, Scientific Institute Eugenio Medea, via della Bontà, 7, San Vito al
Tagliamento (PN) I-33078 Italy (tiziana.zilli@sv.lnf.it or cosimo.urgesi@uniud.it).

© 2015 Taylor & Francis

 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
with epilepsy still present with lower IQ values as
compared to those of healthy controls (Berg et al.,
2008b). Furthermore, neuropsychological impair-
ments in specific cognitive domains are observed
particularly often in chronic epilepsy (Elger,
Helmstaedter, & Kurthen, 2004), but subtle
impairments are frequently highlighted in children
with epilepsy of genetic or unknown cause even in
the absence of intellectual disability (Chilosi,
Brovedani, Moscatelli, Bonanni, & Guerrini,
2006; Rantanen, Eriksson, & Nieminen, 2010;
Rantanen, Nieminen, & Eriksson, 2011). The
altered neuropsychological profile associated with
epilepsy is characterized by deficits in executive
functions, memory and learning, language, and
“psychomotor abilities” (Ay et al., 2009; Caplan
et al., 2008; Germanò et al., 2005; Haverkamp,
Hanisch, Mayer, & Noeker, 2001; Kavros et al.,
2008; Kernan et al., 2012; Oostrom et al., 2005;
Parrish et al., 2007). The impairments seem to be
present before the onset of epilepsy itself (Jackson
et al., 2013; Piccinelli et al., 2010) and to impact
negatively on academic achievement (Hermann
et al., 2006; Piccinelli et al., 2008).
Children with epilepsy are at high risk of devel-
oping behavioral problems, even more so than
children with other chronic conditions, such as
diabetes, that do not affect the central nervous
system (Davies, Heyman, & Goodman, 2003).
Behavioral problems especially involve the emo-
tional and affective axis, with internalizing beha-
viors such as anxiety and depression symptoms.
Furthermore, children with epilepsy exhibit lower
social competence as compared with children with-
out epilepsy (Piccinelli et al., 2010; Russ, Larson,
& Halfon, 2012). Even though emotional and psy-
chosocial impairments in persons with childhood-
onset epilepsy have been consistently reported, a
comprehensive understanding of the factors that
contribute to their onset and course is still lacking
(Oostrom et al., 2003). Many researchers associate
it with the role played by environmental factors,
such as parental ineffective coping strategies, social
stigma, or the child’s and the family’s inadequate
adaptive adjustment to the disease (Oostrom et al.,
2003). However, it is likely that the psychiatric and
psychosocial outcome depends on the interaction
between the above-mentioned environmental
factors and dispositional traits of children.
In this regard, while it is widely acknowledged that
children with epilepsy experience important social
difficulties (review in Drewel & Caplan, 2007),
many studies have so far used self- or parent-report
measures rather than formal neuropsychological
tests, and little is known about emotion recognition
and theory-of-mind competencies, especially in
1037
patients suffering from epilepsy of genetic or
unknown cause. Several studies have provided evi-
dence of social cognition deficits in adults with
Temporal Lobe Epilepsy (TLE). Indeed, TLE has
been associated with impairments in recognition of
facial expressions of fear (Reynders, Broks, Dickson,
Lee, & Turpin, 2005; Shaw et al., 2007), with greater
impairment in early-onset epilepsy both in adults
(Meletti et al., 2009; Sedda et al., 2013) and in chil-
dren (Golouboff et al., 2008; Laurent et al., 2014);
furthermore, lower performance at Theory-of-Mind
tasks has been reported in TLE patients (Schacher
et al., 2006). Along the same lines, frontal lobe epi-
lepsy (FLE) patients seem to be impaired in facial
emotion recognition as well as in inferring mental
states and emotion from gaze (Farrant, 2005).
Conversely, studies on the social cognition abilities
of children suffering from epilepsy of genetic or
unknown cause are scarce. Recently, Cantalupo
et al. (2013) found deficits in facial emotion recogni-
tion in children with a history of febrile seizures, and
Genizi et al. (2012) reported that a group of children
with a diagnosis of benign childhood epilepsy with
centro-temporal spikes showed mild impairments in
processing the affective, but not the cognitive second-
order theory-of-mind aspects, thus pointing to speci-
fic deficits in making inferences on how people repre-
sent the emotion of others. Finally, Lew et al. (2015)
tested social understanding abilities in children with
focal or generalized epilepsy by administering the
Strange Story Task, which evaluates the ability to
understand short passages depicting scenarios that
involve complex mental states as compared to sce-
narios that describe physical events, and the Mind in
the Eyes task, which measures the ability to identify
the correct emotion displayed in photographs of the
eye region of male and female adults. The authors
found that both children affected by generalized epi-
lepsy and those affected by focal epilepsy performed
poorly on understanding the mental stories of the
Strange Story Task compared to healthy controls,
whereas they seemed less compromised in the Mind
in the Eyes task. Importantly, the deficits at the
mental stories of the Strange Situation task were
independent from IQ levels, since differences
between epilepsy and control groups were still
observed when IQ was entered as covariate.
In child neuropsychology, recognition of the
neuropsychological deficits that can predict aca-
demic performance and psychosocial problems is
crucial in order to design appropriate interventions
aimed at minimizing long-term consequences on
educational and behavioral outcome. Given the
wide range of difficulties found in children affected
by epilepsy, neuropsychological assessment cannot
focus on estimating the level of functioning in
1038 ZILLI ET AL.
isolated cognitive abilities, such as language, mem-
ory, and attention, but it must consider the profile
of weaknesses and strengths of the wide spectrum
of children’s cognitive performance, including also
social perception abilities, which may impact on
their social life and psychological development. To
this end, research studies and clinical protocols
have so far used flexible batteries consisting of
several individual measures of neuropsychological
functioning rather than a co-normed multidimen-
sional battery. While using flexible batteries can
detect the presence of impairments in specific cog-
nitive domains, using standardized scores derived
from multiple individual tests, each normed on a
different sample, makes it impossible to compare
the relative pattern of strengths and weaknesses in
different cognitive domains. Indeed, it is widely
recognized (Palmer, Appelbaum, & Heaton, 2004;
Russell, Russell, & Hill, 2005) that using batteries
of separately developed tests is problematic, as
estimated cognitive levels may vary across tests
because of differences between normative samples
(e.g., size and composition) and lack of normative
information about the behavior of the battery as a
whole.
NEPSY-II (A Developmental Neuropsychological
Battery for children aged 3–16 years; Korkman,
Kirk, & Kemp, 2011) is a unique battery that pro-
vides a comprehensive overview of the child’s neu-
ropsychological functioning. It includes co-normed
measures of six neuropsychological domains—
namely, attentional/executive, language, sensori-
motor, visuo-spatial, learning and memory, and
social-perceptual abilities. The US (Korkman et al.,
2007) and Italian (Urgesi et al., 2011) standardiza-
tions of the NEPSY–II showed large intercorrelations
between the NEPSY–II tests both within (in particu-
lar for Language tests) and between domains (in
particular for Language and Attention and
Executive Function tests). These between-domain
intercorrelations in healthy individuals were prob-
ably caused by the similarity between stimulus
presentation procedures and response modality
and by general effects of attention resources on
task performance. These effects may suggest the
possibility that impairment in a cognitive domain
(e.g., language) may induce secondary impairment
in other tasks (i.e., executive functions) that
involve language mediation to perceive stimuli or
to provide response. Using a co-normed battery to
test the neuropsychological profile of children thus
allows estimating the expected amount of variance
in common between different tests and controlling
for the effects of specific deficits on other cognitive
domains. Several studies have documented the
effectiveness of NEPSY-II in identifying the
strengths and weaknesses associated with various
clinical conditions in children, such as restrictive-
type anorexia (Calderoni et al., 2013), high-
functioning autism spectrum disorder (Narzisi,
Muratori, Calderoni, Fabbro, & Urgesi, 2013),
prematurity with very low birth weight (Lind
et al., 2010, 2011; Olivieri et al., 2012), fetal alco-
hol spectrum disorders (Rasmussen et al., 2013),
and organ transplantation (Haavisto, Korkman,
Jalanko, Holmberg, & Qvist, 2010; Haavisto,
Korkman, Holmberg, Jalanko, & Qvist, 2012;
Haavisto et al., 2011).
Because of its widespread clinical use and mul-
tidimensional approach to neuropsychological
evaluation, NEPSY-II tests may be particularly
apt for testing the neuropsychological profile of
clinically referred children with epilepsy. A few
previous studies have used NEPSY (hereafter,
NEPSY refers to its first edition) evaluation with
children with epilepsy. Kolk, Beilmann, Tomberg,
Napa, and Talvik (2001) evaluated 4–9-year-old
children with chronic epilepsy and hemiparesis
(N = 18) or with newly diagnosed epilepsy (N =
12). Using the Estonian version of NEPSY
(Korkman, Kirk, & Fellman, 1998), which had
no test for the evaluation of social perception,
the authors found similar patterns of deficits in
the two groups, albeit more severe in the first,
with particular weaknesses in attention and lan-
guage, visuo-perceptual functions, and short-term
memory. Along the same lines, Bender, Marks,
Brown, Zach, and Zaroff (2007) administered the
earlier US-normed version of NEPSY to evaluate
19 children with epilepsy aged 3–12 years and
found impairments in attention/executive func-
tioning, language, and sensori-motor abilities,
whereas memory skills were less compromised
and visuo-spatial abilities were comparable to
those of nonneurologically impaired peers.
Furthermore, they showed that patients’ age, sei-
zure onset age, seizure frequency, and medication
status did not predict cognitive outcome. These
studies seem to suggest that NEPSY evaluation
may describe the relative patterns of strengths and
weaknesses in children with epilepsy indepen-
dently from associated complications. More
recently, Parisi et al. (2012) used 11 tests of the
Italian NEPSY-II version in 16 children reported
as suffering from benign epilepsy with centro-tem-
poral spikes, in 8 children having this form of
epilepsy plus migraine, and in a further group of
8 children having migraine but not epilepsy.
While migraine-only patients had deficits limited
to short- and long-term verbal memory, patients
with epilepsy, whether or not associated with
migraine, had widespread deficits in tri-
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
dimensional constructive abilities, visuo-percep-
tual processing, verbal comprehension and pho-
nological processing, visual attention, and
executive functions, as well as in short- and
long-term verbal memory. Unfortunately, social
perception abilities were not measured. Thus,
while previous studies have shown widespread
neuropsychological impairments in children with
epilepsy and demonstrated poor psychosocial out-
come (see Lin, Mula, & Hermann, 2012, for a
comprehensive review), there is limited knowledge
about how social perception abilities (namely,
theory of mind and emotion recognition) are
related to this general cognitive and neuropsycho-
logical profile. Thus, an important aim of the
present study was to study how deficits in social
perception are vulnerable in epilepsy indepen-
dently from deficits in other cognitive domains.
METHOD
Participants
Participants included children with uncompli-
cated epilepsy (EC) of genetic or unknown
cause and healthy controls (HC), selected
among the participants to the Italian standardi-
zation sample of NEPSY-II (Urgesi et al., 2011).
For each child in the EC group, two children
from the HC group were randomly selected from
those normative sample participants that were
matched to EC participants for age, sex, hand-
edness, and parents’ education. This was done to
increase the reliability of the comparison
between groups and to define better the expected
performance at each age (Haviland, Nagin, &
Rosenbaum, 2007). EC participants were 23
children (12 boys and 11 girls) aged 7–15 years
(mean = 9.8, SD = 2.6) and all attending main-
stream education; they were recruited from the
pediatric neurology clinic at three Italian
hospitals: Associazione Nostra Famiglia–
IRCCS Medea, Bosisio-Parini (Lecco); Azienda
Ospedaliera Fatebenefratelli (Milano); and
Istituto Neurologico Carlo Besta (Milano). The
same recruitment procedures were used across
the three centers. Inclusion criteria for recruit-
ment in the EC group included: (a) diagnosis of
epilepsy of genetic or unknown cause according
to the International League Against Epilepsy
(ILAE) criteria; (b) absence of intellectual dis-
abilities or borderline intellectual functioning as
evaluated by means of the Italian version of the
WISC-III (Orsini & Picone, 2006; Wechsler,
1039
1991; Full Scale Intelligence Quotient (FSIQ)
>85); (c) absence of other developmental disabil-
ities (i.e. developmental pervasive disorders); (d)
chronological age between 7 and 16 years. EC
had normal neurological examinations, no iden-
tifiable lesions on MRI, and no signs of neuro-
logical abnormalities. The rationale of these
restrictive inclusion criteria, in particular for IQ
level, was to ensure matching the IQ levels of the
epilepsy and control groups and detect the spe-
cific pattern of neuropsychological alterations in
children who suffer from epilepsy but have aver-
age intelligence. While studies have shown that
the majority of children with epilepsy of genetic
or unknown cause present IQ levels within nor-
mal range (>80; Berg et al., 2008a), intellectual
disability is often observed (e.g., Sherman et al.,
2012). Furthermore, comparing children with
epilepsy and normal IQ levels (>80) with con-
trols may still reveal subtle cognitive deficits at
the group level (Berg et al., 2008b). Thus, using
a restrictive criterion for IQ ensured comparable
IQ levels in the two groups and avoided the use
of IQ as a covariate in the analysis (Dennis
et al., 2009). This allowed us to explore the
relational pattern of neuropsychological weak-
nesses and strengths across different cognitive
domains independently of general cognitive def-
icits that may affect performance across multiple
domains. Diagnosis of epilepsy was performed
according to the ILAE classification, and it
was based on clinical and electroencephalo-
graphic findings. Information regarding seizure
history was obtained from available medical
records. In terms of medication, 18 patients with
epilepsy were being treated with at least one type
of antiepileptic drug at the time of neuropsycholo-
gical evaluation, 3 children were not treated, and
for 2 cases this information was not available.
Patients’ clinical characteristics are summarized in
Table 1. Before inclusion into the standardization
sample, HC individuals were screened with stan-
dardized neuropsychological tests of verbal (Marini
et al., 2007) and nonverbal general cognitive abil-
ities (Goodenough, 1975; Raven, 1954) in order to
exclude deficits of verbal or visuospatial abilities.
All research participants were native Italian
speakers.
Informed consent was obtained from all partici-
pants, and their parents signed a written informed
consent. The procedures were approved by the
local Ethics Committee of the Scientific Institute
(IRCCS) E. Medea (Bosisio Parini, Lecco, Italy)
and were in accordance with the Helsinki
Declaration guidelines.
1040 ZILLI ET AL.

TABLE 1
Demographic and clinical variables of children with epilepsy

Age Epilepsy Seizure Onset

Patient Sex (yr) Handedness IQ type Lateralization Localization Age (yr) AED Therapy

1 f 8 left 102 P N/A N/A 4 VPA-LEV-ETS

2 m 12 right 101 P right centro-temporal 8 VPA-ETS
3 m 10 right 107 P right fronto-temporal 8 CBZ
4 f 15 right 98 P right posterior temporal 9 ETS-VPA
5 m 9 right 103 G — — 9 CBZ
6 f 13 right 108 G — — N/A VPA
7 f 7 right 88 G — — N/A VPA
8 f 13 right 115 G — — N/A VPA
9 f 11 right 99 G — — N/A VPA
10 f 8 right 121 P N/A N/A N/A VPA
11 m 12 left N/A P left centro-frontal 9 N/A
12 f 8 right N/A P left centro-temporal 8 N/A
13 f 9 right N/A. P left centro-temporal 8 N/A
14 m 10 right N/A P right multifocal 10 VPA
15 f 9 right N/A P right centro-temporal 7 VPA
16 m 13 right 88 P right frontal 5 CBZ-VPA-BDZ
17 m 7 right 89 G — — 5 VPA
18 m 10 right 110 P N/A N/A 4 VPA-ETS-LEV
19 m 11 right 109 G — — 6 N/A
20 m 14 right 91 P N/A N/A 8 CBZ
21 m 7 right 104 P right parieto-occipital 6 VPA
22 m 15 right 104 G — — 9 N/A
23 f 11 right 124 G — — 1 BDZ-CBZ
Overall f: 11 M: 9.8 left: 2 M: 104 P: 14 M: 6.5
m: 12 DS: 2,6 right: 22 DS: 10 G: 9 DS: 2.4

Note. AED = Antiepileptic drug; LEV = Levetiracetam; ETS = ethosuximide; CBZ = carbamazepine; BDZ = Benzodiazepine.
N/A = not available; P = partial; G = generalized; VPA = Valproate.

Neuropsychological assessment administration procedures in the standardization

Patients and controls underwent a full neuropsycho-
logical evaluation using the 30 (out of 33) tests of
the Italian NEPSY–II version that can be com-
pleted by individuals aged 7–16 years. NEPSY-II
is an age-scaled flexible battery, in which some tests
are submitted to all age groups, whereas others are
age-specific; here we used those tests that can be
administered to all children aged 7–16 years and
limited our sample inclusion criteria accordingly.
Precisely the same procedures (i.e., stimuli, instruc-
tions and scoring rules) detailed in the
commercially available version of the Italian
NEPSY-II (Korkman et al., 2011) were used for
testing both children in the Italian standardization
sample and children with epilepsy in the present
study. It is worth noting that the Italian version of
NEPSY-II is slightly different from the English-lan-
guage version (Korkman et al., 2007), because it
was adapted from the Standardization battery used
during the US national standardization and it was
normed on 800 Italian children aged 3–16 years.
This ensures full comparability of the
sample and in children with epilepsy in the present
study. In particular, the Italian version includes the
Visual Attention subtest, which was taken from the
first English-language version of NEPSY (Korkman
et al., 1998) but was not included in the English-
language version of NEPSY-II (Korkman et al.,
2007), and has slightly broader age ranges for
some tests (e.g., 5–16 years for Design Fluency) as
compared to the English language version. The
NEPSY–II tests were administered in the same
order to all participants by one trained clinician.
Participants were tested individually in two or
three sessions, each lasting approximately 1.5 to 2
hr. Sessions were administered in two or three dif-
ferent days at intervals of fewer than 7 days. The
same examiner evaluated each participant across all
sections. The NEPSY-II tests were administered in
the order suggested by the Italian NEPSY II admin-
istration manual (Urgesi et al., 2011), thus ensuring
that patients and controls performed the test in the
same order. A brief description of the tests included
in the Italian version of NEPSY-II for each of the
six neuropsychological domains is provided below.
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
Attention and executive functioning
This domain includes six tests.
Visual Attention. This task assesses sustained
and selective visual attention abilities. The child is
required to scan a 29.7 × 42 cm sheet and mark
specified visual targets among several similar
distracters.
Design Fluency. This test assesses behavioral
productivity. The child is required to generate
unique designs by connecting two or more dots
presented in a structured or random array contain-
ing five dots each.
Auditory Attention and Response Set. The child
listens to a series of words and points to the appro-
priate circle when he/she hears a target word.
Auditory Attention evaluates selective and sus-
tained auditory attention and requires the child to
point to one circle when one color is named, while
ignoring other colors. Response Set assesses the
ability to shift and maintain a new and complex
response set involving inhibition of automatic
responses and alternating between matching or
contrasting stimuli.
Inhibition. This task evaluates the ability to inhi-
bit automatic responses and shift between congru-
ent or incongruent responses during naming of
visual stimuli. The naming condition (Inhibition
A) requires the child to name the shape of squares
and circles or the up or down direction of arrows;
the inhibition condition (Inhibition B) requires the
child to provide the opposite naming response on
the same stimuli; the switching condition
(Inhibition C) requires the child to provide the
congruent or the incongruent naming response
according to the color of the target. For the pur-
pose of this study, only the time taken to complete
the tasks was entered for statistical analyses,
because preliminary inspection of the data showed
highly skewed distribution of accuracy values.
Clocks. This test evaluates planning and organi-
zation of visuospatial processing and the concept
of time by requiring the child to read or draw the
times on analogical or digital clocks.
Animal Sorting. The test requires the child to
sort eight cards into two groups of four cards
each using various self-initiated sorting criteria.
1041
Language
This domain includes six tests.
Comprehension of Instructions. The test evalu-
ates noncontextual language understanding. The
child is asked to point to a given sequence of
stimuli of different colors and shapes (crosses and
circles) in response to oral instructions of increas-
ing syntactic complexity.
Speeded Naming. This task assesses lexical
retrieval/verbal production speed. In the version
for older children (>7 years of age), the child has
to name as quickly as possible the color, shape,
and size of arrays of geometrical shapes and to
read arrays of letters and numbers. The item with
letters and numbers is only administered to 9–16-
year-old children.
Phonological Processing. The test assesses pho-
nemic awareness and meta-phonological skills. The
child is required to drop or substitute a syllable or
a phoneme in a given word to create a new word.
Word Generation. The test assesses verbal pro-
ductivity. It requires the child to produce as many
words as possible on the basis of semantic or phono-
logical categories; 1 min is allowed for each category.
Repetition of Nonsense Words. This test assesses
phonological encoding and decoding. The child is
asked to repeat nonsense words presented aloud.
Oromotor Sequences. The test evaluates oromo-
tor coordination. The child has to repeat onoma-
topoeic sounds and hard-to-pronounce phrases
consecutively five times.
Memory and learning
This domain comprises seven tests evaluating
verbal and visuo-spatial abilities, with short- and
long-term retrieval.
Memory for Faces. The test assesses face discri-
mination and recognition. The child looks at a
series of faces in an incidental learning procedure
and then, in immediate and delayed recall condi-
tions, is shown three photographs at a time, from
which he/she selects the face that was shown
previously.
Word List Interference. The test assesses verbal
working memory, repetition, and recall of a list of
words following interference by presentation and
1042 ZILLI ET AL.
recall of another list. The child is presented with
two series of words and asked to repeat each
sequence following its presentation. Afterwards
he/she recalls the first and the second sequences
of words in the order of presentation.
Memory for Designs. The test assesses memory
of visual stimuli and spatial location of novel mate-
rial. The child is shown a series of nonfigural
abstract shapes placed on a grid, which are, there-
after, removed from view. In immediate or delayed
recall conditions after each presentation, he/she is
required to select the appropriate shapes from a set
of cards and place them onto an empty grid in the
corresponding positions.
List Memory. The test assesses verbal learning
memory. The child is read a list of words several
times and is asked to recall them after each presenta-
tion as well as in a delayed retrieval condition.
Memory for Names. The test assesses visuo-ver-
bal association learning. The child is asked to learn
the name of children drawn on eight cards and
presented three times each and to recall them
after a period of time (delayed condition).
Narrative Memory. The test assesses story recall
abilities. The child listens to a story and is asked to
repeat it. He/she is then asked questions to elicit
missing details from his or her recall of the story.
Sentence Repetition. The test assesses the ability
to immediately repeat sentences of increasing
length and complexity.
Sensorimotor functions
This domain comprises three tests.
Fingertip Tapping. The test evaluates motor
dexterity in repetitive finger movements and
motor programming in sequences of finger
movements.
Imitating Hand Positions. This test evaluates
ideomotor praxis abilities and requires the child
to imitate, separately with the dominant or non-
dominant hand, various hand/finger positions per-
formed by the examiner.
Manual Motor Sequences. The test assesses
planning and coordination of sequences of hand
movements. It requires the child to imitate five
times series of rhythmic unimanual or bimanual
movements demonstrated by the examiner.
Social perception
This domain includes two tests.
Theory of Mind. The test assesses the ability to
understand mental functions such as belief, inten-
tion, deception, emotion, imagination, and pre-
tending, as well as the ability to understand that
others have their own thoughts and feelings.
Furthermore, it evaluates the capacity to under-
stand how certain emotions are linked to given
social situations. In the verbal task (Theory of
Mind A), the child is read various scenarios or
shown pictures and is then asked questions that
require knowledge of another individual’s point
of view to be correctly answered. In the contextual
items (Theory of Mind B), the child is shown a
series of pictorial descriptions of some social situa-
tions and has to select the photograph depicting
the appropriate emotion that the social settings
generate.
Affect Recognition. The test assesses the ability
to recognize emotional expressions (happy, sad,
anger, fear, disgust, and neutral) from photographs
of children’s faces in several matching tasks. The
child has to match the two faces expressing the
same emotions among three or more alternatives.
Visuo-spatial processing
This domain comprises six tests.
Design Copying. The test assesses constructional
abilities. The child is asked to copy two-dimen-
sional geometric figures of increasing complexity.
Block Construction. The test assesses visuo-spa-
tial and visuo-motor abilities. The child has to
reproduce three-dimensional constructions from
two-dimensional drawings by assembling an
increasing number of blocks.
Picture Puzzles. This test assesses visual discri-
mination, visual scanning, and recognition of part–
whole relationships. The child identifies, on a large
picture, the section from which each of four small
pictures, presented separately, was taken.
Geometric Puzzles. This test investigates the
ability to identify and match geometric shapes of
increasing complexity (design recognition) as well
as mental rotation abilities. The child has to match
two figures, among six, to the corresponding
rotated shapes contained in a grid with other dis-
tracter figures.
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
Route Finding. The test assesses the knowledge of
visual-spatial relations and the ability to orientate on
a map. The child is asked to transfer a route from a
simple schematic map to a more complex one.
Arrows. This test assesses line orientation judg-
ment. The child has to look at an array of arrows
arranged around a target and to indicate which
arrows point to the center of the target.
Data Analysis
Results were analyzed using Statistical package
software “STATISTICA”, version 7 (Statsoft.inc).
The scores obtained by each participant were
expressed as scaled scores (M = 10, SD = 3; with-
out approximation at the low or high extreme)
with respect to the normative values for the corre-
sponding chronological ages (Urgesi et al., 2011).
Normal distribution was verified with the Shapiro-
Wilk’s W test. Six multivariate analyses of variance
(MANOVAs) were then performed, one for each
NEPSY-II domain. Significance threshold was set
at α value < .008, thus applying Bonferroni correc-
tion to control for false discoveries in multiple
comparisons. Effect size was estimated with partial
eta-squared (η2p) measure at the domain level and
Cohen’s d for each test (see Table 2). Post-hoc
univariate analyses were conducted to compare
group means for each variable included in domains
with significant overall group differences. For post-
hoc univariate analyses, we corrected significance
thresholds using a Bonferroni correction procedure
for the number of variables included in each
domain; thus significance threshold was different
for each ANOVA depending on the number of
comparisons performed in each domain (attention
and executive functions: 9 variables, α value < .005;
sensorimotor function and social perception: 3
variables each, α value < .016).
In a supplementary analysis, we also explored
how specific domains contributed to significance
differences in each test at which EC had lower
performance than HC. Six domain scores were
obtained by averaging the individual scaled scores
for all the tests comprised in each cognitive domain
and were entered as covariates of interest into
series of ANCOVAs, one for each test that
revealed between-group differences in the previous
analysis. Considering the post-hoc explorative nat-
ure of this analysis, a noncorrected significance
threshold of α value < .05 was used.
1043
RESULTS
Table 2 shows means, standard deviations, and
Cohen’s d values of the scores obtained by the
two groups (EC, HC).
Group differences for each
neuropsychological domain
The MANOVA for the Attention and Executive
Functions domain showed significantly lower
functioning of EC as compared to HC, F(9, 59)
= 3.16, p < .001, η2p = .325; post hoc univariate
analyses showed that EC performed significantly
worse than HC in Response Set, F(1, 67) = 19.31,
p < .001, Inhibition A, F(1, 67) = 11.69, p = .001,
and Inhibition C, F(1, 67) = 10.68, p = .002,
whereas no statistical differences were seen in
Visual Attention, Auditory Attention, Clocks, or
Design Fluency, all F(1, 67) < 4.1, p > .04.
Nonsignificant between-group differences were
obtained from the MANOVAs for the Language,
F(7, 61) = 1.62, p < .1, η2p = .157, and Memory
and Learning domains, F(7, 61) = 1.62, p = .1, η2p
= .199. Conversely, the MANOVA for the
Sensorimotor domain showed a significantly
lower functioning of the EC group compared to
the HC one, F(3, 65) = 5.64, p < .001, η2p = .206);
post hoc univariate analysis showed that EC per-
formed significantly worse than HC only in
Imitating Hand Positions, F(1, 67) = 13.56, p <
.001, but not in Fingertip Tapping and Manual
Motor Sequences, all F(1, 67) < 3.1, p > .08.
Along the same lines, the MANOVA for the
Social Perception domain revealed significantly
lower functioning of the EC group compared to
the HC one, F(3, 65) = 4.50, p = .006, η2p = .172;
post hoc univariate analysis showed that EC per-
formed significantly worse than HC both in the
Affect Recognition, F(1, 67) = 12.8, p < .001, and
in the Theory of Mind–contextual tasks, F(1, 67)
= 6.19, p = .015, but not in the Theory of Mind–
verbal task, F(1, 67) < 1. Finally, nonsignificant
differences between the two groups were obtained
from the MANOVA in the Visuospatial
Processing domain, F(6, 62) = 2.70, p = .02, η2p
= .207. In sum, the results showed that EC pre-
sented with significant impairments, as compared
to HC, in criterion shifting (Response Set and
Inhibition C), motor imitation (Imitating Hand
Positions), and processing of emotional facial
expressions (Affect Recognition and Theory of
Mind B).
1044 ZILLI ET AL.

TABLE 2
Comparison of the performance of children with epilepsy and healthy controls at NEPSY-II tests

Test EC mean HC mean EC SD HC SD Cohen’s d

Visual Attention 9.71 9.82 4 2.66 0.04 negligible effect

Design Fluency 9.68 10.08 2.18 3.12 00:14 negligible effect
Auditory Attention 9 10:43 03:43 02:01 00:58 medium effect
Response Set 07:46 10:46 03:43 02:22 01:17 very large effect
Inhibition A 6.87 10:19 4.87 03:16 0.92 large effect
Inhibition B 07:55 9.63 4.67 3.69 00:54 medium effect
Inhibition C 07:08 10:31 04:25 3.66 0.89 large effect
Clocks 10.1 10.82 2.79 2.41 0.3 small effect
Animal Sorting 10:12 9.5 02:22 02:27 0.3 small effect
Comprehension of Instructions 5.93 8.93 6.54 5.92 0.53 medium effect
Speeded Naming 09:13 09:39 2.78 3.37 0.09 negligible effect
Phonological Processing 08:48 10.1 05:56 2.69 0.46 medium effect
Word Generation: semantic 08:21 07:57 2.92 06:04 00:14 negligible effect
Word Generation: phonological 08:29 8.4 2.62 3.73 0.04 negligible effect
Repetition of Nonsense Words 09:05 10:56 03:43 1.72 0.7 medium effect
Oromotor Sequences 9.73 09:41 2.7 3.97 0.1 negligible effect
Memory for Faces 08:58 09:54 02:36 2.93 0.39 small effect
Word List Interference: recall 8.68 10:15 03:39 02:37 0.61 medium effect
Word List Interference: repetition 10:42 10:13 4.5 2.62 0.1 negligible effect
Memory for Designs 07:35 9.63 05:17 2.93 0.69 medium effect
List Memory 7.88 9.8 2.98 03:46 0.67 medium effect
Memory for Names 09:13 9.75 03:41 2.75 0.24 small effect
Narrative Memory 09:46 10.87 02:23 2.98 0.6 medium effect
Sentence Repetition 09:37 6.65 3.98 8 00:46 medium effect
Fingertip Tapping 11:55 9.67 06:42 02:36 00:54 medium effect
Imitating Hand Positions 6.72 10.82 6.63 2.61 01:12 very large effect
Manual Motor Sequences 09:15 9.81 2.5 02:14 00:35 small effect
Theory of Mind: verbal task 9.1 9.1 2.68 06:46 0 negligible effect
Theory of Mind: contextual task 9.63 11:32 03:38 02:23 0.77 large effect
Affect Recognition 07:08 10:51 04:01 3.61 01:11 very large effect
Design Copying 11:13 10:32 02:38 03:42 00:32 small effect
Block Construction 7.97 10.05 2.86 02:57 0.96 large effect
Picture Puzzles 12:01 14:26 5.85 05:16 00:51 medium effect
Geometric Puzzles 10.8 9.73 3.6 2.89 0.42 medium effect
Route Finding 8.8 9.7 3.98 3.68 0.3 small effect
Arrows 9.85 9.59 2.46 3.45 0.1 negligible effect

Note. EC = children with epilepsy; HC = healthy controls. Bold denotes significant comparisons.

Relations between impairments in different
cognitive domains in children with epilepsy
When the contribution of individual abilities in
the other neuropsychological domains (i.e.,
Language, Memory and Learning, Sensorimotor
Functions, Social Perception, and Visuo-Spatial
Processing) was partialed out from the between-
group differences in Response Set, Inhibition A,
and Inhibition C, EC still showed significantly
impaired performance as compared to HC.
Indeed, the ANCOVA performed on Response
Set showed that the difference between EC and
HC groups was still significant after removing the
variance in common with the other cognitive
domains, F(1, 62) = 13.14, p < .001; the effects
of the other cognitive domains were
nonsignificant, all F(1, 62) < 1.9, p > .17.
Along the same lines, the ANCOVA for the
Inhibition A tests showed that the performance
of the EC group was impaired as compared with
that of the HC group, F(1, 62) = 9.02, p = .004,
independently from the other cognitive domains,
which, in turn, had no effects, all F(1, 62) < 2.4,
p > .13. Conversely, the ANCOVA performed on
Inhibition C showed that the difference between
the EC and HC groups’ performance was still
significant after removing the variance in com-
mon with the other cognitive domains, F(1, 62) =
6.58, p = .013. However, performance in the
Memory and Learning, F(1, 62) = 5.72, p = .02,
and Language, F(1, 62) = 4.55, p = .037, domains
had relative influence on performance at
Inhibition C; the effects of sensorimotor, social
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
perception, and visuo-spatial domains were not
significant, all F(1, 62) < 1.6, p > .1.
The ANCOVA performed on Imitating Hand
Positions showed that the difference between the
EC and HC groups was still significant after remov-
ing the variance in common with the other cognitive
domains, F(1, 62) = 5.69, p = .02. Visuospatial
processing abilities, however, had a strong effect
on performance, F(1, 62) = 7.86, p = .007, while
the effects of the other cognitive domains were not
significant, all F(1, 62) < 2.6, p > .1. This suggests
that, although visuospatial abilities may influence
performance in Imitating Hand Positions, they
cannot explain for the difficulties showed by the
EC patients when compared with the HC group.
Two ANCOVAs were performed for the Theory
of Mind–Contextual Task and Affect Recognition.
The former showed a strong trend, F(1, 62) = 3.80,
p = .055, toward statistically significant differences
between groups after removing the variance in
common with the other cognitive domains, which,
in turn, had nonsignificant effects, all F(1, 62)
< 3.18, p > .08. In contrast, the latter showed
that the difference between groups’ scores was
still highly significant after removing the variance
in common with the other cognitive domains, F(1,
62) = 9.34, p = .003. The effect of Memory and
Learning domain was significant, F(1, 62) = 4.72,
p = .034, reflecting the recruitment of memory
processes during the Affect Recognition task.
However, since the between-group difference was
still significant after having partialed out the effects
of memory abilities, results showed that EC
patients present with deficits for processing emo-
tional facial expressions independently of general
memory abilities. The effects of the other cognitive
domains on Affect Recognition were nonsignifi-
cant, all F(1, 62) < 2.1, p > .1), with the excep-
tion of a marginally significant effect of
visuospatial abilities, F(1, 62) = 3.61, p = .062.
In sum, while a certain degree of interdepen-
dency was observed between different domains,
the impairments of EC patients in cognitive flex-
ibility, imitation, and processing emotional facial
expressions were independent from deficits in the
other cognitive domains.
DISCUSSION
This study investigated the performance of a group
of children suffering from epilepsy of genetic or
unknown cause and having average intellectual
functioning in a wide neuropsychological assess-
ment. The study aim was to investigate patterns
of vulnerability in the development of
1045
neuropsychological functions in children with epi-
lepsy and with IQ level comparable to that of
healthy controls. To this end, we used a multidi-
mensional battery (NEPSY-II), which evaluates
different neurocognitive domains, in children with
epilepsy of genetic or unknown cause and without
intellectual disability or borderline intellectual
functioning and analyzed the relationships of spe-
cific deficits with those in other cognitive domains.
Results showed that children suffering from epi-
lepsy of genetic or unknown cause present a reli-
able neuropsychological profile characterized by
deficits in executive functioning, sensorimotor abil-
ities, and social perceptual skills. Previous studies
(Bender et al., 2007; Kolk et al., 2001; Parisi et al.,
2012) addressing the clinical validity of the
NEPSY assessment tool (first and second editions)
in children with epilepsy provided partially over-
lapping outcomes, as they were conducted with
children having various types of epilepsy, different
etiologies, different intellectual functioning levels,
and by selecting different sub-sets of NEPSY(-II)
tests. Nonetheless, in partial agreement with these
previous studies, we found deficits of attention and
executive functions and of sensorimotor abilities.
Conversely, our sample of high-functioning chil-
dren with epilepsy of genetic or unknown cause,
whose IQ level was not only within the normal
range but also comparable with that of controls,
did not show any deficits of visuo-spatial functions
and short-term memory. Deficits in these abilities
were previously reported in children with epilepsy
in studies that did not match general cognitive level
in epilepsy and control children groups but
excluded only children with intellectual disability
(Bender et al., 2007; Kolk et al., 2001; Parisi et al.,
2012). It should be noted, however, that the first
version of NEPSY was used in Bender et al. (2007)
and Kolk et al. (2001), which includes slightly
different tests and administration procedures as
compared to NEPSY-II and, crucially, does not
allow for the evaluation of social perception abil-
ities. Indeed, in addition to deficits in attention and
executive functions and sensorimotor processing,
the present study also suggests the presence of
deficits in social perception and emotional proces-
sing that are independent from other cognitive
domains.
Deficits in attention and executive functions
The results concerning the Attention and
Executive Functions domain suggest that epilepsy
of genetic or unknown cause and without intellec-
tual weaknesses is not associated, per se, with
1046 ZILLI ET AL.
relevant deficits on sustained attention on either
the visual (Visual Attention) or the auditory
(Auditory Attention) modality; nor was the chil-
dren’s performance particularly affected by the
need to inhibit automatic responses or learned
behaviors (see findings on the Inhibition B test).
Children’s deficits were significant in a task that
required them to shift from one response criterion
to another by repressing the dominant alternative.
This was true when the criterion shift was tested
in both the auditory (Response Set) and visual
modalities (Inhibition C). Since both tasks are
deemed to evaluate cognitive flexibility
(Korkman et al., 2007), these findings might sug-
gest that epilepsy of genetic or unknown cause
and with average intellectual functioning is asso-
ciated with particular deficits of cognitive flexibil-
ity. However, the specific factors mediating this
association need to be investigated. It is worth
noting that we entered into the analysis only the
time to complete the Inhibition condition tasks,
because the distribution of errors was highly
skewed and could not detect any difference
between the two groups. The results of the analy-
sis of the attention and executive function domain
are, nevertheless, consistent with findings from
previous studies, which reported deficits of execu-
tive functions in children with epilepsy of genetic
or unknown cause, even of recent onset (Borgatti
et al., 2004; Conant, Wilfong, Inglese, &
Schwarte, 2010; D’Agati, Cerminara, Casarelli,
Pitzianti, & Curatolo, 2012; Kavros et al., 2008;
Neri et al., 2012; Parrish et al., 2007; Schubert,
2005). This neuropsychological profile may be
associated with difficulties in controlling behavior
and inhibiting impulsivity, therefore providing
a framework for interpreting the frequent
co-morbidity between epilepsy and attention def-
icit/hyperactivity disorder.
In addition to deficits in tasks requiring criterion
shift, EC were also slower than HC in a relatively
simple task requiring naming, as quickly as possi-
ble, the congruent form of black-and-white geo-
metric designs (Inhibition A). EC had comparable
speed to that of HC when the task required provid-
ing an alternative name, thus inhibiting an auto-
matic response (Inhibition B). This pattern of
slowed response in a simple task and normal
speed in a more difficult one might reflect a general
problem with processing speed, which is function-
ally recovered when the more difficult task recruits
additional attentional resources. In agreement with
this finding, MacAllister et al. (2012) reported
slower average response speed in a subgroup of
ADHD patients with epilepsy versus ADHD
patients without epilepsy. Processing speed deficits
are common in epilepsy, and antiepileptic drugs,
which are known to determine potential “cognitive
slowing” as a side effect, may also exacerbate
them. Therefore, whether processing speed deficits
in our patients represent an epilepsy-related phe-
nomenon or the consequence of pharmacological
treatment, which was present in most patients,
remains an open question. Furthermore, the possi-
ble impact of subclinical seizures on children’s per-
formance in attention and executive functions must
be kept in mind in the interpretation of these find-
ings. All in all, these findings suggest that the
Auditory Attention and Response Set and the
Inhibition subtests of NEPSY-II are useful tools
to evaluate attention and executive function abil-
ities in children with epilepsy.
Deficits in sensorimotor functions
As far as sensorimotor abilities are concerned,
children with epilepsy showed important impair-
ments in Imitating Hand Positions. This task
requires imitating manual gestures demonstrated
by the examiner, starting with the dominant hand
and then switching to the nondominant one. An
impairment in this task can be due to different
causes and it can be produced by impairments in
action perception, motor planning, execution or
coordination.
Previous studies on fine motor control in epi-
lepsy patients showed controversial results.
Indeed, Boelen et al. (2005) compared a sample
of children with epilepsy and healthy controls and
did not found deficits in motor functioning as
evaluated with the movement ABC or a finger
tapping task. Conversely, Henkin et al. (2005)
found deficits in finger tapping in their sample of
children reported as having idiopathic generalized
epilepsy. Finally, Hernandez et al. (2002) demon-
strated that children with FLE had particularly
strong difficulties at tasks requiring sequencing
and alteration between different hand movements:
typically, their movements showed the lack of flex-
ibility in motor execution which was particularly
evident in performing reciprocal or asymmetrical
gestures.
Regarding our sample of children with epilepsy
of genetic or unknown cause, in front of significant
deficits in Imitating Hand Positions, we found
relatively spared performance in tests of unimanual
(Finger Tapping) or bimanual coordination
(Manual Motor Sequences). The Manual Motor
Sequences test requires repeating complex
sequences of movements, which are more compel-
ling for healthy individuals than the postures
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
presented in the Imitating Hand Positions test
(Urgesi et al., 2011). Thus, this pattern of relative
strengths and deficits in sensorimotor abilities sug-
gests that the impairment in our sample of children
with epilepsy of genetic or unknown cause may be
related to more abstract gesture representation,
rather than reflecting difficulties in motor planning
or fine motor coordination. Such gesture represen-
tation is required to perceive and imitate others’
actions and, in those cases in which the action has
a known meaning for the observer, to recognize
them. One possible interpretation of these findings
relies on a deficit in creating shared gesture repre-
sentations, thus having to do more with deficits in
the social perception domain than with deficits in
the sensorimotor one. However, other possible
interpretations deserve to be investigated in future
studies, in particular the relative role of action
perception and inhibitory/executive impairments
that could impact on action encoding and
reproduction.
Deficits in social perception
As far as the social perception domain is con-
cerned, we found important impairments of EC
patients on the Affect Recognition test and on the
Theory of Mind task that requires recognition of
emotional content. Thus, results suggest deficits in
contextual and noncontextual affect recognition.
Evaluation of social perception in routine neu-
ropsychological assessment is uncommon. Also,
the literature on social cognition in children with
epilepsy is scarce. In adults, this competence is
usually addressed in TLE candidates to surgical
resection of lesion site: greatest impairments have
been found on Affect Recognition tasks, particu-
larly when the primary or the surgical lesion
involved the amygdala and the temporal cortex in
the right hemisphere (Hlobil, Rathore, Alexander,
Sarma, & Radhakrishnan, 2008; Meletti et al.,
2009; Sedda et al., 2013). Available data, however,
seem to suggest atypical functioning in social skills
also in patients without focal mesial TLE. For
example, Golouboff et al. (2008) found that chil-
dren with left-TLE were more impaired in recog-
nizing fearful or neutral expressions, whereas those
with right-TLE were more impaired in identifying
disgust, and FLE children in recognizing happi-
ness. Despite such specific patterns, all epilepsy
groups were impaired in emotion processing when
compared to healthy controls. Along the same
lines, Broicher et al. (2012) showed that patients
with mesial TLE had significant impairments in
social perception, including affect recognition; yet
1047
they also found that patients with extramesial epi-
lepsy performed comparably with mesial TLE
patients on most social skill tasks, thus suggesting
a possible common vulnerability in all epilepsy
conditions. Finally, Cantalupo et al. (2013) inves-
tigated facial emotion recognition in a sample of
healthy children with previous history of febrile
seizure: compared with healthy controls without
any history of seizure, they performed significantly
worse when required to match and label five basic
facial emotions, especially disgust and fear.
Finally, both children affected by generalized epi-
lepsy and those affected by focal epilepsy have
been recently found to have deficits to infer mental
state scenarios depicted in passages compared to
healthy controls (Lew et al., 2015).
We found significantly worse performance in EC
patients as compared to controls when they were
required to recognize and identify, on a person’s
face, the expressions of six basic emotions: happi-
ness, sadness, fear, anger, disgust, and neutral. We
also found impaired performance on the Theory-of-
Mind task that involves the contextualization of
emotional expressions—namely, how emotion
relates to social context, and implies the recognition
of the appropriate affect associated with a visual
scene context. Conversely, no deficits were
observed on the Theory-of-Mind task that recruits
understanding mental functions such as belief,
intention, deception, emotion, imagination, and
pretending, or understanding that others have
their own thoughts, ideas, and feelings that may
be different from subjective ones. It is possible
that good language skills, a domain in which the
performance of children with epilepsy did not differ
from controls, helped them to compensate, on the
Theory-of-Mind verbal tasks, for impairments in
the emotional sphere. It is worth noting, however,
that the sensitivity of the Theory-of-Mind subtest to
reveal social perception deficits has been questioned
also in children with high-functioning autism
(Barron-Linnankoski et al., 2015). Interestingly,
when comparing performance in the two subtest
parts, children with autism were specifically
impaired in the verbal task, but not in the contex-
tual emotion recognition task (Narzisi et al., 2013),
a pattern of findings that matches their important
deficits in language domain. Conversely, our sam-
ple of children with epilepsy and average intelli-
gence was particularly impaired in the contextual
but not in the verbal tasks, in keeping with the
pattern of spared language abilities and impaired
performance in action processing tasks. Thus, it is
plausible that nonverbal emotional processing,
which also includes the ability to recognize and
imitate actions and emotions of others, might be
1048 ZILLI ET AL.
particularly compromised in patients with epilepsy.
Nonverbal emotional processing skills are crucial
for the development of appropriate social relations;
indeed, deficits in social communication and
emotion understanding might be associated with
behavioral disorders, increased rates of psycho-
pathology, and difficulties in psychosocial adjust-
ment among children with epilepsy (Golouboff
et al., 2008).
Study limitations and conclusions
The results of this study should be considered in
the light of important limitations. First, although
our sample was relatively homogenous for age and
IQ, the presence of various forms of partial and
generalized epilepsy did not allow us to define
adequate subgroups according to seizure type,
drug treatment, and age of onset. Further studies
are, thus, needed to specify the influence of these
variables on performance at the NEPSY-II tests
and to define the specific neuropsychological pro-
files, if present, of children with different forms of
epilepsy. Similarly, as we limited our sample to
those between the ages of 7 and 16 years in order
to have uniform NEPSY-II administration proce-
dures in all children, this limits the generalization
of the findings to younger populations and future
studies will have to test if the neuropsychological
pattern we found in 7–16-year-old children is age-
dependent.
Caution in the interpretation of the findings is
needed considering the relatively low sample size
of this study, which may not have enough power to
detect subtle deficits in those cognitive domains
that resulted to be preserved in our sample of
children with epilepsy of genetic or unknown
cause. Furthermore, validation studies using other
normed tests are needed to confirm the pattern of
spared and impaired abilities detected in the pre-
sent study and to rule out that it is simply due to
the low sensitivity of some NEPSY-II tests.
An important consideration relates to an intrin-
sic limitation of our study aim. Indeed, we aimed
to identify which is the relation between the weak-
nesses and strengths of neuropsychological perfor-
mance across different cognitive domains in
children with epilepsy and average intelligence.
To this end, we sampled children with comparable
IQ level as that of controls and excluded indivi-
duals with intellectual disabilities or borderline
intellectual functioning. While allowing for a
description of the profile of neuropsychological
performance in children with epilepsy indepen-
dently from other factors (e.g., intellectual
disability) that can explain impaired performance
in a task, this approach prevents it from providing
expectations related to the general pattern of neu-
ropsychological performance that can be detected
in any child suffering from epilepsy. Along the
same lines, our data cannot be interpreted as sug-
gesting that children with epilepsy do not have
major problems in memory, language, visual spa-
tial skills, or sustained attention, but that these
deficits may not be specifically associated with
epilepsy in the absence of low intellectual
functioning.
Despite these limitations, this study shows that
NEPSY-II may be a useful neuropsychological
battery to assess the pattern of strengths and
weaknesses in children with epilepsy with average
intellectual functioning, as our findings of deficits
in attention and executive functions and sensor-
imotor abilities are consistent with the results of
previous studies that used NEPSY (first or sec-
ond versions) evaluations (Bender et al., 2007;
Kolk et al., 2001; Parisi et al., 2012). In addition,
the present study provided evidence of social
perception deficits in children with epilepsy that
are independent from deficits in attention and
executive functions and from abilities in other
domains. Therefore, NEPSY-II might represent
a useful clinical tool to screen for this particular
competence in children and adolescents with
epilepsy.
REFERENCES
Ay, Y., Gokben, S., Serdaroglu, G., Polat, M., Tosun,
A., Tekgul, H., … & Kesikci H. (2009).
Neuropsychologic impairment in children with rolan-
dic epilepsy. Pediatric Neurology, 41, 359–363.
Barron-Linnankoski, S., Reinvall, O., Lahervuori, A.,
Voutilainen, A., Lahti-Nuuttila, P., & Korkman, M.
(2015). Neurocognitive performance of children with
higher functioning autism spectrum disorders on the
NEPSY-II. Child Neuropsychology, 21, 55–57.
Bender, H. A., Marks, B. C., Brown, E. R., Zach, L., &
Zaroff, C. M. (2007). Neuropsychologic performance
of children with epilepsy on the NEPSY. Pediatric
Neurology, 36, 312–317.
Berg, A. T., Langfitt, J. T., Testa, F. M, Levy, S. R.,
DiMario, F., Westerveld, M., & Kulas, J. (2008a).
Global cognitive function in children with epilepsy: A
community-based study. Epilepsia, 49, 608–614.
Berg, A. T., Langfitt, J. T., Testa, F. M, Levy, S. R.,
DiMario, F., Westerveld, M., & Kulas, J. (2008b).
Residual cognitive effects of uncomplicated idio-
pathic and cryptogenic epilepsy. Epilepsy &
Behavior, 13, 614–619.
Boelen, S., Nieuwenhuis, S., Steenbeek, L., Veldwijk, H.,
van de Ven-Verest, M., Tan, I. Y., & Aldenkamp, A. P.
(2005). Effect of epilepsy on psychomotor function in
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
children with uncomplicated epilepsy. Developmental
Medicine and Child Neurology, 47, 546–550.
Borgatti, R., Piccinelli, P., Montirosso, R., Donati,
G., Rampani, A., Molteni, L., … & Balottin, U.
(2004). Study of attentional processes in children
with idiopathic epilepsy by Conners’ Continuous
Performance Test. Journal of Child Neurology, 19,
509–515.
Broicher, S. D., Kuchukhidze, G., Grunwald, T.,
Krämer, G., Kurthen, M., & Jokeit, H. (2012).
“Tell me how do I feel.” Emotion recognition and
theory of mind in symptomatic mesial temporal lobe
epilepsy. Neuropsychologia, 50, 118–128.
Calderoni, S., Muratori, F., Leggero, C., Narzisi, A.,
Apicella, F., Balottin, U., … & Urgesi, C. (2013).
Neuropsychological functioning in children and ado-
lescents with restrictive-type anorexia nervosa: An in-
depth investigation with NEPSY-II. Journal of
Clinical and Experimental Neuropsychology, 35,
167–179.
Camfield, P. R., Gates, R., Ronen, G., Camfield, C.,
Ferguson, A., & MacDonald, G. W. (1984).
Comparison of cognitive ability, personality profile,
and school success in epileptic children with right
versus left temporal lobe EEG foci. Annals of
Neurology, 15, 122–167.
Cantalupo, G., Meletti, S., Miduri, A., Mazzotta, S.,
Rios-Pohl, L., Benuzzi, F., … & Cossu, G. (2013).
Facial emotion recognition in childhood: The effects
of febrile seizures in the developing brain. Epilepsy
and Behaviour, 29, 211–216.
Caplan, R., Siddarth, P., Stahl, L., Lanphier, E., Vona,
P., Gurbani, S., … & Shields W. D. (2008). Childhood
absence epilepsy: Behavioral, cognitive, and linguistic
comorbidities. Epilepsia, 49, 1838–1846.
Chilosi, A. M., Brovedani, P., Moscatelli, M., Bonanni,
P., & Guerrini, R. (2006). Neuropsychological find-
ings in idiopathic occipital lobe epilepsies. Epilepsia,
47, 76–78.
Conant, L. L., Wilfong, A., Inglese, C., & Schwarte, A.
(2010). Dysfunction of executive and related pro-
cesses in childhood absence epilepsy. Epilepsy &
Behavior, 18, 414–423.
D’Agati, E., Cerminara, C., Casarelli, L., Pitzianti, M.,
& Curatolo, P. (2012). Attention and executive func-
tions profile in childhood absence epilepsy. Brain &
Development, 34, 812–817.
Davies, S., Heyman, I., & Goodman, R. (2003). A
population survey of mental health problems in chil-
dren with epilepsy. Developmental Medicine and Child
Neurology, 45, 292–295.
Dennis, M., Francis, D. J., Cirino, P. T., Schachar, R.,
Barnes, M. A, & Fletcher, J. M. (2009). Why IQ is
not a covariate in cognitive studies of neurodevelop-
mental disorders. Journal of the International
Neuropsychological Society, 15(3), 331–343.
Dodson, W. E. (1993). Epilepsy and IQ. In W. E.
Dodson & J. M. Pellock (Eds.), Pediatric epilepsy:
Diagnosis and therapy (pp. 373–385). New York:
Demos.
Drewel, E. H., & Caplan, R. (2007). Social difficulties in
children with epilepsy: Review and treatment recom-
mendations. Expert Review of Neurotherapeutics, 7,
865–873.
Elger, C. E., Helmstaedter, C., & Kurthen, M. (2004).
Chronic epilepsy and cognition. The Lancet
Neurology, 3, 663–666.
1049
Farrant, A., Morris, R. G., Russell, T., Elwes, R.,
Akanuma, N., Alarcón, G., & Koutroumanidis, M.
(2005). Social cognition in frontal lobe epilepsy.
Epilepsy and Behaviuor, 7, 506–516.
Genizi, J., Shamay-Tsoory, S. G., Shahar, E., Yaniv, S.,
& Aharon-Perez, J. (2012). Impaired social behavior
in children with benign childhood epilepsy with cen-
trotemporal spikes. Journal of Child Neurology, 27,
156–161.
Germanò, E., Gagliano, A., Magazù, A., Sferro, C.,
Calarese, T., Mannarino, E., & Calamoneri, F.
(2005). Benign childhood epilepsy with occipital par-
oxysms: Neuropsychological findings. Epilepsy
Research, 64, 137–150.
Golouboff, N., Fiori, N., Delalande, O., Fohlen, M.,
Dellatolas, G., & Jambaqué, I. (2008). Impaired
facial expression recognition in children with tem-
poral lobe epilepsy: Impact of early seizure onset on
fear recognition. Neuropsychologia, 46, 1415–1428.
Goodenough, F. L. (1975). Measurement of intelligence
by drawings. New York, NY: Arno Press.
Haavisto, A., Korkman, M., Holmberg, C., Jalanko, H.,
& Qvist, E. (2012). Neuropsychological profile of
children with kidney transplants. Nephrology,
Dialysis, Transplantation, 27, 2594–2601.
Haavisto, A., Korkman, M., Jalanko, H., Holmberg, C.,
& Qvist, E. (2010). Neurocognitive function of pedia-
tric heart transplant recipients. Journal of Heart and
Lung Transplantation, 29, 764–770.
Haavisto, A., Korkman, M., Törmänen, J., Holmberg,
C., Jalanko, H., & Qvist, E. (2011). Visuospatial
impairment in children and adolescents after liver
transplantation. Pediatric Transplantatio, 15, 184–
192.
Hauser, W. A., & Hesdorffer, D. C. (1990). Facts about
epilepsy. New York: Demos.
Haverkamp, F., Hanisch, C., Mayer, H., & Noeker, M.
(2001). Evidence of a specific vulnerability for defi-
cient sequential cognitive information processing in
epilepsy. Journal of Child Neurology, 16, 901–905.
Haviland, A., Nagin, S. D., & Rosenbaum, P. R. (2007).
Combining propensity score matching and group-
based trajectory analysis in an observational study.
Psychological Methods, 12, 247–267.
Henkin, Y., Sadeh, M., Kivity, S., Shabtai, E., Kishon-
Rabin, L., & Gadoth, N. (2005). Cognitive function
in idiopathic generalized epilepsy of childhood.
Developmental Medicine and Child Neurology, 47,
126–132.
Hermann, B., Jones, J. Sheth, R., Dow, C., Koehn, M.,
& Seidenberg., M. (2006). Children with new-onset
epilepsy: Neuropsychological staus and brain struc-
ture. Brain, 129, 2609–2619.
Hernandez, M. T., Sauerwein, H. C., Jambaqué, I., De
Guise, E., Lussier, F., Lortie, A., … & Lassonde, M.
(2002). Deficits in executive functions and motor
coordination in children with frontal lobe epilepsy.
Neuropsychologia, 40, 384–400.
Hlobil, U., Rathore, C., Alexander, A., Sarma, S., &
Radhakrishnan, K. (2008). Impaired facial emotion
recognition in patients with mesial temporal lobe
epilepsy associated with hippocampal sclerosis
(MTLE-HS): Side and age at onset matters.
Epilepsy Research, 80, 150–157.
Jackson, D. C., Dabbs, K., Walker, N. M., Jones, J. E.,
Hsu, D. A., Stafstrom, C. E., … & Hermann, B. P.
(2013). The neuropsychological and academic
1050 ZILLI ET AL.
substrate of new/recent-onset epilepsies. Journal of
Pediatrics, 162, 1047–1053.
Kavros, P. M., Clarke, T., Strug, L. J., Halperin, J. M.,
Dorta, N. J., & Pal, D. K. (2008). Attention impair-
ment in rolandic epilepsy: Systematic review.
Epilepsia, 49, 1570–1580.
Kernan, C. L., Asarnow, R., Siddarth, P., Gurbani, S.,
Lanphier, E. K., Sankar, R., & Caplan, R. (2012).
Neurocognitive profiles in children with epilepsy.
Epilepsia, 53, 2156–2163.
Kolk, A., Beilmann, A., Tomberg, T., Napa, A., &
Talvik, T. (2001). Neurocognitive development of
children with congenital unilateral brain lesion and
epilepsy. Brain Development, 23, 88–96.
Korkman, M., Kirk, U., & Fellman, V. (1998). NEPSY:
A developmental neuropsychological assessment. San
Antonio, TX: The Psychological Corporation.
Korkman, M., Kirk, U., & Kemp, S. (2007). NEPSY–
II: Second edition. San Antonio, TX: The
Psychological Corporation.
Korkman, M., Kirk, U., & Kemp, S. (2011). NEPSY–II:
Second edition. Firenze: Giunti O.S. Organizzazioni
Speciali. Italian adaptation.
Laurent, A., Arzimanoglou, A., Panagiotakaki, E.,
Sfaello, I., Kahane, P., Ryvlin, P., … & de Schonen,
S. (2014). Visual and auditory socio-cognitive percep-
tion in unilateral temporal lobe epilepsy in children
and adolescents: a prospective controlled study.
Epileptic Disorders, 16, 456–470.
Lew, A. R. Lewis, C., Lunn, J., Tomlin, P., Basu, H.,
Roach, J., … & Martland, T. (2015). Social cognition
in children with epilepsy in mainstream education.
Developmental Medicine & Child Neurology, 57,
53–59.
Lin, J. J., Mula, M., & Hermann, B. P. (2012).
Uncovering the lifespan neurobehavioral comorbid-
ities of epilepsy. Lancet, 380, 1180–1192.
Lind, A., Korkman, M., Lehtonen, L., Lapinleimu, H.,
Parkkola, R., Matomäki, J., & Haataja, L. (2011).
Cognitive and neuropsychological outcomes at 5
years of age in preterm children born in the 2000s.
Developmental Medicine and Child Neurology, 53,
256–262.
Lind, A., Lapinleimu, H., Korkman, M., Lehtonen, L.,
Parkkola, R., Haataja, L., & PIPARI Study Group.
(2010). Five-year follow-up of prematurely born chil-
dren with postnatally developing caudothalamic
cysts. Acta Paediatrica, 99, 304–307.
MacAllister, W. S., Vasserman, M., Vekaria, P., Miles-
Mason, E., Hochsztein, N., & Bender, H. A. (2012).
Neuropsychological endophenotypes in ADHD with
and without epilepsy. Applied Neuropsychology–
Child, 1, 121–128.
Marini, A., Lorusso, M. L., D’Angelo, G., Civati, F.,
Turconi, A. C., & Fabbro, F. (2007). Evaluation of
narrative abilities in patients suffering from Duchenne
Muscular Dystrophy. Brain and Language, 102, 1–12.
Meletti, S., Benuzzi, F., Cantalupo, G., Rubboli, G.,
Tassinari, C. A., & Nichelli, P. (2009). Facial emo-
tion recognition impairment in chronic temporal lobe
epilepsy. Epilepsia, 50, 1547–1559.
Narzisi, A., Muratori, F., Calderoni, S., Fabbro, F., &
Urgesi, C. (2013). Neuropsychological profile in
high functioning autism spectrum disorders.
Journal of Autism and Developmental Disorders, 43,
1895–1909.
Neri, M. L., Guimarães, C. A., Oliveira, E. P., Duran,
M. H., Medeiros, L. L., Montenegro, M. A., … &
Guerreiro, M. M. (2012). Neuropsychological
assessment of children with rolandic epilepsy:
Executive functions. Epilepsy & Behavior, 24,
403–407.
Nolan, M. A., Redoblado, M. A., Lah, S., Sabaz, M.,
Lawson, J. A., Cunningham, A. M., … & Bye, A. M.
(2003). Intelligence in childhood epilepsy syndromes.
Epilepsy Research, 53, 139–150.
Olivieri, I., Bova, S. M., Urgesi, C., Ariaudo, G.,
Perotto, E., Fazzi, E., … & Orcesi, S. (2012).
Outcome of extremely low birth weight infants:
What’s new in the third millennium?
Neuropsychological profiles at four years. Early
Human Development, 88, 241–250.
Oostrom, K. J., Schouten, A., Kruitwagen, C. L., Peters,
A. C., Jennekens-Schinkel, A., & Dutch Study Group
of Epilepsy in Childhood (2003). Behavioral pro-
blems in children with newly diagnosed idiopathic
or cryptogenic epilepsy attending normal schools are
in majority not persistent. Epilepsia, 44, 97–106.
Oostrom, K. J., van Teeseling, H., Smeets-Schouten, A.,
Peters, A. C., Jennekens-Schinkel, A., & Dutch Study
of Epilepsy in Childhood (DuSECh) (2005). Three to
four years after diagnosis: Cognition and behaviour
in children with ‘epilepsy only. A prospective, con-
trolled study. Brain, 128, 1546–1555.
Orsini, A., & Picone, L. (2006). WISC-III. Contributo alla
taratura italiana [WISC-III. Italian Standardization].
Firenze: Giunti O.S. Organizzazioni Speciali.
Palmer, B. W., Appelbaum, M. I., & Heaton, R. K.
(2004). Rohling’s interpretive method and inherent
limitations on the flexibility of “flexible batteries.”
Neuropsychology Review, 14, 171–176.
Parisi, P., Matricardi, S., Tozzi, E., Sechi, E., Martini,
C., & Verrotti, A. (2012). Benign epilepsy of child-
hood with centro-temporal spikes (BECTS) versus
migraine: A neuropsychological assessment. Childs
Nervous System, 28, 2129–2135.
Parrish, J., Geary, E., Jones, J., Seth, R., Hermann, B.,
& Seidenberg, M. (2007). Executive functioning in
childhood epilepsy: Parent-report and cognitive
assessment. Developmental Medicine and Child
Neurolology, 49, 412–416.
Piccinelli, P., Beghi, E., Borgatti, R., Ferri, M.,
Giordano, L., Romeo, A., … & Balottin, U. (2010).
Neuropsychological and behavioural aspects in chil-
dren and adolescents with idiopathic epilepsy at diag-
nosis and after 12 months of treatment. Seizure, 19,
540–546.
Piccinelli, P., Borgatti, R., Aldini, A., Bindelli, D., Ferri,
M., Perna, S., … & Balottin, U. (2008) Academic
performance in children with rolandic epilepsy.
Developmental Medicine and Child Neurology, 50,
353–356.
Rantanen, K., Eriksson, K., & Nieminen, P. (2011).
Cognitive impairment in preschool children with epi-
lepsy. Epilepsia, 52, 1499–1505.
Rantanen, K., Nieminen, P., & Eriksson, K. (2010)
Neurocognitive functioning of preschool children
with uncomplicated epilepsy. Journal of
Neuropsychology, 4, 71–87.
Rasmussen, C., Tamana, S., Baugh, L., Andrew, G.,
Tough, S., & Zwaigenbaum, L. (2013).
Neuropsychological impairments on the NEPSY-II
 NEUROPSYCHOLOGICAL PROFILE IN PEDIATRIC EPILEPSY
among children with FASD. Child Neuropsychology,
19, 337–349.
Raven, J. C. (1954). Standard progressive matrices.
Firenze: Giunti OS.
Reynders, H. J., Broks, P., Dickson, J. M., Lee, C. E.,
& Turpin, G. (2005). Investigation of social and
emotion information processing in temporal lobe
epilepsy with ictal fear. Epilepsy Behaviour, 7,
419–429.
Russ, S. A., Larson, K., & Halfon, N. (2012). A national
profile of childhood epilepsy and seizure disorder.
Pediatrics, 129, 256–264.
Russell, E. W., Russell, S. L., & Hill, B. D. (2005). The
fundamental psychometric status of neuropsychologi-
cal batteries. Archives of Clinical Neuropsychology,
20, 785–794.
Schacher, M., Winkler, R., Grunwald, T., Kraemer,
G., Kurthen, M., Reed, V., & Jokeit, H. (2006).
Mesial temporal lobe epilepsy impairs
advanced social cognition. Epilepsia, 47, 2141–
2146.
Schubert, R. (2005). Attention deficit disorder and epi-
lepsy. Pediatric Neurology, 32, 1–10.
1051
Sedda, A., Rivolta, D., Scarpa, P., Burt, M., Frigerio,
E., Zanardi, G., … & Bottini, G. (2013). Ambiguous
emotion recognition in temporal lobe epilepsy: The
role of expression intensity. Cognitive, Affective, &
Behavioral Neuroscience, 13, 452–463.
Shaw, P., Lawrence, E., Bramham, J., Brierley, B.,
Radbourne, C., & David, A. S. (2007). A prospective
study of the effects of anterior temporal lobectomy on
emotion recognition and theory of mind.
Neuropsychologia, 45, 2783–2790.
Sherman, E. M. S., Brooks, B. L., Fay-Mcclymont, T.
B., & MacAllister, W. S. (2012). Detecting epilepsy-
related cognitive problems in clinically referred chil-
dren with epilepsy: Is the WISC-IV a useful tool?
Epilepsia, 53(6), 1060–1066.
Urgesi, C., Campanella, F., & Fabbro, F. (2011).
NEPSY–II: Second Edition. Contributo alla taratura
italiana [NEPSY–II: Second edition. Italian
Standardization]: Firenze: Giunti O.S.
Organizzazioni Speciali.
Wechsler, D. (1991). Wechsler Intelligence Scale for
Children (3rd ed.). San Antonio, TX: The
Psychological Corporation.
Copyright of Journal of Clinical & Experimental Neuropsychology is the property of
Psychology Press (UK) and its content may not be copied or emailed to multiple sites or
posted to a listserv without the copyright holder's express written permission. However, users
may print, download, or email articles for individual use.