Benign childhood epilepsy with centrotemporal spikes and the multicomponent model of attention: A matched control study

Epilepsy & Behavior 19 (2010) 69–77

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Benign childhood epilepsy with centrotemporal spikes and the multicomponentmodel of attention: A matched control study

Caterina Cerminara a,⁎, Elisa D'Agati a, Klaus W. Lange b, Ivo Kaunzinger b, Oliver Tucha c, Pasquale Parisi d,Alberto Spalice e, Paolo Curatolo a

a Unit of Child Neurology and Psychiatry, Department of Neuroscience, University of Rome Tor Vergata, Rome, Italyb Department of Experimental Psychology, University of Regensburg, Regensburg, Germanyc Department of Psychology, University of Groningen, Groningen, The Netherlandsd Pediatric Department, II Faculty of Medicine University of Rome La Sapienza, Rome, Italye Pediatric Department, I Faculty of Medicine University of Rome La Sapienza, Rome, Italy

⁎ Corresponding author. Pediatric Neurology Unit, DeVergata University of Rome, Via Montpellier 1, 00133, R

E-mail address: [email protected] (C.

1525-5050/$ – see front matter © 2010 Elsevier Inc. Aldoi:10.1016/j.yebeh.2010.07.008

a b s t r a c t
a r t i c l e i n f o
Article history:Received 25 May 2010Revised 7 July 2010Accepted 7 July 2010Available online 16 August 2010

Keywords:Benign childhood epilepsy withcentrotemporal spikesAttentionSpike indexElectroencephalography

Although the high risk of cognitive impairments in benign childhood epilepsy with centrotemporal spikes(BCECTS) is now well established, there is no clear definition of a uniform neurocognitive profile. This studywas based on a neuropsychological model of attention that assessed various components of attention in 21children with BCECTS and 21 healthy children. All participants were tested with a computerized test batteryusing the multicomponent model of attention performance. In comparison with healthy participants, thechildren with BCECTS showed significant impairment in the measure of selectivity and in one measure ofintensity of attention (arousal). Our results did not correlate with the electroclinical variables of age at onsetof seizures and spike index on sleep EEGs. To the best of our knowledge, this is the first study in which themulticomponent model of attentional function has been used in children with BCECTS to provide a clearerneuropsychological profile of these patients.

partment of Neuroscience, Torome, Italy. Fax: 06-20900018.Cerminara).

l rights reserved.

© 2010 Elsevier Inc. All rights reserved.

1. Introduction

Benign childhood epilepsy with centrotemporal spikes (BCECTS),or benign rolandic epilepsy (BRE), is one of the most commonchildhood epilepsy syndromes and represents about 20% of epilepsyin children younger than 15 years of age [1–3]. Characteristically, theseizures begin between 3 and 10 years of age, with a peak at 7 to 8,and resolve by puberty. Although BCECTS is considered a benign formof childhood epilepsy that occurs in children who show normalmental development, the risk of cognitive impairment is higher whencomparing the test performance of children with BCECTS with that ofhealthy sex- and age-matched children.

In the last two decades, a wide spectrum of neuropsychologicaland learning disabilities, such as speech and sound disorders, readingdisabilities, attention deficit, and visuomotor and behavior difficulties,have been reported in children with BCECTS [4]. The heterogeneity ofneuropsychological deficits in children with this syndrome contrib-utes to the confusion in this area, even though many studies havetouched on this topic. The impact of epilepsy on cognitive function iscomplex, with many variables that can influence cognitive ability andinteract, making it difficult to determine which factors contribute to

impairment. Cognition and attention are closely related, and the lackof a specific neuropsychological profile of children with BCECTS maybe due to a confused definition of attention.

Attentional functioning can be considered a building block forother more complex forms of cognitive activity. It might be better toconsider attention as a construct of cognitive psychology rather than acognitive function. Recent neuropsychological theories of attentioninclude unitary concepts of attention within multidimensionalmodels, with several distinct components of functions of attention[5]. In their multicomponent model of attention, Van Zomeren andBrouwer include the concept of alertness, subdivided into tonic andphasic alertness, vigilance/sustained attention, selective attention,divided attention, and strategy/flexibility [6].

Attention is impaired in many idiopathic and nonidiopathic typesof epilepsy and is influenced by many different factors. A betterdefinition of the epileptic syndromes could help in the choice of thebest attentional model study, and this could contribute to define aneurocognitive related-syndrome profile. In our study, we used themulticomponent model of attention to demonstrate the existence ofspecific attentional dysfunctions in children with BCECTS. The highrisk of cognitive impairment in BRE is now well established [7,8].However, conflicting results and the heterogeneity of study param-eters combine to form a inhomogeneous neuropsychological profileof children with BCECTS [9,10]. Children with BCECTS have sustainedattention difficulties. Some authors have suggested that right-sided

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70 C. Cerminara et al. / Epilepsy & Behavior 19 (2010) 69–77

interictal epileptiform activity in childrenwith BCECTS could interferewith right hemisphere activity including sustained attention [11,12].Other studies on the impact of laterality of discharges on the typeof cognitive deficits observed have often led to inconsistent results[13–15].

These children also show selective and divided attention difficul-ties if they have epileptiform discharges during sleep [16]. Severalstudies suggest a link between age at onset [17] of epilepsy andfrequency of spikes on the EEG recording [18], which also appear to betwo possible causal factors for attention deficits. Attention outcomesin BCECTS are important because an intact attention system permitsthe child to efficiently select and access sensory stimuli, informationin his or her memory, or motor responses [19]. Our study was de-signed to assess several components of attention, as suggested by themulticomponentmodel, in childrenwith BCECTS and healthy childrenusing a computerized test battery for attention performance (TAP),which consists of a selective attention task, an impulsivity task, a taskmeasuring focused attention, a measure of divided attention, twotests measuring arousal (tonic and phasic alertness), and a vigilancetask [20]. The second goal was to determine whether someelectroclinical variables, including age at onset of seizures and spikeindex on sleep EEGs, lead to different attention dysfunctions.

2. Methods

2.1. Participants

Onehundred twenty childrenwith BCECTSwere recruited from theDepartment of Child and Adolescent Neuropsychiatry of Tor VergataUniversity and from the Pediatric Department of the I Faculty ofMedicine and II Faculty of Medicine of La Sapienza University inRome. The diagnosis of BCECTS according to the ILAE classification, andbased on clinical history and a recent EEG recording, was confirmed byneuropediatricians in all the pediatric neurology departments.Patients were selected on the basis of their age, diagnosis, intellectualfunction (IQ), andwillingness to participate in the study. ChildrenwithBCECTSwhowere younger than 7 or older than 14 years of age, had anIQ below 85, had uncorrected hearing or visual impairments, or hadpsychiatric comorbidity were excluded from the study. Intellectualability (IQ) was measured using the Wechsler Intelligence Scale forChildren, Third Edition [21]. The IQ cutoff of 85 is 1 SD below themean(mean IQ=100) and was chosen to ensure that participants wereable to understand the instructions for the TAP.

Twenty-one children with BCECTS (12 boys, 9 girls) with a meanage of 9.86±1.59 years were asked to complete a neuropsychologicaltest battery (see Table 1). In addition, 21 healthy children who werematched to the children with BCECTS on the basis of age, sex, andhandedness participated in this study. The healthy children, recruitedin schools, were selected from a pool of subjects who voluntarilyparticipated in the neuropsychological assessment. None of them hadany history of neurological or psychiatric disease or displayed signs ofBCECTS or learning disability. The diagnosis of Attention DeficitHyperactivity Disorder according to DSM-IV-TR criteria was excluded

Table 1Characteristics of patients with rolandic epilepsy and matched healthy participants.

Ro/Coa Ro-EO/Co-EO

Ro-LO/Co-LO

Ro-HSI/Co-HSI

Ro-LSI/Co-LSI

N (eachgroup)

21 9 12 11 9

Sex (F/M) 9/12 3/6 6/6 6/5 3/6Age (years) 9.86±1.59b 9.22±1.64 10.33±1.43 9.45±1.44 10.33±1.80

Note. One patient was not classifiable on the basis of the EEG pattern.aRo, patients with rolandic epilepsy; Co, healthy control participants; EO, early onset ofseizures; LO, late onset of seizures; HSI, high spike index on sleep EEG; LSI, low spikeindex on sleep EEG.bMean±SD.

in all participants [22]. This exclusion was relevant to 36 childrenwith BCECTS who had a diagnosis of ADHD at their evaluation forrecruitment in the study. At the time of the study, no healthy par-ticipant was taking medication known to affect the central nervoussystem. Prior to the start of this study, all parents were informed of theaims and nature of the study and gave written consent.

2.2. Electroclinical aspects of children with BCECTS

In 9 patients seizures first occurred between 3 and 7 years ofage (early onset), and in 12, between 8 and 12 years of age (lateonset). None of the children had frequent seizures, and no patientswere taking antiepileptic drugs. The EEG background rhythm wasalways normal for age. EEG paroxysmal abnormalities (typically slowdiphasic, high-voltage centrotemporal spikes) were unilateral in 11children and bilateral in 10. One patient was not classifiable on thebasis of the EEG pattern (see Table 1).

Sleep EEGs typically showed activation of interictal epilepticdischarges (IEDs). The index of IEDs was evaluated by counting visuallyand manually each single epileptic spike on the most active lead; thespike count was stored for consecutive 1-minute epochs in computermemory. The spike index (number of spikes in a stage/time spent in thatstage) in total sleep time and individual sleep stage was calculated [23].A marked activation of IEDs during a sleep recording was considered ahigh spike index (HSI) in patients with a spike index N10/minute and alow spike index (LSI) in patients with a spike index b5/minute.

2.3. Procedure

All participants were tested with a computerized test battery thatconsisted of a selective attention task, an impulsivity task, a taskmeasuring focused attention, a measure of divided attention, twotests measuring arousal, and a vigilance task. Although selectiveattention, impulsivity, focused attention, and divided attention areregarded as aspects of selectivity of attention, arousal and vigilancerepresent expressions of intensity of attention [20,24]. Test proce-dures were presented on a computer screen and instructions weregiven orally. Participants were instructed to perform the computer-ized tasks as quickly as possible but to maintain a high level ofaccuracy. In each test, reaction times for correct responses, variabilityin reaction time, number of omission errors (lack of response to targetstimuli), and/or number of commission errors (responses to nontar-get stimuli) were calculated. To familiarize the participants with thetasks, a brief sequence of practice trials preceded each test. Testswere performed only after participants had completed practice trialswithout errors. Participants were assessed individually in a quietroom, and the examiner was present during the entire assessment.

In the alertness tasks, participants were asked to respond bypressing a button when a visual stimulus (a cross about 1.2×1.8 cm)appeared on a computer screen. A total of 40 trials were undertaken.In the first 20 trials, the stimulus appeared on the screenwithout priorwarning (tonic alertness task), whereas during the second 20 trials, awarning tone preceded the appearance of the stimulus (phasicalertness task). The time span between the warning tone and theappearance of the stimulus was random (between 300 and 700 ms).Measures of tonic and phasic alertness were calculated on the basis ofthe reaction time of the participant [20,24]. In addition, variability inreaction time and number of omission errors were measured.

In the vigilance task, a structure consisting of two rectangles (eachabout 1×2 cm)was presented in the center of the screen. One rectanglewas situated on top of the other. These rectangleswere alternatelyfilledwith a pattern (stimulus) for 500 ms with an interstimulus interval of1000 ms. The duration of the test was 15 minutes. A total of 600 stimuli(changes in pattern location) were presented. The participants wererequested to press the response button when there was no change inpattern location. The target rate (i.e., no change in pattern location)was

71C. Cerminara et al. / Epilepsy & Behavior 19 (2010) 69–77

about one target stimulus perminute for a total of about 18 targets. Theintervals between target stimuli were irregular. Reaction time forcorrect responses, variability in reaction time, number of omissionerrors, and number of commission errors were calculated [20,24]. Thetaskmeasured vigilance by requiring the participant to remain alert andready to react to infrequently occurring target stimuli over a relativelylong and unbroken period.

The divided attention task requires participants to concentratesimultaneously on a visual task and an acoustic task presented on acomputer. In the visual task, a series of matrices (about 9.5×11 cm)appeared in the center of the screen. Each matrix, consisting ofa regular array of 16 dots and crosses (4×4), was displayed for2000 ms. The subjects were asked to press the response button whenthe crosses formed the corners of a square (visual target). In theacoustic task, the participants were requested to listen to a continuoussequence of alternating high (2000 Hz) and low (1000 Hz) soundsand to press the response button when irregularities occurred in thesequence (acoustic target). A total of 100 visual and 200 acousticstimuli were presented including 17 visual and 16 acoustic targets.Reaction time for correct responses, variability in reaction time,number of omission errors (lack of response to target stimuli), andnumber of commission errors (responses to nontarget stimuli) werecalculated as a measure of divided attention [20,24].

The go/no go task consisted of five different patterns that werebriefly presented on the computer screen one at a time. Two of thesefive patterns were defined as target stimuli. When one of thesepatterns appeared on the screen, the participant had to press a button.The task required participants to produce a simple motor response tospecific cues while inhibiting the response in the presence of othercues. Reaction time, as well as numbers of right and wrong reactions,was measured. This task measured inhibition and impulsivity [24].

In the incompatibility task, arrows (about 1.4 cm wide and 3.8 cmlong) pointing to the left or the right were presented briefly on the leftor the right side of a fixation point in the center of the screen. Theparticipants were requested to press a response button on the sideindicated by the direction of the arrow, independently of the positionof the arrow. If the arrow's position and its orientation matched, thetrial was classified as compatible; if presentation and orientation didnot coincide, the trial was classified as incompatible. There were atotal of 57 trials. The sequence of trials was random, with about half ofthe trials compatible and half incompatible. Reaction time, variabilityin reaction time, and the number of commission errors were cal-culated, thereby providing a measure of selective attention as thecapacity to reject irrelevant information [20,24].

In the visual scanning task, a series of 5×5 matrices (about 8.8×8.8 cm)were presented in the center of the computer screen. Eachmatrixconsistedof a regular patternof 25 squares (eachabout1.2×1.2 cm), eachof which had an opening on one side (top, bottom, left or right side). Asquarewith anopening at the topwasdefinedas the critical stimulus. Thisoccurred only once in a matrix and was randomly distributed across thematrix. The subject was asked to press the left response button when amatrix contained the critical stimulus or the right response button whenthe critical stimulus was not present. There were a total of 50 trials(25 critical and 25 noncritical trials). Reaction time for correct responses,variability in reaction time, number of omission errors, and number ofcommission errors were calculated. This task assessed inhibition orimpulsivity as a measure of selective attention [20,24].

2.4. Data analysis

Wilcoxon signed-rank tests for matched-pair samples were usedfor statistical analysis. Participants were matched with respect to sexand age. Independent samples were compared with Mann–Whitney-U tests. For statistical analysis, the α level was 0.05. All statisticalanalyses were carried out using SPSS Version 15. Furthermore,effect sizes for the differences between paired observations were

computed [25]. Following Cohen's guidelines for interpreting effectsizes, negligible effects (db0.20), small effects (dN0.20), mediumeffects (dN0.50), and large effects (dN0.8) were distinguished [26,27].

3. Results

3.1. Comparisons between patient group and control group

3.1.1. AlertnessThe comparison between the patient and control groups using

Wilcoxon tests revealed a significant difference with respect to reac-tion time (Z=–2.09, P=0.037), but not in the number of omissionerrors (Z=–1.63, P=0.102) in the tonic alertness task. The patientgroup differed from the control group in reaction time (Z=–2.56,P=0.011), but not in the number of omission errors (Z=–1.00,P=0.317) in the phasic alertness task. Analysis of effect sizes revealedsmall to negligible differences in reaction time and number of omis-sion errors in the tonic alertness task, and small to medium effect sizedifferences in reaction time and number of omission errors in thephasic alertness task (see Table 2).

3.1.2. VigilanceNo significant differences between patients and healthy partici-

pants were observed in reaction time (Z=–0.07, P=0.940), numberof commission errors (Z=–1.05, P=0.295), and number of omissionerrors (Z=–0.59, P=0.554). Analysis of effect sizes revealed negli-gible to large effect sizes in reaction time, number of commissionerrors, and number of omission errors.

3.1.3. Divided attentionIn the divided attention task, the patient group made significantly

more omission errors (Z=–2.06, P=0.039) than healthy participants,whereas no significant differences were observed in reaction time(Z=–0.029, P=0.768) and the number of commission errors (Z=–1.86, P=0.063) between the patient and control groups. Analysisof the effect sizes revealed a medium effect size for the number ofomission errors, and negligible to small effects in reaction time andnumber of commission errors.

3.1.4. ImpulsivityIn the go/no go task, the comparison between the patient and con-

trol groups revealed significant differences in reaction time (Z=–2.02,P=0.044) and number of commission errors (Z=–2.24, P=0.025).Furthermore, no significant differences were observed in number ofomission errors (Z=–1.49, P=0.137). Analysis of effect sizes revealedsmall to medium effect sizes for reaction time, number of commissionerrors, and number of omission errors.

3.1.5. Focused attentionOn the incompatibility task, the patient group made significantly

more commission errors (Z=-2.68, P=0.007) than healthy partici-pants, whereas no significant differences were observed in reactiontime (Z=–0.85, P=0.394). The differences between the patient andcontrol groups represented negligible or medium effects.

3.1.6. Selective attentionIn the visual scanning task, the patient group made significantly

more commission errors (Z=–2.55, P=0.011) and omission errors(Z=–2.77, P=0.006) than the healthy participants. No significantdifferences were observed in reaction time (Z=–1.62, P=0.106). Thedifferences between the patient and control groups represented smallor medium effect sizes.

Table 2Comparison of test performance between patients with rolandic epilepsy and control children.

Children with rolandic epilepsy Healthy children Za P db

(N=21) (N=21)

Intensity of attentionTonic arousal (tonic alertness task)

Reaction time (ms) 377.57±165.04c 294.50±37.80 –2.09 0.037d 0.49Number of omission errorse 0.19±0.51 0.00±0.00 –1.63 0.102 f

Phasic arousal (phasic alertness task)Reaction time (ms) 360.71±160.15 274.67±37.51 –2.56 0.011d 0.52Number of omission errors 0.10±0.30 0.24±0.54 –1.00 0.317 0.21

Vigilance (vigilance task)Reaction time (ms) 814.07±165.03 833.88±129.13 –0.07 0.940 0.09Number of commission errors 10.19±16.74 6.29±6.24 –1.05 0.295 0.23Number of omission errors 7.29±4.65 6.48±3.96 –0.59 0.554 0.12

Selectivity of attentionDivided attention (divided attention task)

Reaction time (ms) 824.95±96.06 811.26±57.59 –0.29 0.768 0.12Number of commission errors 5.62±6.61 3.10±3.90 –1.86 0.063 0.41Number of omission errors 7.43±4.17 5.00±3.54 –2.06 0.039 d 0.56

Impulsivity (go/no go task)Reaction time (ms) 748.10±244.99 657.24±67.14 –2.02 0.044 d 0.41Number of commission errors 2.90±3.56 0.81±1.17 –2.24 0.025 d 0.54Number of omission errors 1.95±4.40 0.14±0.36 –1.49 0.137 0.40

Focused attention (incompatibility task)Reaction time (ms) 581.26±302.48 562.29±100.73 –0.85 0.394 0.06Number of commission errors 15.90±10.59 6.14±6.15 –2.68 0.007 d 0.77

Selective attention (visual scanning task)Reaction time (ms) 3582.38±2251.70 4356.57±1639.45 –1.62 0.106 0.31Number of commission errors 1.52±2.36 0.14±0.36 –2.55 0.011 d 0.57Number of omission errors 8.48±4.52 4.67±2.97 –2.77 0.006 d 0.69

a Z value, Wilcoxon test.b Effect size index according to Cohen [25].c Mean±SD.d Pb0.05.e Commission errors are responses to nontarget stimuli; omission errors are failures to respond to target stimuli.f Effect size could not be calculated because of missing correlation coefficient.


3.2. Comparisons between patients with early-onset and late-onsetseizures

The comparison, using Mann–Whitney U tests, between patientgroups, based on the onset of seizures, revealed no significant dif-ferences in any of the test measures of attention used in this study(see Table 3).

3.3. Comparison between patients with early onset of seizures andhealthy children

The comparison between patients with early onset of seizures andthe control group revealed a significant difference only in the numberof omission errors (Z=–2.02, P=0.044) in the visual scanning task,with a medium effect size (see Table 4).

3.4. Comparison between patients with late onset of seizures and healthyparticipants

The patient group made significantly more commission errorsin the divided attention task (Z=–2.99, P=0.003), go/no go task(Z=–2.77, P=0.006), and visual scanning task (Z=–2.05, P=0.041)than healthy participants. There was also a significant difference inreaction time in the go/no go task (Z=–2.67, P=0.008). Thedifferences between the patient and control groups representedmedium effect sizes (see Table 5).

3.5. Comparisons between patients with low and high spike indexes

Comparison between the patient groups on the basis of spike index,usingMann–WhitneyU tests, revealedno significant differences in anyof the test measures of attention used in this study (see Table 6).

3.6. Comparison between patients with high spike index and healthychildren

The comparison between patients with HSI and controls revealedsignificant differences in the number of omission errors (Z=–2.14,P=0.032) in the visual scanning task and in the number of com-mission errors in the incompatibility task (Z=–2.50, P=0.013), witha medium effect size (see Table 7).

3.7. Comparison between patients with low spike index and healthyparticipants

The patient group made significantly more omission errors on thedivided attention task (Z=–2.26, P=0.024) and the visual scanningtask (Z=–2.08, P=0.037) than healthy participants. The differencesbetween the patient and control groups represented medium effectsizes (see Table 8).

4. Discussion

Recent developments in research on cognitive abilities in BCECTSsupport the view that children with BCECTS show deficient perfor-mance in various neuropsychological areas, without a definition ofa uniform profile [28]. Cognitive impairment in BRE is now wellestablished. However, evidence regarding impairment of the atten-tional system in BCECTS appears to be less conclusive. Danielsson andPetermann could not find a single pattern of dysfunction or a typicalprofile or any significant differences in attention tests in patients withBCECTS [29]. Chaix et al. did not find attention impairments inpatients with BCECTS [30]. Furthermore, they evaluated sustained andselective attention without a complete test battery or a specific modelof attentional functions.

Table 4Comparison of test performance between patients with rolandic epilepsy with early onset of seizures and age- and sex-matched control children.

Children with rolandic epilepsywith early onset (N=9)

Healthy children(N=9)

Za P Db


Reaction time (ms) 348.39±57.60c 287.89±43.60 –1.96 0.051 0.87Number of omission errorsd 0.22±0.67 0.00±0.00 –1.00 0.317 e

Phasic arousal (phasic alertness task)Reaction time (ms) 325.22±51.80 268.61±47.00 –1.84 0.066 0.71Number of omission errors 0.00±0.00 0.33±0.71 –1.34 0.180 e



Reaction time (ms) 811.56±72.34 825.22±63.57 –0.77 0.441 0.19Number of commission errors 5.22±6.04 4.44±5.17 0.00 1.00 0.09Number of omission errors 7.67±3.12 5.67±4.27 –1.20 0.231 0.42

Impulsivity (go/no go task)Reaction time (ms) 676.72±76.85 667.83±66.22 –0.30 0.767 0.09Number of commission errors 1.11±0.93 1.44±1.42 –0.53 0.595 0.20Number of omission errors 0.00±0.00 0.22±0.44 –1.41 0.157 e

Focused attention (incompatibility task)Reaction time (ms) 524.17±131.38 596.44±132.62 –1.01 0.314 0.31Number of commission errors 15.33±12.52 5.22±2.54 –1.78 0.075 0.79

Selective attention (visual scanning task)Reaction time (ms) 3927.00±2075.59 4657.83±2113.37 –0.41 0.678 0.29Number of commission errors 1.44±2.45 0.11±0.33 –1.51 0.131 0.52Number of omission errors 8.78±4.55 4.56±2.01 –2.02 0.044f 0.84

a Z value, Wilcoxon test.b Effect size index according to Cohen [25].c Mean±SD.d Commission errors are responses to nontarget stimuli; omission errors are failures to respond to target stimuli.e Effect size could not be calculated due to missing correlation coefficient.f Pb0.05.

Table 3Comparison of test performance between patients with rolandic epilepsy with early onset of seizures and those with late onset of seizures.

Children with rolandic epilepsy Children with rolandic epilepsy Za P db

with early onset (N=9) with late onset (N=12)


Reaction time (ms) 348.39±57.60c 399.46±214.21 –0.57 0.602 0.33Number of omission errorsd 0.22±0.67 0.17±0.39 –0.23 0.917 0.09

Phasic arousal (phasic alertness task)Reaction time (ms) 325.22±51.80 387.33±207.07 –0.25 0.808 0.41Number of omission errors 0.00±0.00 0.17±0.39 –1.26 0.554 e



Reaction time (ms) 811.56±72.34 835.00±112.75 –0.43 0.702 0.25Number of commission errors 5.22±6.04 5.92±7.27 –0.39 0.702 0.10Number of omission errors 7.67±3.12 7.25±4.94 –0.39 0.702 0.10

Impulsivity (go/no go task)Reaction time (ms) 676.72±76.85 801.62±312.31 –0.96 0.345 0.55Number of commission errors 1.11±0.93 4.25±4.22 –1.68 0.111 1.03Number of omission errors 0.00±0.00 3.42±5.45 –2.14 0.111 e

Focussed attention (incompatibility task)Reaction time (ms) 524.17±131.38 624.08±386.18 –0.28 0.808 0.35Number of commission errors 15.33±12.52 16.33±9.45 –0.07 0.972 0.09

Selective attention (visual scanning task)Reaction time (ms) 3927.00±2075.59 3323.92±2432.14 –0.99 0.345 0.27Number of commission errors 1.44±2.45 1.58±2.39 –0.23 0.862 0.06Number of omission errors 8.78±4.55 8.25±4.69 –0.39 0.702 0.11

a Z value, Mann–Whitney U test for independent samples.b Effect size index according to Cohen [25].c Mean±SD.d Commission errors are responses to nontarget stimuli; omission errors are failures to respond to target stimuli.e Effect size could not be calculated because of missing correlation coefficient.


Table 5Comparison of test performance between patients with rolandic epilepsy with late onset of seizures and age- and sex-matched control children.

Children with rolandic epilepsywith late onset (N=12)


Za P Db



Phasic arousal (phasic alertness task)Reaction time (ms) 387.33±207.07 279.21±30.00 –1.73 0.084 0.52Number of omission errors 0.17±0.39 0.17±0.39 0.00 1.00 0.00



Reaction time (ms) 835.00±112.75 800.79±53.03 –0.86 0.388 0.26Number of commission errors 5.92±7.27 2.08±2.35 –2.99 0.003f 0.70Number of omission errors 7.25±4.94 4.50±2.97 –1.70 0.090 0.66

Impulsivity (go/no go task)Reaction time (ms) 801.62±312.31 649.29±69.61 –2.67 0.008f 0.57Number of commission errors 4.25±4.22 0.33±0.65 –2.77 0.006f 0.94Number of omission errors 3.42±5.45 0.08±0.29 –1.89 0.058 0.60


Selective attention (visual scanning task)Reaction time (ms) 3323.92±2432.14 4130.62±1228.29 –1.73 0.084 0.32Number of commission errors 1.58±2.39 0.17±0.39 –2.05 0.041f 0.59Number of omission errors 8.25±4.69 4.75±3.62 –1.89 0.059 0.57


Table 6Comparison of test performance between patients with rolandic epilepsy with a low spike index (LSI) and patients with rolandic epilepsy with a high spike index (HSI).

Children with rolandic epilepsywith LSI (N=9)

Children with rolandic epilepsywith HSI (N=11)

Za P Db


Reaction time (ms) 346.33±83.88c 408.32±215.87 –0.42 0.710 0.38Number of omission errorsd 0.33±0.71 0.09±0.30 –0.86 0.603 0.44

Phasic arousal (phasic alertness task)Reaction time (ms) 325.56±95.13 389.00±205.09 –0.68 0.503 0.40Number of omission errors 0.11±0.33 0.09±0.30 –0.15 0.941 0.06




Impulsivity (go/no go task)Reaction time (ms) 686.72±86.13 811.68±322.65 –1.48 0.152 0.53Number of commission errors 2.56±2.92 3.45±4.16 –0.43 0.710 0.25Number of omission errors 1.44±2.96 2.55±5.54 –0.35 0.824 0.25


Selective attention (visual scanning task)Reaction time (ms) 2798.94±1962.55 4222.77±2460.80 –1.78 0.080 0.64Number of commission errors 1.11±1.45 2.00±2.97 –0.08 0.941 0.38Number of omission errors 7.00±3.16 10.09±5.11 –1.49 0.152 0.73

a Z value, Mann–Whitney U test for independent samples.b Effect size index according to Cohen [25].c Mean±SD.d Commission errors are responses to nontarget stimuli; omission errors are failures to respond to target stimuli.


Table 7Comparison of test performance between patients with rolandic epilepsy with a high spike index and age- and sex-matched control children.

Children with rolandic epilepsywith HSI (N=11)


Za P Db








Focused attention (incompatibility task)Reaction time (ms) 651.04±408.15 563.27±90.66 –0.27 0.790 0.20Number of commission errors 18.73±10.70 4.91±2.51 –2.50 0.013f 1.23



Table 8Comparison of test performance between patients with rolandic epilepsy with a low spike index (LSI) and age- and sex-matched control children.

Children with rolandic epilepsywith LSI (N=9)


Za P Db






Reaction time (ms) 792.56±112.31 806.78±53.39 –0.30 0.767 0.18Number of commission errors 4.11±4.86 1.56±1.88 –1.77 0.076 0.57Number of omission errors 6.56±4.56 3.44±1.24 –2.26 0.024f 0.82


Focused attention (incompatibility task)Reaction time (ms) 497.11±76.40 547.17±113.47 –0.89 0.374 0.33Number of commission errors 13.67±10.28 8.00±8.92 –1.26 0.208 0.43





Recent neuropsychological theories of attention include unitaryconcepts of attention within multidimensional models, with severaldistinct components or functions of attention. On the basis of themulticomponent model of Posner and colleagues [31,32], whoincluded selective attention, arousal, and vigilance as components ofattention in their model, Van Zomeren and Brouwer delineated atheoretical framework of attentional functions [6]. Our study is thefirst in which this model has been used in children with BCECTS.

In accordance with the new multicomponent model of attentionof Van Zomeren and Brouwer the participants were tested with acomputerized test battery for attention performance, which consistedof a selective attention task, an impulsivity task, a task measuringfocused attention, ameasure of divided attention, two testsmeasuringarousal, and a vigilance task [6]. Although tonic alertness refers to arelatively stable level of attention that changes slowly with diurnalphysiological variations of the organism, phasic alertness is the abilityto enhance the activation level following a stimulus of high priority.The ability to sustain attention enables a subject to direct attentionto one or more sources of information over a relatively long andunbroken period. Vigilance is the ability to maintain attention overa prolonged period during which infrequent response-demandingevents occur. Selective attention is defined as the ability to focusattention in the face of distracting or competing stimuli. Dividedattention requires a simultaneous response to multiple tasks or mul-tiple task demands. Although selective attention, impulsivity, focusedattention, and divided attention are regarded as aspects of selectivityof attention, arousal and vigilance represent expressions of intensity ofattention [6].

Our study analyzed various components of attention in 21 childrenwith BCECTS and 21 healthy children. Some epilepsy-related variablesthat could have an impact on attentional functioning, such as age atonset of epilepsy and the spike index, were also evaluated. The resultsof this study clearly indicate impairment in selectivity (impulsivity,focused attention, selective attention, aspects of divided attention)and in one measure of intensity (arousal) of attention in childrenwith rolandic epilepsy. The other measure of intensity of attention(vigilance) showed no impairment in the patients with BCECTS.

These results did not correlate with the electroclinical variablesof age at onset of seizures and spike index on sleep EEGs. Fewstudies have evaluated the impact of age at onset of seizures on thedevelopment of attentional processes. The results of the study ofDeltour et al. suggest the presence of short-term memory orattentional capacity limitation, regardless of the modality, in childrenwith earlier onset of seizures [13]. According to our results, age at onsetof seizures does not appear to influence the development of otherexecutive and attentional processes. Other studies have demonstrateda correlation between the frequency of epileptiform discharges onwaking and/or sleep EEGs and cognitive difficulties [14,16,18,33].

Conversely, we found no correlation between the results of thetests we used and the sleeping spike rate. Our data demonstrate thatEEG centrotemporal spikes during sleep are not sufficient to impairattention. Similarly, Titomanlio et al. compared 16 children aged10–16 years in remission from BCECTS with control children, usingcomputerized tasks. Patients made significantly more errors thancontrols on the double-choice reaction time task, which suggeststhat some subtle cognitive deficits could therefore persist over timedespite normalization of electroclinical performance [34].

Finally, one difficulty in assessing studies of attention may beconfusion over the definition of attention. It is not clear in somestudies of attention and BCECTS if attention is being evaluated, orwhether the existence of attention deficit hyperactivity disorder(ADHD) is being evaluated. The diagnosis of ADHD according to DSM-IV-TR [22] criteria was excluded in all of our study participants.The distinction between these two conditions is important. Recentfindings in attention research in children and adults, using functionalmagnetic resonance imaging (fMRI) and an attention network test,

demonstrate that the impairments associated with attention arelocalized in distinct brain networks and are probably not associatedwith ADHD [35]. However, these distinctions are only now becomingappreciated, and confusion between the two disorders remains in theliterature.

In conclusion, our data confirm an impact of BCECTS on attentionalability. In our children with BCECTS, the impairment in the selectivityof attention seems to be due to the impulsivity of these subjects; infact, they make more commission errors than healthy children. In thealertness tasks, a measure of arousal, our patients show slow reactiontime compared with controls.

Prospective studies looking systematically at the different aspectsof attention in its modalities are needed, because often the quality ofstudy design and the extreme variation of methodology stronglycontribute to the lack of a clear and specific neuropsychological profilein children with BCECTS.

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Benign childhood epilepsy with centrotemporal spikes and the multicomponent model of attention: A matched control study