Abstract

Although research on adults with frontal lobe epilepsy (FLE) has increased in recent years, delays in frontal lobe development preclude the generalization of these findings to children. This study compared children with FLE with typically developing children on cognitive and executive tests. Additionally, the differences between children with early and late seizure onset were explored. Results indicated comparable intelligence among all groups; however, the FLE cohort performed worse than controls on executive tests. The age of seizure onset differentially affected executive performance, such that early FLE onset resulted in greater executive dysfunction. The implications of these findings are discussed.

Introduction

Support linking executive abilities with the frontal lobes has emerged from functional neuroimaging research, as fMRI studies have revealed significant activation in the prefrontal cortex during the performance of executive tasks (Berman et al., 1995). There is also compelling evidence that executive processes emerge in infancy and develop throughout childhood into early adulthood (Anderson, 1998; Diamond & Taylor, 1996), which is consistent with frontal lobe development. Perhaps, the most prominent developmental peak has been identified between the ages of 7 and 10, during that time the prefrontal cortex undergoes an accelerated maturational progression. Anderson's (2002) model of executive function further explores the developmental trajectories of the frontal lobes and emerging executive abilities. According to Anderson (2002), executive functioning can be conceptualized as encompassing four distinct, but integrative, functional domains, namely attentional control, information processing, cognitive flexibility, and goal setting. Although each of these domains is comprised of discrete executive abilities, they work together in a cohesive fashion to produce purposeful behavior.

Regardless, much remains unclear about the neuropsychological effects of frontal lobe epilepsy (FLE) on executive functioning, particularly in pediatric populations. Although research on adults with FLE has increased in recent years, delays in frontal lobe development preclude the generalization of these findings to children. Not surprisingly, most published research on executive functioning has focused on adult populations.

Although research on children with FLE has been minimal, several significant implications have emerged from the few studies conducted. One such finding involves the impact of FLE on intelligence. The vast majority of studies have suggested that the intellectual abilities of patients with FLE tend to be spared (e.g., Mateer & Williams as cited in Hernandez et al., 2001; Nolan et al., 2004; Williams & Sharp, 2000), regardless of the nature of seizure characteristics. The same cannot be said for executive abilities, although findings from pediatric FLE studies have been inconsistent.

Culhane-Shelburne, Chapieski, Hiscock, and Glaze (2002) hypothesized that the nature of the specific executive batteries employed (i.e., subjective vs. objective tests) could differentially affect conclusions drawn. Although deficits were observed on the objective measures of executive function, particularly those addressing planning, sequencing, and problem-solving abilities, results from caregiver-report measures were demonstrative of average executive functioning in home and school environments. Riva, Saletti, Nichelli, and Bulgheroni (2002) analyzed the impact of seizure frequency, lateralization of epileptic foci, and age of seizure onset on the executive performances of eight FLE youth. Frequent seizures were associated with increased inattention and impulsivity, whereas left seizure focus was related to impairments in categorization, verbal memory, and visuospatial perception. Additionally, children with FLE onset prior to age 6 evidenced deficits in cognitive flexibility. Although findings from a follow-up study (Riva et al., 2005) also revealed a differential effect of the age of seizure onset, neither the lateralization nor the frequency of seizures were correlated with executive test performance. Further complicating the relationship between FLE and executive dysfunction were the results from McDonald, Delis, and Norman (2005) research, which found that none of the epileptic variables considered (i.e., age of onset, duration of epilepsy, seizure frequency) were associated with a specific executive profile.

Clearly, much about the neuropsychological sequelae of FLE remain uncertain. Consequently, the current study was undertaken to further examine the executive abilities of FLE youth, with the specific goal of examining the differential effects of the age of seizure onset on neurocognitive performance. As such, two hypotheses were explored for the current study:

  • Hypothesis 1: Regardless of the age of seizure onset, children with FLE will demonstrate more difficulty on the measures of executive function compared with their neurotypical peers

  • Hypothesis 2: Children with early-onset FLE will perform worse than those with later seizure onset on tests of executive functioning.

Materials and Methods

Participants

Twenty children between the ages of 8 and 18 with complex partial seizures of frontal lobe origin (n = 20; 13 males, 7 females) were age- and gender-matched with normal controls (n = 20). Inclusion in the FLE sample required a principle diagnosis of FLE based on EEG findings. Each of these participants were recruited from a large, ongoing study at Children's Healthcare of Atlanta; children with FLE were diagnosed by a pediatric epileptologist. Excluded from the study were those individuals who (a) displayed non-frontal areas of seizure focus on EEG evaluation, (b) had a history of status epilepticus, (c) achieved a Full-Scale IQ score that was ≤70, or (d) had a history of any other neurological condition besides FLE, with the exception of Attention-Deficit/Hyperactivity Disorder (ADHD), which is known to be highly co-morbid with FLE (Prévost, Lortie, Nguyen, Lassonde, & Carmant, 2006). Healthy controls were also required to have a Full-Scale IQ score ≥70. Control participants with ADHD were also permitted access to the study, although none of the controls involved had this diagnosis. Given the developmental peak known to occur in the prefrontal cortex between the ages of 7 and 10 (Anderson, 2002), it was decided that the FLE cohort would be divided into early and late seizure onset groups using age 7 as the delineation between these groups.

Procedures

Both parental consent and participant assent were required for participation in this study. All participants were evaluated in the same office. In order to establish a general estimate of intelligence, participants were first screened using the two-subtest version of the Wechsler Abbreviated Scale of Intelligence (WASI), which has demonstrated high reliability and validity estimates in previous studies (Wechsler, 1999). Participants were then administered an identical battery of neuropsychological tests known to be sensitive to executive functioning. Additionally, parents were asked to complete a questionnaire addressing executive ability in the context of the day-to-day environment. They also provided information about socioeconomic status using the Hollingshead Four-Factor Index of Social Status (Hollingshead, 1975).

Measures

Delis–Kaplan Executive Function System

Verbal Fluency Test

The Category Fluency, Total Switching, and Total Switching Accuracy conditions from the “Delis–Kaplan Executive Function System (D-KEFS) Verbal Fluency Test” were used to evaluate initiation, sustained attention, working memory, and self-monitoring skills (Delis, Kaplan, & Kramer, 2001). In addition to these skills, successful performance on the Category Fluency condition requires efficiency and maintenance of effort. The Switching Total component also assesses planning and organization, whereas the Switching Accuracy score provides an estimate of cognitive flexibility. Research findings on the Letter Fluency task have been inconsistent with respect to its ability to differentiate ADHD children from normal control groups (Loge, Staton, & Beatty, 1990; Mahone, Koth, Cutting, Singer, & Denckla, 2001); therefore, the Letter Fluency subtest was excluded from analysis.

Trail-Making Test

From the “Trail-Making Test,” the Number Sequencing and Letter Sequencing tasks were used as measures to evaluate efficiency and maintenance of effort, whereas the Number–Letter Switch condition provided estimates of planning/organization, cognitive flexibility, and working memory skills. Although the Visual Scanning and Motor Speed conditions were not included for analysis, a qualitative review of the results did not suggest any noteworthy dysfunction in either group's performance.

Behavior Rating Inventory of Executive Function

Parents were asked to complete the “Behavior Rating Inventory of Executive Function (BRIEF)” in order to assess executive functioning in the context of the daily environment (Gioia, Isquith, & Guy, 2001). Four subscales were included for analysis based on the specific skills being addressed in this study, namely the Shift, Working Memory, Plan/Organize, and Monitor scales. Prior to these analyses, data from the “BRIEF” were screened for differences on the Inconsistency and Negativity validity scales. No group differences were noted.

Statistical Analysis

Statistical calculations were performed using the SPSS 12.0 computer software package (2003). Independent sample t-tests, chi-square tests, and Fisher's exact tests were performed to screen for potential demographic differences between each of the FLE and control groups. Additionally, point-biserial correlation coefficients were calculated in order to examine the relationships between the various epilepsy characteristics and neuropsychological performance.

Given the exploratory nature of this study, an alpha level of 0.01 was adopted when investigating the hypotheses. Violations of any parametric assumptions were managed by data transformations, which were subsequently examined for normality and homoscedasticity. Any transformed data that met these assumptions were evaluated with independent sample t-tests and confirmatory Mann–Whitney U-analyses. When data transformation attempts were unsuccessful, one of the three approaches was undertaken based on the distribution of the data. Specifically, data that were normally distributed and heterogeneous were evaluated with separate variance t-tests, whereas non-normal and homogenous data were analyzed using the Mann–Whitney U-tests. When non-normality and heterogeneity of variance precluded the use of t-tests and the Mann–Whitney U-analyses, the individual performances of the FLE participants were considered in terms of deviation from the expected test mean. In these instances, impairment was defined as any achieved mean that was >1 SD below the expected test mean. Although not as powerful as parametric or nonparametric methods, this approach was deemed both reasonable and justifiable based on the exploratory nature of this study.

Demographics

No significant group differences emerged on any of the demographic variables examined, including those addressing gender, ethnicity, socioeconomic status, or handedness. Similarly, no significant age differences were noted when the FLE group was divided based on early and late seizure onset nor did differences emerge when these groups were compared with the typically developing cohort (Table 1).

Table 1.

Demographic characteristics of the FLE and control groups

Characteristic Whole sample
 
Early FLE onset
 
Late FLE onset
 
 FLE (n = 20) Controls (n = 20) FLE (n = 9) Controls (n = 9) FLE (n = 11) Controls (n = 11) 
Age (years) 
 Mean 12.4 12.7 10.9 11.2 13.6 14.0 
SD 2.8 2.9 2.7 3.1 2.3 2.3 
Gender (%) 
 Men 65.0 65.0 66.7 66.7 63.6 63.6 
 Women 35.0 35.0 33.3 33.3 36.4 36.4 
Ethnicity (%) 
 Caucasian 65.0 50.0 44.4 55.6 81.8 45.5 
 African American 25.0 50.0 44.4 44.4 9.1 54.5 
 Latin American 10.0 0.0 11.2 0.0 9.1 0.0 
Socioeconomic status 
 Mean 47.03 50.53 50.57 50.50 44.28 48.67 
SD 11.05 7.63 10.05 7.73 11.56 7.65 
Handedness (%) 
 Right 75.0 95.0 88.8 88.8 63.6 100.0 
 Left 25.0 5.0 11.2 11.2 36.4 0.0 
ADHD (%) 
 Diagnosis 55.0 0.0 44.4 0.0 54.5 0.0 
 No diagnosis 45.0 100.0 55.6 0.0 45.5 100.0 
Characteristic Whole sample
 
Early FLE onset
 
Late FLE onset
 
 FLE (n = 20) Controls (n = 20) FLE (n = 9) Controls (n = 9) FLE (n = 11) Controls (n = 11) 
Age (years) 
 Mean 12.4 12.7 10.9 11.2 13.6 14.0 
SD 2.8 2.9 2.7 3.1 2.3 2.3 
Gender (%) 
 Men 65.0 65.0 66.7 66.7 63.6 63.6 
 Women 35.0 35.0 33.3 33.3 36.4 36.4 
Ethnicity (%) 
 Caucasian 65.0 50.0 44.4 55.6 81.8 45.5 
 African American 25.0 50.0 44.4 44.4 9.1 54.5 
 Latin American 10.0 0.0 11.2 0.0 9.1 0.0 
Socioeconomic status 
 Mean 47.03 50.53 50.57 50.50 44.28 48.67 
SD 11.05 7.63 10.05 7.73 11.56 7.65 
Handedness (%) 
 Right 75.0 95.0 88.8 88.8 63.6 100.0 
 Left 25.0 5.0 11.2 11.2 36.4 0.0 
ADHD (%) 
 Diagnosis 55.0 0.0 44.4 0.0 54.5 0.0 
 No diagnosis 45.0 100.0 55.6 0.0 45.5 100.0 

Notes: No significant differences were noted on any of the demographic comparisons; FLE = frontal lobe epilepsy; ADHD = Attention-Deficit/Hyperactivity Disorder.

Clinical characteristics

The age of seizure onset for the entire FLE sample ranged from 6.0 months to 15.7 years (M = 7.2; SD = 4.0). Seizure frequency was described as being daily for seven participants (35%), weekly for four participants (20%), and monthly for five participants (25%). Four children (20%) had experienced a seizure within the last 12 months but not within the past 3 months. Information related to the lateralization of epileptic foci was not available for three FLE participants. For the remaining children, seizure focus was documented as being left-sided in six participants (35%), right-sided in two participants (12%), and bilateral in nine participants (53%). None of the participants' seizures were the result of post-traumatic injury. Regarding treatment, 10 of the FLE participants (50%) were treated with one anticonvulsant medication, whereas the remaining 10 participants (50%) were prescribed more than one anticonvulsant. Further, 11 of the 20 FLE participants (55%) had a co-morbid diagnosis of ADHD. It should also be noted that three of the participants had non-frontal lesions, including right parietal balloon cell dysplasia, mild vermian hypoplasia, and left temporal ganglioglioma.

When the FLE cohort was divided based on the age of epileptic onset, the resulting groups were comparable in terms of seizure frequency (p = .27), lateralization of epileptic foci (p = .88), number of anticonvulsants prescribed (p = 1.00), and ADHD diagnosis (p = 1.00). Further, results from a series of point-biserial correlations indicated that neuropsychological test performance was not differentially affected by differences in the age of FLE onset, method of pharmacological treatment, or seizure lateralization; however, a significant negative correlation was observed between seizure frequency and the Number–Letter Switch condition of the Trail-Making Test (r = .65; p < .01), suggesting that individuals with less frequent seizures (i.e., monthly) performed better than those with frequent seizures (i.e., weekly) on this task.

Results

Intellectual Functioning

Results from an independent sample t-test revealed similar intellectual ability when FLE participants (M = 98.20; SD = 15.36) were compared with normal controls (M = 106.55; SD = 11.49) on the WASI, t(38) = −1.95, p = .06. Although this indicates a statistical trend for IQ scores to be lower in the FLE group, it was presumed that significant findings on executive measures were not attributable to differences in overall cognitive functioning based on similar IQ scores. Similar findings emerged when the FLE group was subdivided into two smaller groups based on the age of seizure onset and compared in cognitive testing, t(18) = 0.10, p = .92.

Comparisons of children with seizure onset before age 7 to normal controls were also comparable—t(16) = −1.17, p = .26—as were those involving the late FLE onset and control groups, t(20) = −0.99, p = .37.

Executive Functioning

FLE versus neurotypical controls

Comparisons of FLE youth with neurotypical controls were indicative of significant differences in the Verbal Fluency Test (Table 2). An independent sample t-test found that FLE youth (M = 8.30; SD = 2.76) produced significantly fewer responses than normal controls (M = 12.20; SD = 2.17) on a measure of semantic fluency, t(38) = −4.98, p < .01. FLE participants experienced greater difficulty when asked to generate words while alternating between categories. Also, deficits both in the number of words produced, t(38) = −4.20, p < .01, and in the accuracy of switching, U = 78.00, p < .01, were noted.

Table 2.

Neuropsychological performances of the FLE and control groups

Test FLE (n = 20) Controls (n = 20) p-value 
WASI-2 Subtest Versiona 
 Full-Scale IQ 98.20 (15.36) 106.55 (11.49) .06 
D-KEFS Verbal Fluency Testb 
 Category Fluency 8.30 (2.76) 12.20 (2.17) <.01* 
 Switching Total 6.95 (3.66) 11.25 (2.75) <.01* 
 Switching Accuracy 7.40 (3.82) 11.50 (2.63) <.01* 
D-KEFS Trail-Making Testb 
 Number Sequencing 8.44 (2.83) 12.56 (1.69) <.01* 
 Letter Sequencing 6.60 (3.63) 11.45 (2.14) <.01* 
 Number–Letter Switch 7.21 (3.69) 10.58 (2.65) .01* 
BRIEF, Parent Report Formc 
 Shift 65.11 (14.22) 45.42 (6.95) <.01* 
 Working Memory 72.00 (13.36) 50.45 (9.22) <.01* 
 Plan/Organize 61.50 (8.97) 50.45 (11.47) <.01* 
 Monitor 67.32 (10.14) 48.42 (7.41) <.01* 
Test FLE (n = 20) Controls (n = 20) p-value 
WASI-2 Subtest Versiona 
 Full-Scale IQ 98.20 (15.36) 106.55 (11.49) .06 
D-KEFS Verbal Fluency Testb 
 Category Fluency 8.30 (2.76) 12.20 (2.17) <.01* 
 Switching Total 6.95 (3.66) 11.25 (2.75) <.01* 
 Switching Accuracy 7.40 (3.82) 11.50 (2.63) <.01* 
D-KEFS Trail-Making Testb 
 Number Sequencing 8.44 (2.83) 12.56 (1.69) <.01* 
 Letter Sequencing 6.60 (3.63) 11.45 (2.14) <.01* 
 Number–Letter Switch 7.21 (3.69) 10.58 (2.65) .01* 
BRIEF, Parent Report Formc 
 Shift 65.11 (14.22) 45.42 (6.95) <.01* 
 Working Memory 72.00 (13.36) 50.45 (9.22) <.01* 
 Plan/Organize 61.50 (8.97) 50.45 (11.47) <.01* 
 Monitor 67.32 (10.14) 48.42 (7.41) <.01* 

Notes: All scores reported as mean (SD). FLE = frontal lobe epilepsy.

aThe Wechsler Abbreviated Scale of Intelligence (WASI) index reported as standard scores (M = 100; SD = 30).

bThe Delis–Kaplan Executive Function System (D-KEFS) subtests reported in scaled scores (M = 10; SD = 3).

cBehavior Rating Inventory of Executive Function (BRIEF) indices reported in T scores (M = 50; SD = 15).

*Significant at p < .01.

A Mann–Whitney U-test indicated that the FLE group (mean rank = 10.83) performed significantly worse than normal controls (mean rank = 26.17) on the numerical sequencing condition of the Trail-Making Test, U = 24.00, p < .01. Following the rank transformation, independent sample t-tests revealed a similar performance pattern with respect to letter sequencing skills, t(38) = −5.21, p < .01, and the ability to alternate between letters and numbers sequentially, t(38) = −2.58, p = .01.

On the “BRIEF,” the parents of FLE youth rated their children as demonstrating significantly greater difficulties than neurotypical youth when required to shift between tasks, t(38) = 4.35, p < .01, and plan/organize their responses, t(38) = 3.45, p < .01. Additionally, the Mann–Whitney U-analyses revealed significantly less robust functioning when FLE youth were compared with controls with respect to working memory, U = 40.00, p < .01, and behavioral monitoring, U = 28.50, p < .01.

Executive performance by age of seizure onset

Results from a Mann–Whitney U-test indicated that children with early FLE onset (mean rank = 5.56) performed significantly worse than neurotypical controls (mean rank = 13.44) on a measure of semantic fluency (Category Fluency), U = 5.00, p < .01. This pattern of performance was also observed with regard to the number of words generated during a fluency switching condition (Switching Total), U = 7.00, p < .01. In contrast, children with late FLE onset demonstrated analogous performances to those of matched controls on both Category Fluency (U = 17.50; p = .04) and Switching Total conditions (U = 30.00; p = .39). When performances of the early and late FLE onset cohorts were compared, both semantic fluency (U = 28.50; p = .30) and switching fluency (U = 22.50; p = .11) were similar. With regard to the Switching Accuracy trial, four of the nine children (44.4%) with early FLE onset demonstrated deficient performances while 5 of the11 late-onset youth (45.5%) were impaired.

When required to switch between connecting strings of numbers and letters on a paper-and-pencil test (Trail-Making Test, Number-Letter Switching), children with early FLE onset group (mean rank = 6.33) demonstrated poorer performance compared with matched controls (mean rank = 12.67), U = 12.00, p = .01. In contrast, the late FLE onset participants (mean rank = 8.11) performed similar to matched controls (mean rank = 10.89) on this task, U = 28.00, p = .30. Analogous functioning between groups was also observed when the early and late FLE onset groups were compared on the measures of numerical sequencing (Number Sequencing, U = 36.50, p = .73), letter sequencing (Letter Sequencing, U = 25.50, p = .19), and number–letter switching (Number-Letter Switching, U = 29.00, p = .34).

A qualitative review of FLE participants' individual test scores revealed that just one of the nine children with early FLE onset (11.1%) exhibited impaired functioning on the Number Sequencing task; however, Letter Sequencing proved more challenging for these youth, as seven of the nine participants (77.8%) exhibited deficient performances. In contrast, neither the numerical nor alphabetic sequencing conditions were overwhelmingly problematic for the late FLE onset cohort, as just 4 of the 11 children (36.4%) struggled on either task.

It was hypothesized that children with early onset of FLE would be described as having more executive difficulties than their neurotypical peers in daily life. Comparisons of obtained and expected test means revealed that participants with early FLE onset were rated as having clinically significant impairment in their shifting (55.6%) and self-monitoring skills (66.7%). Further, results form a Mann–Whitney U-test indicated that early-onset youth (mean rank = 13.44) were rated as having significantly less practiced working memory skills compared with normal controls (mean rank = 5.66), U = 5.00, p < .01. The same could not be said when participants were evaluated on the Plan/Organize scale, as parents of both FLE (mean rank = 11.94) and neurotypical children (mean rank = 7.06) reported similar functioning, U = 18.50, p = .05 (Table 3).

Table 3.

Neuropsychological performances of the early onset FLE and control groups

Test FLE (n = 9) Controls (n = 9) p-value 
WASI-2 Subtest Versiona 
 Full-Scale IQ 97.00 (11.54) 103.22 (15.05) .26 
D-KEFS Verbal Fluency Testb 
 Category Fluency 7.67 (2.50) 12.56 (1.88) <.01* 
 Switching Total 5.78 (3.83) 11.44 (2.24) <.01* 
 Switching Accuracy 6.67 (4.21) 11.56 (2.00)  
D-KEFS Trail-Making Testb 
 Number Sequencing 9.11 (1.83) 13.11 (1.45)  
 Letter Sequencing 5.56 (3.25) 12.11 (1.97)  
 Number–Letter Switch 6.67 (3.71) 11.11 (2.26) .01* 
BRIEF, Parent Report Formc 
 Shift 59.33 (10.06) 44.22 (8.50)  
 Working Memory 72.22 (13.83) 47.11 (7.67) <.01* 
 Plan/Organize 61.67 (9.61) 49.67 (12.53) .05 
 Monitor 63.67 (10.32) 45.67 (8.09)  
Test FLE (n = 9) Controls (n = 9) p-value 
WASI-2 Subtest Versiona 
 Full-Scale IQ 97.00 (11.54) 103.22 (15.05) .26 
D-KEFS Verbal Fluency Testb 
 Category Fluency 7.67 (2.50) 12.56 (1.88) <.01* 
 Switching Total 5.78 (3.83) 11.44 (2.24) <.01* 
 Switching Accuracy 6.67 (4.21) 11.56 (2.00)  
D-KEFS Trail-Making Testb 
 Number Sequencing 9.11 (1.83) 13.11 (1.45)  
 Letter Sequencing 5.56 (3.25) 12.11 (1.97)  
 Number–Letter Switch 6.67 (3.71) 11.11 (2.26) .01* 
BRIEF, Parent Report Formc 
 Shift 59.33 (10.06) 44.22 (8.50)  
 Working Memory 72.22 (13.83) 47.11 (7.67) <.01* 
 Plan/Organize 61.67 (9.61) 49.67 (12.53) .05 
 Monitor 63.67 (10.32) 45.67 (8.09)  

Notes: All scores reported as mean (SD). FLE = frontal lobe epilepsy.

aThe Wechsler Abbreviated Scale of Intelligence (WASI) index reported as standard scores (M = 100; SD = 30).

bThe Delis–Kaplan Executive Function System (D-KEFS) subtests reported in scaled scores (M = 10; SD = 3).

cBehavior Rating Inventory of Executive Function (BRIEF) indices reported in T scores (M = 50; SD = 15).

*Significant at p < .01.

Statistical analysis precluded by violations of parametric assumptions.

Children with later onset of FLE (mean rank = 11.06) were also described as having planning and organization abilities that were similar to those of their neurotypical peers (mean rank = 7.94), U = 26.50, p = .22. In contrast, the vast majority of these late-onset youth were rated as having clinically significant impairments in their shifting (63.6%), working memory (72.7%), and self-monitoring skills (81.8%). When the late-onset cohort was compared with the early-onset group, however, no significant differences were noted on any of the four BRIEF domains assessed (Table 4).

Table 4.

Neuropsychological performances of the late onset FLE and control groups

Test FLE (n = 11) Controls (n = 11) p-value 
WASI-2 Subtest Versiona 
 Full-Scale IQ 99.18 (18.41) 103.44 (7.62) .37 
D-KEFS Verbal Fluency Testb 
 Category Fluency 8.89 (2.42) 11.44 (2.24) .04 
 Switching Total 8.78 (3.07) 9.89 (2.32) .39 
 Switching Accuracy 7.67 (3.16) 11.33 (1.73)  
D-KEFS Trail-Making Testb 
 Number Sequencing 7.78 (3.56) 10.22 (3.73)  
 Letter Sequencing 7.56 (3.09) 10.89 (1.62)  
 Number–Letter Switch 8.44 (3.17) 9.89 (3.10) .30 
BRIEF, Parent Report Formc 
 Shift 70.44 (16.80) 47.80 (7.55)  
 Working Memory 62.00 (7.11) 50.11 (9.78)  
 Plan/Organize 59.33 (8.52) 53.78 (10.41) .22 
 Monitor 69.33 (8.85) 48.00 (4.98)  
Test FLE (n = 11) Controls (n = 11) p-value 
WASI-2 Subtest Versiona 
 Full-Scale IQ 99.18 (18.41) 103.44 (7.62) .37 
D-KEFS Verbal Fluency Testb 
 Category Fluency 8.89 (2.42) 11.44 (2.24) .04 
 Switching Total 8.78 (3.07) 9.89 (2.32) .39 
 Switching Accuracy 7.67 (3.16) 11.33 (1.73)  
D-KEFS Trail-Making Testb 
 Number Sequencing 7.78 (3.56) 10.22 (3.73)  
 Letter Sequencing 7.56 (3.09) 10.89 (1.62)  
 Number–Letter Switch 8.44 (3.17) 9.89 (3.10) .30 
BRIEF, Parent Report Formc 
 Shift 70.44 (16.80) 47.80 (7.55)  
 Working Memory 62.00 (7.11) 50.11 (9.78)  
 Plan/Organize 59.33 (8.52) 53.78 (10.41) .22 
 Monitor 69.33 (8.85) 48.00 (4.98)  

Notes: All scores reported as mean (SD). FLE = frontal lobe epilepsy.

aThe Wechsler Abbreviated Scale of Intelligence (WASI) index reported as standard scores (M = 100; SD = 30).

bThe Delis–Kaplan Executive Function System (D-KEFS) subtests reported in scaled scores (M = 10; SD = 3).

cBehavior Rating Inventory of Executive Function (BRIEF) indices reported in T scores (M = 50; SD = 15).

*Significant at p < .01.

Statistical analysis precluded by violations of parametric assumptions.

Discussion

As predicted by Hypothesis 1, children with FLE demonstrated similar intellectual abilities when compared with age- and gender-matched controls, regardless of the age at which seizures first commenced. These findings are consistent with those of previous studies (Mateer & Williams as cited in Hernandez et al., 2001; Nolan et al., 2004; Williams & Sharp, 2000). Although these findings suggest that intelligence is seemingly spared in children and adolescents with FLE, precaution should be taken before generalizing these findings to larger FLE populations. Specifically, exclusionary criteria prevented children with Full-Scale IQ scores <70 from participating in this study. Further, there was a statistical trend toward significance in comparing the FLE and control groups, suggesting that overall cognitive difficulties may underlie some of the differences detected.

Although this was an exploratory study involving a relatively small FLE sample, consideration of the results nonetheless allows for an initial attempt at formulating a neurocognitive profile for FLE youth. This is a speculative profile, one that would greatly benefit from future exploration of frontal lobe function. Compared with their neurotypical peers, children whose frontal lobe seizures emerge prior to age 7 exhibit significantly more impairment on objective tests of executive functioning than do individuals with later seizure onset. These deficits may become especially apparent as neuropsychological tests increase in complexity, irrespective of the verbal or the nonverbal nature of the tasks. Specifically, early FLE onset is likely to produce deficits in efficiency and maintenance of effort, working memory, cognitive flexibility, and self-monitoring. As such, these youth may struggle when asked to generate verbal responses in accordance with semantic criteria, particularly when required to do so while alternating between two categories. In the “real world,” this deficit may manifest as difficulty with retrieving and generating spontaneous answers in response to direct questioning. Further, children with early seizure onset may struggle in their nonverbal sequencing abilities when required to sequence strings of letters or alternately sequence both numbers and letters. Notably, although the planning and organizational skills of early FLE onset youth may emerge as being problematic during these objective tests, these difficulties may be less apparent based on the subjective parent report alone.

In contrast to early FLE onset youth, children with late-onset seizures (i.e., at, or beyond, age 7) are more likely to demonstrate abilities that are comparable with those of neurotypical youth on objective measures of executive function; however, subjective ratings may prove inconsistent with these results, as parents of late-onset youth tend to report deficits in shifting, working memory, and self-monitoring skills. These contradictory findings may relate to the differential impact of environment on the manifestation of executive skills. Specifically, when provided a more structured, less distracting atmosphere, children with late FLE onset are likely to be more successful in exercising their executive skills, whereas the opposite may be true in less restrictive environments (e.g., home and school settings). Future studies may help to clarify these differences in assessment findings. Regardless, the objective performances exhibited by children with late FLE onset on executive tests are likely to be analogous to those of their neurotypical peers.

The present study was conducted as a pilot project that should be viewed as being exploratory in nature. Although attempts were made to develop a well-controlled, generalizable research design, there are several limitations that warrant discussion. A primary weakness was the size of the clinical and control samples; however, the number of FLE youth included constitutes one of the largest reported in pediatric FLE research. As a result of the small samples, a number of comparisons were evaluated using qualitative, rather than quantitative, methods. Although lacking in power, this approach allowed for the analysis of an often ignored, but nonetheless pertinent, epileptic feature, age of seizure onset.

The multivariate nature of this research design was also of concern, as comparing a relatively small number of participants on multiple domains increases the risk of making Type II errors. To guard against these errors, a more conservative alpha level of 0.01 was adopted. Indeed, most p-values were significantly less than the .01 significance level employed, thus lending support to the strength of these findings; however, it is possible that with larger samples and/or a less conservative p-value, the results would vary.

The omission of several seizure characteristics (e.g., lateralization/localization of seizure focus) was another study limitation, as any one of these variables may have affected test performance. The decision to include children with ADHD in the FLE cohort was another potential flaw since children with ADHD, alone, are known to perform more poorly on executive measures; however, the advantage is the application of a typical population who frequent presents with both conditions (Dunn, Austin, Harezlak, & Ambrosius, 2003).

Finally, difficulty related to the objective assessment of executive function was of concern. Much has been written about the lack of ecological validity reported for executive function tests. Upton and Thompson (1996) indicate that the “inadequacy” of executive tests is evident in the “quantitatively different results” that are often observed, and dependent on, “qualitatively different deficits” (p. 220). Indeed, these discrepancies were evident when test performance was compared using both quantitative and qualitative methods. These findings underscore the marked difficulty of developing a novel, executive task that is ecologically valid, child-friendly, and specific to frontal lobe function. Until such a test is developed; however, it is likely that neuropsychologists will continue to augment objective assessments with subjective reports.

Despite the limitations of this research study, several notable strengths are also apparent. First, this is the largest study conducted to date comparing children with FLE to matched controls on executive measures. Although other studies have compared smaller samples of FLE children to those with other epilepsy typologies and/or standardization samples (e.g., Culhane-Shelburne et al., 2002; Hernandez et al., 2003), none have explicitly focused on differences between FLE youth and matched controls. As such, this study provides valuable information about the functioning of FLE children while highlighting a population that is in need of additional research.

One of the biggest methodological weaknesses plaguing previous FLE studies is the tendency to ignore the impact of various FLE features on neurocognitive functioning. In response to this limitation, the current study included analyses of several of these epileptic variables, thus allowing the author to rule out their potential confounding effects on executive findings. Seizure variables explored in this study include the age of epileptic onset, frequency of seizures, nature of pharmacological treatment, and co-morbid diagnosis of ADHD.

Clinical Implications and Future Directions

Future studies should include larger samples so as to increase the statistical power attributed to the findings. This would also permit the categorization of FLE youth into more precisely defined, theoretically supported groups. These studies should also investigate seizure variables that were not included in the present study, such as the amount of time elapsed since the commencement of seizures and the lateralization/localization of epileptic foci. Findings from this research would undoubtedly prove an invaluable, educational resource for frontal lobe function.

Future studies should also seek to explore the potential impact of FLE on other non-executive abilities. This would not only aid in the development of an empirically sound, neurocognitive profile for FLE youth but also promote the employment of more pertinent and practical treatment recommendations. Research on pediatric populations in general, and FLE youth specifically, would benefit immensely from the creation of new, developmentally appropriate, executive tests.

Funding

The funding for this study was provided by Children's Healthcare of Atlanta Friends Research Fund.

Conflict of Interest

None declared.

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