EXECUTIVE FUNCTION AS A PREDICTOR OF EMOTIONAL ...

EXECUTIVE FUNCTION AS A PREDICTOR OF EMOTIONAL, BEHAVIOURAL,

AND SOCIAL COMPETENCE PROBLEMS IN CHILDREN WITH EPILEPSY

A Thesis Submitted to the Committee on Graduate Studies in Partial Fulfillment of the

Degree of Master of Science in the Faculty of Arts and Science

TRENT UNIVERSITY

Peterborough, Ontario, Canada

© Copyright by Sarah Healy 2016

Psychology M.Sc. Graduate Program

January 2017

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ABSTRACT

Executive function as a predictor of emotional, behavioural, and social competence

problems in children with epilepsy

Sarah Healy

The study aimed to examine the association between different components of executive

function (EF) and emotional, behavioural, and social competence problems (EBSP) in

children with epilepsy. Although there is evidence of an association between EBSP and

EF in typically developing children, little research has examined this relation in children

with epilepsy. The sample comprised of 42 children with epilepsy, aged 6.0 to 18.1 years

old. Results showed that EBSP were associated with EF in these children; however,

different components of EF were related to different EBSP. Shifting was a significant

predictor of emotional, behavioural, and social competence problems in children with

epilepsy, whereas inhibition was a significant predictor of behavioural problems. This

suggests that children with epilepsy, with different EF profiles may be at-risk for

developing different types of problems. These results may aid researchers and clinicians

with the development of new techniques to identify and treat children with EBSP.

Keywords: epilepsy, executive function, emotional problems, behavioural problems,

social competence.

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ACKNOWLEDGMENTS

I would first like to express my sincere gratitude to my thesis advisor, Dr. Nancie

Im-Bolter from Trent University, for her continuous support with my data collection,

analysis, and thesis writing. Her guidance and assistance were critical to the development

of this thesis. I could not have hoped for a better thesis advisor!

I would also like to thank Dr. Janet Olds from the Children’s Hospital of Eastern

Ontario for her direction and comments on this thesis, and for allowing me to collect data

from her assessments.

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TABLE OF CONTENTS

Page

ABSTRACT ii

TABLE OF CONTENTS iv

LIST OF TABLES v

OVERVIEW 1

INTRODUCTION 2

METHODS 22

Participants 22

Procedure 23

Measures 23

RESULTS 26

DISCUSSION 35

Future Research 41

Conclusion 42

REFERENCES 43

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LIST OF TABLES

Page

Table 1. Summary of Research Looking at the Association Between EF 20

Components and EBSP in Typically Developing Children

Table 2. Demographics of Participants 26

Table 3. Executive Function and Emotional, Behavioural and Social Competence 27

Scores

Table 4 Correlations of Seizure and Treatment Related Variables with Emotional 30

Behavioural, and Social Problems

Table 5 Results of a Hierarchical Multiple Regression to Predict Behavioural 31

Problems from Global EF Composite, Seizure Control, and Anticonvulsant

Medication (n = 32)

Table 6 Results of a Hierarchical Multiple Regression to Predict Behavioural 34

Problems from Shifting, Inhibition, Seizure Control, and Number of

Anticonvulsant Medications (n=34)

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LIST OF ABBREVIATIONS

BRIEF Behaviour Rating Inventory of Executive Functioning

CBCL Child Behavior Checklist

EBSP Emotional, behavioural, and/or social competence problems

EF Executive function

WISC-IV Wechsler Intelligence Scale for Children-Fourth Edition

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Executive function as a predictor of emotional, behavioural, and social competence

problems in children with epilepsy

Overview

Children with epilepsy are far more likely to have emotional, behavioural,

and/or social competence problems (EBSP) than their peers without epilepsy (Freilinger

et al., 2006; Gebauer-Bukurov, Markovic, Sekulic, & Bozic, 2015; Jakovljević &

Martinović, 2006) or their peers with other chronic illnesses (Dunn, Austin, & Huster,

1997). In typically developing children, researchers have consistently found an

association between EBSP and executive function (EF) (e.g., Alduncin, Huffman,

Feldman, & Loe, 2014; Hughes, 1998; Karasinski, 2015; Levens & Gotlib, 2010; Mocan,

Stanciu, & Visu-Petra, 2014; Razza & Blair, 2009). EF refers to high-level cognitive

processes that provide control over thought, action, and emotion (Carlson & White, 2013;

Juric, Richards, Introzzi, Andres, & Urquijo, 2013). Although an association between

EBSP and EF has been suggested in children with epilepsy (Baum et al., 2010; Giancola,

Roth, & Parrott, 2006; Kananaugh, Scarborough, & Salorio, 2015), little research has

looked at EF as a potential predictor of EBSP. Moreover, researchers in the area of

epilepsy often focus on EF in general as opposed to specific, validated components of EF.

Thus, it is unclear whether these studies are truly examining EF or other complex

cognitive processes often associated with EF (e.g., attention). Additionally, it makes it

difficult to discern whether the child’s EF profile differs depending on the problem that

they present with. The aim of the current study is to extend and clarify the literature by

investigating whether specific components of EF are differentially associated with

emotional problems, behavioural problems, and/or social competence issues.

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Epilepsy and Emotional, Behavioural, and Social Competence Problems

Epilepsy is one of the most prevalent neurological disorders in the world. Every

year, approximately 15,500 Canadians are diagnosed with epilepsy, with approximately

85% of those individuals diagnosed before the age of 18 (Epilepsy Canada, 2013; Reilly

& Ballantine, 2011). Epilepsy is defined as a disorder that involves recurrent seizures

(Reilly & Ballantine, 2011), which are the result of an epileptiform discharge in the brain

that causes cerebral neurons to excessively discharge into the brain (Lee, 2010). Seizures

are typically classified into three main types: generalized, simple partial, and complex

partial (ILAE, 1981; Lee, 2010). Generalized seizures occur when an epileptiform

discharge initially and simultaneously affects both cerebral hemispheres. This type of

seizure may or may not disrupt the individual’s consciousness. In contrast, simple partial

seizures are defined as seizures in which the epileptiform discharge is confined to one

specific part of one cerebral hemisphere. Consciousness is usually not impaired during

this type of seizure. Finally, complex partial seizures occur when the epileptiform

discharge initially occurs in one specific part of one cerebral hemisphere but then spreads

to other brain areas. This type of seizure often results in impaired consciousness (e.g.,

decreased or distorted alertness and responsiveness; ILAE, 1981).

In addition to recurrent seizures, epilepsy can cause significant impairment in

many areas of an individuals life such as learning (Sillanpää, 2004), academic

achievement (Lee, 2010), employment (Smeets, van Lierop, Vanhoutvin, Aldenkamp, &

Nijhuis, 2007), and quality of life (e.g., Jennum, Gyllenborg, & Kjellberg, 2011).

Interestingly, learning problems, low academic achievement, lower employment rates,

and a lower quality of life has been linked to emotional, behavioural, and social

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competence problems (EBSP) in children with epilepsy (e.g., Andelman, 2000; Colman

et al., 2009; Gest, Sesma, Masten, & Tellegen, 2006; von Stumm et al., 2011). This

finding is significant as children with epilepsy are significantly more likely to have EBSP

than typically developing children; with prevalence rates up to four times higher in

children with epilepsy (Freilinger et al., 2006).

Emotional problems. Emotional or internalizing problems can be defined as the

tendency to self blame as well as the inability to control or regulate emotions during

negative or stressful events (Zahn-Waxler, Klimes-Dougan, & Slattery, 2000). The most

commonly researched emotional problems in children with epilepsy are depression and

anxiety disorders. When examining depression in individuals with epilepsy, researchers

have consistently reported elevated rates of depression, with prevalence rates from 10%

to 20% in individuals with well controlled seizures and from 20% to 60% in individuals

who do not have well-controlled seizures (Lee, 2010). When looking specifically at

children with epilepsy, rates of depression are also higher than compared to the general

population (23% to 26% vs. 2% to 9%; Baki et al., 2004; Plioplys, 2003). In addition to

depression, anxiety disorders have also been found to be more prevalent in individuals

with epilepsy (15% to 25%) than the general population (2% to 3%; Lee, 2010). A recent

study by Jones and colleagues (2015) showed that specific phobias, separation anxiety,

and social phobia are the most frequently diagnosed types of anxiety in children with

epilepsy (Jones et al., 2015).

Elevated rates of emotional problems in children with epilepsy are significant as

children with emotional disorders are more likely to score lower on measures of

academic achievement and quality of life (well-being and life satisfaction; Andelman,

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2000; Ekinci, Titus, Rodopman, Berkem, & Trevathan, 2009; Tosun et al., 2008).

Additionally, depression and anxiety have been shown to be a significant contributing

factor for suicide amongst children with epilepsy (Ekinci et al., 2009), with one study

reporting a suicidal ideation rate of 20.3% in 177 children with epilepsy (Jones, Siddarth,

Gurbani, Shields, & Caplan, 2013).

Behavioural problems. Behavioural or externalizing problems refer to

undesirable behaviours that are intended to harm or disrupt those around them (Zahn-

Waxler et al., 2000). The most commonly examined behavioural problems in children

with epilepsy are rule breaking and aggressive behaviour. Children with epilepsy are

more likely to have behavioural problems than both typically developing children and

children affected by other chronic illnesses (Dunn et al., 1997; van Mil et al., 2009), with

behavioural problems occurring at a prevalence rate of 30% and even higher rates in

children with untreated epilepsy (Kariuki et al., 2012). Furthermore, when compared to

typically developing peers, children with epilepsy are much more likely to partake in risk

taking behaviour, such as alcohol and drug use (Alfstad et al., 2011), and are significantly

more aggressive (e.g., Juhász, Behen, Muzik, Chugani, & Chugani, 2001; Whitman,

Hermann, Black, & Chhabria, 1982) and disobedient (e.g., Epir, Renda, & Baser, 1984).

These findings are important because children with behavioural problems have

been shown to have difficulties in many aspects of their lives. For example, research

suggests that certain behavioural problems, such as aggressive behaviour, are

significantly related to a child’s school placement; with children exhibiting behavioural

problems more likely to be placed in special classrooms than typically developing

children (Sabbagh, Soria, Escolano, Bulteau, & Dellatolas, 2006). With regards to long-

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term difficulties, researchers have found that children with behavioural problems are

more likely to have financial difficulties, employment issues, and mental health problems

well into adulthood (Colman et al., 2009; von Stumm et al., 2011).

Social competence. Social competence refers to a child’s ability to successful

communicate and interact with peers; including the ability to develop and maintain

friendships, the ability to resolve social conflicts, and the ability to achieve mutually

beneficial goals (Guralnick & Neville, 1997). Children with epilepsy are more likely to

have problems with social competence than their typically developing peers (Gebauer-

Bukurov, Markovic, Sekulic, & Bozic, 2015; Jakovljević & Martinović, 2006). In one

study, Jakovljević and Martinović (2006) compared the prevalence rates of clinical levels

of social competence issues in children with and without epilepsy; finding prevalence

rates of 5.7% and 2.1% respectively. This supports the view that children with epilepsy

are more likely to suffer from social competence problems than typically developing

children.

Although emotional and behavioural problems may decrease as a child grows

older, issues with social competence are persistent, with social competence scores found

to remain consistent even 6 years after epilepsy onset (Zhao et al., 2015). These elevated

rates of social competence difficulties are significant because social competence

problems in childhood have been linked with later employment difficulties, low academic

achievement, and lower quality of life (Gest, Sesma, Masten, & Tellegen, 2006; Jones,

Greenberg, & Crowley, 2015; Kok et al., 2014). Furthermore, researchers have suggested

that children with low social competence scores are at risk for developing both emotional

and behavioural problems (Kok et al., 2014; Schulte & Barrera, 2010); which in turn puts

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these children at risk for the above mentioned problems.

Although there is consensus within the research community that children with

epilepsy are at a greater risk for EBSP, to date, much research on epilepsy has focused on

seizure control. Although important, this line of research does little to advance our

knowledge of the other difficulties, such as EBSP, that children with epilepsy commonly

experience. This is important as researchers have suggested that children with epilepsy

are more likely to experience EBSP than typically developing children whether they have

attained seizure control or not. For example, Kwong and colleagues (2016) found that

children with epilepsy, despite having good seizure control, still had a greater risk of

emotional problems when compared to children with another chronic illness.

Furthermore, despite the fact that a large portion of children diagnosed with epilepsy will

become seizure-free before adulthood, many individuals continue to experience EBSP as

well as other resultant problems such as lower quality of life, low academic achievement,

and low employment rates well into adulthood (e.g., Filippini, Boni, Giannotta, & Gobbi,

2013). Therefore, it is imperative for researchers to attain a better understanding of

factors that place children with epilepsy at risk for developing EBSP.

When examining potential correlates of EBSP in children with epilepsy, many

agree that the cause of EBSP in children with epilepsy is most likely multifactorial;

consisting of environmental factors, seizure related factors, treatment factors, and

cognitive factors (Kwong et al., 2016). Environmental factors refer to experiences or

situations (e.g., family stress) that a child is exposed to that may increase or decrease the

likelihood of a child presenting with EBSP. Seizure related factors refer to factors

directly associated with the child’s epilepsy diagnosis (e.g., seizure frequency, seizure

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type) that may alter the likelihood of a child presenting with EBSP. Treatment factors

refer to factors related to treatment (e.g., number of anticonvulsant medications) that may

increase or decrease the likelihood of a child presenting with EBSP. Finally, cognitive

factors refer to factors associated with cognitive processes (e.g., executive function) that

may increase or decrease the likelihood of a child presenting with EBSP.

Research findings do suggest the importance of environmental correlates of

EBSP in children with epilepsy. More specifically, research has suggested that parent-

child relations and family stress may be important predictors of EBSP in children with

epilepsy (e.g., Pianta & Lothman, 1994; Sbarra, Rimm-Kaufman, & Pianta, 2002). This

makes sense when we consider that poor parent-child relations and family stress have

been found to be important predictors of EBSP in typically developing children as well

(Giannakopoulos, Mihas, Dimitrakaki, & Tountas, 2009; Harland, Reijneveld, Brugman,

Verloove-Vanhorick, & Verhulst, 2002). Although important, poor parent-child relations

and family stress are not unique to children with epilepsy, and therefore unlikely to be the

cause of increased rates of EBSP in children with epilepsy compared to their peers

without epilepsy. When investigating correlates of EBSP that are specific to epilepsy, to

date, many researchers have examined variables associated with the seizures that children

with epilepsy experience. The most commonly researched variables include age of onset,

duration, seizure types, seizure frequency, and seizure control.

Seizure Related Variables and Emotional, Behavioural, and Social Competence

Problems in Children with Epilepsy

Emotional problems. When examining the potential relation between emotional

problems and seizure related variables the results have been equivocal. For example, Eom

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and colleagues (2014) investigated the association between emotional problems and

epilepsy duration, seizure type, and etiology of epilepsy diagnosis in 598 children with

epilepsy. Emotional problems were not found to be associated with any of these

variables, a result other researchers have also reported (e.g., Kavanaugh, Scarborough, &

Salorio, 2015; Rodenburg, Meijer, Dekovic, Aldenkamp, 2006). Conversely, Turky,

Beavis, Thapar, and Kerr (2008) examined potential predictors of emotional problems in

56 children and adolescents with epilepsy and found that seizure frequency was a

significant predictor. Other studies have also reported a significant association between

emotional problems, epilepsy duration, seizure frequency, and seizure control (e.g.,

Kwong et al., 2016; Oğuz, Kurul, & Dirik, 2002).

It is possible that emotional problems have an association with some seizure

related variables only. Seizure type and age at diagnosis seem to be unrelated to

emotional problems, however, seizure frequency, epilepsy duration, and seizure control

may be important correlates of emotional problems in children with epilepsy. This is

likely because these seizure related variables can serve as proxies for disease severity;

with higher seizure frequency, longer epilepsy duration, and lack of seizure control being

indicative of a more severe condition. Although there are exceptions (e.g., “catastrophic

epilepsies”), the literature suggests that seizure type and age of diagnosis, on the other

hand, may not be related to disease severity (e.g., Arain, Hamadani, Islam, & Abou-

Khalil, 2007; Asadi-Pooya & Farazdaghi, 2016).

Behavioural problems. The relationship between behavioural problems and

seizure-related variables has also been less than clear-cut. For example, a study by Zhao

and colleagues (2015) investigated behavioural problems and potential correlates in

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children with and without epilepsy. As expected, results showed that children with

epilepsy were more likely to present with behavioural problems than the healthy controls;

however, children with generalized versus partial seizures did not differ on the

prevalence rate of behavioural problems. This suggests that seizure type may not be an

important correlate of behavioural problems in children with epilepsy. Other researchers

also have failed to find an association between behaviour problems and seizure

frequency, age of onset, and duration of epilepsy (e.g., Freilinger et al., 2006; Pianta &

Lothman, 1994; van Mil et al., 2009).

An exception to these general findings is that by Sbarra and colleagues (2002),

who looked at potential correlates of behavioural problems in 29 adolescents with

epilepsy. They found that whether or not the adolescent had obtained seizure control was

a significant predictor of behaviour problems, accounting for over 20% of the variability

in behaviour problem scores. It is possible once again, that certain seizure related

variables, such as seizure control, may be important predictors of behavioural problems

while others are not. However, the sample of participants recruited by Sbarra and

colleagues (2002) were within a fairly specific age range (14 to 21 years) unlike the other

studies that have failed to find a relationship between seizure related variables and

behaviour problems (e.g., 5 to 18 years old; Freilinger et al., 2006). Since Sbarra and

colleagues recruited only adolescents (aged 14-21) it is unclear whether their findings can

be generalized to younger children with epilepsy. Furthermore, as behavioural problems

have been shown to mitigate as a child ages (Zhao et al., 2015), adolescents with epilepsy

still experiencing behavioural problems may be experiencing more severe behavioural

issues than the adolescents with epilepsy whose behavioural problems have resolved.

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Social competence. Although there is research that suggests that there is no

relation between social competence and seizure related variables in children with

epilepsy (e.g., Zhao et al., 2015), the majority of research suggests that there is a relation

between the two. For example, Almane, Jones, Jackson, Seidenberg, and Hermann (2014)

examined potential correlates of social competence in children with partial epilepsy and

with generalized epilepsy, as well as typically developing children. Results showed

children with generalized epilepsy scored significantly lower than children with partial

epilepsy on measures of total social competence. This suggests that seizure type may be

an important predictor of problems with social competence. Other research supports this

finding (Gebauer-Bukurov, Markovic, Sekulic, & Bozic, 2015) and also indicates that

seizure severity (Dunn et al., 1997) and seizure control (Gebauer-Bukurov et al., 2015)

may be important predictors. It should be highlighted however, that these studies either

focus on adolescents (e.g., Gebauer-Bukurov et al., 2015) or children with recent onset

epilepsy (e.g., Almane et al., 2014; Dunn et al., 1997) making it difficult to determine

whether the findings generalize to younger children with epilepsy or children who have

had epilepsy for a longer duration of time.

The conflicting results in this area of research may be the result of the manner in

which researchers are collecting information about the participants’ EBSP. A number of

studies have used self-report (e.g., Turky et al., 2008; Gebauer-Bukurov et al., 2015),

however, there is research that suggests this may not be the most reliable source. For

example, Goodman, Ford, Simmons, Gatward, and Meltzer (2000) found that parent or

teacher reports of a child or adolescent’s emotional and behavioural function were more

reliable measures when compared to self reports. Furthermore, the accuracy of self-

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reports may be age dependent; research suggests that self-report may be inconsistent in

children due to their undeveloped cognitive skills and lack of self-insight (Edelbrock,

Costello, Dulcan, Kalas, & Conover, 1985). In adolescents, accuracy of self-report may

depend on the problem that the adolescent presents with self-report measures being more

sensitive for detecting internalizing problems than behavioural problems (Hope et al.,

1999).

Regardless of the conflicting results in the literature that examines the

association between seizure-related variables and EBSP in children with epilepsy, it has

become widely accepted amongst the research community that the predictive power of

these variables is low (Sbarra et al., 2002). Therefore, researchers have turned to other

potential predictors of EBSP, such as treatment factors, in children with epilepsy.

Anticonvulsant Medications and Emotional, Behavioural, and Social Competence

Problems in Children with Epilepsy.

Anticonvulsant medication, one of the most recommended treatments for seizures,

comes with a wide range of side effects that may cause a child with epilepsy to be more

susceptible to EBSP. For example, common side effects of anticonvulsant medication

include aggression, fatigue, dizziness, irritability, fatigue, and depression (Dreisbach,

Ballard, Russo, & Schain, 1982; Lee, 2010). Some research suggests that children taking

anticonvulsant medication are more susceptible to these side effects than adults taking the

same medications (Lee, 2010). Although the side effects of these medications have been

reduced significantly in the last decade, only 60% of individuals with epilepsy are able to

obtain seizure control by taking just one type of anticonvulsant medication (Donner &

Snead, 2006). This means that some individuals have to take multiple types of

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anticonvulsant medication; increasing the likelihood of experiencing medication side

effects (Lee, 2010). As a result, researchers have also looked at the number of

anticonvulsant medications as a potential predictor of EBSP in children with epilepsy.

Once again, the findings in this area are conflicting; however, research has

generally failed to demonstrate a link between number of anticonvulsant medications and

emotional problems (Caplan et al., 2005; Titus, Kanive, Sanders, & Blackburn, 2008),

behavioural problems (van Mil et al., 2009) or social competence (Jakovljević &

Martinović, 2006). Interestingly, researchers have reported that EBSP in children with

epilepsy often manifest simultaneously or even before first seizure onset (Austin et al.,

2001; Baum et al., 2010). Therefore, Dunn, Auston, and Huster (1997) suggested that it is

unlikely that medication is a strong correlate of these problems.

The research reviewed to this point does not offer a clear picture of possible

predictors of EBSP in children with epilepsy. Therefore, it is important to examine other

factors that may be correlated with EBSP, such as cognitive factors. More specifically,

researchers have found a strong association between executive function (EF) and EBSP

in both typically developing children (Alduncin, Huffman, Feldman, & Loe, 2014;

Hughes, 1998; Karasinski, 2015; Levens & Gotlib, 2010; Mocan et al., 2014; Razza &

Blair, 2009) and children with epilepsy (Baum et al., 2010; Giancola, Roth, & Parrott,

2006; Kavanaugh et al., 2015). Moreover, researchers have found an increased

prevalence of EF problems in children with epilepsy when compared to typically

developing children (de Lima, Moreira, da, Mota Gomes, & Maia-Filho, 2014; Thomas et

al., 2014). This suggests that the increased rate of EF problems in children with epilepsy

may be associated with the increased rate of EBSP in these children.

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Executive Function

EF can be defined as a collection of high-level cognitive processes (e.g., inhibition)

that allow for mental control and self-regulation (Carlson & White, 2013; Juric et al.,

2013). EF is especially important in novel environments and situations where success of

the individual is dependent on their ability to adjust or change behaviours (Huizinga,

Dolan, & van der Molen, 2006). There has been much debate about the cognitive

processes thought to make up EF. Previously, the construct of EF was examined in a

purely empirical manner; descriptions of EF were based on aggregated results of

measures (e.g., exploratory factor analysis) presumed to tap EF. These measures,

however, were not adequately validated and therefore it was unclear whether they tapped

EF or other processes not related to EF. Additionally, these measures did not control for

the “task-impurity problem” (Miyake, Friedman, Emerson, Witzki, & Howerter, 2000).

That is, EF by definition operates with and controls other cognitive processes that are not

directly related to the EF component. Therefore, it was unclear whether a so-called EF

component actually reflected EF or whether it was the result of variance in non-executive

skills, such as motor abilities (Miyake et al., 2000).

In an influential paper, Miyake and colleagues (2000) examined processes

commonly hypothesized to be components of EF; shifting of mental sets (or cognitive

flexibility), inhibition of prepotent responses, and updating of the contents of working

memory. Using latent variable analysis Miyake and colleagues (2000) found evidence for

these three related but distinct components of EF, as hypothesized. Shifting of mental sets

refers to deliberately switching back and forth from one task or mental set to another (St

Clair-Thompson & Gathercole, 2006). Inhibition of prepotent responses refers to one’s

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ability to inhibit or stop dominant or automatic responses when necessary (Carlson &

White, 2013; Huizinga et al., 2006). Updating of the contents of working memory

involves monitoring and coding information based on task relevance and then revising or

updating the items held in working memory to make sure only relevant information is

kept. Miyake et al.’s (2000) findings have been replicated in adults (Fisk, & Sharp, 2004;

Wasserman & Wasserman, 2013) and children (Lehto, Juujarvi, Kooistra, & Pulkkinen,

2003). A key finding of this research is that although EF can be viewed holistically as

related processes that may be applied simultaneously to a task, each process also can

contribute independently to a task (Miyake et al., 2000; Wasserman & Wasserman,

2013). This means each component can be examined separately and may contribute

uniquely to different cognitive tasks as well as different aspects of emotional,

behavioural, and social processes. Examining the differential relations between

components of EF and emotional, behavioural, and social processes could assist in the

development of specialized interventions that target the specific EF component that may

be not be developing optimally (Wasserman & Waserman, 2013).

To date, research looking at the association between EF and EBSP in children with

epilepsy has been very limited. A review of the research investigating the association

between EF and ESBP in typically developing children would help inform our

understanding of the relation that may exist in children with epilepsy.

Executive Function and Emotional, Behavioural, and Social Competence Problems

in Typically Developing Children

Researchers have become increasingly interested in the relation between EBSP

and EF in typically developing children. Results of these studies suggest that specific

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components of EF (i.e., shifting, inhibition, updating) may be correlated with different

emotional, behavioural, and social problems in typically developing children.

Shifting of mental sets (shifting). To date, the literature suggests a strong

relation between shifting and emotional problems in typically developing children. For

example, Mocan, Stanciu, and Visu-Petra (2014) investigated the potential link between

shifting and emotional problems in 108 school-aged children (7 to 11 years). They found

that although children with higher levels of emotional symptoms (specifically anxiety and

depression) did not score lower on measures of shifting, the high emotion group did show

slower response times than children with fewer emotion symptoms. This suggests that

children with emotional problems are slower to shift mental sets than children without

these problems. Furthermore, Ghassabian and colleagues (2014) investigated the

potential link between internalizing problems (i.e., emotionally reactive,

anxious/depressed, and withdrawn behaviour) and different components of EF in 802

typically developing children. They found that shifting, inhibition, and updating were

significantly associated with each of the above-mentioned internalizing problems.

Furthermore, when Ghassabian et al. examined the significant link between early low

positive emotionality, defined as a child’s low mood states and low environmental

interaction, and later internalizing problems, results showed that shifting, but not

inhibition, updating, or early internalizing problems, significantly mediated the

relationship between positive emotionality and withdrawn behaviour; suggesting a

meaningful relation between shifting and internalizing problems. Other researchers have

also reported a link between shifting and emotional problems (Emerson, Mollet,

Harrison, 2005; Karasinki, 2015).

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Research examining the potential relationship between shifting and behavioural

problems has been limited and suggests a weak association between the two. Although

some researchers have found a significant relation between shifting and behavioural

problems (e.g., Karasinski, 2015; Young et al., 2009), this association was significantly

weaker than the relation with other EF components (i.e., inhibition; Young at al., 2009)

or the relation was no longer significant when controlling for other components of EF

(i.e., inhibition and updating; Karasinksi, 2005).

To date, there appears to be no research that has looked at the relation between

shifting and social competence in typically developing children. In fact, research on

social competence and EF looks at the relation between social competence and a general

EF composite score, which combines shifting, inhibition, and updating (e.g., Devine,

White, Ensor, & Hughes, 2016; Holmes, Kim-Spoon, & Deater-Deckard, 2016). Indirect

evidence for an association between shifting and social competence is provided by

Hughes, Dunn, and White (1998); they found that “hard to manage” children, who

showed impaired social relations, scored significantly worse on one measure of shifting

than the typically developing peer group.

Inhibition of prepotent responses (inhibition). Many researchers looking at

inhibition and emotional problems in typically developing children have failed to find a

relation between the two (Emerson et al., 2005; Ghassabian et al., 2014; Hill et al., 2013,

Kyte, Goodyer, & Sahakian, 2005). For example, Kyte and colleagues (2005) found that

adolescents with depression did not significantly differ from the control group on

measures of inhibition. However, Kaiser and colleagues (2003) found that adults

diagnosed with depression showed impairments on a measure of response inhibition

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compared to adults without depression. This suggests that age may moderate the

association between inhibition and emotional problems.

In contrast, much research suggests a strong relation between inhibition and

behavioural problems in typically developing children (Hughes, 1998; Karasinski, 2015;

Nigg et al, 2006; Raaujmakers et al., 2008; Young et al., 2009). For example,

Raaujmakers and colleagues (2008) were interested in looking at how specific

components of EF may be associated with problem behaviours in preschool children.

They found that the only EF component significantly associated with aggressive

behaviour was inhibition. This association remained significant even when attention was

controlled for. Furthermore, Young et al. (2009) showed that inhibition, updating, and

shifting were significantly associated with externalizing behaviours in both early and late

adolescence. However, the association between inhibition and externalizing behaviours

was significantly stronger than that between updating and externalizing behaviours or

shifting and externalizing behaviour. These results suggest a strong relation between

inhibition and behavioural problems.

Inhibition has also been found to be related to social competence in typically

developing children (e.g., Balaraman, 2003; Hughes, Dunn, & White, 1998; Olson,

1989). For example, Fahie and Symons (2003) found that children who scored worse on

measures of inhibition also tended to have more social problems. Furthermore, the

NICHD Early Child Care Research Network (2003) not only found that inhibition was

significantly related to social competence scores, but also that inhibition partially

mediated the relation between family environment and social competence. This suggests

that the relation between environmental factors and social competence may be partially

18

the result of the child’s inhibition abilities. Finally, the results of a study by Gewirtz,

Stanton-Chapman, and Reeve (2009) suggested that early inhibition problems might be a

risk factor for later social competency difficulties.

Updating of working memory (updating). Although there is evidence of a

potential relation between updating and emotional problems in adults (Levens & Gotlib,

2010), very little research has looked at the potential relation between updating and

emotional problems in children. To date, researchers that have looked at this association

have reported mixed results. For instance, Ghassabian and colleagues (2014) found that

updating was significantly associated with emotional reactivity, anxiety/depression, and

withdrawn behaviour in 802 typically developing children. However, other researchers

have been unable to replicate these findings (Emerson et al., 2005; Hill et al., 2013).

Conversely, research suggests a strong association between updating and

behavioural problems in children; with higher externalizing behaviours related to lower

updating ability (Cassidy, 2016; Karasinski, 2015; Séguin, Nagin, Assaad, & Tremblay,

2004; Young et al., 2009). For example, Séguin and colleagues (2004) found that three

different measures of updating were significantly related to aggression and impulsivity.

Furthermore, when Séguin et al. controlled for IQ and general memory, updating and

aggression remained significantly related.

Many researchers have found a relation between updating and social competence

(Alloway et al., 2005; Hughes et al., 1998; Kofler et al., 2011; McQuade, Murray-Close,

Shoulberg, & Hoza, 2013). For example, McQuade and colleagues (2013) found that

impaired central executive working memory scores (used to tap updating) were

significantly correlated with peer rejection, low overall social competence, relational

19

aggression, and deficits in conflict resolution in typically developing elementary school

students. Moreover, Kofler and colleagues (2011) found a significant relation between

central executive working memory scores and social problems in a sample of both

typically developing children and children with ADHD.

In summary, the research with typically developing children reviewed above

suggests that emotional problems are most strongly related to shifting; with a weaker

association found between emotional problems and updating. There appears to be no

direct association between emotional problems and inhibition. With regards to

behavioural problems, the research suggests a weak relation with shifting but a strong

relation to both inhibition and updating. When looking at social competence, there is little

research looking at the association with shifting; but the literature suggests that both

inhibition and updating are strongly related to social competence. A summary of these

findings can be found in Table 1. Overall, these findings indicate that children with

emotional, behavioural, or social competence problems may exhibit different profiles of

EF deficits.

Executive Function and Emotional, Behavioural, and Competence Problems in

Children with Epilepsy

Children diagnosed with epilepsy have been found to score lower on measures

of general EF than their typically developing peers (Lindgren et al., 2004; Neri et al.,

2012; Neuenschwander et al., 2013) and peers with other chronic illnesses (Conant,

Wilfong, Inglese, & Schwarte, 2010). Researchers looking at shifting ability in children

with epilepsy have found some evidence that shifting may be impaired in children with

idiopathic or cryptogenic epilepsy (Schouten, Oostrom, Peters, Verloop, & Jennekens-

20

Table 1

Summary of Research Looking at the Association between EF Components and EBSP in

Typically Developing Children

No Research Little or no relation Strong relation

Emotional problems

Shifting ✔

Inhibition ✔

Updating ✔

Behavioural problems

Shifting ✔

Inhibition ✔

Updating ✔

Social competence

Shifting ✔

Inhibition ✔

Updating ✔

Schinkel, 2000) and frontal lobe epilepsy (McDonald et al., 2005). There is also evidence

that children with epilepsy score lower on measures of inhibition (Chevalier, Metz-Lutz,

& Segalowitz, 2000; McDonald et al., 2005; Rathouz et al., 2014) and updating (Roberts

& Husain, 2015) compared to children without epilepsy.

Although research suggests a potential relation between EBSP and EF in children

with epilepsy (Baum et al., 2010; Kavanaugh et al., 2015), these studies often focus on

EF in general as opposed to specific, validated components of EF (i.e., shifting of mental

sets, inhibition of prepotent responses, updating of working memory). For example,

21

Baum and colleagues (2010), who defined EF as a factor including measures of attention,

problem solving, and visual construction, found that low EF scores were associated with

higher rates of internalizing, externalizing, and total problems in children with at least

one recognized seizure. The problem with using a general EF factor that incorporates

complex measures of EF is that it makes it difficult to determine whether these studies

are truly assessing EF or whether they are instead assessing other complex cognitive

processes (e.g., attention, problem solving). Furthermore, in order to gain a better

understanding of the association between EBSP and EF, it is important to know if

specific components of EF are associated with different EBSP in children with epilepsy.

A review of the literature reveals no studies that have looked at the association

between EBSP and specific components of EF in children with epilepsy. However, in

young adults, Gul and Ahmed (2014) found that task-shifting was a significant predictor

of displaced aggression in these individuals, which suggests shifting may be a predictor

of behaviour problems in adults with epilepsy. However, it is unclear whether the results

of this study can be generalized to children with epilepsy.

Given this gap in the literature, the aim of the current study is extend and clarify

the literature by investigating specific components of EF in children with epilepsy to

determine if there is an association between EF and EBSP in children with epilepsy.

Based on the above review of typically developing children and adults with epilepsy, it is

predicted that after controlling for seizure related variables (e.g., seizure control, seizure

type, medication):

1) EBSP will be significantly associated with general EF (e.g., Baum et al., 2010;

Kavanaugh et al., 2015);

22

2) Emotional problems will be associated with shifting (e.g., Emerson et al., 2005;

Karasinki, 2015; Mocan et al., 2014);

3) Behavioural problems will be associated with inhibition, shifting, and updating (e.g.,

Cassidy, 2016; Gul & Ahmed, 2014; Karasinski, 2015; Raaujmakers et al., 2008;

Séguin, Nagin, Assaad, & Tremblay, 2004; Young et al., 2009); and

4) Social competence scores will be associated with inhibition and updating (Alloway

et al., 2005; Balaraman, 2003; Fahie & Symons, 2003; Hughes et al., 1998; Kofler et

al., 2011; McQuade et al., 2013).

Methodology

Participants

Children diagnosed with epilepsy that underwent a neuropsychological

assessment at the Children’s Hospital of Eastern Ontario (CHEO) between 2004 and

2015, by a neuropsychologist whose practice includes children with seizure-related

disorders, were considered for this study. These children were typically referred for a

neuropsychological assessment because of potential learning difficulties. Only the most

recent neuropsychological assessment was used for this study. Although most children

were administered a standardized test of intelligence during their assessment, intellectual

functioning was not used as an exclusion criteria.

Inclusion and exclusion criteria. Only children between the age of 6 and 18

years at the time of assessment were included in the study. Additional inclusion criteria

were: a) a formal diagnosis of epilepsy and b) measures of EF and EBSP completed by

mothers. Children were excluded if epilepsy was diagnosed after a brain injury (e.g.,

traumatic brain injury; stroke) or if the child presented with additional

23

neurodevelopmental disorders such as autism.

Procedure

The psychology charts of 73 children assessed between 2004 and 2015 were

available for review. Psychology data included measures of intelligence, EF, and EBSP.

In order to ensure reliability of data extraction from the files, 10% of the files were

double checked by a neuropsychologist. Corresponding medical charts were also

reviewed to extract information about the child’s demographic background (gender, age

at assessment), as well as information about the child’s medical history (age at diagnosis,

type of seizure, seizure frequency, medication use, additional diseases/disorders in

addition to epilepsy). It should be noted that although the way seizures are classified has

been revised, the previous method of classification is used in this thesis, as it is most

relevant to the literature.

In order to maintain informant consistency, questionnaires completed by the

mother were used. After applying inclusion and exclusion criteria, a total of 42

participants remained (18 males and 24 females). Participants ranged in age from 6.0 to

18.1 years old (M = 12.5, SD = 3.37).

Measures

Background information. Demographic and seizure related variables were

collected directly from the participant’s medical record. Only information collected prior

to, or at the same time as, the neuropsychological assessment was included in the study.

All information in the medical charts collected after the assessment was disregarded.

With regard to seizure related variables, the present study included age at epilepsy

diagnosis, seizure duration in months, seizure type (generalized, partial, complex partial),

24

and whether the participant had obtained seizure control (defined as having gone three or

more months without a seizure). Information was also collected on the number of

anticonvulsant medications that the child was taking. Unfortunately, information on

seizure frequency and information on family history of epilepsy was not consistently

available in the medical charts, and therefore was not included.

Intelligence. The Wechsler Intelligence Scale for Children- Fourth Edition

(WISC-IV; Wechsler, 2004) was used to measure intelligence. The WISC-IV consists of

10 different subtests, which provide four standardized scores: Verbal Comprehension

(vocabulary, similarities, comprehension), Working Memory (digit span, letter-number

sequencing), Perceptual Reasoning (block design, matrix reasoning, and picture

concepts), and Processing Speed (coding, symbol search). The WISC-IV also provides a

Full-Scale IQ score. For the purpose of this thesis, the Full-Scale IQ score was used to

ensure that participants with intellectual disorders (i.e., Full-Scale IQ scores below 70)

did not differ from children without intellectual disorders on various predictor and

outcome variables. As the two groups were not found to be significantly different, all

children were grouped together for the analyses.

Executive function. The Behaviour Rating Inventory of Executive Functioning

(BRIEF), developed by Gioia, Isquith, Guy, and Kenworthy (2000) is a widely used

clinical and research parent report questionnaire that assesses EF skills in individuals

aged 5 to 18. The BRIEF contains 86 items, which are grouped to make up eight different

scores of EF: emotional control, inhibition, initiation, monitor scales, organization of

materials, planning/organizing, shifting, and working memory. These eight subsections

are then grouped in two global index scores: behavioural regulation (inhibition, emotional

25

control, behaviour, and shifting) and metacognition (initiation, working memory,

planning/organizing, organizing, of materials, and monitoring). These two components

are also combined to give an overall global executive composite score (Nguyen et al.,

2014). A higher score on a BRIEF subscale indicates more dysfunction in that specific

area; with scores 65 or higher indicating the clinical range.

In keeping with the EF components identified by Miyake et al. (2000), the

shifting, working memory, and inhibition subscale scores were used to represent shifting

of mental sets, updating of the contents of working memory, and inhibition of prepotent

responses, respectively, in the current study. In addition, the overall global executive

composite score was used to represent the child’s overall EF.

Social-emotional and behavioural functioning. The Child Behavior Checklist

(CBCL; Achenbach, 1991) is a parent report questionnaire that measures behaviour and

emotional problems in children aged 6 to 18 years. The CBCL contains 118 items that

make up eight subscales: aggressive behaviour, rule breaking behaviour,

anxious/depressed, attention problems, social problems, thought problems, somatic

complaints, and withdrawn/depressed, which are grouped together to provide a total

internalizing and externalizing problem behaviour score, as well as a total problem

behaviour score. The CBCL also provides clinicians with scores on three social

competence subscales: activity, school, and social, which form a total social competence

score. For the purposes of the current study, emotional, behavioural, and social

competence problems were represented by total internalizing, total externalizing, and

total social competence scores, respectively. Higher scores on internalizing and

externalizing problem behaviour indicate more problems whereas higher scores on social

26

competence indicate better social competence.

Results

A summary of the participants’ seizure and treatment-related data can be found in

Table 2. Means and standard deviations for scores on the measures of EF and EBSP can

Table 2

Demographics of Participants

Characteristic Participants (n = 42)

Males 18 (42.86%)

Females 24 (57.14%)

IQ 79.27 (range 46-114, SD = 15.10)

Age at diagnosis (months) 81.00 (0.00 – 193.00, SD = 58.20)

Age at assessment (months) 149.69 (72.00-217.00, SD = 40.44)

Duration of epilepsy (months) 68.70 (1.00 – 206.00, SD = 56.90)

Seizure control

Yes 47.62%

No 33.33%

Uncertain 19.05%

Anticonvulsant medication

None 16.67%

One type 35.71%

Two types 26.19%

Three or more types 16.67%

Uncertain 4.76%

Seizure type

Generalized 35.71%

27

Partial 23.81%

Complex partial 26.19%

Uncertain 14.28%

be found in Table 3. As indicated above, scores of 65 or more on the measure of EF are

considered to be in the clinical range. With respect to EF, participants, on average, scored

in the clinical range for updating only. On the EBSP measure, scores for emotional,

behavioural, and social competence problems, on average, were not in the clinical range.

Data screening. An important assumption of linear regression is that the

independent and dependent variables are linearly related to one another. Analysis of

scatterplot diagrams showed that the global executive composite score and the three

individual components of EF, shifting, inhibition, and updating, were all linearly related

Table 3

Executive Function and Emotional, Behavioural and Social Competence Scores (N = 42)

Measure Mean SD Range

EF total composite score 63.00 13.01 37.00-91.00

Shifting 59.17 14.82 38.00-98.00

Inhibition 57.19 11.72 40.00-78.00

Updating 66.55 13.05 45.00-87.00

Emotional Problems 57.45 12.01 33.00-79.00

28

Behavioural Problems 54.57 11.06 33.00-76.00

Social Competence 40.17 8.40 24.00-59.00

to all three of the independent variables; emotional problems, behavioural problems, and

social competence problems; with higher emotional and behavioural problems being

associated with greater EF problems, and lower social competence problems being

associated with greater EF problems. Furthermore, analysis of histograms revealed that

all variables entered in the regression (independent and dependent) were normally

distributed around the mean. An examination of the residual plots for each regression

indicated homoscedasticity. An examination of the Variance Inflation Factors (VIF) for

the EF predictors revealed no VIF above two. This indicates that although the predictors

may be moderately correlated with one another, the correlation is not significant enough

to cause concern of multicollinearity. Furthermore no Tolerance values were found to be

below .05, again suggesting that multicollinearity was not an issue.

A correlation analysis was conducted to determine if any of the seizure or

treatment variables were correlated with emotional, behavioural, and social competence

problems (See Table 4). This analysis showed that none of the seizure or treatment

related variables were significantly related to emotional or social competence problems;

however, both seizure control and number of anticonvulsant medications were

significantly correlated with behavioural problems.

Hypothesis 1. A bivariate regression was completed to determine how well the

global EF composite score predicted emotional problems and social competence

29

problems. The analyses showed that the global EF composite was significantly correlated

with emotional problems (r(40) = .54, p = .0004) and social competence (r(34) = -.55, p =

.001). A hierarchical multiple regression was done to determine if the global EF

composite score remained a significant predictor of behavioural problems after

controlling for seizure control and number of anticonvulsant medications. Results of this

30

Table 4

Correlations of Seizure and Treatment Related Variables with Emotional, Behavioural,

and Social Problems.

1 2 3 4 5 6 7 8

1. Emotional problems --- .62** -.32 -.17 .00 -.21 -.07 .20

2. Behavioural problems --- -.39* -.20 .13 .01 -.43* .37*

3. Social competence

problems

--- .18 -.14 .08 .00 -.15

4. Age at diagnosis --- -.75** .08 .20 -.25

5. Epilepsy duration --- -.10 -.26 .12

6. Seizure type --- -.13 .05

7. Seizure control --- -.58**

8. Anticonvulsant

medication

---

Mean 57.45 54.57 40.17 81.02 68.67 2.14 ---a 1.45

SD 12.01 11.06 8.40 58.20 56.89 .83 ---a .99

*p < .05, ** p < .001

aAs seizure control was a dummy variable (coded 0 = no seizure control and 1= seizure

control), mean and standard deviation is not reported.

31

regression are summarized in Table 5. Seizure control and number of anticonvulsant

medications were entered in Step 1. This regression model was statistically significant

and accounted for approximately 15% of the variance in behaviour problems; R2adj = .15,

F(2,29) = 3.83, p = .034. Seizure control was a significant predictor of behavioural

problems, t (29) = -2.07, p = .048; uniquely accounting for 12% of the variance in

Table 5

Results of a Hierarchical Multiple Regression to Predict Behavioural Problems from

Global EF Composite, Seizure Control, and Anticonvulsant Medication (n = 32)

b SE β ΔR² F

Step 1 .21 3.83*

Seizure control -9.75* 4.72 -.43

Medication .58 2.34 .05

Step 2 .50 46.96**

Global EF .67** .10 .74

Total R2 .67

*p < .05; **p < .0001

behavioural problems. Global EF composite was then entered in Step 2. This regression

model was also statistically significant and accounted for approximately 67% of the

32

variance in behavioural problems; R2adj = .67, F (3,28) = 22.24, p < .0001. Taken

together, these results support the first hypothesis, that global EF composite would be a

significant predictor of emotional, behavioural, and social competence problems, even

after controlling for seizure and treatment related variables

Hypothesis 2. A correlation analysis indicated that shifting, inhibition, and

updating were significantly correlated with emotional problems (r = .63, p < .0001; r =

.26, p = .05; r = .36, p = .009, respectively), that shifting was significantly correlated with

inhibition and updating (r = .53, p < .0001; r = .59, p < .0001, respectively), and that

inhibition was correlated was updating (r = .63, p< .0001). As mentioned above, none of

the seizure or treatment-related variables were significantly related to emotional

problems.

A standard multiple regression was conducted in order to determine whether

shifting, inhibition, or updating was a significant, unique predictor of emotional problems

in children with epilepsy. The regression model was statistically significant and the three

components of EF accounted for approximately 36% of the variance in emotional

problems; R = .64, R2adj = .36, F(3, 38) = 8.71, p = .0002. Only shifting was a significant

unique predictor of emotional problems; t (38)= 4.18, p = .0002, Sr2unique= .27; explaining

27% of the variance in emotional problems. Both inhibition and updating were not

significant predictors; t (38)= -.72, p = .48 and t (38)= -.23, p = .82 respectively. These

findings support the prediction made in the second hypothesis; that shifting would be a

significant predictor of emotional problems.

Hypothesis 3. The third hypothesis predicted that all three components of EF

would be significant predictors of behavioural problems in children with epilepsy. A

33

correlation analysis showed that shifting, inhibition, and updating were significantly

related to behavioural problems (r = .69, p < .0001; r = .76, p < .0001; r = .51, p = .0003,

respectively).

A hierarchical multiple regression was conducted in order to determine whether

shifting, inhibition, or updating were significant, unique predictors of behavioural

problems in children with epilepsy, after controlling for seizure control and number of

anticonvulsant medications. The results of this regression are summarized in Table 6.

Seizure control and number of anticonvulsant medications were entered in Step 1. This

regression model was statistically significant and accounted for approximately 14% of

the variance in behaviour problems; R2adj = .14, F(2,31) = 3.62, p = .039; however,

individually seizure control and number of medications were not unique significant

predictors. The three EF components were then entered in Step 2. The regression model,

which included all five predictors, was statistically significant, R2adj= .72, F(5, 28) =

18.02, p < .0001; accounting for approximately 72% of the variance in behavioural

problems. Consistent with the third hypothesis, both shifting (t(28) = 3.92, p = .0005,

Sr2unique= .13) and inhibition (t(28) = 4.20, p = .0002, Sr2

unique= .15) were significant

predictors of behavioural problems, even after controlling for seizure control and number

of anticonvulsant medications. Updating, however, was not found to be a significant

predictor.

Hypothesis 4. A standard multiple regression was conducted in order to

determine whether shifting, inhibition, or updating were significant, unique predictors of

social competence problems in children with epilepsy. The regression model was

statistically significant and the three components of EF accounted for approximately 28%

34

of the variance in social competence problems; R = .59, R2adj = .28, F(3, 31) = 5.50, p =

.004. When looking at the contributions of the individual predictors, shifting was a

significant predictor of social competence problems; t(31) = -2.84, p = .02, Sr2unique= .13;

uniquely explaining 13% of the variance in social competence problems. Both inhibition

and updating were not significant predictors; t (31) = .85, p = .40 and t (31) = -1.57, p =

Table 6

Results of a Hierarchical Multiple Regression to Predict Behavioural Problems from

Shifting, Inhibition, Seizure Control, and Number of Anticonvulsant Medications (n=34)

b SE β ΔR² F

Step 1 .19 3.62*

Seizure control -8.55 4.50 -.38

Medication .96 2.20 .09

Step 2 .57 18.02**

Shifting .35** .09 .47 .

Inhibition .50** .12 .51

Updating -.09 .11 -.11

Total R2 .72

Note: Medication = number of anticonvulsant medications

*p < .05; ** p < .001

35

.13 respectively. These results do not support the fourth hypothesis, which predicted

inhibition and updating, but not shifting, would be significant predictors of social

competence problems.

Discussion

The aim of this study is to look at specific components of EF as potential

predictors of EBSP in children with epilepsy. As predicted, overall EF is a significant

predictor of EBSP; however, when the three aspects of EF are separated, different

components are associated with each type of problem. As expected, shifting predicts

emotional problems and shifting and inhibition predict behavioural problems; however,

contrary to our hypothesis, shifting not inhibition or updating predicts social competence.

General EF and EBSP in children with epilepsy

Our findings indicate that greater EF impairment is associated with greater EBSP

in children with epilepsy. This is consistent with the literature examining EF and EBSP in

children with epilepsy (e.g., Alfstad et al., 2016; Baum et al., 2010; Kavanaugh et al.,

2015), with typical development (e.g., Ghassabian et al., 2014; Young et al., 2009), and

with neurodevelopmental disorders; such as autism (e.g. Visser, Berger, Van, Prins, &

Teunisse, 2015) and Down syndrome (e.g., Jacola, 2013). These findings have led

researchers to suggest that EF deficits may be an important predictor of EBSP in

children. That is, EF affects a wide range of cognitive functions, such as planning,

problem solving skills, and behaviour control. Therefore, as demands placed on the child

become increasingly complex, their difficulties with EF become more and more

problematic, potentially resulting in the manifestation of EBSP (Alfstad et al., 2016).

This hypothesis is supported by the results of a study by Kertz, Belden, Tillman, and

36

Luby (2015) who found that preschool EF scores were predictive of depression and

anxiety severity up to 7.5 years later; suggesting deficits in EF are present before the

appearance of EBSP in these children. These findings, combined with the current study

findings, suggest that early assessment of EF may help clinicians identify children at risk

for developing EBSP. EF is a broad construct, however, and associated with a number of

different skills. It is important to look at the different aspects of EF, as opposed to EF in

general, in order to clarify whether different aspects of EF are associated with different

problems. It is possible for two individuals to perform similarly when given a measure of

general EF yet have very different EF profiles when looking at the different aspects.

Moreover, measures of so-called global EF are assumed to tap the different components

of EF (i.e., inhibition, shifting, and updating), but this may not be the case (Miyake et al.,

2000).

EF and emotional problems in children with epilepsy

As expected, we find that greater difficulties in shifting are associated with

greater emotional problems in children with epilepsy. This is consistent with research

with typically developing children (Emerson et al., 2005; Karasinki, 2015; Mocan et al.,

2014; White, McDermott, Degnan, Henderson, & Fox, 2011); longitudinal studies

indicate that shifting measured in preschoolers predicts the severity level of a child’s later

anxiety and depression (Kertz et al., 2015). Although researchers are still unsure of the

causes of emotional problems in children, much research suggests the importance of the

contribution of shifting to these problems (Kertz et al., 2015). It has been suggested that

better shifting ability serves as a protective factor against emotional problems, even in

children who are unable to inhibit undesirable behaviours, by allowing the child to

37

appropriately regulate negative and stressful situations. That is, children with better

shifting skills are able to change their focus away from negative or stressful events, and

to focus on new, more relevant information. Some researchers speculate that shifting

deficits may result in sustained attention on negative or stressful events (Kertz et al.,

2015), which may result in individuals continuously reflecting and replaying negative

events. This constant rumination and reflection on pessimistic or challenging experiences

has been found to be associated with not only the development, but also the maintenance,

of emotional problems (Demeyer, De Lissnyder, Koster, & De Raedt, 2012).

Furthermore, increased rumination on these types of events has been found to be

associated with lengthened depressive episodes (Nolen-Hoeksema, Morrow, &

Fredrickson, 1993).

These findings have potential implications for intervention for children with

epilepsy. That is, in order to reduce the risk of emotional problems in children with

epilepsy, it may be important to reduce the frequency that these children are ruminating

on negative or stressful experiences. This could be accomplished with the integration of

shifting training in their interventions. The addition of shifting training could help these

children improve their ability to shift between different mental sets (or increase cognitive

flexibility), and as a result, decrease the amount of time a child with epilepsy spends

ruminating on these negative or stressful experiences. In fact, research examining

treatments that target components of EF, such as shifting and inhibition, showed these

types of interventions were successful in reducing the amount of time that a typically

developing adult reflected and replayed negative events (Kertz et al., 2015; Siegle,

Ghinassi, & Thase, 2007). This suggests that positive outcomes with regard to emotional

38

functioning might be possible by reducing the amount of time that children with epilepsy

are focusing on negative and stressful experiences.

Behavioural Problems in Children with Epilepsy

Consistent with our initial hypothesis, we find that inhibition and shifting are

significant predictors of behavioural problems in children with epilepsy, something also

found in typically developing children (Hughes, 1998; Karasinski, 2015; Nigg et al,

2006; Raaujmakers et al., 2008; Young et al., 2009). Shifting has also been found to be a

significant predictor of behaviour problems in adults with temporal lobe epilepsy (Gul &

Ahmed, 2014). Recall that inhibition refers to the ability to inhibit dominant and often

inappropriate responses (Carlson & White, 2013; Huizinga et al., 2006). Inhibition is seen

as an essential component of regulating behaviour; therefore, many researchers have

proposed that inhibition difficulties are an important predictor of behaviour problems

(e.g., Nigg et al., 2006). Inhibition is important for monitoring and correcting behaviour,

and as such, it is reasonable to expect that individuals with dysfunctional inhibition skills

will be more likely to act inappropriately. Deficits in inhibition may cause an individual

to blurt out things without thinking, act aggressively, or to take part in deviant or rule-

breaking behaviours. Moreover, there is evidence that inhibition deficits are present

before the manifestation of behavioural problems and are good predictors of later

behavioural problems (Nigg et al., 2006). This suggests that it is important for clinicians

to assess specific aspects of EF (such as inhibition) in order to identify and support at-risk

children before a problem arises.

There is also research that suggests that assessing a child’s shifting skills may be

important for understanding the underlying causes of their behaviour problems. For

39

example, deficits in shifting may result in inflexible thoughts in negative or challenging

situations (Visser et al., 2015), which may result in persistence of behaviour that is not

appropriate for that situation or difficulty shifting attention to new and relevant

information. Due to this lack of attention to important information, the child may then

respond to situations inappropriately (Visser et al., 2015). Understanding the underlying

mechanisms of behavioural problems can assist in changing the attributions that

clinicians and parents have for a child’s behaviour problems. Specifically, these problem

behaviours may be the result of deficits with shifting of attention, as opposed to the child

purposely behaving badly.

Contrary to expectations, updating is not a significant predictor of behavioural

problems in children with epilepsy. It is possible that this association is subtler in

children with epilepsy and we lacked the power to detect an effect due to our small

sample size and restricted range in updating scores. It should be noted, however, that the

mean score achieved by children in the current study on the BRIEF- updating subscale is

above the cutoff for the clinical range. This indicates children with epilepsy have

significant difficulties with this aspect of EF. Clearly, more research should be done with

a larger sample of children in order to obtain a clearer picture of the role updating plays

in behavioural problems, if any.

Social Competence Problems in Children with Epilepsy

Inconsistent with our fourth hypothesis, we find that shifting, but not inhibition

or updating, significantly predicts social competence problems in children with epilepsy.

However, almost no research has looked at the potential association between shifting and

social competence, even in typically developing children. Despite the lack of research,

40

researchers have indirectly suggested the possibility of a relation between the two

variables (Hughes et al., 1998; Stichter, Christ, Herzog, O’Donnell, & O’Connor, 2016).

For instance, better shifting skills result in the child being able to attend and process more

relevant social information than children with poor shifting skills. This leads to the

likelihood that children with good shifting skills are more likely to respond appropriately

and acceptably in social situations. These acceptable responses will increase the child’s

confidence in social situations, encouraging them to become involved in social

interactions (Stichter et al., 2016). On the other hand, children with poor shifting skills

are less likely to respond appropriately and acceptably in social situations. This may

result in the child having a negative association with social interactions and make it more

likely that the child will avoid these interactions out of fear of additional inappropriate or

unsuccessful social encounters. This is significant because research not only suggests that

social competence is increased by more frequent social interaction, but also that negative

social interactions may result in decreased social competence (National Institute of Child

Health and Human Development Early Child Care Research Network, 2008; Spivak &

Farran, 2016). Therefore, children with poor shifting skills, who are more likely to have

negative social interactions and to avoid future potentially negative social interactions,

are at an increased risk of developing social competence problems. This has led some

researchers to suggest that intervention targeting specific aspects of EF, such as shifting,

may also improve social competence (Stichter et al., 2016). However, because of the

limited research that has been done on the association between shifting and social

competence problems, particularly in children with epilepsy, more research is needed to

confirm this relation.

41

Counter to our hypothesis and the results found in typically developing children

(Alloway et al., 2005; Balaraman, 2003; Hughes et al., 1998; Kofler et al., 2011;

McQuade et al., 2013; Olson, 1989), we did not find that inhibition and updating were

significant predictors of social competence problems in children with epilepsy. It is

possible that our small and heterogeneous sample (in terms of epilepsy type and age)

were factors. Research with children with epilepsy suggests that predictors of EBSP may

differ depending on the age of the child (e.g., Sbarra et al., 2002; Zhao et al., 2015).

Therefore, it may be the case that different aspects of EF predict social competence in

different age groups in children with epilepsy. More studies that focus on specific types

of epilepsy and smaller age ranges are needed. It should be noted that scores on the

inhibition and updating measures had a much more limited range of scores than the

shifting subscale. This limited range of scores may have affected our analyses.

Future Research

We acknowledge that the sample size in the current study is quite small and

heterogenous in that children with many different types of epilepsy were included. In

addition, most of the participants included in this study were referred for a

neuropsychological assessment because of potential learning difficulties. This makes it

unclear whether these findings can be generalized to the broader population of children

with epilepsy or to children with specific types of epilepsy. Moreover, some researchers

suggest that individuals with different types of epilepsy may show different patterns of

EF deficits (Culhane-Shelburne, Chapieski, Hiscock, & Glaze, 2002; Hernandez et al.,

2003; Smith, 2016). Therefore, it is important to examine these groups separately to get a

better understanding of their EBSP and potential predictors.

42

Regardless, the current findings highlight that children with epilepsy experience

difficulties with EF, which are associated with their EBSP. It is important that further

research, with larger sample sizes, more restricted age ranges, and specific types of

epilepsy is conducted to confirm how specific aspects of EF contribute to EBSP in this

population.

Conclusions

In conclusion, the results of this study suggest that specific aspects of EF

contribute to EBSP in children with epilepsy. This information may be helpful in

developing targeted interventions to help these children. Furthermore, because some

literature suggests that deficits in EF are present before the manifestation of EBSP,

clinicians may be able to assess specific aspects of EF to identify children who are at-risk

for developing EBSP. Earlier identification and intervention may assist in increasing

quality of life and outcomes in children with epilepsy.

43

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