The heterogeneity of ADHD: evidence from neuropsychological subtyping

Theses Booklet

Takács Ádám

Supervisor: Prof. Dr. Csépe Valéria

2013

EÖTVÖS LORÁND UNIVERSITY, FACULTY OF EDUCATION AND PSYCHOLOGY,

DOCTORAL SCHOOL OF PSYCHOLOGY

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Contents Topics and main questions of the thesis ................................................................................................. 2

Impairment of executive functions (EF) in ADHD .................................................................................... 3

Theses ...................................................................................................................................................... 5

Study 1: Fluency strategies and compensatory behavior in ADHD ......................................................... 5

Study 2: Neuropsychological profiles and behavioral ratings in ADHD .................................................. 7

Study 3: Identifying subtypes with the Strengths and Difficulties Questionnaire .................................. 9

Summary ............................................................................................................................................... 10

Publications in the topic of the dissertation ......................................................................................... 12

References ............................................................................................................................................. 13

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Topics and main questions of the thesis The aim of the thesis was to investigate the heterogeneity of the Attention Deficit Hyperactivity

Disorder (ADHD) by using methods from cognitive neuropsychology and dimensional

psychiatry. Several studies confirmed that ADHD is too complex and heterogeneous to assign

all cases to two categories (i.e., ADHD or non-ADHD). However, no useful splitting is possible

for all the assumed subtypes of similar though not identical characteristics, neither for clinical

practice nor for taxonomic research. Severity and frequency of the symptoms could vary in a

broad range depending on gender, age, cohort, culture, type of information source in diagnosis,

the clinician’s decision criteria, and the diagnostic instruments (including rating scales,

interviews, and neuropsychological tests) (Carr, Henderson, & Nigg, 2010; Lahey & Willcutt,

2010; Nigg, Tannock, & Rohde, 2010). Such inconsistencies could yield various subtype

distributions.

The DSM-IV (APA, 2000) and the upcoming DSM-5 (APA, 2013, http://www.dsm5.org/) do

not provide us a reliable manual to handle the temporal instability of ADHD subtypes, or a

method to combine information from parents and teachers, and do not answer the question of

low validity of hyperactive-impulsive and inattentive symptoms (Nigg et al., 2010; Stefanatos

& Baron, 2007).

The stability of the diagnosis could be enhanced by using neuropsychological methods with

decreasing the possibility of measurement reactivity, responder and observer bias. The

diagnostic protocol in ADHD often suffers from lack of this perspective. The main reason of

this blind spot could be the ambiguous cognitive background of the syndrome (Sjöwall, Roth,

Lindqvist, & Thorell, 2012).

The large variability between the different neuropsychological findings in ADHD could be

explained by compensatory mechanisms. It was demonstrated in imaging studies that a slower

development in the prefrontal cortex could lead to compensatory activation in other brain areas

under executive tasks (Arnsten & Rubia, 2012; Fassbender & Schweitzer, 2006; Shaw et al.,

2007). It was hypothesized that the faster developing motor areas or the posterior region could

play the main role in compensatory behavior (Arnsten & Rubia, 2012). To interpret the

neuropsychological findings, it could be worthwhile to take into account the compensator

participants or subgroups. We investigated this question in the second chapter of the

dissertation.

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Information from ADHD rating scales and from neuropsychological assessments often

discrepant; the relation between cognitive profile and symptom constellation is ambiguous

(Jonsdottir, 2006). However, the overall symptom severity corresponds to deficits in other

fields, including school and work achievement, social and general functioning (Lahey &

Willcutt, 2010). Combining information from different sources could be problematic because

of the different methodology: symptoms are usually investigated with categorical assessments

(ADHD/typical development), but cognitive research is often based on dimensional methods

(continuous background variables, like inhibition or working memory, see Nigg, Willcutt,

Doyle, & Sonuga-Barke, 2005; Sjöwall et al., 2012). We demonstrated a possible dimensional

approach with reanalyzing a previous clinical database (G. Mészáros, Tárnok, Oláh, & Gádoros,

2008) in the third chapter.

The DSM-IV-TR subtypes of ADHD were based on the broadly accepted view that the two

main symptom dimensions of ADHD predict different cognitive and social development

trajectories and risks. However, the observed temporal stability does not support this approach,

so it is hard to keep this structure (Nigg et al., 2010). Findings of latent class analyses (LCA)

may provide a dimensional alternative to the dominant categorical approach that characterizes

the DSM. Latent class analysis is a model-based classification or clustering method that allows

us to identify a set of mutually exclusive groups or subtypes (Hudziak et al., 1998). Previous

research using LCA in various samples provided well-interpretable and useful evidence in

regard to understanding the structure of ADHD, and to the refinement of genetic analyses (Elia

et al., 2009; Hudziak et al., 1998; Hudziak, Wadsworth, Heath, & Achenbach, 1999; Neuman

et al., 1999; Rasmussen et al., 2004; Todd et al., 2001). The neuropsychological homogeneity

of latent classes in ADHD has not yet been investigated. The fourth chapter of the dissertation

provides possible answers to this question.

Impairment of executive functions (EF) in ADHD The importance of studying the neuropsychological background of ADHD was emphasized by

Barkley’s (1997) work, who stated the research criteria in this field as follows:

- The main theory should include explanations on the levels of behavior and

neuropsychology as well.

- The combined and independent presence of inattentive and hyperactive-impulsive

symptoms, and their causalities should be explained.

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- The theory should provide predictive power and possible hypothesis for the diagnosis

and its lifelong development.

- ADHD should be investigated in line with the state-of-the-art developmental

psychological theories.

The first theoretically designed explanation of the atypical executive achievement in ADHD

was Barkley’s (1997) model of inhibitory dysfunction that secondarily disrupts other EF

components, such as working memory, affective and drive regulation, development of

internalized language and adaptive behavior. This inhibitory impairment could lead to motor

control, dysfluency, language and pragmatic deficits. Inhibitory control deficits are often

reported in ADHD, however, meta-analytic studies did not find this a sufficient criterion for the

syndrome (Nigg & Casey, 2005; Sergeant, Geurts, & Oosterlaan, 2002; Willcutt, Doyle, Nigg,

Faraone, & Pennington, 2005). The Dual-Pathway model (Sonuga-Barke, 2002) gives a

different view. In this theory, delay aversion and poor inhibitory control are independent co-

existing characteristics of ADHD, and these two cognitive impairments could modify the

symptoms via school work and family interactions. Despite its theoretical advantages, the

model has not been validated experimentally (Geurts, van der Oord, & Crone, 2006; Sjöwall et

al., 2012).

The cognitive neuropsychological approach of ADHD is controversial (for an overview see

Stefanatos & Baron, 2007). The observed heterogeneity in ADHD should be based on

multifactorial etiology, but the core neuropsychological evidence is related to executive

functions. The transition from models of a single core deficit to multiple-deficit models

represents a paradigm shift in the way that the neuropsychology of ADHD is conceptualized.

A certain research perspective within the multifactor approach sheds light on the role of emotion

regulation, which could explain some of the variance of ADHD symptoms (Sjöwall et al.,

2012). Other studies focused on the high frequency of co-morbidity between ADHD and

dyslexia, revealing the importance of language and communication in ADHD (de Jong et al.,

2009; McGrath et al., 2011; Willcutt et al., 2010).

Differences can be found in EF research according to their definition of this cognitive construct

(Hugdahl et al., 2009). As a theoretical framework, we used the concept of Miyake et al. (2000)

to understand the relationships between three executive functions: mental set shifting, inhibiting

prepotent responses and updating the contents of WM. According to the multifactorial models

we tested the impairments of language and communication (de Jong et al., 2009; McGrath et

al., 2011; Willcutt et al., 2010).

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Theses

1. Compensatory mechanisms enhance the neuropsychological heterogeneity of ADHD.

2. Dimensional research methods could lead to better understanding of the heterogeneous

symptomatology than classical categorization.

3. A possible source of heterogeneity could the different methods of combining

information from parental and teacher reports.

Study 1: Fluency strategies and compensatory behavior in ADHD The aim of our study was to investigate the effect of compensation on the heterogeneity of

ADHD. We used a complex measurement (verbal and nonverbal fluency) to detect natural

compensatory behavior. Verbal fluency tasks have been commonly used in neuropsychological

assessment to detect executive dysfunctions and lexical access. Solving these tasks requires

control of organized search, generation of items within a specific category (semantic or

phonemic), and with respect to the time limit (which is usually sixty seconds) to produce a self-

generated strategy for finding the relevant items, or at least inhibit the irrelevant ones (Matute,

Rosselli, Ardila, & Morales, 2004; Ross, Lindsay Foard, Berry Hiott, & Vincent, 2003; Vik &

Ruff, 1988). The two main types of fluency tasks are the verbal fluency with lexical

requirement, and the nonverbal fluency with visuospatial requirement.

According to the lexical organization model, two stores are activated differently in fluency

tasks: (1) a long-term store (“topicon”) that contains common words which are easy to access,

(2) and a more extensive lexicon that is needed to search after the former is exhausted (Hurks

et al., 2010). The achievement in the first quarter minute of the fluency measurement is related

to the automatically activated production from the topicon, while later word generation is based

on effortful control. The authors suggest (Hurks et al., 2004) that children with ADHD may

have a developmental delay in automatic processing of abstract verbal information. This finding

was not replicated yet.

Only one study concerning ADHD focused on the strategic scoring opportunities in verbal

fluency tasks (Tucha et al., 2005), nonetheless the classical (quantitative) analysis shows, as it

is, a part of the real achievement. If the fluency scoring protocol measures the number and types

of clusters, i.e., a group of similar words, and the switching between those in the oral

performance, then it could result in more sensitive indices of language and executive

computation (Tucha et al., 2005). This different approach of verbal fluency focuses on the better

specified individual cognitive profiles due to including additional tasks relying on separate

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skills of strategy using. The qualitative scoring system (adapted to Hungarian language by

Mészáros, Kónya, & Kas, (in press) highlights the self-generated strategy-use, which consists

of two procedures: clustering and switching.

The analogue nonverbal fluency task measures visuospatial flexibility, fluency, and

productivity (Korkman, Kirk, & Kemp, 1998). Generating new patterns in the test rely on

several components of the EF, such as planning, monitoring, working memory, and inhibition

(Tucha et al., 2005). Based on three successive designs, figural clusters can be identified,

labeled as Rotation Strategy and Enumerative Strategy (addition/subtraction strategies in the

terminology of Tucha et al., 2005). In the Enumerative Strategy further lines are added to or

subtracted from the previous design (Tucha et al., 2005). When using Rotation Strategy, the

design rests basically the same, but the entire or a smaller part of it is rotated. To the best of our

knowledge, there is only one study with adult patients in the ADHD literature applying

qualitative scoring in verbal fluency tasks (Tucha et al., 2005), and to date we have not had

results on children with ADHD. We investigated executive and language strategies of children

with ADHD in fluency tasks.

22 children with ADHD (19 boys and 3 girls) between ages of 8 and 12 years, and their matched

(on gender, age, and education level) counterparts were recruited to participate in the study. As

the results indicate, the clinical group differs from the TD group on the measurements of

executive functions: prepotent response inhibition in the Stroop task and word generating in the

semantic fluency. In line with previous studies, children with ADHD showed strong deficit in

the spatial WM task (Corsi Blocks) compared to controls (de Jong et al., 2009; Martinussen &

Tannock, 2006). The obtained results in verbal fluency are in line with some previous studies

(Fischer, Barkley, Edelbrock, & Smallish, 1990; McGee, Williams, Moffitt, & Anderson, 1989;

Reader, Harris, Schuerholz, & Denckla, 1994; Tucha et al., 2005). In our approach we argue

that the reduced efficiency of children with ADHD in semantic fluency task is based on

suboptimal shifting strategy between clusters, and lack of ability of producing word clusters.

This disadvantage can be localized in time to the first fifteen seconds. This result is similar to

that of previous findings (Hurks et al., 2004). According to the lexical organization model, the

group difference that appeared in the level of topicon indicates that children with ADHD have

an impairment in accessing and/or activating common words, however the executive process

of searching the lexicon extensively is intact (Hurks et al., 2004).

For identifying the main patterns of strategy-using during fluency tests, agglomerative

hierarchical cluster analyses was conducted. The analysis yielded a four clusters structure to

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demonstrate the heterogeneity of executive and language functions in the verbal fluency task.

As an interpretation we could remark that cases in the first and third clusters did not use efficient

strategies, while the performance of children in the first cluster was ordinary or high indicated

by correct responses (unlike the third one). The fourth cluster consisted of well-performing

typically developing participants, who used the most efficient switching strategy compared to

the remaining groups. The most important cluster was the second one, where children with

average performance and high proportion of strategy using could be found. However, we did

not obtain a compensatory group in the design fluency task. We suggest that children with

ADHD are able to compensate in the field of self-generated language using strategies even

though achievement in verbal fluency tasks depends partly on the executive functions. Children

with ADHD should be able to strategically solve the fluency tasks when they can lean on their

language skills. Therefore, children with ADHD who can reach a higher level in language or

executive tasks would be able to use strategies to solve them.

Study 2: Neuropsychological profiles and behavioral ratings in ADHD To understand the cognitive background of atypical development we should clarify the

relationship between our screening measurements and the cognitive functions. Moreover, we

need a clear theoretical model to systemize them (Kóbor, Takács, & Csépe, 2010; Korkman et

al., 1998). However, most of the EF concepts only provide lists (e.g., planning, organizing,

inhibition, monitoring, working memory, selective attention, shifting, etc.), or a narrowed focus

to a sole component (Hugdahl et al., 2009). The executive functions are required when we face

to complex, control needed tasks. However, it is a long lasting debate, whether the EF could be

a list of functions as an umbrella term (Hugdahl et al., 2009), or it could be a hierarchical model

based on different subfunctions (Miyake et al., 2000).

A neuro-psychometric approach could be helpful in understanding the structure of executive

functions, and also in clinical research. The three-component model of Miyake et al. (2000),

which was based on confirmatory factor analysis, has not been tested yet in child clinical

settings.

Person-oriented methods (like configural frequency analysis, latent structure models, dense

point, hierarchical clustering) can handle the phenomenon of symptom instability. Not only the

behavioral changes in ADHD, but also the typical and atypical developmental states of the

executive functions are specific and complex processes with meaningful coherence and

structure (Bergman, Magnusson, & El-Khouri, 2003; Formann, 1984; Morris, Blashfield, &

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Satz, 1981; von Eye & Bergman, 2003). Nevertheless, in a therapeutic approach the personal

focus could be relevant; however group comparisons cannot serve this purpose (Nigg et al.,

2005). Moreover, hierarchical clustering requires smaller sample size than latent variable

methods (Collins & Lanza, 2010).

We hypothesized that there would be at least five different cognitive clusters in our sample

according to the three-factor model of Miyake et al. (2000). We expected a group of children

with atypical inhibition, shifting, and updating related to both inattentive and hyperactive-

impulsive syndromes, one cluster with solely updating problems related to inattentive behavior,

one with impairment in inhibition and high hyperactive-impulsive ratings, a group

characterized by shifting problems related to both types of ADHD syndromes, and a last group

with normal neuropsychological profile and few or no behavioral problems.

We used the database of the Vadaskert Child Psychiatry Hospital (G. Mészáros et al., 2008) for

the analysis. 85 children participated in the study (ADHD group: 38 boys, 4 girls, M = 11.5

year, SD = 1.1; TD group: 36 boys, 7 girls, M = 11.2, SD = 1.7). Six different clusters were

identified (see Figure 1.), where two were TD-like, two were ADHD-like groups, and two were

sub-threshold categories. The executive factors were not totally independent in our sample:

Shifting and Updating composed separate clusters, but only if the cognitive symptoms were not

severe. Interestingly, the Updating factor was the most relevant in our obtained structure,

Shifting could modulate the separation, but Inhibition had only a limited contribution to our

model. Our clusters also varied in the severity of cognitive impairment. This result was also

reflected by the LCA studies which reported different symptom severity classes (Elia et al.,

2009).

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Figure 1: Descriptive values of the six-cluster solution on the three quasi-absolute variables used for classification. HC: homogeneity coefficient.

We assumed that the atypical neuropsychological clusters would be characterized by different

ADHD symptoms. However, there was no difference between our clusters in symptoms ratings,

i.e., scores of Inattention and Hyperactivity-Impulsivity scales did not differ. The cognitive

clusters and the behavior subtypes partly converge in our sample.

Study 3: Identifying subtypes with the Strengths and Difficulties

Questionnaire Developing short and well-functioning screening tools is of urgent need due to the increasing

prevalence of child and adolescent mental health disorders over the last 50 years (Hagquist,

2007). The Strengths and Difficulties Questionnaire (SDQ) is a widely used tool for identifying

child behavioral problems. This brief questionnaire is also suitable for rapid screening of

population and to detect atypicalities in the individual profiles (R. Goodman, 1997). We used

the SDQ for three aims: (1) investigating the inner structure of the questionnaire by CFA; (2)

comparing the latent classes of the SDQ Hyperactivity items with the previous LCA studies in

ADHD; (3) and finally examining the neuropsychological profiles of the revealed (subclinical)

groups.

Previous research supported the original five-factor model (Emotional problems, Hyperactivity,

Conduct problems, Peer relationship problems, and Prosocial behavior) or an alternative three-

factor solution (Externalization, Internalization, Prosocial behavior). Those two models were

integrated in a second-order factor model (A. Goodman, Lamping, & Ploubidis, 2010). In our

study, a fourth type bifactor model yielded the best fit to data compared to other models (Kóbor,

Takács, & Urbán, in press). In the bifactor model, specific components refer to the five SDQ-

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traits, and the General Problems factor refers to an impression about the problem severity of

the child. Our model suggests regarding the Total Difficulties Score as more seriously at risk

of various externalizing problems.

For the first time, we conducted a latent class analysis on the Hyperactivity scale items of the

Strengths and Difficulties Questionnaire in order to identify distinct subgroups of subclinical

ADHD in a multi-informant framework.

Besides non-symptomatic groups, mild and severe combined classes, mild inattentive-

impulsive classes, and among boys, a mild hyperactive-impulsive class was obtained. The

cross-informant analyses demonstrated that quite similar subgroups were detached regardless

of informant; however, the teacher classes were somewhat more elaborated. The results are in

line with the previous latent class analytic studies (Elia et al., 2009; Hudziak et al., 1999).

The special focus of our research was to understand the neuropsychological profiles of the latent

classes. Both subclinical groups (Combined and Inattentive-Impulsive) differed from the non-

symptomatic one. The Combined class had a general functional impairment indicated by the

results of the intelligence tasks. The Inattentive-Impulsive group had lower achievement in

phonological awareness than the other two. The prepotent response inhibition, measured by

Stroop task was not related to the latent class solution, in contrast to the primary inhibition

deficit theory (Barkley, 1997). However, according to our results of intelligence and

phonological awareness, we support the multifactorial approach of ADHD (McGrath et al.,

2011; Willcutt et al., 2010).

Summary Our first neuropsychological study demonstrated that compensatory mechanisms could

enhance the neuropsychological heterogeneity of ADHD.

We suggest that children with ADHD are able to compensate in the field of self-

generated language using strategies.

However, it cannot be seen a compensatory group in the design fluency task, which is a

frequently used EF test without lexical component. Children with ADHD can solve

strategically the fluency tasks when they can lean on their language skills,

notwithstanding with the visuospatial compensation theory (Fassbender & Schweitzer,

2006). This means that in clinical diagnostics the complex, language-based

neuropsychological tasks are important to detect natural compensatory behavior in

ADHD. If we could reveal the atypical but efficient ways in problem solving (not just

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in the fluency tasks), we are also able to use them in the treatment, which might give us

effective developing methods.

We demonstrated in our clinical database reanalysis that dimensional research methods

could lead to better understanding of the heterogeneous symptomatology than classical

categorization.

Previous variable based methods (e.g. group differences) suggested general executive

functions deficit in ADHD (G. Mészáros et al., 2008), in line with the primary inhibition

deficit theory (Barkley, 1997). However, the Updating factor was the most relevant in

our cluster structure, Shifting had a modulator effect for the separation, but Inhibition

had only a limited contribution to our model.

We presented how a person-oriented statistical approach can be useful in the field of

cognitive neuropsychology despite the usually low sample sizes. As we have predicted,

Miyake and his colleagues' (2000) executive factors were able to segment children from

both referred and non-referred samples.

My last thesis was that a possible source of heterogeneity is the different ways of

combining information from parental and teacher reports. We successfully

underpinned by our latent class analysis, where the teachers’ class solution was more

chiseled than the parents’ structure, in line with the previous LCA studies (Althoff et al.,

2006).

The clinical database reanalysis and our LCA study both emphasize the importance of the

subclinical variance in the ADHD dimension. According to our results, we support the

dimensional approach in research and in practice as well. We emphasize the usefulness of

measuring language and communication performance besides executive functions in ADHD.

The results presented in this dissertation are in line with the critics of the DSM-IV and the

DSM-5 (Hauser & Johnston, 2013; Nigg et al., 2010). It was a wide agreement between

researchers that resolving the complex issue of the informant effect should have been a goal of

the DSM-5. Unfortunately, the new manual do not meet this hope. To resolve the problem of

discrepancy between cognitive neuropsychological information and behavioral symptoms, we

need more dimensional analysis and neurocognitive evidence in order to achieve a reliable

framework for the DSM-6 (Insel, 2013, April 29.).

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Publications in the topic of the dissertation

Kóbor, A., Takács, Á., & Urbán, R. (in press). The Bifactor Model of the Strengths and

Difficulties Questionnaire. European Journal of Psychological Assessment.

Takács, Á., Kóbor, A., Tárnok, Zs., & Csépe, V. (in press). Verbal fluency in children with

ADHD: Strategy using and temporal properties. Child Neuropsychology.

Kóbor, A., Takács, Á., Urbán, R., Csépe, V. (2012) The latent classes of subclinical ADHD

symptoms: Convergences of multiple informant reports. Research in Developmental

Disabilities, 33(5), 1677-1689.

Kóbor, A., Takács, Á., Csépe, V. (2012) Towards a dimensional approach: screening and

diagnosing subclinical groups. ADHD in practice, 4 (1), 7-9.

Kóbor A., Takács Á., Csépe V. (2010) A végrehajtó funkciók neuro-pszichometriai

perspektívából. Pszichológia, 30 (3) 233-252.

Takács Á., Kóbor A., Csépe V. (2010) Zavarok a diagnózisban? A figyelmi atipikusság

„intuitív diagnosztikája” és neuropszichológiai profilja. Pszichológia, 30 (3) 253-271.

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