Executive Function (High-level Cognitive Processes)

Executive function (EF) is an umbrella term for a triad of high-level cognitive processes- response inhibition, working memory updating and switching – associated with frontal regions of the brain (Collette et al., 2005; Friedman et al., 2006, 2007, 2008; Huizinga, Dolan, & van der Molen, 2006; Lehto, Juujarvi, Kooistra, & Pulkkinen, 2003; Miyake et al., 2000; Miyake & Friedman, 2012; van der Sluis, de Jong, & van der Leij, 2007).

Traditionally, executive function was viewed and measured as a unified cognitive

construct with complex EF tasks (such as the Wisconsin Card Sort Task). However, Miyake and Friedman’s (2012) comprehensive research on the latent factor structure of executive function indicates that EF is comprised of a set of abilities both related through common EF (synonymous with response inhibition) and distinct to each other (updating specific and switching specific) (see Figure 6). Inhibition is the ability to override inappropriate

responses, regulate appropriate behaviour and control attention by focussing on relevant information and filtering out distracting information; updating is the ability to hold and continuously update information in working memory from moment to moment; and switching is the ability to rapidly adapt to changing task demands (Diamond, 2013; Miyake et al., 2000; Miyake & Friedman, 2012).

Figure 6 Miyake and Friedman’s (2012) 3-factor model of EF

37

Extensive research confirms the 3-factor structure of EF proposed by the model (Collette et al., 2005; Friedman et al., 2006, 2007, 2008; Huizinga et al., 2006; Lehto et al., 2003;

Miyake et al., 2000; Miyake & Friedman, 2012; van der Sluis et al., 2007); and the structure is relatively stable across development as it is confirmed to be present in children (Huizinga et al., 2006; Lehto et al., 2003; Rose, Feldman, & Jankowski, 2011; van der Sluis et al., 2007), adolescents (Huizinga et al., 2006), and adults (Friedman et al., 2006, 2007, 2008; Miyake et al., 2000). These EFs develop gradually from early childhood reaching maturity in early adulthood (Huizinga et al., 2006; Lehto et al., 2003; van der Sluis et al., 2007).

A range of brain areas play a role in competent executive functioning (see Figure 7), the main area of importance is the prefrontal cortex, although other subcortical areas (basal ganglia, thalamus and cerebellum) play a role through their rich connections to pre-frontal brain areas (Powell & Voeller, 2004). The main prefrontal areas necessary for executive function are: (1) the anterior cingulate circuit (important for attentional control, error awareness, and tasks requiring effort) (Powell & Voeller, 2004), (2) the dorsolateral circuit (important for filtering distractions, phonological decoding, set maintenance, and working memory) (Powell & Voeller, 2004), and (c) orbitofrontal circuit (important for decision making, self-monitoring and integrating emotion and cognition) (Powell & Voeller, 2004).

Figure 7 Powell and Voeller’s (2004) Diagram of brain areas underpinning EF

Response Inhibition appears to be supported by activation in the anterior cingulate cortex, left inferior frontal gyrus, temporo-parietal regions, dorsolateral prefrontal cortex, frontal striatal regions and inferior parietal cortex (Alvarez & Emory, 2006; Bench et al., 1993;

Booth et al., 2005; Casey et al., 1997; Garavan, Ross, Murphy, Roche, & Stein, 2002; Kiefer, Marzinzik, Weisbrod, Scherg, & Spitzer, 1998; Liotti, Woldorff, Perez, & Mayberg, 2000;

Taylor, Kornblum, Lauber, Minoshima, & Koeppe, 1997). Working memory updating appears to be underpinned by activation in fronto-polar, left middle frontal area, dorsal cingulate, pre-motor cortex, dorsolateral cortex and ventro-lateral prefrontal cortex, as well as posterior parietal cortex (Collette et al., 1999; Owen, McMillan, Laird, & Bullmore, 2005). Switching appears to be underpinned by activation in temporo-parietal cortex, dorsolateral prefrontal cortex, right orbitofrontal cortex, left middle and inferior frontal regions, as well as additional parietal brain regions (Collette et al., 2005; Fink et al., 1997).

The neural underpinnings of EFs appear to be consistent with Miyake and Friedman’s (2012) model of executive function, as shared and distinct activation is found (Collette et al., 2005).

Core EFs – response inhibition, updating, switching- are differentially implicated in and facilitate higher order cognitive processes such as planning, reasoning, fluid intelligence

39

(Diamond, 2013; Friedman & Miyake, 2016; Miyake et al., 2000, p. 200; Miyake &

Friedman, 2012; Snyder et al., 2015). Diamond’s (2013) outlines an EF framework for understanding how the core EFs are related to each other and how in combination they facilitate higher order cognitive processes such as planning, reasoning and fluid

intelligence and self-regulation (see Figure 8). This facilitation to “higher-order cognitive processes” could theoretically be extended to a wide range of complex human

behaviours, for instance EFs have been found to contribute also to reading ability, math ability, self-regulation and socio-emotional wellbeing (Blair & Razza, 2007; Carlson &

Wang, 2007; Christopher et al., 2012; Diamond, 2013; Friedman et al., 2006, 2008; Miyake et al., 2000; Vohs & Baumeister, 2011). EFs appear distinguishable at the behavioural level, as they contribute differentially to complex human behaviours. For instance,

inhibition is found to uniquely relate to attentional problems, cognitive failures, emotional regulation, math ability and emerging literacy (Carlson & Wang, 2007; Friedman et al., 2007; Friedman & Miyake, 2004; van der Sluis et al., 2007); updating is found to relate to fluid intelligence, crystallised intelligence, verbal reasoning and attentional problems (Friedman et al., 2006, 2007; van der Sluis et al., 2007): and switching is found to relate to reading ability, non-verbal reasoning and effortful control (Blair & Razza, 2007; van der Sluis et al., 2007). This highlights the importance for implementing measures of key EFs (instead of higher order cognitive processes) as a first step in understanding how they may be implicated in behaviourally diverse disorders.

Diamond’s (2013) framework has implications for understanding how impairments within an EF brain system may have knock on effects for a range of behavioural level

impairments. If the key EFs are a cognitive hub for facilitating a wide range of complex behaviours, then a disorder characterised by EF impairments may have additional (non-core) symptoms as well as core symptoms (which are required for diagnosis of a specific condition), and may result in comorbid diagnosis such as is the case between dyslexia and ADHD. Understanding each condition within an EF framework emphasises the redundancy and limitation of diagnosing disorders at the symptom level, as an EF dysfunction category may more appropriately explain conditions, enhance diagnostics and targeted

intervention. Such a framework may provide an explanation of core (reading) and

non-core (socio-emotional) symptoms of dyslexia and why dyslexia is highly comorbid with ADHD. An adapted version of Diamond’s (2013) framework extending to reading ability is outlined in Figure 8. Extending this framework to include reading ability has potential for explaining the core and non-core features of dyslexia, however it is unclear from typical and atypical populations which key EFs are predictive of reading ability.

Figure 8 Diamond’s (2013) EF Framework adapted to include reading ability, question marks indicate that paths (direct/indirect) to reading ability are unclear from previous research

Key EF impairments have been implicated in a range of psychological disorders which appear distinct at the behavioural level such as autism and ADHD (Barkley, 1997;

Biederman et al., 2004; Gau & Chi-Yung Shang, 2010; Ozonoff & Jensen, 1999; Ozonoff, Pennington, & Rogers, 1991). This highlights the strength of EF as a neuro-cognitive endophenotype for a range of disorders. A number of researchers suggest that common EF (response inhibition) mechanisms may be the EF that explains overlapping disorders.

Robbins et al. (2012) argue that a response inhibition endophenotype may be a useful transdiagnostic endophenotype for explaining a range of complex disorders and the range of behaviours associated with them. They suggest response inhibition is at the core of

41

both impulsive and compulsive behaviours which are capable of characterising

psychological disorders ranging from ADHD to schizophrenia and autism (Robbins et al., 2012) (see Figure 9). It is important to note however that dyslexia is not included under Robbins et al. (2012) framework of disorders characterised by common EF impairments.

This may be due to no study to date exploring EF as an endophenotype in dyslexia, and, a lack of clarity on whether dyslexia is associated with an EF impairment (see section 2.6 for detailed discussion).

Figure 9 Robbins et al. (2012) depiction of response inhibition as a central mechanism in impulsive-compulsive behaviours

Common EF (response inhibition) mechanisms could be a potential explanation for the overlap between dyslexia and ADHD. ADHD has previously been conceptualised as a disorder stemming from response inhibition impairments (Barkley, 1997) which result in higher order cognitive impairments and self-regulatory difficulties. Response inhibition (Brosnan et al., 2002) and other key EF impairments are also observed in dyslexia (Moura et al., 2015), as well as socio-emotional issues which could be due to self-regulatory

difficulties (Dahle et al., 2011; Heiervang et al., 2001; Knivsberg & Andreassen, 2008;

Mugnaini et al., 2009). EF is highly heritable, linked to psychopathology and self-regulatory behaviour (Friedman et al., 2008), and has been proposed as a candidate endophenotype for explaining ADHD and comorbid reading problems (Kegel & Bus, 2013; Rommelse et al., 2009). Key EFs appear to be differentially implicated in a range of complex behaviours, suggesting that they may also differentially relate to core and non-core behaviour in dyslexia and possibly explain overlap with behaviourally distinct ADHD features.

However, issues in establishing which EFs are impaired in dyslexia and comorbid dyslexia-ADHD make it difficult to extend an explanation to overlapping impairments and to core and non-core issues of dyslexia.