Cognitive variability in adults with ADHD and AS: Disentangling the roles of executive functions and social cognition

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Abstract

Attention-deficit/hyperactivity disorder (ADHD) and Asperger's Syndrome (AS) share a heterogeneous cognitive profile. Studies assessing executive functions (EF) and social cognition in both groups have found preserved and impaired performances. These inconsistent findings would be partially explained by the cognitive variability reported in these disorders. First, the present study explored the inter-individual variability in EF and social cognition in both patient groups. Second, we compared differential characteristics and commonalities in the cognitive profiles of EF and social cognition between ADHD, AS and control adults. We assessed 22 patients with ADHD, 23 adults with AS and 21 matched typically developing subjects using different measures of EF (working memory, cognitive flexibility and multitasking) and social cognition (theory of mind and decision-making). Group comparisons and multiple case series analyses (MCSA) were conducted. The between-group comparisons showed an EF deficit in working memory in ADHD and a theory of mind (ToM) impairment in AS. The MCSA evidenced that, compared to controls, ADHD patients had a higher inter-individual variability in EF, while individuals with AS had a more heterogeneous profile in social cognition tasks compared to both groups. Finally, the AS and ADHD groups presented higher task-related variability compared to controls and shared a common heterogeneous profile in EF. This is the first study to compare variability in EF and social cognition profiles of ADHD and AS. We propose that heterogeneity in EF performance is a link between ADHD and AS which may explain the overlap of symptomatology between both diagnoses. In addition, patients with AS seem to show a unique heterogeneous profile in ToM which may explain the low probability of finding AS symptoms in patients with ADHD.

Highlights

► Patients with ADHD and AS present variability in performance on cognitive tasks. ► The ADHD group obtained deficits in working memory. ► The AS group showed impairments in ToM. ► ADHD and AS patients shared a common heterogeneous profile in executive functions. ► Patients with AS seem to show a unique heterogeneous profile in ToM.

Introduction

Attention-deficit/hyperactivity disorder (ADHD) and Asperger's Syndrome (AS) are neurodevelopmental disorders that persist into adulthood with a heterogeneous cognitive profile (Geurts et al., 2008, Happe et al., 2006b, Hill and Bird, 2006, Nigg et al., 2005, Sonuga-Barke, 2002). Although ADHD diagnosis in patients with AS are part of the exclusionary criteria for AS (American Psychiatric Association, 2000), an overlap of symptoms between both disorders has been extensively reported (Ames and White, 2011, Dickerson Mayes et al., 2012, Gillberg and Billstedt, 2000, Memari et al., 2012, Rommelse et al., 2011, Taurines et al., 2012).

The term executive functions (EF) refers to several higher-order cognitive functions required to goal-oriented behavior (Hill, 2004, Sonuga-Barke et al., 2008). From a neurocognitive perspective, ADHD and AS share a common executive dysfunction associated with deficits in fronto-striatal circuits (Castellanos and Proal, 2012, Corbett et al., 2009, Cortese et al., 2012, Rommelse et al., 2011). However, studies exploring EF in each group separately have found inconsistent results. Although many reports suggest that ADHD is strongly associated with inhibitory problems, working memory, and planning difficulties (Alloway, 2011, Balint et al., 2008, Desjardins et al., 2010, Kofman et al., 2008, Martinussen et al., 2005, Nigg, 2005) other studies failed to find deficits across these domains (Nigg et al., 2002, Sonuga-Barke, 2002). Regarding patients with AS, recent reviews have also shown inconsistent findings on EF measures. Even though planning and cognitive flexibility have been the most robustly reported deficits, results have also been mixed, as some studies did not show any differences (Hill and Bird, 2006, Kaland et al., 2008, Liss et al., 2001, Rajendran et al., 2005). In addition, recent studies have found that when patients are faced with more ecological tasks designed to evaluate EF (e.g., the Hotel task for multitasking assessment), adults with ADHD (Torralva, Gleichgerrcht, Lischinsky, Roca, & Manes, 2012) and patients with AS (Hill & Bird, 2006) who do not show impairments in traditional tests, do present deficits in this area.

Most studies with children have directly compared EF in ADHD and patients with AS, which indicate that both groups might have a different EF profile (Corbett et al., 2009, Ehlers et al., 1997, Goldberg et al., 2005, Semrud-Clikeman et al., 2010, Sergeant et al., 2002). Happe, Booth, Charlton, and Hughes (2006), reported that EF deficits in children with autism spectrum disorders (ASD), most of whom had an AS diagnosis, were less severe and more prone to improvement over time than in children with ADHD. However, the developmental progression of these neurocognitive abilities in adults remains unknown.

Another important area of study within ADHD and AS is social cognition. This construct refers to information processing related to inter-subjectivity and interactions between co-specifics, including theory of mind (ToM), decision-making, empathy, emotional processing, among others. Although deficits in social cognition were long believed to constitute a core deficit in individuals with AS (Happe et al., 2006a, Happe et al., 2006b), recent studies have also found impairments in ADHD patients (Ibanez et al., 2011, Uekermann et al., 2010). Theory of mind (ToM) is one of the most robustly proven social cognition deficits in patients with AS (Baron-Cohen et al., 1997, Baron-Cohen et al., 2001, Zalla et al., 2009b). However, the selection of a sensitive task to evaluate this function remains controversial. Several studies have reported ToM deficits in AS adults employing the Faux Pas test (FPT; Torralva et al., 2012b, Zalla et al., 2009b), but normal performance using the Reading the Mind in the Eyes test (RMET; Baron-Cohen et al., 1997, Baron-Cohen et al., 2001, Torralva et al., 2012b). Nonetheless, two studies found impaired performance using the latter (Ponnet et al., 2004, Spek et al., 2010). Regarding individuals with ADHD, prior research has focused mostly on children (Uekermann et al., 2010), finding that ToM deficits are not strongly present in these patients (Geurts, Broeders, & Nieuwland, 2010). To our knowledge, ToM abilities have not been compared between adults with ADHD and patients with a specific AS diagnosis. Nevertheless, there are some comparative studies between patients with ADHD and ASD where no differences between groups were detected (Buitelaar et al., 1996, Nyden et al., 2010), and one study showed a selective ToM impairment in the ASD group (Dyck, Ferguson, & Shochet, 2001).

In addition, decision-making is a social cognition domain that is starting to be explored across the ADHD and AS literature. In patients with AS, no deficits in this process have been found (Johnson et al., 2006, Solomon et al., 2011, Torralva et al., 2012b), whereas in ADHD individuals, both impairment (Mantyla et al., 2012, Matthies et al., 2012) and intact behavioral performance have been reported (Ibanez et al., 2012). Nonetheless, no previous decision-making studies comparing both disorders have been published.

In sum, both EF and social cognition domains have been considered preserved and impaired in individuals with ADHD and AS. One of the facts that could be associated with this inconsistent findings is the cognitive variability reported in both ADHD (Castellanos et al., 2006, Nigg, 2005, Sonuga-Barke, 2005) and AS (Baez et al., 2012, Happe et al., 2006b, Hill and Bird, 2006, Towgood et al., 2009). Braver (2012) states that cognitive variability can be differentiated between intra-individual (variability in performance in the same individual on a single test or on multiple tests) and inter-individual or trait-related variation (variability among individuals in the same group). Several reports have found high intra-individual variability in measures of reaction times in subjects with ADHD (Castellanos et al., 2005, Di Martino et al., 2008, Klein et al., 2006) and recently, also in children with high functioning autism (Geurts et al., 2008). Only a few studies with AS patients have reported a high inter-individual variation between these individuals (Baez et al., 2012, Hill and Bird, 2006, Towgood et al., 2009).

Most of the ADHD and AS studies have been focused on group comparison analyses (e.g., analyses of variance) which are problematic for individuals with high variability in performance because of the averaging artifact (Shallice & Evans, 1978). In other words, these analyses cannot describe the domains in which a single member shows abnormal performance. Therefore, a significant difference between groups is not necessarily an index of individual's impairment on this measure (Hill and Bird, 2006, Nigg et al., 2005, Willcutt et al., 2008). A recently developed methodology called multiple case series analysis (MCSA; Hill and Bird, 2006, Towgood et al., 2009) has been used to overcome these obstacles. By exploring the ranges of performance in an extended battery of cognitive tests, this new approach detects the domains in which a given individual displays sub-normal or supra-normal performance.

The current study aimed to explore inter-individual variability in EF and social cognition in ADHD, AS, and controls employing MCSA. We expected to find higher variability in performance across participants from both patient groups compared to controls. Furthermore, ADHD patients’ performance was expected to be more variable in EF, while AS individuals would exhibit a heterogeneous profile in social cognition tasks.

In addition, by using the traditional group comparison analysis, we compared differential characteristics and commonalities in the cognitive profiles of EF and social cognition between ADHD, AS, and controls. We expected to find impairments in working memory in the ADHD group and deficits in cognitive flexibility in patients with AS. Moreover, we hypothesized that both groups would show difficulties in solving the more ecological task of EF (Hotel multitasking). Regarding social cognition domains, we expected that the AS group would be impaired in performance on ToM tests and patients with ADHD would have difficulties performing decision-making tasks. Finally, we also hypothesized that MCSA would reveal patterns of cognitive profile varying within and/or between individuals, while variation would not be established in group comparison analyses.

Section snippets

Participants

Sixty-six participants were recruited. Twenty-two ADHD patients (M = 35.2 years, SD = 12.7), 23 adults diagnosed with AS (M = 33.0 years, SD = 9.8), and 21 typically developing subjects (M = 38.2 years, SD = 14.4) were assessed (see Table 1). Patients in the ADHD and AS groups were selected from a large outpatient population of the Institute of Cognitive Neurology (INECO) using the following inclusion criteria: (1) subjects older than 18 years old; (2) diagnosed with ADHD or AS according to the diagnostic

Demographic data

No differences in age, F(2, 63) = 0.99, p = .37, sex, X2(2) = 2.30, p = .31, years of formal education, F(2, 63) = 0.39, p = .67, or intellectual level F(2, 63) = 0.08, p = .91, were observed between groups (see Table 1).

Group differences analysis

Table 2 summarizes the group comparisons. A one-way analysis of variance was performed on each measure of the tests.

Discussion

In the present study we compared profiles of EF and social cognition between adults with ADHD and AS (relative to typically developing individuals), and explored the underlying variability in performance across these cognitive domains. Individuals with ADHD demonstrated an EF deficit in working memory, while patients with AS showed social cognition difficulties in ToM. A detailed analysis of individual cases revealed an increased task-related variability among both patient groups compared to

Conflict of interest

None to declare.

Acknowledgments

This study was partially supported by grants CONICET, INECO Foundation, and FONDECYT (1130920). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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  • Cited by (0)

    1

    Both authors have equal contribution to the manuscript.

    2

    This work is part of the PhD dissertation [M.L. Gonzalez-Gadea] ongoing by the author at UNC, Argentina.

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