Cognitive variability in adults with ADHD and AS: Disentangling the roles of executive functions and social cognition
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.
References (85)
- et al.
Insensitivity to future consequences following damage to human prefrontal cortex
Cognition
(1994) The variable nature of cognitive control: A dual mechanisms framework
Trends in Cognitive Sciences
(2012)- et al.
Large-scale brain systems in ADHD: Beyond the prefrontal-striatal model
Trends in Cognitive Sciences
(2012) - et al.
Characterizing cognition in ADHD: Beyond executive dysfunction
Trends in Cognitive Sciences
(2006) - et al.
Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability
Biological Psychiatry
(2005) - et al.
Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development
Psychiatry Research
(2009) - et al.
Decomposing intra-subject variability in children with attention-deficit/hyperactivity disorder
Biological Psychiatry
(2008) - et al.
Autism and ADHD: How far have we come in the comorbidity debate?
Neuroscience & Biobehavioral Review
(2011) - et al.
The paradox of cognitive flexibility in autism
Trends in Cognitive Sciences
(2009) - et al.
Intra-individual variability in ADHD, autism spectrum disorders and Tourette's syndrome
Neuropsychologia
(2008)
Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: Examining profiles across domains and ages
Brain & Cognition
Executive dysfunction in autism
Trends in Cognitive Sciences
Executive processes in Asperger syndrome: Patterns of performance in a multiple case series
Neuropsychologia
Intra-subject variability in attention-deficit hyperactivity disorder
Biological Psychiatry
A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder
Journal of the American Academy of Child and Adolescent Psychiatry
Decision-making patterns and sensitivity to reward and punishment in children with attention-deficit hyperactivity disorder
International Journal of Psychophysiology
Risky decision making in adults with ADHD
Journal of Behavior Therapy and Experimental Psychiatry
A modified card sorting test sensitive to frontal lobe defects
Cortex
Neuropsychologic theory and findings in attention-deficit/hyperactivity disorder: The state of the field and salient challenges for the coming decade
Biological Psychiatry
Neuropsychological executive functions and DSM-IV ADHD subtypes
Journal of the American Academy of Child and Adolescent Psychiatry
Causal heterogeneity in attention-deficit/hyperactivity disorder: Do we need neuropsychologically impaired subtypes?
Biological Psychiatry
Attention-deficit/hyperactivity disorder and social dysfunctioning
Clinical Psychological Review
Adults with autism spectrum disorders and ADHD neuropsychological aspects
Research in Developmental Disabilities
Cognitive theories of autism
Developmental Review
A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes
Neuroscience & Biobehavioral Review
How specific is a deficit of executive functioning for attention-deficit/hyperactivity disorder?
Behavioral Brain Research
The involvement of the frontal lobes in cognitive estimation
Cortex
Assessing multitasking in children with ADHD using a modified Six Elements Test
Archives of Clinical Neuropsychology: The Official Journal of the National Academy of Neuropsychologists
Psychological heterogeneity in AD/HD—a dual pathway model of behaviour and cognition
Behavioral & Brain Research
Causal models of attention-deficit/hyperactivity disorder: From common simple deficits to multiple developmental pathways
Biological Psychiatry
Executive dysfunction and delay aversion in attention deficit hyperactivity disorder: Nosologic and diagnostic implications
Child & Adolescent Psychiatric Clinics of North America
Neuropsychological functioning in adult bipolar disorder and ADHD patients: A comparative study
Psychiatry Research
Advantages of the multiple case series approach to the study of cognitive deficits in autism spectrum disorder
Neuropsychologia
Social cognition in attention-deficit hyperactivity disorder (ADHD)
Neuroscience & Biobehavioral Review
The relationship of working memory, inhibition, and response variability in child psychopathology
Journal of Neuroscience Methods
Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review
Biological Psychiatry
Stimulus-reward association and reversal learning in individuals with Asperger Syndrome
Research in Autism Spectrum Disorders
A comparison of working memory profiles in children with ADHD and DCD
Child Neuropsychology
Diagnostic and statistical manual of mental disorders: DSM-IV-TR
Are ADHD traits dissociable from the autistic profile? Links between cognition and behaviour
Journal of Autism and Developmental Disorders
Integrating intention and context: Assessing social cognition in adults with Asperger syndrome
Frontiers in Human Neuroscience
[Neuropsychological impairments in adult attention deficit hyperactivity disorder: A literature review]
Psychiatria Hungarica
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.