Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development
Introduction
Executive function (EF) is an overarching term that refers to mental control processes that enable physical, cognitive, and emotional self-control (Denckla, 1996, Lezak, 1995, Pennington and Ozonoff, 1996) and are necessary to maintain effective goal-directed behavior (Welsh and Pennington, 1988). Executive functions generally include response inhibition, working memory, cognitive flexibility (set-shifting), planning and fluency (Ozonoff and Strayer, 1997, Pennington and Ozonoff, 1996). Deficits in EF are frequently observed in neurodevelopmental disorders, including autism and attention deficit hyperactivity disorder (ADHD).
Autism is a severe neurodevelopmental disorder characterized by impairment in communication, reciprocal social interaction, and a markedly restricted repertoire of activities and interests (American Psychiatric Association, 2000). The symptoms of autism fall on a continuum of severity referred to as autism spectrum disorder (ASD), which include autistic disorder, Asperger syndrome, and pervasive developmental disorder—not otherwise specified (PDD–NOS). Autism is often further divided into those with mental retardation and those functioning in the average or above average range of intelligence (often called high functioning autism or HFA). In addition to the core features, deficits in EF have been widely reported (e.g., (Geurts et al., 2004, Goldberg et al., 2005, Hughes et al., 1994, Ozonoff et al., 1991, Pennington and Ozonoff, 1996)). The primacy of EF deficits in 57 autism (Russell, 1997), especially in terms of planning, cognitive flexibility and working memory, remains an ongoing debate (for a review, see Hill, 2004).
ADHD is also a neurologically mediated disorder that exists on a continuum. ADHD is characterized by varying degrees of inattention, impulsivity and hyperactive behavior (American Psychiatric Association, 2000). ADHD is further divided into those individuals meeting symptom criteria in all the aforementioned areas (Combined type), those primarily evidencing attention problems (Predominantly inattentive type) and those with mostly hyperactive and impulsive symptoms (Predominantly hyperactive-impulsive type). Significant EF deficits in individuals with ADHD have been reported; however, there is still some inconsistency regarding particular impairments in domains of functioning. In a comprehensive meta-analysis, Willcutt et al., 2005 found that studies most consistently report response inhibition and vigilance deficits in ADHD. Other impairments have been found in working memory (e.g., (Kempton et al., 1999, Rhodes et al., 2005)), planning (e.g., (Kempton et al., 1999, Rhodes et al., 2005)), and flexibility (Vance et al., 2003).
Few studies have directly compared EF across ADHD and ASD groups and studies investigating these groups separately report inconsistent findings. Some have proposed that EF deficits are core to ASD (Russell, 1997) and ADHD (Barkley, 1997). Pennington and Ozonoff (1996) suggested that deficits in domains of EF could be disassociated across disorders resulting in distinct EF profiles, a notion that has received some foundational support. Specifically, impaired motor and response inhibition in ADHD is well supported (e.g., (Barkley et al., 1992, Geurts et al., 2004, Pennington and Ozonoff, 1996). Deficits in planning and set-shifting have been shown to be more pronounced in individuals with HFA than ADHD and typical development (Geurts et al., 2004, Ozonoff et al., 2004, Ozonoff and Strayer, 1997, Sergeant et al., 2002). Similarly, more impairment in HFA as compared with ADHD has also been demonstrated with verbal working memory (Pennington and Ozonoff, 1996) and spatial working memory (Goldberg et al., 2005, Landa and Goldberg, 2005).
Studies are beginning to emerge directly comparing autism and ADHD groups with their typically developing counterparts (Corbett and Constantine, 2006, Goldberg et al., 2005, Ozonoff and Jensen, 1999, Verte et al., 2006). These studies have generally found EF deficits across both diagnostic groups, with ostensibly more severe and global deficits in ASD. Deficits within the ADHD groups tend to be more consistently restricted to behavioral disinhibition and vigilance (Corbett and Constantine, 2006, Goldberg et al., 2005, Ozonoff and Jensen, 1999, Verte et al., 2006). However, there is evidence that individuals with ADHD may also have deficits in planning, set-shifting, and spatial working memory (e.g., Kempton et al., 1999).
Recently, Goldberg et al. (2005) examined inhibition, planning, set-shifting and working memory in a sample of children 8 to 12 years of age with HFA, ADHD and typical development. Participants were carefully assessed to screen out comorbid impulsivity or hyperactivity in autism. Using a computerized battery (CANTAB®), the study reported that response inhibition, planning, and set-shifting were similar across the three groups of ASD, ADHD and typical development and only impaired spatial working memory in the ADHD and HFA groups were reported (Goldberg et al., 2005). However, age and level of functioning on this measure may explain the limited sensitivity (Goldberg et al., 2005, Landa and Goldberg, 2005).
Since deficits in EF are present in several neurodevelopmental disorders, the issue of discriminant validity must be considered as to how disorders with different behavioral phenotype can share similar neuropathological substrates (Ozonoff and Jensen, 1999). Geurts et al. (2004) expanded on this notion using a comprehensive neuropsychological battery in children between 6 and 12 years and reported that children with ADHD demonstrated EF deficits in inhibition and verbal fluency while children with HFA showed deficits across most of the EF measures.
Verte et al. (2006) recently reported significant differences for children with ADHD and HFA in inhibition and response variability compared to children with Tourette Syndrome or typical development. Further, poorer inhibition and more response variability were associated with symptoms of ADHD, while poor working memory was associated with more symptoms of autism. Taken together, the majority of the studies conclude that children with ASD exhibit more pronounced deficits in EF than children with ADHD.
Converging evidence from a variety of methods including chart review (Goldstein and Schwebach, 2004), parent and teacher questionnaires (Gadow et al., 2004) and neuropsychological measures (Corbett and Constantine, 2006) conclude that a high percentage of children with ASD evidence symptoms of ADHD, some warranting a comorbid diagnosis. The etiology of both neurodevelopmental disorders has a strong genetic basis with heritability estimates for autism to be 0.9 (Baron-Cohen and Belmonte, 2005, Zafeiriou et al., 2007) and estimates for ADHD to be 0.7 (Faraone et al., 2005). Furthermore, there are some preliminary findings of a genetic linkage between these disorders at chromosomal locations 2q24 and 16p13 (Fisher et al., 2002, Ogdie et al., 2003, Smalley et al., 2005). Even without consideration of comorbid features, various neuroscientific models have highlighted the common behavioral features, biological pathways and neuroanatomical correlates between ASD and ADHD implicating the frontostriatal system including the frontal lobes and basal ganglia (Damasio and Maurer, 1978, Ozonoff and Jensen, 1999, Pennington and Ozonoff, 1996, Stuss and Benson, 1984). Structural and functional neuroimaging studies show frontal lobe dysfunction in autism (e.g., (Carper and Courchesne, 2000, Carper and Courchesne, 2005, Courchesne et al., 2001, McAlonan et al., 2005, Muller et al., 2001), and ADHD (e.g., (Faraone and Biederman, 1998, Kates et al., 2002, Lou et al., 1984, Mostofsky et al., 2002, Smith et al., 2006, Sowell et al., 2003, Zang et al., 2005)). These brain regions are important in EF, and, as discussed, both disorders have been associated with deficits in EF (e.g., (Barkley, 1997, Goldberg et al., 2005, Pennington and Ozonoff, 1996, Russell, 1997)).
Furthermore, many children with ASD display ADHD symptomatology, suggesting that the disorders may share similar traits or are often comorbid (Corbett and Constantine, 2006, Gadow et al., 2004, Geurts et al., 2004, Ghaziuddin et al., 1992, Goldberg et al., 2005, Goldstein and Schwebach, 2004, Verte et al., 2006). Yet, the limited studies that have compared these two disorders generally exclude comorbid features (Geurts et al., 2004, Goldberg et al., 2005). Conversely, based on population-based investigation, it has been shown that children diagnosed with ADHD may show autistic traits (Reiersen et al., 2007), which punctuates the importance of investigating comorbid features.
Although we recognize the value of elucidating EF in clearly defined prototypical cases of autism and ADHD, this may not be representative or generalizable to many children on the spectrums of autism or ADHD. Thus, we conducted a comprehensive neuropsychological study to compare and contrast six domains of EF (response inhibition, working memory, flexibility/shifting, planning, fluency and vigilance), in children with ASD, ADHD and typical development deliberately allowing comorbid ADHD features in the children with ASD. We hypothesized that children with ASD would demonstrate greater impairment across a broad range of EF tasks. Simultaneously, we investigated the performance of EF and related it to the level of ADHD symptoms across these groups. We predicted that specific measures of vigilance and behavioral inhibition would be associated with ADHD symptoms across the groups.
Section snippets
Participants
The participants in this study included 18 children with high functioning (IQ > 70) ASD (autism = 12, Asperger = 3, PDD-NOS = 3); 18 children with ADHD (combined = 16, primarily inattentive = 1, primarily hyperactive/impulsive = 1); and 18 typically developing children (TYP). The demographic information for the groups is presented in Table 1. Regarding medication, seven ADHD participants were receiving stimulant medication, one of whom was also being treated with clonidine, and two of whom were receiving
Results
Descriptive statistics for the 54 participants across the three groups are presented in Table 1. Chi square analysis demonstrated that the three groups did not differ relative to gender, χ2 (2, N = 54) = 14.52, P > 0.05. Univariate ANOVA demonstrated that the three groups did not differ relative to age, F(2,51) = 0.04 P > 0.10. There was a significant difference in Full Scale IQ, F(2,51) = 6.38, P < 0.005. Post hoc planned comparisons revealed that this difference was due to the ASD group being significantly
Discussion
The overarching goal of this investigation was to profile EF deficits for two major childhood disorders, ASD and ADHD, compared with children with typical development while not controlling for ADHD symptoms. The initial aim was accomplished by assessing performance using a comprehensive neuropsychological battery of EF measures across six domains (response inhibition, vigilance, working memory, flexibility/shifting, planning and fluency). We confirmed our hypothesis that children with ASD
Acknowledgments
Funding was provided by a NIH Career Development Award to Blythe Corbett (5 K08NMHO72958). Additionally, the authors thank the Perry Family Foundation and the Debber Family Foundation for their generous support of our research. We express our sincere gratitude to Josh Day and Meridith Brandt for the participant recruitment.
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