Conceptual and Perceptual Set-shifting executive abilities in young adults with Asperger's syndrome

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Highlights

  • Individuals with AS experience difficulties with extradimensional/conceptual shifts (between categories, sets, or rules).

  • The dissociation between intra- and extradimensional shifting in AS suggests selective frontal-striatal deficits.

  • Preliminary evidence supports a particular type of executive dysfunction and specifically, set-shifting difficulties in AS.

Abstract

Neuropsychological models of frontal lobe functioning have led to a greater appreciation of the dissociations among various aspects of executive functions. Theories of executive function have been proposed to account, at least in part, for the unique social and emotional difficulties experienced by individuals with Asperger's syndrome (AS). Given the paucity of research regarding the neural correlates of executive function in AS, this investigation research involves an examination of a well-established measure of executive, fronto-striatal function in young adults with AS. Findings provide preliminary evidence to support a specific type of executive dysfunction and in particular, extradimensional or conceptual set-shifting difficulties in individuals with AS that implicates prefrontal cortex and frontal-striatal function.

Introduction

Impairments in executive functions (EF) have been implicated in the autism spectrum disorder (ASD) literature since empirical investigation of EF began over two decades ago (Ozonoff, South, & Provencal, 2005), however, the neural substrates of EF in Asperger's syndrome (AS) are still not well understood. One of the most prominent brain regions implicated in EF is the frontal cortex and its connections to striatal brain regions (Schroeter, Zysset, Wahl, & von Cramon, 2004). Anatomical and metabolic abnormalities in frontostriatal pathways have been reported in adults with ASD (Abell et al., 1999, Carper and Courchesne, 2005, McAlonan et al., 2002). Moreover, frontal lobe pathology has been hypothesized by some to represent the underlying cause of the clinical symptoms of ASD, such as perseveration, rule-bound behaviours, and obsessionality (Russell, 1997). Further, deficits in cognitive flexibility and empathy often observed in individuals with ASD are also evident in the behaviour of individuals with frontal lobe damage (Grattan, Bloomer, Archambault, & Eslinger, 1990).

One method of investigating the integrity of the frontal-striatal cortex in AS is to examine set-shifting performance and in particular, to compare extradimensional (ED) and intradimensional (ID) set-shifts. Successful set-shifting performance on the Intra-Extradimensional (IED) Set Shift task of the Cambridge Neuropsychological Test Automated Battery (CANTAB; Cambridge Cognition, 2007) requires the ability to make both extradimensional and intradimensional set-shifts (Watson, Azizian, & Squires, 2006). ED set-shifts occur when an individual shifts from a previously reinforced categorization rule to a new rule (e.g., from sorting stimuli by colour to sorting by shape). ID set-shifts occur when an individual maintains a previously reinforced categorization rule when presented with perceptually novel exemplars (e.g., continuing to sort by shape but shifting from sorting triangles to sorting circles). Furthermore, the processes that underlie ID and ED set-shifts have been reported as cognitively and neurophysiologically distinct (Watson et al., 2006; see Rogers, Andrews, Grasby, Brooks, & Robbins, 2000 for a review). Ozonoff et al. (2004) argue that only the ED shift requires conceptual flexibility (i.e., shifting from one concept or cognitive set to another). In contrast, the ID set-shift is believed to only require perceptual flexibility (i.e., shifting from one exemplar to another within the same cognitive set).

Neurophysiological dissociations between ED and ID set-shifts have been demonstrated using the IED Set Shift task of the CANTAB (Downes et al., 1989, Robbins et al., 1994, Robbins et al., 1998). While this task is similar to popular measures of executive function such as the Wisconsin Card Sorting Test (WCST; Berg, 1948), it was developed to examine specific components of cognition, particularly those related to frontal-striatal regions of the brain (Kaufmann et al., 2012, Ozonoff et al., 2004, Robbins et al., 1994), and it is designed to offer experimental control in parsing the cognitive and neuropsychological correlates of ID and ED set-shift performance (Watson et al., 2006). Data from studies employing this task suggest that ED shifts, but not ID shifts, depend on the integrity of the frontostriatal system (Watson et al., 2006). Individuals with insult to the prefrontal cortex (PFC; Owen, Roberts, Polkey, Sahakian, & Robbins, 1991), Parkinson's disease (Downes et al., 1989), Huntington's disease (Lawrence et al., 1996), and schizophrenia (e.g., Elliott, McKenna, Robbins, & Sahakian, 1995) demonstrate ED set-shift impairments despite intact ID set-shifting abilities. Similarly, lesion studies of non-human primates in a similar paradigm are commensurate with these findings (e.g., Dias et al., 1996, Dias et al., 1997). Rogers et al. (2000) also reported similar findings in a PET study of typically developing adults; ED set-shifts (and not ID set-shifts) were correlated with activation of bilateral prefrontal regions, further supporting the hypothesis that ED set-shifts (but not ID set-shifts) are dependent upon prefrontal and frontal-striatal activity. These findings are also consistent with other imaging work that reports PFC circuitry in ED set-shifting (Konishi et al., 1998, Konishi et al., 1999, Konishi et al., 2002, Smith et al., 2004, Watson et al., 2006). Furthermore, the IED Set Shift task has been used in functional imaging, animal, and human lesion studies (Baker et al., 1996, Dias et al., 1996, Owen et al., 1996, Roberts et al., 1988), which permit cross-species comparisons and inferences about the underlying neural circuitry involved in task performance (Ozonoff et al., 2004).

To date, four known investigations have used the IED shift task with individuals with ASD (Hughes et al., 1994, Ozonoff et al., 2000, Ozonoff et al., 2004, Turner, 1997), and results from these studies are mixed. Hughes and colleagues documented intact ID shifting but impaired ED shifting in participants with autistic disorder (AD) and a comorbid diagnosis of mental retardation. Further, Turner (1997) replicated these findings in individuals with AD and mental retardation; however, no deficits were found in a group of higher functioning individuals with AD and without mental retardation. Similarly, Ozonoff et al. (2000) found no ED shifting difficulties in individuals with high-functioning (intellectual abilities within the average range) autism relative to IQ-matched, typically developing controls. Most recently, Ozonoff et al. (2004) found ED (and not ID) shifting difficulties in participants with AD, relative to age-, sex-, and IQ-matched controls. The authors argue that the findings provide evidence to support specific types of executive dysfunction and specifically, attention shifting, in individuals with AD that implicate PFC function. At the cognitive level, shifting within a category or rule does not appear problematic (ID shifts); however, shifting between categories, sets, or rules (ED shifts) is particularly challenging for individuals with AD. Further, the results are purported to contribute to the accumulating evidence of frontal lobe involvement in AD. Although the neural circuitry that causes autistic symptomatology is likely widely distributed throughout the brain, the results indicate that the PFC is involved in these circuits at some level and consequently, the PFC should remain an active area of future investigation (Ozonoff et al., 2004). Hughes et al. (1994) also argue that the lack of association between performance on ID and ED shifting suggests separable elements of executive control and different types of executive dysfunction consistent with neuroanatomical studies. Further, this fractionation of function is proposed to create opportunities for explaining the heterogeneity of symptoms observed in ASD.

Section snippets

Study rationale and research questions

This study examined the integrity of the prefrontal and frontal-striatal cortices by investigating particular components of cognition associated with these brain regions. No known studies have examined the neural substrates of set-shifting in young adults with AS using the IED task, which is supported by lesioned animal and human neuroimaging evidence to preferentially involve the prefrontal and frontal-striatal system. This investigation was therefore interested in better understanding the

Method

This research was part of a larger tri-university collaboration conducted through the universities of Calgary, Saskatchewan, and Manitoba. The overarching goal of this research initiative was to investigate the unique emotional and executive abilities of young adults with ASD and to subsequently utilize that information to support individuals with AS as they transition into adulthood (Montgomery et al., 2008). The clinical sample included 34 young adults diagnosed with AS (M = 18.86 years, range

Results

The performance of individuals with AS on the measure of intra- and extradimensional set-shifting abilities was first examined descriptively and subsequently compared to the performance of their typically developing peers, utilizing a single independent t-test. Means and standard deviations for both groups are presented in Table 2.

As predicted, individuals with AS performed similarly to their typically developing peers on the intradimensional set-shift; however, they made more errors than their

Discussion

The overarching aim of this study was to examine the integrity of the prefrontal and frontal-striatal cortices in AS using the IED task (in which the neural underpinnings may be better understood relative to other executive function measures). Specifically, performance on measures of ID and ED shifting were explored in an effort to understand the neural substrates of hypothesized executive dysfunction in young adults with AS. Given findings from previous research that suggested that ED shifts

Conclusions

Converging evidence from human lesion, animal lesion, and human functional neuroimaging studies provides strong support for the role of the prefrontal and frontal-striatal systems in performance on the IED task. Previous work implicates these brain regions in performance at a specific stage of the IED task (i.e., the extradimensional shift engages the prefrontal and frontal-striatal systems, whereas the intradimensional shift does not; Rogers et al., 2000, Watson et al., 2006). The present

Acknowledgements

This research would not have been possible without the generous financial support of the Alberta Centre for Child, Family and Community Research, and the Scottish Rite Charitable Foundation, as well as Lloyd and Florence Cooper's doctoral award in integrative medicine. (The authors declare that they have no conflict of interest with these aforementioned individuals and organizations).

Many thanks to an exceptional group of colleagues who made significant contributions to the data collection and

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