Abstract
Researchers have proposed that autism spectrum disorder (ASD) is characterized, at least in part, by executive function (EF) difficulties associated with the integrity of the frontal lobe. Given the paucity of research regarding EFs in young adults with high functioning ASD (HF-ASD), this research involves an examination of various indices of EF related to inhibition, planning, and generativity. Results indicate that although young adults with HF-ASD as a group met normative expectations on all measures of EF, they also exhibited considerable individual variability relative to their age- and sex-matched typically developing peers. These findings have important research and clinical implications, including the need to carefully consider the impact of the research comparison group, and to recognize individual variability in executive functioning among young adults with HF-ASD.
The term executive function (EF) was introduced by A. R. Luria (1966) who proposed the existence of a cognitive system responsible for intentionality and the formulation of thoughts and actions, as well as the identification and application of goal-appropriate cognitive routines and evaluation of outcomes. More recently, EFs are described as a group of cognitive abilities that include response inhibition, sequencing of behaviors, cognitive flexibility, self-regulation of behaviors, planning, and organization of behavior (Eslinger, 1996, 2008; Jurado & Rosselli, 2007; Kodituwakku, Kalberg, & May, 2001). EFs necessitate flexibility in cognition and behavior, requiring abilities to attend to currently relevant information, hold and manipulate information, switch between cognitive strategies and behavioral responses, and inhibit inappropriate behaviors (Allport, 1989; Knight & Stuss, 2002; Kodituwakku et al., 2001). Denckla (1996) also proposed that EFs are “future-oriented” processes. Most researchers now agree that EFs are not basic cognitive processes such as motor activity, sensation, perception, attention, or memory but instead involve the integration and management of these more basic cognitive processes (Connor, Sampson, Bookstein, Barr, & Streissguth, 2000).
Researchers have proposed that autism spectrum disorder (ASD) is characterized, at least in part, by executive difficulties associated with the integrity of the frontal lobe (Baron-Cohen et al., 1999; Casanova, Buxhoeveden, Switala, & Roy, 2002; Horwitz, Rumsey, Grady, & Rapoport, 1988; Luna et al., 2002; Penn, 2006; Russell, 1997). Preference for sameness, difficulties switching attention, poor impulse control, and perseveration are characteristics of both ASD and executive difficulties that stem from frontal lobe damage (Baddeley & Wilson, 1988; Hill, 2004a; Rajendran & Mitchell, 2007). Individuals with ASD have demonstrated deficits in EFs, and these deficits have been linked to the frontal lobe and more specifically, the prefrontal cortex (PFC) in both typically developing individuals and those with ASD (e.g., Penn, 2006). After damage to the PFC, knowledge of social rules and conventions no longer guides decision making and social behavior, yet these executive impairments are not accounted for by a loss of intellectual resources or psychosocial stressors (Eslinger & Robinson-Long, 2010; Stuss, Gallup, & Alexander, 2001). Parallels can be drawn between the outcomes of those with frontal lobe and PFC damage, and the clinical characteristics of individuals with ASD who do not have intellectual or language impairments, referred to from here on as high functioning ASD (HF-ASD). A seemingly selective impairment in social and emotional decision making (despite intact intellectual, language and memory abilities) is also characteristic of individuals with HF-ASD. In addition, despite knowledge of social rules and conventions, this knowledge often does not guide social behavior in individuals with HF-ASD (Montgomery, McCrimmon, Schwean, & Saklofske, 2010).
Theories of EFs in ASD relate characteristic symptomatology to deficits in domain-general executive control processes, including inhibition, planning, and generativity (Dennis, 1991; Ozonoff, 1997; Ozonoff, Strayer, McMahon, & Filloux, 1994; Robbins, 1996). Deficits in these executive processes have also been proposed as a causal factor for the restricted and repetitive behavior patterns characteristic of individuals with ASD, as well as difficulties in communication and reciprocal social interaction (Damasio & Maurer, 1978). Indeed, Pennington and Ozonoff’s (1996) review suggested that individuals with ASD demonstrated impairment on at least one EF task. Another review conducted by Hill (2004a) found deficits in the executive domains of planning, inhibition, generativity, and also self-monitoring (Hughes & Russell, 1993; Ozonoff et al., 2004; Rumsey & Hamburger, 1988; Russell, Jarrold, & Hood, 1999). Similarly, Corbett, Constantine, Hendren, Rocke, and Ozonoff (2009) found that children with ASD displayed poor performance relative to typically developing controls on measures of inhibition, working memory, flexibility/shifting, and vigilance. Importantly, however, preserved performance in many of these executive domains has also been documented (Boucher, 1988; Hughes, Russell, & Robbins, 1994; Ozonoff & Jensen, 1999; Russell & Hill, 2001).
Neuropsychological models of EF appear to provide insight into the challenges faced by individuals with HF-ASD. To this end, three classic neuropsychological domains of EF (namely, inhibition, planning, and generativity) are reviewed as they relate to individuals on the spectrum. Although these three specific EFs in no way provide an exhaustive review of EFs, they were chosen because there are previous equivocal research findings in each of these executive domains, and these particular EFs appear to be important in understanding the rigid and routinized behaviors associated with ASD.
Inhibition
Response inhibition is the interference or prevention of a behavioral response in the presence of the stimulus for that response (Russo et al., 2007). Inhibition is viewed as a critical aspect of EFs, and classic measures such as the Stroop task (Stroop, 1935) and the more recent, standardized version of the Stroop task called the Color-Word Interference task (Delis, Kaplan, & Kramer, 2001) are thought to provide an index of inhibitory abilities. Some researchers have reported that children and adolescents with ASD do not appear to have inhibitory difficulties on these tasks (Adams & Jarrold, 2009; Christ, Kester, Bodner, & Miles, 2011; Eskes, Bryson, & McCormick, 1990; Ozonoff & Jensen, 1999), or on other measures of inhibition such as the Go/No-Go, Stop-Signal, and negative priming tasks (Ozonoff et al., 1994; Ozonoff & Strayer, 1997). Ozonoff and Strayer (1997) found that individuals with ASD did not manifest difficulties inhibiting the processing of irrelevant stimuli, compared with their age-, IQ-, and gender-matched typically developing peers. In contrast, difficulties with the inhibition of a prepotent or previously learned response have been documented in individuals with ASD (Hughes & Russell, 1993; Russell, Hala, & Hill, 2003; Russell, Mauthner, Sharpe, & Tidswell, 1991). Despite negative feedback regarding their performance, individuals with ASD continued to engage in behaviors that were not rewarded. The mental inflexibility and perseveration characteristic of individuals with ASD is likely to have contributed to this observed inability to incorporate performance feedback and adapt behavior accordingly. Importantly, the lack of consistency in the inhibitory literature warrants further investigation of this EF.
Planning
Planning is a complex, dynamic operation that requires fluid monitoring, re-evaluation, and updating (Hill, 2004b) and involves an understanding of ongoing contextual changes, an ability to look ahead and predict, to make choices, and then to implement the plan and revise it accordingly. Planning abilities are frequently assessed utilizing Tower tasks (e.g., Delis et al., 2001). Planning deficits have been found in children and adolescents with ASD (Bennetto, Pennington, & Rogers, 1996; Booth, Charlton, Hughes, & Happé, 2003; Hughes, 1996; Hughes et al., 1994; Ozonoff & Jensen, 1999; Ozonoff & McEvoy, 1994; Ozonoff, Pennington, & Rogers, 1991; Prior & Hoffmann, 1990; Rumsey & Hamburger, 1988). Planning measures have also purportedly been used to accurately identify an ASD diagnosis (Ozonoff & McEvoy, 1994). Importantly, however, some researchers suggest that planning ability is more closely related to intellectual abilities than to autistic symptomatology (Mari, Castiello, Marks, Marraffa, & Prior, 2003). Given previous mixed findings, planning abilities also appear to be an executive domain in need of further investigation.
Generativity
The lack of spontaneity and initiative, poverty of speech and action, and difficulties engaging in pretence observed in ASD have been attributed to difficulties generating novel thoughts and behaviors (Turner, 1997; Wing & Gould, 1979). Furthermore, impairments in generativity, which are frequently measured by Fluency tasks (Delis et al., 2001), have also been proposed to relate to the restricted and repetitive behaviors, as well as the preference for sameness and routine that are characteristic of ASD. Moreover, the generation and regulation of novel thoughts and behavior is believed to require executive processes (Hill, 2004a, 2004b). Deficits in generativity in ASD have been observed in drawings (Lewis & Boucher, 1991), production of pretence in pretend play (Jarrold, Boucher, & Smith, 1996; Wing, Gould, Yeates, & Brierly, 1977), and in measures of word fluency (Manjiviona & Prior, 1999; Minshew, Goldstein, Muenz, & Payton, 1992; Nyden, Gillberg, Hjelmquist, & Heiman, 1999; Ozonoff et al., 1991; Rumsey & Hamburger, 1988). Turner (1999) found that children and adults with autistic disorder (AD) were impaired in the generation of novel responses on verbal and design/visual fluency tasks as compared with age- and IQ-matched control groups. Furthermore, their poor performance on design fluency tasks (that measure visual fluency) was correlated with high levels of repetitive behavior. Turner suggested that impaired generativity negatively affects the execution of routine behavior in the face of changing circumstances or when trouble-shooting is necessary. Consequently, adaptability is also compromised. Similarly, Spek, Schatorjé, Scholte, and van Berckelaer-Onnes (2009) found that adults with AS were impaired on multiple verbal fluency measures (i.e., semantic and phonemic fluency), and these impairments were not attributable to a lack of the use of strategies or to difficulties in switching between strategies. In contrast, other investigators report no such generativity difficulties (Boucher, 1988; Scott & Baron-Cohen, 1996). Scott and Baron-Cohen (1996) found that high functioning (i.e., intellectual abilities within the normative range) individuals with autism did not display a global generativity deficit. Boucher (1988) reported that high functioning individuals with AD performed equally well to typically developing controls in their verbal fluency abilities when asked to generate words in response to familiar category cues; however, they exhibited relative difficulties when generating miscellaneous words. Mixed findings in the generativity literature also suggest that further examination of this EF is warranted (Hill, 2004a, 2004b).
Shortcomings of the EF Literature in ASD
Although there is some evidence that individuals with ASD experience deficits in EFs, there are shortcomings within the literature that need to be addressed. There is a lack of consensus regarding which executive processes are compromised in ASD, and very little is known about the specific profile of executive strengths and weaknesses in HF-ASD as many of the investigations have been conducted with individuals with AD or a mixed ASD group (e.g., Asperger syndrome [AS] and AD with varying intellectual and language capabilities). The sheer number of permutations between the various EFs studied, the ways that levels of EFs are attained, the developmental levels of participants, and the comparison groups utilized, has complicated the development of a definitive theory of EFs among persons with ASD (Russo et al., 2007).
Study Rationale
Given the heterogeneity in research measures and samples used, and the equivocal results of previous studies, further study of EFs in young adults with HF-ASD is needed. These individuals experience significant and pervasive social and emotional difficulties, and restricted, repetitive interests, activities, and behavior consistent with ASD symptomatology, despite intact language and cognition. Hill and Bird (2006) argued that any EF deficits that are related causally to autistic symptomatology should be found in their most pure forms in high functioning individuals with ASD, making this an important group to study.
The current study also aims to extend the research literature in young adults with HF-ASD as relatively few studies have been published on young adults with ASD and even fewer with young adults with HF-ASD (for a review, see Hill & Bird, 2006). From a developmental perspective, early to late adolescence is a stage in which the frontal and prefrontal cortices undergo intensive structural and functional maturational changes (Gerra et al., 2000; Kolb & Whishaw, 1996; Spear, 2000a, 2000b). Thus, by focusing on an adult population with HF-ASD, issues concerning the late maturation of the frontal lobes (Mesulam, 2002) are less pronounced, which again makes this particular young adult population an important group to study.
In light of the mixed findings evident in previous EF research, and the limited studies of high functioning young adults with ASD, this investigation was designed to examine EFs in this particular population to ascertain whether these young adults do indeed experience EF difficulties in relation to a matched group of typically developing individuals, as well as the normative data from one of the most prominent EF assessment instruments—the Delis–Kaplan Executive Function System (D-KEFS). It is also important to note that this article reports on a research program involving participants who were previously diagnosed with Asperger disorder/syndrome (AS). In the newest iteration of the Diagnostic and Statistical Manual of Mental Disorders (5th ed.; DSM-5; American Psychiatric Association [APA], 2013), these individuals would be most aptly described as having ASD without intellectual or early language impairments, and they are therefore referred to in this article as individuals with HF-ASD.
Research Questions
Method
This research was part of a larger tri-university collaboration conducted through the universities of Calgary, Saskatchewan, and Manitoba. The overarching goal of the broader research program was to investigate the unique emotional and executive abilities of young adults, ages 16 to 21 years, with HF-ASD and to subsequently utilize that information to support these individuals as they transition into adulthood (Montgomery et al., 2008). The investigation into emotional abilities and more specifically, emotional intelligence has been previously reported (Brady et al., 2014).
Participants
Participants with HF-ASD were recruited from schools, mental health settings, university clinics, and service organizations for those with pervasive developmental disorders in Calgary, Alberta and Winnipeg, Manitoba. In addition, media campaigns in both provinces highlighting the research project also resulted in inquiries about participation. Control group participants were recruited from the Calgary site through advertisements in local papers and community newsletters, posters placed in various community centers (e.g., recreation and leisure centers), and on the University of Calgary campus.
The sample was comprised of 34 young adults diagnosed with AS (M = 18.86 years, range = 16.3–21.5 years, 76.5% male) and 34 age- and sex-matched typically developing young adults (M = 18.90 years, range = 16.0–21.5 years). There were no concerns regarding attrition; all participants who decided to participate completed all research requirements. Participants were compensated with a gift certificate (valued at $50.00 Canadian) for the time they spent partaking in this study.
Inclusionary Criteria
Clinical diagnosis. Clinical participants must have received a diagnosis of AS from a licensed medical doctor, psychologist, or psychiatrist (as this research was conducted just prior to the diagnostic changes that occurred as a result of the new DSM-5 (APA, 2013). These participants were required to provide documentation specifying the professional who provided their AS diagnosis, as well as information pertaining to their developmental history (which included language development). This information was subsequently reviewed by the research team to ensure adherence to the fourth edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR; APA, 2000) criteria for AS prior to inclusion in the study. Retrospective review of each participant’s diagnostic and developmental history also revealed coherence with the recent fifth edition of the DSM (APA, 2013) and its criteria for an ASD diagnosis without an accompanying intellectual or language impairment.
Validation of diagnosis. To further validate the AS diagnosis, participants were required to meet a classification within the moderate to high ranges of likelihood of having AS on the Krug Asperger Disorder Index (KADI; Krug & Arick, 2003), a measure designed to distinguish individuals with AS from other forms of high functioning autism, as well as from typically developing individuals.
Intellectual ability. All participants were required to demonstrate verbal IQ (VIQ), nonverbal or performance IQ (PIQ), and full-scale IQ (FSIQ) in the average or higher ranges (i.e., standard scores of 85 or greater) on the Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler, 1999). These inclusionary criteria were necessary to ensure not only the validity of the clinical diagnosis for the individuals with AS, but also that potential poor performance on the EF tasks was not attributable to lower cognitive ability. The control participants were not matched according to VIQ, PIQ, or FSIQ, as research has shown that individuals with AS often present with an uneven or uncommon profile of intellectual abilities that results in challenges in IQ matching (Jarrold & Brock, 2004; Mottron, 2004). Moreover, the purpose of the control group was to provide a comparison of individuals typical of the normative population (who do not share this uneven profile of intellectual abilities). Importantly, however, both groups exhibited relatively similar FSIQ. The VIQ, PIQ, and FSIQ performance for the sample are presented in Table 1. HF-ASD participants and age- and sex-matched typically developing peers did not differ with respect to age, t(66) = −0.106, p = .916; VIQ, t(66) = 1.777, p = .080; PIQ, t(66) = −0.401, p = .689; or FSIQ, t(66) = 0.982, p = .330.
Typical early language development. Participants must not have experienced a language delay in early childhood (i.e., single words by 2 years of age and communicative two- to three-word phrases by 3 years of age). The age- and sex-matched typically developing cohort was also required to exhibit normal language development.
Neurological integrity. Finally, all participants were required to have no history of head injury.
Intelligence Quotients for Individuals With High Functioning ASD and Typically Developing Peers.
Note. All scores are presented in standardized form, with a mean of 100 and a standard deviation of 15. ASD = autism spectrum disorder.
Inclusionary Measures
The Krug Autism Spectrum Disorder Index (KADI; Krug & Arick, 2003) is a standardized measure designed to discriminate between AS and other forms of high functioning autism in individuals ages 6 to 21 years. It is a norm-referenced (ASD norm group), 32-item report completed by a clinician with ratings provided by close friends, parents, or relatives of the individual. The KADI was standardized on 486 individuals, with results showing that 130 of these had a diagnosis of AS and 162 had a diagnosis of AD. In addition, 194 typically developing controls were included in the standardization sample. The KADI demonstrates internal reliability of .89 and excellent stability over a 2-week period (.98; Krug & Arick, 2003). Furthermore, 90% agreement was demonstrated for interrater reliability. With reference to evidence for validity, the KADI demonstrated specificity of .94, sensitivity of .78, and positive predictive power of .83. Mean scores differed significantly for the various groups in the standardization sample, demonstrating support for the clinical validity of the instrument. The KADI is based on a distribution with a mean of 100 and a standard deviation of 15. It is important to note that rather than reflecting numbers of individuals in the general population who manifest the characteristics, this scale reflects the number of participants with AS who had a score in the various ranges. For example, if an individual receives a score of 100 or higher, interpretation standards indicate that 50% of individuals with AS scored the same as or higher than that individual. Inclusion in this study required individuals to have a score of 80 or higher (i.e., standard score in the 80–115 range) corresponding to the “somewhat likely,” “likely,” and “very likely” (to have AS) KADI qualitative classification ranges. The KADI is one of the most reliable and valid screens for identifying individuals with AS (Campbell, 2005; Stoesz, Montgomery, Smart, & Hellsten, 2011).
The Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler, 1999) is an individually administered, standardized, and abbreviated test of cognitive intelligence for individuals ages 8 to 89 years. It contains four subtests (Vocabulary, Similarities, Block Design, and Matrix Reasoning) and yields a measure of verbal and performance (nonverbal) intelligence, as well as a full-scale IQ. The WASI was standardized on a sample of 2,245 American individuals, stratified according to 1997 U.S. census data. Internal consistency estimates are high and range from .92 to .98 for the IQ scores. Stability coefficients for the VIQ range from .92 to .97. Scores on the WASI are highly correlated with scores on the Wechsler Intelligence Scale for Children – Third Edition (WISC-III; range = .69–.74 for subtests; .76–.87 for IQ scores) and the Wechsler Adult Intelligence Scale – Third Edition (WAIS-III; .66–.88 for subtest scores; .84–.92 for IQ scores), which provides evidence of its validity. In addition, factor analysis and intercorrelations of subtest scores provide evidence for the construct validity of the WASI (Lindskog & Smith, 2001). The WASI was administered following the standardized instructions outlined in its administration manual. Raw scores were converted to norm-referenced standard scores (M = 100, SD = 15).
EF Measures
The Delis-Kaplan Executive Function System (D-KEFS; Delis et al., 2001) is a standardized set of nine tests that assesses key components of EFs mediated by the frontal lobe, including mental flexibility, abstract thinking, problem solving, inhibition, planning, concept formation, and creativity in both verbal and spatial modalities. The D-KEFS is intended to provide assessment of broad, yet primarily independent, EFs in individuals ages 8 to 89 years, and consequently, each test in this battery may be administered alone or in combination with others. The subtests included in the D-KEFS are modifications of well-known traditional tests of EF (Lopez, Lincoln, Ozonoff, & Lai, 2005).
The D-KEFS was standardized on a stratified sample of 1,750 nonclinical individuals in the United States based on 2000 U.S. census data. Reliabilities of the D-KEFS tests are comparable with other commonly available tests of EF (Delis, Kramer, Kaplan, & Holdnack, 2004). As the D-KEFS consists of distinct subtests, comparison with single measures of EF has not been conducted. Rather, correlational analyses of conditions for each D-KEFS subtest in relation to each other in typically functioning individuals are provided. Results indicate that (a) the relative contribution of each EF differs between age groups (as would be expected in developmental neuropsychological theory) and (b) overall low correlations between tests indicate that each measures distinct, relatively independent EFs (Delis et al., 2001). Validity of the D-KEFS subtests was provided through the use of intercorrelations of measures within the individual D-KEFS tests, correlations between D-KEFS tests with other related tasks, and findings from pilot studies with clinical populations (Delis et al., 2001). All D-KEFS subtests were administered following the standardized instructions outlined in its administration manual. Raw scores were converted to norm-referenced standard scores (M = 100, SD = 15).
The Color-Word Interference subtest is based on the Stroop (1935) procedure for measuring inhibition. The participant’s ability to inhibit an automatic verbal response (reading the printed words) to generate a conflicting response (of naming the dissonant ink colors in which the words are printed) is assessed. There are two baseline conditions that measure key component skills of the higher-level tasks: basic naming of color patches (Condition 1) and basic reading of color-words printed in black ink (Condition 2). Condition 3, Inhibition, is the traditional Stroop task, for which the participant must inhibit reading the words to name the dissonant ink colors in which those words are printed. It is this third condition that was used in this research, after accounting for normative performance on the first two baseline conditions.
The Tower subtest is a modification and improvement of the Tower of Hanoi (Borys, Spitz, & Dorans, 1982) and Tower of London (Morris, Ahmed, Syed, & Toone, 1993) tests, both commonly used measures of planning ability. Participants are shown a display consisting of three pegs with several disks in a pre-arranged format. The objective is to transfer the entire tower to one of the other pegs, moving only one disk at a time and never a larger one onto a smaller one.
The Verbal Fluency subtest is a measure of the ability to generate verbal labels fitting within provided categories. It is comprised of three tasks. In the Letter Fluency task, the examinee is asked to say as many words as they can that begin with a specified letter in 60 s. Three such trials are given, each with a different letter. In the Category Fluency task, examinees are asked to name as many words belonging to a specific category as they can in 60 s. Two such trials are given with a different category for each. Finally, in the Category Switching task, examinees are asked to provide words belonging to a specific category, alternating between two categories. Although all of the verbal fluency measures were administered to ensure the more basic fluency abilities were evident, the Category Switching Verbal Fluency score was the only score used in all analyses reported in this study. The switching component of this task requires the greatest cognitive flexibility, and thus, it appears to be the most complex verbal fluency task, making it the most suitable for an investigation of complex EFs.
The Design/Visual Fluency subtest is a counterpart to the Verbal Fluency subtest. This task presents the individual with a row of boxes, each of which contains an array of dots. The examinee is asked to connect the dots using only four lines, making a different design each time in 60 s. In the Filled Dots condition, the boxes shown to the participant contain five filled dots. In the Empty Dots Only condition, the boxes shown to the participant contain five filled and five unfilled dots, and the participant is asked to connect only the empty dots, inhibiting the previously correct response of connecting the filled dots. In the final Category Switching task, the participant is asked to switch between connecting filled and empty dots. Again, although all visual fluency tasks were administered to ensure the less complex visual fluency abilities were intact, it is the Category Switching Visual Fluency task score that was used in all analyses conducted in this study. This particular score was utilized because it requires the greatest cognitive flexibility, and thus, it appears to be the most complex visual fluency task, again making it the most suitable for an investigation of complex EFs.
Results
D-KEFS Normative Sample Comparison
The first research question examined the performance of young adults with HF-ASD on executive measures of inhibition, planning, and generativity, measured respectively by the Color-Word Interference, Tower, Verbal Fluency Category Switching, and Design/Visual Fluency Category Switching subtests of the D-KEFS. Means and standard deviations on the EF measures for those with HF-ASD and the typically developing comparison group are presented in Table 2.
Descriptive Statistics for All Executive Function Variables for the Total Sample.
Note. All variables are based on a sample size of 34, and all scores presented are in standardized form. D-KEFS = Delis–Kaplan Executive Function System. HF-ASD = high functioning autism spectrum disorder.
p < .01, two-tailed.
As a group, participants with HF-ASD exhibited average planning and generativity abilities, and low average inhibitory abilities (relative to the D-KEFS normative data). Importantly, however, further inspection of the range of standard scores indicated that there was considerable variability in performance on all of the EF measures; subtest scores ranged from well below average to well above average on all measures. These findings highlight the heterogeneity of EF performance in HF-ASD and they serve as a reminder of the importance of individual differences and EF score variability both within and between individuals with HF-ASD.
Age- and Sex-Matched Typically Developing Peers Comparison
To investigate how the EF performance profile of young adults with HF-ASD compared with age- and sex-matched typically developing peers (recruited as part of the tri-university research program), independent samples t tests were conducted, using a Bonferroni correction to control for the multiple comparisons (four comparisons; p = .0125). Means and standard deviations of EF measures for individuals with HF-ASD and the matched typically developing comparison group are also presented in Table 2.
Descriptive comparisons of standard scores indicated that the sample of individuals with HF-ASD showed a trend toward lower scores than the matched typically developing comparison group on all EF measures except Verbal Fluency. Descriptive comparisons also revealed more variability (as indexed by the standard deviations and range of scores) in the performance of individuals with HF-ASD compared with matched typically developing peers, on all measures of EF function except Verbal Fluency. Thus, the performance of individuals with HF-ASD on EF measures of inhibition, planning, and visual generativity was more variable than their matched typically developing peers.
Results from the independent t tests revealed a significant difference between groups in mean performance on EF measures of inhibition, t(66) = −2.83, p < .01, d = 0.69, and visual fluency/generativity, t(66) = −3.52, p < .01, d = 0.86. Nonsignificant differences between groups were observed on the planning measure, t(66) = −1.94, p = .06, and the verbal fluency/generativity measure, t(66) = −0.32, p = .75.
Discussion
Inhibition
Low average inhibitory abilities were found in the group with HF-ASD, and relative to age- and sex-matched typically developing peers, individuals with HF-ASD exhibited poorer performance on measures of inhibition. Importantly, however, although the difference between groups in inhibitory performance was statistically significant, the average performance of both the HF-ASD and typically developing groups was within the normative range, according to the D-KEFS standardization data. As a group, individuals with HF-ASD exhibited inhibitory abilities within the low average range; this finding suggests intact inhibitory abilities in many individuals with HF-ASD. However, further exploration of this group’s scores revealed greater variability in performance, ranging from well below average to well above average in comparison with both the usual standard deviation of 3 and the matched sample for this study. This finding underscores the importance of individual differences when examining inhibitory performance in HF-ASD. In sum, it appears that although individuals with HF-ASD as a group exhibited poorer inhibitory abilities relative to their matched typically developing peers, these impairments are not substantial, on average, when compared with normative expectations (i.e., the D-KEFS standardization data). Importantly however, it is critical that consideration be given to each individual case.
It is difficult to relate these results to the current literature as studies examining inhibition in young adults with HF-ASD are rare. Although inhibition has been explored in AS and mixed groups of ASD (i.e., variations of AD [with diverse intellectual and language abilities], and AS), few investigators have looked exclusively at individuals with AS/HF-ASD. Furthermore, findings from studies of inhibition in ASD have been mixed, with some reporting inhibitory atypicalities and deficits (e.g., Chan et al., 2011; Kana, Keller, Minshew, & Just, 2007; Mosconi et al., 2009) whereas others have found no inhibitory difficulties (e.g., Adams & Jarrold, 2009; Christ, Holt, White, & Green, 2007; Christ et al., 2011; Geurts, Begeer, & Stockmann, 2009; Ozonoff & Jensen, 1999; Ozonoff & Strayer, 1997). The current investigation provides preliminary evidence to suggest that overall, inhibitory abilities are consistent with normative expectations and consequently appear to be spared in many individuals with HF-ASD. These findings are consistent with the only known study of inhibition in adults with AS that also concluded that inhibitory abilities are not compromised in this population (Ambery, Russell, Perry, Morris, & Murphy, 2006).
Planning
Average planning abilities were found in the group with HF-ASD, and there appears to be very little difference in planning abilities relative to age- and sex-matched typically developing controls. Thus, most individuals with HF-ASD exhibited planning abilities within the normative range (i.e., relative to the D-KEFS normative data). Similar to inhibitory findings, there was slightly more variability in the planning performance of individuals with HF-ASD (as evidenced by the larger standard deviation and relative to matched typically developing peers), which again highlights the importance of understanding individual differences.
Analysis of planning abilities for the participants in this study are again difficult to discuss in the context of the current literature due to the paucity of research in young adults with AS/HF-ASD. Although studies have identified planning deficits, they have often been found in individuals with AD or mixed ASD groups (e.g., Bennetto et al., 1996; Booth et al., 2003; Hughes, 1996; Hughes et al., 1994; Ozonoff & Jensen, 1999; Ozonoff & McEvoy, 1994; Ozonoff et al., 1991; Prior & Hoffmann, 1990; Rumsey & Hamburger, 1988). In contrast to research that has reported planning measures as useful diagnostic tools in which to accurately identify an ASD diagnosis (Ozonoff & McEvoy, 1994; Ozonoff et al., 1991), the present results suggest this may not be the case. Importantly however, the current findings regarding planning abilities in HF-ASD are preliminary in nature and given the limited research in this area, it is clear that further exploration of these abilities is required.
Design Fluency/Visual Generativity
The HF-ASD sample displayed average visual fluency abilities, and although there were statistically significant performance differences between the HF-ASD group and the matched typically developing group (who displayed above average mean scores), those differences were again not clinically relevant as the individuals with HF-ASD still met normative performance expectations (as assessed by the D-KEFS). Similar to findings from the inhibitory and planning measures, there was slightly greater variability in the performance of individuals with HF-ASD than their age- and sex-matched typically developing peers. In sum, it appears that although individuals with HF-ASD as a group exhibited poorer visual fluency abilities relative to their matched typically developing peers, these impairments are not substantial when compared with normative expectations.
Preliminary findings from this study are inconsistent with those reported in previous research that has found visual fluency deficits in AS (Lewis & Boucher, 1991); however, no known studies have examined visual fluency in young adults with AS/HF-ASD, and few studies have utilized the category switching version of the visual fluency task that was used in this study. Consequently, preliminary findings from the present study require further investigation.
Verbal Fluency/Verbal Generativity
Individuals with HF-ASD exhibited overall average verbal fluency abilities that did not differ significantly from their age- and sex-matched typically developing peers. As well, HF-ASD individuals displayed more uniformly average verbal fluency abilities in comparison with the other measured EF subscales.
Current preliminary findings of unimpaired verbal generativity in the HF-ASD group are consistent with several studies that reported no verbal fluency concerns; however, this previous research was conducted with samples of children with HF-ASD (Boucher, 1988; Scott & Baron-Cohen, 1996). In contrast, other investigations of children with ASD have reported verbal fluency deficits (Nyden et al., 1999; Ozonoff et al., 1991). In light of these previous studies, our preliminary findings may suggest that the executive impairment found in some samples of children with AS/HF-ASD diminishes over time; however, longitudinal study is required to further examine this possibility. Furthermore, the inconsistency between the current findings and previous research may be attributed, at least in part, to the diversity in ASD groups studied (i.e., individuals with various ASD diagnoses including AD and AS; for example, Boucher et al., 2005; Dunn, Gomes, & Sebastian, 1996), and varying verbal fluency tasks. Importantly, however, the current findings are preliminary, and in light of the limited research in this area, it is evident that further investigation into verbal generativity in young adults with HF-ASD is needed.
Concluding Remarks
In summary, it appears that the HF-ASD group met normative expectations on all measures of EF (i.e., standard scores within the normative range on the D-KEFS), despite exhibiting more variability in their performance on most measures of EF, and demonstrating poorer inhibitory and visual fluency/generativity abilities relative to the age- and sex-matched typically developing control group (recruited as part of the broader tri-university research program). These findings highlight the critical importance of comparison groups to illuminate subtle inter- and intraindividual differences. When compared with age- and sex-matched typically developing peers with similar intellectual abilities, conclusions regarding a trend toward lower inhibition and visual generativity scores could be drawn. Importantly, however, closer examination of the performance of the HF-ASD group reveals that scores in these executive domains are well within the average range (relative to D-KEFS normative data).
Despite previous research that suggests EF deficits, and associated PFC and broader frontal lobe impairment in ASD, preliminary findings from this study indicate the contrary. Overall, the HF-ASD group did not exhibit EF deficits on measures of inhibition, planning, and generativity, but instead exhibited group performance that was well within normative expectations. In fact, the overall normative performance of the HF-ASD group on all EF measures underscores the need to consider executive abilities as relative strengths that may serve as compensatory factors for areas of normative or individual weakness when supporting individuals with HF-ASD. Finally, the significant variability in EF performance, which ranged from well below average to well above average, highlights the importance of examining individual differences in EFs both within groups of individuals with HF-ASD and within individuals themselves. Indeed, heterogeneity appears to be one of the most consistent patterns found among the executive abilities of the individuals with HF-ASD in this study.
Clinical Implications
Individualizing Assessment and Treatment
The heterogeneity in performance, relative to matched typically developing peers, on most EF measures in this study has important clinical implications. This heterogeneity suggests the adoption of a cognitive neuropsychological perspective (e.g., Towgood, Meuwese, Gilbert, Turner, & Burgess, 2009) that utilizes a neuropsychological case series approach (in which differences within individuals rather than across individuals are the basis for individualizing assessment and treatment planning) would be beneficial. As the use of group-level analysis alone in the study of EFs in ASD risks missing cognitive characteristics that may be both theoretically and clinically important for many individuals, and may even be misleading because of an “averaging artifact,” this approach instead focuses on intra- and interindividual profiles of performance. Consistent with this neuropsychological perspective, findings from the present study highlight the individual differences evident in EFs both within and between persons with HF-ASD. Practically speaking, this means each individual is likely to present with diverse executive skills, thus reinforcing that it is prudent to assess and treat using individualized approaches that appropriately address the broad range of EFs evident within these individuals.
Limitations
One should be mindful that the clinical sample studied here was representative of individuals with HF-ASD in the mid- to late-adolescent and early adulthood years and consequently, the results may not be generalizable to other developmental periods or clinical populations. In addition, many of the typically developing individuals who participated in this study were university students, and consequently, this community-based sample may not accurately reflect the broader typically developing population of young adults. Finally, the present study did not examine comorbidities in our sample such as concurrent attention and anxiety diagnoses, and how they may contribute to our research findings. Consequently, all conclusions drawn from this study should be done with these reservations in mind.
Future Research
Experimental and Longitudinal Research
The present study used a nonexperimental design, with primarily simple means comparisons. Consequently, causation was not directly examined. Although challenging in clinical research, future investigation of EFs in HF-ASD would benefit from randomized or quasi-randomized experimental designs that would allow for further exploration of the nature of EFs in HF-ASD. Furthermore, longitudinal study is needed to understand the developmental trajectories of EFs in the broader ASD population (i.e., those with and without intellectual and language impairments) and how they may (or may not) differ from those evident in typically developing populations, as well as other clinical populations (e.g., individuals with ADHD).
Individual Differences and Comparison Groups
The heterogeneity in performance of individuals with HF-ASD reported here suggests that future research would benefit from an examination of the applicability of the group performance to individual members of the group. Thus, base rate data may be much more useful than statistical significance results, particularly in clinical decision making. As seen in this study, aggregate group data do not always adequately represent the individual members of the group. Furthermore, the comparison group utilized can also have a significant impact on the findings. Hence, the choice of comparison group and an understanding of the individual differences that comprise both the control and target groups are critically important components for future research to consider.
Footnotes
Acknowledgements
Many thanks to an exceptional group of colleagues who made significant contributions to the data collection and entry involved in the larger tri-university research initiative of which this study was a part of. Dr. Yvonne Hindes, Ms. Jo-Anne Burt, and Ms. Candace Kohut deserve special mention for the critical role they played in the research consortium.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: 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.
