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Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncny20
Neurocognitive performance of children with higher functioning Autism Spectrum disorders on the NEPSY-II a
ab
a
Sarianna Barron-Linnankoski , Outi Reinvall , Anne Lahervuori , b
a
Arja Voutilainen , Pekka Lahti-Nuuttila & Marit Korkman
a
a
Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland b
Department of Pediatric and Adolescent Medicine, Helsinki University Central Hospital, Helsinki, Finland Published online: 08 Jan 2014.
To cite this article: Sarianna Barron-Linnankoski, Outi Reinvall, Anne Lahervuori, Arja Voutilainen, Pekka Lahti-Nuuttila & Marit Korkman (2015) Neurocognitive performance of children with higher functioning Autism Spectrum disorders on the NEPSY-II, Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, 21:1, 55-77, DOI: 10.1080/09297049.2013.873781 To link to this article: http://dx.doi.org/10.1080/09297049.2013.873781
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/termsand-conditions
Child Neuropsychology, 2015 Vol. 21, No. 1, 55–77, http://dx.doi.org/10.1080/09297049.2013.873781
Neurocognitive performance of children with higher functioning Autism Spectrum disorders on the NEPSY-II
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Sarianna Barron-Linnankoski1, Outi Reinvall1,2, Anne Lahervuori1, Arja Voutilainen2, Pekka Lahti-Nuuttila1, and Marit Korkman1† 1
Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland Department of Pediatric and Adolescent Medicine, Helsinki University Central Hospital, Helsinki, Finland
2
This study examined patterns of strengths and weaknesses in the neurocognitive performance of children with higher functioning autism spectrum disorder (ASD). The participants were 30 children with higher functioning ASD ranging from 6 to 11 years, and 60 typically developing (TD) children, who were matched with the children with higher functioning ASD in terms of age, gender, and maternal education. The TD children were drawn from the Finnish standardization sample for the NEPSY-II. The cognitive abilities of the children with higher functioning ASD were assessed with the WISC-III, and the neurocognitive performance of the children with higher functioning ASD and TD children on the NEPSY-II was compared. The children with higher functioning ASD were found to have strengths in verbal reasoning skills with respect to the population mean and weaknesses in setshifting, verbal fluency, and narrative memory in comparison with the TD children. Minor weaknesses were also observed in facial memory and fine and visuomotor skills. Keywords: Autism spectrum disorder; Asperger syndrome; Neurocognitive performance; Children; NEPSY-II.
Autism spectrum disorders (ASD) are characterized by core impairments in social communication and interaction and restricted repetitive behaviors (Hyman, 2013). The term high-functioning ASD has often been used to refer to individuals with Asperger syndrome, High-Functioning Autism (HFA), and Pervasive Developmental Disorders Not Otherwise Specified (PDDNOS; Oliveras-Rentas, Kenworthy, Roberson, Martin, & Wallace, 2012; Scheeren, Koot, & Begeer, 2012; Volker et al., 2010). These individuals demonstrate normal range intelligence. Asperger syndrome has been considered to differ †Deceased This study was supported by the Finska Läkaresällskapet, the Emil Aaltonen Foundation, and the Sigrid Jusélius Foundation. We thank all the children and parents who participated in the study. We express our gratitude to Lennart von Wendt† for his dedication to this project. We also warmly thank Susan Laitala, Annina Mara, Annina Marila, and Mia Nykopp for participation in data collection; Taina Nieminen-von Wendt for her collaboration; and Laura Hokkanen for her comments on the manuscript. Address correspondence to Sarianna Barron-Linnankoski, Institute of Behavioural Sciences, P.O. Box 9, FI-00014 University of Helsinki, Finland. E-mail: [email protected]
© 2014 Taylor & Francis
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from HFA and PDDNOS by its relative preservation of linguistic development. In the last decades, a large body of research has focused on assessing whether Asperger syndrome can be separated from other ASDs, especially from HFA, with respect to neurophysiological, cognitive, and behavioral factors (Frith, 2004; Miller & Ozonoff, 2000; Ozonoff, South, & Miller, 2000; Planche & Lemonnier, 2012; Williams, Goldstein, Kojkowski, & Minshew, 2008). These studies indicate that Asperger syndrome belongs to the same continuum of autism spectrum and is not qualitatively separable from other ASDs. In line with this research, the new Diagnostic and Statistical Manual of Mental Disorders, fifth edition (DSM-V; American Psychological Association [APA], 2013) defines Asperger syndrome under a single umbrella disorder, Autism spectrum disorder (Hyman, 2013). In this study, we will use the term higher functioning ASD to refer to individuals with Asperger syndrome and HFA. Three core cognitive deficits have been considered to underlie behavioral characteristics and processing styles in individuals with ASD: deficits in executive functioning (EF), weak central coherence (WCC), and deficits in the theory of mind (ToM) skills. The term EF is typically used to refer to multiple cognitive functions that are especially important for responding in an adaptive way in nonroutine situations (Diamond, 2013; Lezak, 2004). These multiple cognitive functions include planning, inhibition, working memory, flexibility, initiation, and monitoring actions (Hill, 2004; Rabbitt, 1997). Deficits in EFs are considered to underlie many nonsocial and social characteristics of ASD (Frith, 2004; Hill, 2004). Impairments in EFs have been suggested to account for symptoms such as rigidity, stereotyped behaviors, routines, and restricted interests (Hill, 2004; Lopez, Lincoln, Ozonoff, & Lai, 2005). In other words, individuals with ASD may have difficulty coping with nonroutine situations due to their EF deficits and often prefer routine situations, exhibit repetitive actions and benefit from external structure (Hill, 2004). With respect to social characteristics, the relationship between EF and ToM has been much discussed. Studies concerning typically developing (TD) children indicate that performance in EF tasks predicts performance in ToM tasks but the performance in ToM tasks does not predict the performance in EF tasks (Hughes, 1998; Hughes & Ensor, 2007). Similar results have also been found in children with higher functioning autism (Pellicano, 2007). However, the nature of the EF-ToM relationship is still not clear (Hill, 2004; Pellicano, 2007). The WCC theory introduced by Frith (1989, 2003) has been suggested to account for symptoms such as attention to detail, “islets of ability,” detachment from context, and reduced top-down processing. In relation to WCC, individuals with ASD have been suggested to have weakness in making global inferences from stories (Happé, 1994; Jolliffe & Baron-Cohen, 2000; Norbury & Bishop, 2002) and subtle impairments in visual processing abilities, such as visual discrimination, spatial vision, and motion perception (Dakin & Frith, 2005; Happé & Frith, 2006; Simmons et al., 2009) in comparison to TD individuals. Also, the tendency for local processing has been suggested to affect recognition of faces (Deruelle, Rondan, Gepner, & Tardif, 2004; Rondan & Deruelle, 2007) and facial emotions (Happé & Frith, 2006) in children with higher functioning ASD. Deficits in ToM skills have been suggested to account for the social impairment that individuals with ASD have in the ability to attribute mental states to other people and in understanding that other people may have mental states different from one´s own (BaronCohen, 2000; Baron-Cohen, Leslie, & Frith, 1985; Leslie & Frith, 1988). It is currently thought that these three core cognitive constructs, namely EF, WCC, and ToM, are complementary rather than mutually exclusive in explaining the processing abnormalities in persons with ASD (Frith, 2003).
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Apart from research on these core cognitive constructs, evidence of strengths and weaknesses in the neurocognitive performance in individuals with ASD has accumulated in the last decades. Only few studies have investigated the comprehensive neurocognitive performance of children with higher functioning ASD. In a study by Hooper, Poon, Marcus, and Fine (2006), a reanalysis of the validation study of the NEPSY – A Developmental Neuropsychological Assessment (NEPSY; Korkman, Kirk, & Kemp, 1998), a comprehensive, pediatric, and multidomain neuropsychological battery, the children with higher functioning ASD (HFA) showed significantly poorer performance than control children in the NEPSY subtests of attention and executive functions, language, memory and learning, sensorimotor functions, and visuospatial processing. Also, in a study by Narzisi, Muratori, Calderoni, Fabbro, and Urgesi (2012), children with higher functioning ASD (Autistic Disorder or PDDNOS) were found to have widespread neuropsychological impairments on the NEPSY-II (Korkman, Kirk, & Kemp, 2007) in subtests of attention and executive functions, language, learning and memory, sensorimotor processing, and social perception. Williams, Goldstein and Minshew (2006) compared the performance of children with higher functioning ASD (HFA) and control children in a wide range of neurocognitive tasks. Children with higher functioning ASD were found to have impairments in complex language, complex memory, sensory-perceptual, and motor domains. More studies have focused on single domains of neurocognitive performance. In the domain of attention and EF, many studies in children and adults with higher functioning ASD report difficulties in tasks requiring planning and mental flexibility (Ambery, Russell, Perry, Morris, & Murphy, 2006; Corbett, Constantine, Hendren, Rocke, & Ozonoff, 2009; Geurts, Verté, Oosterlaan, Roeyers, & Sergeant, 2004; Hill & Bird, 2006; Kenworthy et al., 2005; Miller & Ozonoff, 2000; Ozonoff & Jensen, 1999; Sinzig, Morsch, Bruning, Schmidt, & Lehmkuhl, 2008; Szatmari, Tuff, Finlayson, & Bartolucci, 1990; Verté, Geurts, Roeyers, Oosterlaan, & Sergeant, 2006). With respect to inhibitory control, some studies have reported deficient functioning (Geurts et al., 2004; Johnson et al., 2007), while others have failed to find any differences between individuals with higher functioning ASD and TD individuals (Ambery et al., 2006; Bishop & Norbury, 2005; Hill & Bird, 2006; Ozonoff & Jensen, 1999). Studies on fluency in children and adults have also offered mixed findings of intact and impaired abilities in both design and verbal fluency (Ambery et al., 2006; Happé, Booth, Charlton, & Hughes, 2006; Hill & Bird, 2006; Kleinhans, Akshoomoff, & Delis, 2005; Robinson, Goddard, Dritschel, Wisley, & Howlin, 2009; Verté et al., 2006). Regarding language abilities little research has focused on examining basic receptive and expressive skills in children with higher functioning ASD, especially regarding children previously diagnosed with Asperger syndrome. A study by Szatmari, Archer, Fisman, Streiner, and Wilson (1995) showed that children with Asperger syndrome performed just below normal or within a standard deviation of normal scores in a variety of tasks measuring receptive and expressive language skills. Saalasti et al.’s study (2008) found that children with Asperger syndrome demonstrated more difficulties in following verbal instructions in comparison to TD children. Noterdaeme, Wriedt, and Höhne´s study (2010) showed that children with HFA had more receptive and expressive language difficulties than children with Asperger syndrome, yet more than 30% of the children with Asperger syndrome had difficulties in receptive language tasks of word and sentence comprehension. A larger body of research has focused on deficits in the social use of language, or in pragmatics, in children with higher functioning ASD (Adams, Green, Gilchrist, & Cox, 2002; Landa, 2000).
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Regarding memory and learning, the findings on the performance of children with higher functioning ASD in working memory tasks have been mixed. Studies on verbal working memory have provided evidence of normal capacity or strength (e.g., Cui, Gao, Chen, Zou, & Wang, 2010; Williams, Goldstein, Carpenter, & Minshew, 2005; Zinke et al., 2010) and weakness (Alloway, Rajendran, & Archibald, 2009; Manjiviona & Prior, 1999). As to more complex verbal material, children with higher functioning ASD have been reported to have more difficulties than TD children in story memory tasks (Fein et al., 1996; Williams et al., 2006). Studies concerning visuospatial working memory have also yielded evidence of both preserved (Alloway et al., 2009; Geurts et al., 2004; Ozonoff & Strayer, 2001) and impaired (Cui et al., 2010; Goldberg et al., 2005; Williams et al., 2005; Zinke et al., 2010) performance in children with higher functioning ASD. Children with higher functioning ASD have been observed to have deficits in facial recognition memory (Kuusikko-Gauffin et al., 2011; Szatmari et al., 1990; Wolf et al., 2008) although spared performance has also been reported (O´Hearn, Schroer, Minshew, & Luna, 2010). Deficits in gross and fine motor skills and in visual-motor integration skills have been frequently reported in children with higher functioning ASD (Gillberg, 1989; Ham, Corley, Rajendran, Carletta, & Swanson, 2008; Klin, Volkmar, Sparrow, Cichetti, & Rourke, 1995; Lopata, Hamm, Volker, & Sowinski, 2007; Manjiviona & Prior, 1995; Szatmari, Bartolucci, & Bremner, 1989; Szatmari et al., 1990; Volker et al., 2010). In addition, children with higher functioning ASD have been found to have deficits in imitating hand postures and finger positions (Ham et al., 2008). Regarding social perception, individuals with higher functioning ASD have been reported to pass first and second order tests of theory of mind, involving inferring a person’s own mental state and reasoning about what one person thinks of another person’s thoughts (Bowler, 1992; Ozonoff, Pennington, & Rogers, 1991). BaronCohen, O´Riordan, Stone, Jones, and Plaisted (1999) proposed that children with higher functioning ASD have ToM deficits at a higher level than either first- or second-order false belief tasks. Children, adolescents, and adults with higher functioning ASD have been found to have impaired performance in Happé´s Strange Stories task that comprise higher order social communication such as pretense, jokes, white lies, indirect requests, figures of speech, and irony (Happé, 1994; Kaland et al., 2002). Further, children with ASD have been found to have difficulties in emotion recognition (Kuusikko-Gauffin et al., 2009; Rump, Giovanelli, Minshew, & Strauss, 2009). Also, qualitative differences in the ability to identify a range of emotions have been reported (Grossman, Klin, Carter, & Volkmar, 2000; Wong, Beidel, Sarver, & Sims, 2012). Research on visuospatial abilities in children with higher functioning ASD is relatively scant. While Klin et al. (1995) reported deficits in visuospatial abilities in children with Asperger syndrome, other studies have not found differences between children with higher functioning ASD and TD children (Edgin & Pennington, 2005; Semrud-Clikeman, Walkowiak, Wilkinson, & Christopher, 2010). Research on vision and visual perception in individuals with ASD has, however, provided evidence of subtle differences in visual processing capabilities between individuals with higher functioning ASD and TD individuals, although the findings have been somewhat varying (see Dakin & Frith, 2005; Simmons et al., 2009, for reviews). Altogether, the available data obtained by neurocognitive research in higher functioning individuals with ASD provide mainly specific information of single areas of
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functioning. Thus, not much is known about the comprehensive neurocognitive performance of these individuals across the whole spectrum of domains. In addition, most neurocognitive studies have included children and adolescents or children, adolescents, and adults pooled into the same sample instead of examining neurocognitive performance in narrower age ranges. Recent studies in individuals with higher functioning ASD indicate age-related changes in neurocognitive performance (Happé et al., 2006; Kuusikko-Gauffin et al., 2011). Hence, neurocognitive studies separately assessing children, adolescents, and adults with higher functioning ASD are needed. Finally, ASDs are commonly diagnosed during the early school years. This gives cause for further specification of the neurocognitive performance of young school-age children with higher functioning ASD. The purpose of the present study was to compare the neurocognitive performance of higher functioning children with ASD and TD children. We aimed at defining patterns of both strengths and weaknesses in the neurocognitive profile of children with higher functioning ASD. We also intended to evaluate the findings with respect to the three cognitive constructs, namely EF, WCC, and ToM, considered central to ASD. We attempted to take into account the aforementioned issues by assessing performance across the different neurocognitive domains using the developmental neuropsychological assessment NEPSY-II (Korkman, Kirk, & Kemp, 2008a) and by including only children in our sample. On the basis of earlier research, we expected higher functioning children with ASD to show deficits foremost in the subtests of attention and EF, social perception, and sensorimotor skills.
METHOD Participants Thirty children with Asperger syndrome were recruited from the Hospital for Children and Adolescents at the Pediatric Neurology Unit in Helsinki University Central Hospital (HUCH) and from a private neuropsychiatric center in Helsinki for the higher functioning ASD group. The inclusion criteria for the higher functioning ASD group were (a) age between 6 years 0 months and 11 years 11 months and (b) a clinical diagnosis of Asperger syndrome. The age limit of 11 years 11 months was selected for the present study because there is evidence that pubertal timing, which is often used to define the onset of adolescence, takes place at the age 12 or 13 in the majority of individuals (Bellis, Downing, & Ashton, 2006; Patton & Viner, 2007). Furthermore, in other neurocognitive studies, 12-year-old participants have also been included in the “older” or adolescent group (Happé et al., 2006; Kuusikko-Gauffin et al., 2011). The exclusion criteria for the higher functioning ASD group included diagnoses of major genetic (e.g., Fragile X) or neurologic (e.g., epilepsy) disorders. Prior to the study, participants had been clinically diagnosed with Asperger syndrome based on the criteria of the International Statistical Classification of Diseases and Related Health Problems, 10th revision (ICD-10; World Health Organization [WHO], 1993) by experienced child neurologists and/or multidisciplinary teams in the field of child neurology. The average age of receiving the clinical Asperger syndrome diagnosis was 7.5 years. In this study, the clinical diagnoses of Asperger syndrome were confirmed based on both standard ICD-10 (WHO, 1993) and Diagnostic and Statistical Manual of
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Mental Disorders, fourth edition (DSM-IV; American Psychological Association [APA], 1994) at clinical case conferences together with the qualified nurses, psychologists, and/or neuropsychologists who participated in the data collection and the senior pediatric neurologist responsible for the research project. The Autism Diagnostic InterviewRevised (ADI-R; Lord, Rutter, & LeCouteur, 1994; Rutter, LeCouteur, & Lord, 2003) and the patient medical records were used as supplementary sources of diagnostic criteria. The ADI-R was conducted as a part of this study if it had not been done previously during the clinical diagnostic procedures. All participants showed no early language delays and attended mainstream schools. One child had a diagnosis of a mild unilateral sensorineural hearing loss according to patient medical records. Eight children were diagnosed with attention deficit disorder, and 5 children were diagnosed with specific learning disorder based on the patient medical records. Of the specific learning disorders, 4 children had difficulties in reading, and 1 child had difficulties in visual perception. Three participants were taking psychostimulant medication according to parent reports. Maternal education levels were divided into low (elementary or comprehensive school), medium (matriculation examination or vocational education), and high (polytechnic or university education). Sixty TD children were selected from the appropriate strata of the standardization sample of the Finnish version of the NEPSY-II: A Developmental Neuropsychological Assessment, second edition (Korkman et al., 2008a). First, potential TD children for the TD group were selected to match each child in the higher functioning ASD group as carefully as possible for age, gender, and maternal education. Then, 2 TD children for each child with Asperger syndrome were randomly selected from the potential TD children. The standardization sample was recruited during the years 2006 and 2007. It consisted of 923 TD children aged between 3 and 15, except for the age groups of 10, 12, and 14 years. Therefore, each 10-year-old child with Asperger Syndrome (n = 8) in our study was matched as consistently as possible with one 9-year-old and one 11-year-old TD child. In the other age groups, the age difference between each child with Asperger syndrome and the matched TD children was within 6 months. On the basis of patient medical records or parent reports, all TD children attended regular school classes and had no language or learning difficulties, nor any neurologic or psychiatric diagnoses based on parent reports. The demographic variables of the higher functioning ASD and TD groups are summarized in Table 1.
Table 1 Demographic Variables for the ASD and TD Groups. Background Data Age in years M (SD) Range Gender Boys n (%) Girls n (%) Maternal Education Low n (%) Medium n (%) High n (%)
ASD (n = 30)
TD (n = 60)
9.1 (1.3) 6.6–11.1
9.1 (1.4) 6.2–11.2
28 (93.3) 2 (6.7)
56 (93.3) 4 (6.7)
2 (6.7) 9 (30.0) 19 (63.3)
4 (6.7) 18 (30.0) 38 (63.3)
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Measures General cognitive abilities of the individuals with higher functioning ASD were assessed with eight subtests of the Finnish version of the Wechsler Intelligence Scale for Children, third edition (WISC-III; Wechsler, 1999). The full battery of WISC-III subtests was not administered due to time constraints. Our selection of specific WISC-III subtests was based on psychometric and clinical rationale, as well as on previous studies concerning intellectual functioning in individuals with higher functioning ASD. We selected eight subtests on the basis of psychometric rationale in order to obtain more valid and reliable estimates of Full Scale IQ (FSIQ), Verbal IQ (VIQ), and Performance IQ (PIQ) in comparison to shorter versions of the WISC-III (Sattler, 2001). We selected four verbal and four performance subtests in order to acquire information equally from both of these domains. Further, based on clinical rationale and previous studies, we selected specific WISC-III subtests with regard to research findings of cognitive strengths and weaknesses in individuals with higher functioning ASD (Barnhill, Hagiwara, Myles, & Simpson, 2000; Ghaziuddin & Mountain-Kimchi, 2004; Noterdaeme et al., 2010) and administration length of the subtests. The eight WISC-III subtests selected for the purposes of this study were Information, Similarities, Arithmetic, Comprehension, Picture Completion, Coding, Block Design, and Object Assembly. The Finnish version of WISC-IV was not yet available at that time. Neurocognitive performance was assessed with the Finnish version of the NEPSY-II (Korkman et al., 2008a). The NEPSY-II is a comprehensive neuropsychological assessment comprising 29 subtests from six domains of performance: attention and EF, language, memory and learning, sensorimotor skills, social perception, and visuospatial processing. In this study, 16 age-appropriate NEPSY-II subtests, two to four subtests from each domain, were chosen in order to provide a comprehensive neuropsychological profile. The Auditory Attention and Response Set consisted two parts, which were analyzed separately, and the Inhibition subtest consisted of three parts, which were also analyzed separately, thus adding up to 19 NEPSY-II subtests. The NEPSY- II subtests administered in this study were Auditory Attention and Response Set, Design Fluency, Inhibition (i.e., Inhibition Naming, Inhibition, and Inhibition Switching) and Visual Attention in the Attention and EF domain; Comprehension of Instructions and Word Generation in the Language domain; Memory for Designs, Memory for Faces, and Narrative Memory in the Memory and Learning domain; Imitating Hand Positions and Visuomotor Precision in the Sensorimotor domain; Affect Recognition and Theory of Mind in the Social Perception domain; and Design Copying, Picture Puzzles, and Geometric Puzzles in the Visuospatial Processing domain. Subtests were selected on the basis of the EF, WCC, and ToM theories about ASD and previous research on higher functioning ASD. In addition, the selection of subtests was influenced by the findings of the “special group” study on children with Asperger Syndrome reported in the NEPSY-II, United States edition (Korkman et al., 2007). A standard score of ≥ 8 represented an average or above average performance, a standard score of 6 or 7 slightly below average, and a score of 5 or below significantly below average (Korkman, Kirk, & Kemp, 2008b).
Procedure Ethical approval for the study was given by the ethics review board at HUCH. All participants and parents received written information about the study. The information
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letter for children was specifically designed for them by making it shorter and using easier vocabulary than in the information letter designed for parents. All children received their own assent form, and parents received their own consent form. In addition, children and parents received oral information about the study prior to the assessments. Written informed consent was obtained from at least one caregiver of the children. Children participated voluntarily. Additionally, the majority of children (80%) gave written assent. The parents also filled a data form on demographic, educational, and medical variables. The parental ADI-R interviews were conducted by trained professionals, who were psychologists or qualified nurses. The WISC-III and NEPSY-II assessments were conducted for the participants with higher functioning ASD in approximately three sessions, each session lasting 1.5 hours. Statistical Analysis Statistical analyses were performed with the SPSS software (PASW 18; SPSS Inc., Chicago, IL). The missing values of the NEPSY-II subtest scores were replaced using the regression method imputation function in SPSS based on all NEPSY-II variables, age, gender, and maternal education. Imputation was carried out for 11 randomly missing values of the 1676 observations (
Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncny20
Neurocognitive performance of children with higher functioning Autism Spectrum disorders on the NEPSY-II a
ab
a
Sarianna Barron-Linnankoski , Outi Reinvall , Anne Lahervuori , b
a
Arja Voutilainen , Pekka Lahti-Nuuttila & Marit Korkman
a
a
Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland b
Department of Pediatric and Adolescent Medicine, Helsinki University Central Hospital, Helsinki, Finland Published online: 08 Jan 2014.
To cite this article: Sarianna Barron-Linnankoski, Outi Reinvall, Anne Lahervuori, Arja Voutilainen, Pekka Lahti-Nuuttila & Marit Korkman (2015) Neurocognitive performance of children with higher functioning Autism Spectrum disorders on the NEPSY-II, Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, 21:1, 55-77, DOI: 10.1080/09297049.2013.873781 To link to this article: http://dx.doi.org/10.1080/09297049.2013.873781
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/termsand-conditions
Child Neuropsychology, 2015 Vol. 21, No. 1, 55–77, http://dx.doi.org/10.1080/09297049.2013.873781
Neurocognitive performance of children with higher functioning Autism Spectrum disorders on the NEPSY-II
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Sarianna Barron-Linnankoski1, Outi Reinvall1,2, Anne Lahervuori1, Arja Voutilainen2, Pekka Lahti-Nuuttila1, and Marit Korkman1† 1
Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland Department of Pediatric and Adolescent Medicine, Helsinki University Central Hospital, Helsinki, Finland
2
This study examined patterns of strengths and weaknesses in the neurocognitive performance of children with higher functioning autism spectrum disorder (ASD). The participants were 30 children with higher functioning ASD ranging from 6 to 11 years, and 60 typically developing (TD) children, who were matched with the children with higher functioning ASD in terms of age, gender, and maternal education. The TD children were drawn from the Finnish standardization sample for the NEPSY-II. The cognitive abilities of the children with higher functioning ASD were assessed with the WISC-III, and the neurocognitive performance of the children with higher functioning ASD and TD children on the NEPSY-II was compared. The children with higher functioning ASD were found to have strengths in verbal reasoning skills with respect to the population mean and weaknesses in setshifting, verbal fluency, and narrative memory in comparison with the TD children. Minor weaknesses were also observed in facial memory and fine and visuomotor skills. Keywords: Autism spectrum disorder; Asperger syndrome; Neurocognitive performance; Children; NEPSY-II.
Autism spectrum disorders (ASD) are characterized by core impairments in social communication and interaction and restricted repetitive behaviors (Hyman, 2013). The term high-functioning ASD has often been used to refer to individuals with Asperger syndrome, High-Functioning Autism (HFA), and Pervasive Developmental Disorders Not Otherwise Specified (PDDNOS; Oliveras-Rentas, Kenworthy, Roberson, Martin, & Wallace, 2012; Scheeren, Koot, & Begeer, 2012; Volker et al., 2010). These individuals demonstrate normal range intelligence. Asperger syndrome has been considered to differ †Deceased This study was supported by the Finska Läkaresällskapet, the Emil Aaltonen Foundation, and the Sigrid Jusélius Foundation. We thank all the children and parents who participated in the study. We express our gratitude to Lennart von Wendt† for his dedication to this project. We also warmly thank Susan Laitala, Annina Mara, Annina Marila, and Mia Nykopp for participation in data collection; Taina Nieminen-von Wendt for her collaboration; and Laura Hokkanen for her comments on the manuscript. Address correspondence to Sarianna Barron-Linnankoski, Institute of Behavioural Sciences, P.O. Box 9, FI-00014 University of Helsinki, Finland. E-mail: [email protected]
© 2014 Taylor & Francis
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from HFA and PDDNOS by its relative preservation of linguistic development. In the last decades, a large body of research has focused on assessing whether Asperger syndrome can be separated from other ASDs, especially from HFA, with respect to neurophysiological, cognitive, and behavioral factors (Frith, 2004; Miller & Ozonoff, 2000; Ozonoff, South, & Miller, 2000; Planche & Lemonnier, 2012; Williams, Goldstein, Kojkowski, & Minshew, 2008). These studies indicate that Asperger syndrome belongs to the same continuum of autism spectrum and is not qualitatively separable from other ASDs. In line with this research, the new Diagnostic and Statistical Manual of Mental Disorders, fifth edition (DSM-V; American Psychological Association [APA], 2013) defines Asperger syndrome under a single umbrella disorder, Autism spectrum disorder (Hyman, 2013). In this study, we will use the term higher functioning ASD to refer to individuals with Asperger syndrome and HFA. Three core cognitive deficits have been considered to underlie behavioral characteristics and processing styles in individuals with ASD: deficits in executive functioning (EF), weak central coherence (WCC), and deficits in the theory of mind (ToM) skills. The term EF is typically used to refer to multiple cognitive functions that are especially important for responding in an adaptive way in nonroutine situations (Diamond, 2013; Lezak, 2004). These multiple cognitive functions include planning, inhibition, working memory, flexibility, initiation, and monitoring actions (Hill, 2004; Rabbitt, 1997). Deficits in EFs are considered to underlie many nonsocial and social characteristics of ASD (Frith, 2004; Hill, 2004). Impairments in EFs have been suggested to account for symptoms such as rigidity, stereotyped behaviors, routines, and restricted interests (Hill, 2004; Lopez, Lincoln, Ozonoff, & Lai, 2005). In other words, individuals with ASD may have difficulty coping with nonroutine situations due to their EF deficits and often prefer routine situations, exhibit repetitive actions and benefit from external structure (Hill, 2004). With respect to social characteristics, the relationship between EF and ToM has been much discussed. Studies concerning typically developing (TD) children indicate that performance in EF tasks predicts performance in ToM tasks but the performance in ToM tasks does not predict the performance in EF tasks (Hughes, 1998; Hughes & Ensor, 2007). Similar results have also been found in children with higher functioning autism (Pellicano, 2007). However, the nature of the EF-ToM relationship is still not clear (Hill, 2004; Pellicano, 2007). The WCC theory introduced by Frith (1989, 2003) has been suggested to account for symptoms such as attention to detail, “islets of ability,” detachment from context, and reduced top-down processing. In relation to WCC, individuals with ASD have been suggested to have weakness in making global inferences from stories (Happé, 1994; Jolliffe & Baron-Cohen, 2000; Norbury & Bishop, 2002) and subtle impairments in visual processing abilities, such as visual discrimination, spatial vision, and motion perception (Dakin & Frith, 2005; Happé & Frith, 2006; Simmons et al., 2009) in comparison to TD individuals. Also, the tendency for local processing has been suggested to affect recognition of faces (Deruelle, Rondan, Gepner, & Tardif, 2004; Rondan & Deruelle, 2007) and facial emotions (Happé & Frith, 2006) in children with higher functioning ASD. Deficits in ToM skills have been suggested to account for the social impairment that individuals with ASD have in the ability to attribute mental states to other people and in understanding that other people may have mental states different from one´s own (BaronCohen, 2000; Baron-Cohen, Leslie, & Frith, 1985; Leslie & Frith, 1988). It is currently thought that these three core cognitive constructs, namely EF, WCC, and ToM, are complementary rather than mutually exclusive in explaining the processing abnormalities in persons with ASD (Frith, 2003).
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Apart from research on these core cognitive constructs, evidence of strengths and weaknesses in the neurocognitive performance in individuals with ASD has accumulated in the last decades. Only few studies have investigated the comprehensive neurocognitive performance of children with higher functioning ASD. In a study by Hooper, Poon, Marcus, and Fine (2006), a reanalysis of the validation study of the NEPSY – A Developmental Neuropsychological Assessment (NEPSY; Korkman, Kirk, & Kemp, 1998), a comprehensive, pediatric, and multidomain neuropsychological battery, the children with higher functioning ASD (HFA) showed significantly poorer performance than control children in the NEPSY subtests of attention and executive functions, language, memory and learning, sensorimotor functions, and visuospatial processing. Also, in a study by Narzisi, Muratori, Calderoni, Fabbro, and Urgesi (2012), children with higher functioning ASD (Autistic Disorder or PDDNOS) were found to have widespread neuropsychological impairments on the NEPSY-II (Korkman, Kirk, & Kemp, 2007) in subtests of attention and executive functions, language, learning and memory, sensorimotor processing, and social perception. Williams, Goldstein and Minshew (2006) compared the performance of children with higher functioning ASD (HFA) and control children in a wide range of neurocognitive tasks. Children with higher functioning ASD were found to have impairments in complex language, complex memory, sensory-perceptual, and motor domains. More studies have focused on single domains of neurocognitive performance. In the domain of attention and EF, many studies in children and adults with higher functioning ASD report difficulties in tasks requiring planning and mental flexibility (Ambery, Russell, Perry, Morris, & Murphy, 2006; Corbett, Constantine, Hendren, Rocke, & Ozonoff, 2009; Geurts, Verté, Oosterlaan, Roeyers, & Sergeant, 2004; Hill & Bird, 2006; Kenworthy et al., 2005; Miller & Ozonoff, 2000; Ozonoff & Jensen, 1999; Sinzig, Morsch, Bruning, Schmidt, & Lehmkuhl, 2008; Szatmari, Tuff, Finlayson, & Bartolucci, 1990; Verté, Geurts, Roeyers, Oosterlaan, & Sergeant, 2006). With respect to inhibitory control, some studies have reported deficient functioning (Geurts et al., 2004; Johnson et al., 2007), while others have failed to find any differences between individuals with higher functioning ASD and TD individuals (Ambery et al., 2006; Bishop & Norbury, 2005; Hill & Bird, 2006; Ozonoff & Jensen, 1999). Studies on fluency in children and adults have also offered mixed findings of intact and impaired abilities in both design and verbal fluency (Ambery et al., 2006; Happé, Booth, Charlton, & Hughes, 2006; Hill & Bird, 2006; Kleinhans, Akshoomoff, & Delis, 2005; Robinson, Goddard, Dritschel, Wisley, & Howlin, 2009; Verté et al., 2006). Regarding language abilities little research has focused on examining basic receptive and expressive skills in children with higher functioning ASD, especially regarding children previously diagnosed with Asperger syndrome. A study by Szatmari, Archer, Fisman, Streiner, and Wilson (1995) showed that children with Asperger syndrome performed just below normal or within a standard deviation of normal scores in a variety of tasks measuring receptive and expressive language skills. Saalasti et al.’s study (2008) found that children with Asperger syndrome demonstrated more difficulties in following verbal instructions in comparison to TD children. Noterdaeme, Wriedt, and Höhne´s study (2010) showed that children with HFA had more receptive and expressive language difficulties than children with Asperger syndrome, yet more than 30% of the children with Asperger syndrome had difficulties in receptive language tasks of word and sentence comprehension. A larger body of research has focused on deficits in the social use of language, or in pragmatics, in children with higher functioning ASD (Adams, Green, Gilchrist, & Cox, 2002; Landa, 2000).
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Regarding memory and learning, the findings on the performance of children with higher functioning ASD in working memory tasks have been mixed. Studies on verbal working memory have provided evidence of normal capacity or strength (e.g., Cui, Gao, Chen, Zou, & Wang, 2010; Williams, Goldstein, Carpenter, & Minshew, 2005; Zinke et al., 2010) and weakness (Alloway, Rajendran, & Archibald, 2009; Manjiviona & Prior, 1999). As to more complex verbal material, children with higher functioning ASD have been reported to have more difficulties than TD children in story memory tasks (Fein et al., 1996; Williams et al., 2006). Studies concerning visuospatial working memory have also yielded evidence of both preserved (Alloway et al., 2009; Geurts et al., 2004; Ozonoff & Strayer, 2001) and impaired (Cui et al., 2010; Goldberg et al., 2005; Williams et al., 2005; Zinke et al., 2010) performance in children with higher functioning ASD. Children with higher functioning ASD have been observed to have deficits in facial recognition memory (Kuusikko-Gauffin et al., 2011; Szatmari et al., 1990; Wolf et al., 2008) although spared performance has also been reported (O´Hearn, Schroer, Minshew, & Luna, 2010). Deficits in gross and fine motor skills and in visual-motor integration skills have been frequently reported in children with higher functioning ASD (Gillberg, 1989; Ham, Corley, Rajendran, Carletta, & Swanson, 2008; Klin, Volkmar, Sparrow, Cichetti, & Rourke, 1995; Lopata, Hamm, Volker, & Sowinski, 2007; Manjiviona & Prior, 1995; Szatmari, Bartolucci, & Bremner, 1989; Szatmari et al., 1990; Volker et al., 2010). In addition, children with higher functioning ASD have been found to have deficits in imitating hand postures and finger positions (Ham et al., 2008). Regarding social perception, individuals with higher functioning ASD have been reported to pass first and second order tests of theory of mind, involving inferring a person’s own mental state and reasoning about what one person thinks of another person’s thoughts (Bowler, 1992; Ozonoff, Pennington, & Rogers, 1991). BaronCohen, O´Riordan, Stone, Jones, and Plaisted (1999) proposed that children with higher functioning ASD have ToM deficits at a higher level than either first- or second-order false belief tasks. Children, adolescents, and adults with higher functioning ASD have been found to have impaired performance in Happé´s Strange Stories task that comprise higher order social communication such as pretense, jokes, white lies, indirect requests, figures of speech, and irony (Happé, 1994; Kaland et al., 2002). Further, children with ASD have been found to have difficulties in emotion recognition (Kuusikko-Gauffin et al., 2009; Rump, Giovanelli, Minshew, & Strauss, 2009). Also, qualitative differences in the ability to identify a range of emotions have been reported (Grossman, Klin, Carter, & Volkmar, 2000; Wong, Beidel, Sarver, & Sims, 2012). Research on visuospatial abilities in children with higher functioning ASD is relatively scant. While Klin et al. (1995) reported deficits in visuospatial abilities in children with Asperger syndrome, other studies have not found differences between children with higher functioning ASD and TD children (Edgin & Pennington, 2005; Semrud-Clikeman, Walkowiak, Wilkinson, & Christopher, 2010). Research on vision and visual perception in individuals with ASD has, however, provided evidence of subtle differences in visual processing capabilities between individuals with higher functioning ASD and TD individuals, although the findings have been somewhat varying (see Dakin & Frith, 2005; Simmons et al., 2009, for reviews). Altogether, the available data obtained by neurocognitive research in higher functioning individuals with ASD provide mainly specific information of single areas of
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functioning. Thus, not much is known about the comprehensive neurocognitive performance of these individuals across the whole spectrum of domains. In addition, most neurocognitive studies have included children and adolescents or children, adolescents, and adults pooled into the same sample instead of examining neurocognitive performance in narrower age ranges. Recent studies in individuals with higher functioning ASD indicate age-related changes in neurocognitive performance (Happé et al., 2006; Kuusikko-Gauffin et al., 2011). Hence, neurocognitive studies separately assessing children, adolescents, and adults with higher functioning ASD are needed. Finally, ASDs are commonly diagnosed during the early school years. This gives cause for further specification of the neurocognitive performance of young school-age children with higher functioning ASD. The purpose of the present study was to compare the neurocognitive performance of higher functioning children with ASD and TD children. We aimed at defining patterns of both strengths and weaknesses in the neurocognitive profile of children with higher functioning ASD. We also intended to evaluate the findings with respect to the three cognitive constructs, namely EF, WCC, and ToM, considered central to ASD. We attempted to take into account the aforementioned issues by assessing performance across the different neurocognitive domains using the developmental neuropsychological assessment NEPSY-II (Korkman, Kirk, & Kemp, 2008a) and by including only children in our sample. On the basis of earlier research, we expected higher functioning children with ASD to show deficits foremost in the subtests of attention and EF, social perception, and sensorimotor skills.
METHOD Participants Thirty children with Asperger syndrome were recruited from the Hospital for Children and Adolescents at the Pediatric Neurology Unit in Helsinki University Central Hospital (HUCH) and from a private neuropsychiatric center in Helsinki for the higher functioning ASD group. The inclusion criteria for the higher functioning ASD group were (a) age between 6 years 0 months and 11 years 11 months and (b) a clinical diagnosis of Asperger syndrome. The age limit of 11 years 11 months was selected for the present study because there is evidence that pubertal timing, which is often used to define the onset of adolescence, takes place at the age 12 or 13 in the majority of individuals (Bellis, Downing, & Ashton, 2006; Patton & Viner, 2007). Furthermore, in other neurocognitive studies, 12-year-old participants have also been included in the “older” or adolescent group (Happé et al., 2006; Kuusikko-Gauffin et al., 2011). The exclusion criteria for the higher functioning ASD group included diagnoses of major genetic (e.g., Fragile X) or neurologic (e.g., epilepsy) disorders. Prior to the study, participants had been clinically diagnosed with Asperger syndrome based on the criteria of the International Statistical Classification of Diseases and Related Health Problems, 10th revision (ICD-10; World Health Organization [WHO], 1993) by experienced child neurologists and/or multidisciplinary teams in the field of child neurology. The average age of receiving the clinical Asperger syndrome diagnosis was 7.5 years. In this study, the clinical diagnoses of Asperger syndrome were confirmed based on both standard ICD-10 (WHO, 1993) and Diagnostic and Statistical Manual of
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Mental Disorders, fourth edition (DSM-IV; American Psychological Association [APA], 1994) at clinical case conferences together with the qualified nurses, psychologists, and/or neuropsychologists who participated in the data collection and the senior pediatric neurologist responsible for the research project. The Autism Diagnostic InterviewRevised (ADI-R; Lord, Rutter, & LeCouteur, 1994; Rutter, LeCouteur, & Lord, 2003) and the patient medical records were used as supplementary sources of diagnostic criteria. The ADI-R was conducted as a part of this study if it had not been done previously during the clinical diagnostic procedures. All participants showed no early language delays and attended mainstream schools. One child had a diagnosis of a mild unilateral sensorineural hearing loss according to patient medical records. Eight children were diagnosed with attention deficit disorder, and 5 children were diagnosed with specific learning disorder based on the patient medical records. Of the specific learning disorders, 4 children had difficulties in reading, and 1 child had difficulties in visual perception. Three participants were taking psychostimulant medication according to parent reports. Maternal education levels were divided into low (elementary or comprehensive school), medium (matriculation examination or vocational education), and high (polytechnic or university education). Sixty TD children were selected from the appropriate strata of the standardization sample of the Finnish version of the NEPSY-II: A Developmental Neuropsychological Assessment, second edition (Korkman et al., 2008a). First, potential TD children for the TD group were selected to match each child in the higher functioning ASD group as carefully as possible for age, gender, and maternal education. Then, 2 TD children for each child with Asperger syndrome were randomly selected from the potential TD children. The standardization sample was recruited during the years 2006 and 2007. It consisted of 923 TD children aged between 3 and 15, except for the age groups of 10, 12, and 14 years. Therefore, each 10-year-old child with Asperger Syndrome (n = 8) in our study was matched as consistently as possible with one 9-year-old and one 11-year-old TD child. In the other age groups, the age difference between each child with Asperger syndrome and the matched TD children was within 6 months. On the basis of patient medical records or parent reports, all TD children attended regular school classes and had no language or learning difficulties, nor any neurologic or psychiatric diagnoses based on parent reports. The demographic variables of the higher functioning ASD and TD groups are summarized in Table 1.
Table 1 Demographic Variables for the ASD and TD Groups. Background Data Age in years M (SD) Range Gender Boys n (%) Girls n (%) Maternal Education Low n (%) Medium n (%) High n (%)
ASD (n = 30)
TD (n = 60)
9.1 (1.3) 6.6–11.1
9.1 (1.4) 6.2–11.2
28 (93.3) 2 (6.7)
56 (93.3) 4 (6.7)
2 (6.7) 9 (30.0) 19 (63.3)
4 (6.7) 18 (30.0) 38 (63.3)
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Measures General cognitive abilities of the individuals with higher functioning ASD were assessed with eight subtests of the Finnish version of the Wechsler Intelligence Scale for Children, third edition (WISC-III; Wechsler, 1999). The full battery of WISC-III subtests was not administered due to time constraints. Our selection of specific WISC-III subtests was based on psychometric and clinical rationale, as well as on previous studies concerning intellectual functioning in individuals with higher functioning ASD. We selected eight subtests on the basis of psychometric rationale in order to obtain more valid and reliable estimates of Full Scale IQ (FSIQ), Verbal IQ (VIQ), and Performance IQ (PIQ) in comparison to shorter versions of the WISC-III (Sattler, 2001). We selected four verbal and four performance subtests in order to acquire information equally from both of these domains. Further, based on clinical rationale and previous studies, we selected specific WISC-III subtests with regard to research findings of cognitive strengths and weaknesses in individuals with higher functioning ASD (Barnhill, Hagiwara, Myles, & Simpson, 2000; Ghaziuddin & Mountain-Kimchi, 2004; Noterdaeme et al., 2010) and administration length of the subtests. The eight WISC-III subtests selected for the purposes of this study were Information, Similarities, Arithmetic, Comprehension, Picture Completion, Coding, Block Design, and Object Assembly. The Finnish version of WISC-IV was not yet available at that time. Neurocognitive performance was assessed with the Finnish version of the NEPSY-II (Korkman et al., 2008a). The NEPSY-II is a comprehensive neuropsychological assessment comprising 29 subtests from six domains of performance: attention and EF, language, memory and learning, sensorimotor skills, social perception, and visuospatial processing. In this study, 16 age-appropriate NEPSY-II subtests, two to four subtests from each domain, were chosen in order to provide a comprehensive neuropsychological profile. The Auditory Attention and Response Set consisted two parts, which were analyzed separately, and the Inhibition subtest consisted of three parts, which were also analyzed separately, thus adding up to 19 NEPSY-II subtests. The NEPSY- II subtests administered in this study were Auditory Attention and Response Set, Design Fluency, Inhibition (i.e., Inhibition Naming, Inhibition, and Inhibition Switching) and Visual Attention in the Attention and EF domain; Comprehension of Instructions and Word Generation in the Language domain; Memory for Designs, Memory for Faces, and Narrative Memory in the Memory and Learning domain; Imitating Hand Positions and Visuomotor Precision in the Sensorimotor domain; Affect Recognition and Theory of Mind in the Social Perception domain; and Design Copying, Picture Puzzles, and Geometric Puzzles in the Visuospatial Processing domain. Subtests were selected on the basis of the EF, WCC, and ToM theories about ASD and previous research on higher functioning ASD. In addition, the selection of subtests was influenced by the findings of the “special group” study on children with Asperger Syndrome reported in the NEPSY-II, United States edition (Korkman et al., 2007). A standard score of ≥ 8 represented an average or above average performance, a standard score of 6 or 7 slightly below average, and a score of 5 or below significantly below average (Korkman, Kirk, & Kemp, 2008b).
Procedure Ethical approval for the study was given by the ethics review board at HUCH. All participants and parents received written information about the study. The information
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letter for children was specifically designed for them by making it shorter and using easier vocabulary than in the information letter designed for parents. All children received their own assent form, and parents received their own consent form. In addition, children and parents received oral information about the study prior to the assessments. Written informed consent was obtained from at least one caregiver of the children. Children participated voluntarily. Additionally, the majority of children (80%) gave written assent. The parents also filled a data form on demographic, educational, and medical variables. The parental ADI-R interviews were conducted by trained professionals, who were psychologists or qualified nurses. The WISC-III and NEPSY-II assessments were conducted for the participants with higher functioning ASD in approximately three sessions, each session lasting 1.5 hours. Statistical Analysis Statistical analyses were performed with the SPSS software (PASW 18; SPSS Inc., Chicago, IL). The missing values of the NEPSY-II subtest scores were replaced using the regression method imputation function in SPSS based on all NEPSY-II variables, age, gender, and maternal education. Imputation was carried out for 11 randomly missing values of the 1676 observations (
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