Neuropsychological functioning in adults with Asperger syndrome F I O N A Z . A M B E RY

Institute of Psychiatry, London, UK

A I L S A J. RU S S E L L K AT I E P E R RY ROBIN MORRIS

autism © 2006 SAGE Publications and The National Autistic Society Vol 10(6) 551–564; 068507 1362-3613(200611)10:6

Institute of Psychiatry, London, UK

University of East London, UK Institute of Psychiatry, London, UK

D E C L A N G. M . M U R P H Y

Institute of Psychiatry,

London, UK

There is some consensus in the literature regarding the cognitive profile of people with Asperger syndrome (AS). Findings to date suggest that a proportion of people with AS have higher verbal than performance IQ, a non-verbal learning disability (NVLD) and impairments in some aspects of executive function (EF). However, there are few published studies on adults with AS and many have compared the AS group to an autistic control group alone. We compared cognitive functioning in 27 AS adults without a history of language delay and 20 normal controls who did not differ significantly in age, gender and IQ. People with AS had significant impairments on a test of visual memory and on EF tasks measuring flexibility and generativity, but not inhibition. There was no significant difference between verbal and performance IQ. Our results suggest that impairments on tests requiring flexibility of thought and generation occur at all ages and across a range of autistic disorders including AS.

A B S T R AC T

K E Y WO R D S

Asperger syndrome; executive functioning; memory; neuropsychology

Correspondence should be addressed to: D R F I O N A Z . A M B E RY , Department of Psychological Medicine, PO Box 50, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, UK. e-mail: [email protected]

ADDRESS

Introduction There have been numerous studies of neuropsychological functioning in people with autistic spectrum disorders (ASD). These consistently report impairments in executive functioning (Liss et al., 2001; Ozonoff et al., 1994), with additional evidence of visuo-perceptual difficulties (Klin et al., 1995) and memory deficits (Blair et al., 2002; Williams et al., 2005). www.sagepublications.com DOI: 10.1177/1362361306068507

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10(6) However, there has been little research focused specifically on neuropsychological functioning in people with Asperger syndrome (AS), and in particular adults with this condition. Such studies have examined one aspect of cognitive functioning (Morris et al., 1999) or used an autistic control group rather than healthy controls (Klin et al., 1995). Thus, it has not yet been established whether the cognitive deficits found in children with AS also occur in adults and whether the specific cognitive deficits reported in studies comparing AS to HFA are also present when people with AS are compared to healthy controls. Studies of cognitive functioning in AS have shown: (1) similarities to people with a non-verbal learning disability (NVLD: a term describing a cluster of cognitive deficits in non-verbal functioning such as non-verbal problem solving and visuo-spatial functioning) (Voeller, 1986); (2) discrepancies between verbal and performance IQ (PIQ) scores in favour of verbal IQ (VIQ); and (3) impairments in executive functioning. Klin et al. (1995) suggested that abnormalities in the development of the right hemisphere in AS may perhaps underpin at least some of the clinical symptoms. However, Klin et al.’s study did not include healthy controls, and it is not clear whether non-verbal function is impaired in AS compared to a healthy population. Some studies reported that children and adolescents with AS have significantly higher VIQ than PIQ (Klin et al., 1995; Miller and Ozonoff, 2000), whereas others did not (Manjiviona and Prior, 1999). Tager-Flusberg and Joseph (2003) analysed the cognitive profiles of children with autistic disorders and found that verbal/non-verbal discrepancies in either direction were more common in this group than in normal controls. However, this study did not examine groups diagnosed as AS and HFA and it is not therefore known whether the discrepancy is more likely to be in the VIQ > PIQ direction in an AS group. A frequent finding in cognitive studies of people with ASD is impairment in aspects of executive function (EF). Included in the range of EF impairments are: (1) significantly more perseverative errors on the Wisconsin Card Sorting Test (WCST: Liss et al., 2001; Prior and Hoffmann, 1990; Rumsey, 1985; Shu et al., 2001) and a computerized attentional setshifting test (Hughes et al., 1994; Ozonoff et al., 2000; AS impaired but not HFA); (2) deficits in planning on the Tower of Hanoi or Tower of London tests (Hughes et al., 1994; Rumsey, 1985); (3) significantly reduced output on fluency tests (Rumsey and Hamburger, 1988; Turner, 1999); and (4) impairment in spatial working memory (Morris et al., 1999). By contrast, no deficits have been reported in response inhibition (Ozonoff and Jenson, 1999; Ozonoff and Strayer, 1997). Further, some studies comparing AS and HFA have found differential patterns of impairment on EF tasks. For example, deficits on tests of response inhibition have been found in HFA AU T I S M

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but not AS (Rinehart et al., 2002). Other studies have found no differences in executive functioning between AS and HFA (e.g. Manjiviona and Prior, 1999). In summary, there is evidence that children with AS may have specific cognitive deficits. However, many of the studies have used inexact diagnostic criteria and/or have not used a healthy control sample. Those studies examining adults with AS have explored single cognitive functions (Blair et al., 2002; Morris et al., 1999) or were prior to the DSM-IV and ICD-10 diagnostic criteria (Rumsey, 1985). To date, there appear to be no published studies of the full neuropsychological profile of a relatively homogeneous sample of adults with AS defined using recognized diagnostic criteria (e.g. ICD-10). Hence, we examined cognitive functioning in adults with AS. We hypothesized: (1) deficits on tests of visual memory and visual perceptual processing; (2) a verbal–performance IQ differential in favour of VIQ; and (3) EF deficits that affect tasks of set shifting and flexibility but not response inhibition.

Method Participants We recruited 27 adults with AS from a specialist assessment service at the South London and Maudsley NHS Trust (see Table 1 for sample characteristics). All participants were diagnosed by a psychiatrist (DM) and satisfied the first three ICD-10 (World Health Organization, 1992) criteria for AS, namely: (1) qualitative abnormalities in reciprocal social interaction; (2) restricted, repetitive and stereotyped patterns of behaviour, interests and activities; (3) no clinically significant general delay in spoken or receptive language or cognitive development. The study did not use the ICD-10 criterion 4, namely, not meeting the criteria for any other pervasive developmental disorder, because this would preclude a diagnosis of AS in nearly all cases. In keeping with other studies (Howlin, 2003; Kim et al.,

Table 1

Background characteristics of patient and control groups Sex M/F

AS (n = 27)

22/5

Controls (n = 20)

16/4

Mean (SD) range Age (years)

VIQ

PIQ

37.6 (14.6) 19–67 33.5 (12) 21–58

106.1 (15.7) 82–135 107.05 (13.1) 93–140

103.7 (19.2) 75–147 109.4 (18.5) 80–140

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10(6) 2000) we diagnosed people with AS who met criteria for autism but had no significant delay in language development. In addition, where parental informants were available we employed the Autism Diagnostic Instrument (ADI: Lord et al., 1994) (N = 12), and where participants were willing we also used the Autistic Diagnostic Observation Schedule (ADOS) (N = 4). Participants also brought documentation such as school reports to aid diagnosis. Any cases where there was no reliable informant regarding language development were excluded. All participants underwent mental state and physical examination, routine laboratory blood tests, chromosome analysis, and structural magnetic resonance imaging to exclude clinically detectable neuropathology. The AS group were compared to 20 normal controls who did not differ in age, sex, VIQ, PIQ and years of education. All subjects had a VIQ above 80, were medication/drug free, and had grossly intact language. We excluded people with: (1) developmental language delay, including dyslexia; (2) comorbid diagnoses of psychosis, attention deficit hyperactivity disorder, personality disorder and/or substance misuse; (3) physical or neurological impairments affecting brain function (e.g. epilepsy); and (4) genetic disorders such as fragile X syndrome. AU T I S M

Neuropsychological testing We administered tests of: (1) overall intellectual functioning (Canavan et al., 1986); (2) memory (recall and recognition in both verbal and visual modalities); (3) EF (including tests of response inhibition, generativity and mental flexibility); (4) language; and (5) visuo-spatial perception. General intellectual ability Canavan et al.’s (1986) short-form version of the Wechsler Adult Intelligence Scale–Revised (WAIS–R: Wechsler, 1986) was used, which comprises five subtests: vocabulary, comprehension, similarities, block design and object assembly. This provides prorated verbal, performance and full-scale IQ scores. Age-scaled scores for each subtest were also calculated. Memory tests The Doors and People Test of Verbal and Visual Recall and Recognition (Baddeley et al., 1994) was used. The battery divides into four separate sections yielding composite scores for verbal and visual memory, recall and recognition and forgetting. In addition, tests of prose recall and verbal associate learning were administered using the Wechsler Memory Scale–Revised (Wechsler, 1987) logical memory and verbal paired associates tests.

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Executive function 1 Stroop Colour-Word Reading Test (Trenerry et al., 1989). This version requires reading colour words followed by incongruent colour naming. The measure was the number of colours named in 120 seconds. 2 Wisconsin Card Sorting Test (WCST: Heaton et al., 1993). The study used the 128-card version with six set shifts across three sorting categories (colour, shape and number). The measures used were: (1) perseverative responses, (2) perseverative errors, (3) non-perseverative errors, (4) number of categories achieved and (5) failure to maintain set. 3 Controlled Oral Word Association Test (COWAT: Benton and Hamsher, 1989). The study used the letters F, A and S. Language comprehension The British Picture Vocabulary Scale–Revised (Dunn et al., 1997) was used. This requires pointing to one out of four pictures, given a single word. The total number of correct responses was used for the analysis. Visual perception Two tests were administered from the Visual Object and Space Perception Test (VOSP: Warrington and James, 1991), measuring visuo-spatial (cube analysis) and visual perception (object decision).

Procedure All tests were administered by trained psychologists (FA and KP) following standard instructions from the test manuals. Testing time was up to 21⁄2 hours and participants completed the tests in the same order on one occasion. Three controls and four AS subjects were unable to complete the Stroop due to colour-blindness. Statistical analysis Analysis was completed using the Statistical Package for Social Sciences for Windows version 11. Groups were compared using an independent sample t-test (two-tailed), with statistical significance defined as p < 0.05. To explore the profile of impairment the AS scores were transformed into Z-scores, based on the control data.

Results 1 Intellectual functioning. There were no significant differences between the two groups on measures of overall intellectual functioning (VIQ, t(d.f. 45) = 0.225, n.s.; PIQ, t(d.f. 45) = 1.02, n.s.; see Table 1) or on any of the WAIS–R subtests. The VIQ–PIQ discrepancy scores were 555

10(6) calculated by subtracting the PIQ score from the VIQ score. Thus, a positive score indicates that VIQ is higher than PIQ. There was no difference in the mean discrepancy score (control mean, –1.8 (22.7); AS mean, 2.37 (17.21); t(d.f. 45) = –0.717, n.s.). In the AS group the scores ranged from –33 to +30. The scores showed a relatively normal distribution, with 17 subjects having positive scores and 10 subjects having negative scores. Sixteen (59%) AS subjects had discrepancy scores that were greater than 12 points, as compared to 25 percent in the normal population (Grossman, 1983), with 10 showing VIQ > PIQ and six showing PIQ > VIQ. Memory. The AS group were not impaired on the Doors and People Verbal Memory Index (see Table 2). Also, there were no deficits on the WMS–R story recall test or paired associate learning tests. However, the AS group were impaired on the Doors and People Visual Memory Index (t(45) = 2.0, p < 0.05). Executive functioning. There was no significant group difference on the Stroop test interference score (see Table 2). However, on the WCST people with AS made more perseverative errors than controls (t(45) = –2.06, p < 0.05). The controls made more conceptual-level responses than the AS group (t(45) = 1.99, p < 0.05). The AS group produced fewer words on the verbal fluency test (t(45) = 2.05, p < 0.05). To determine whether the impairment might relate to language ability more generally, the verbal fluency measure was correlated with the BPVS score. There was no correlation in either group. Furthermore, the significant fluency result remained significant after covarying for BPVS score. Language comprehension. There were no significant group differences on the BPVS test of single-word comprehension than controls (see Table 2). Visual perception. People with AS were not significantly impaired on either the object decision test or the cube analysis test (see Table 2).

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Z-scores were calculated for the AS group (see Figure 1). The controls are represented as the line at zero. The mean AS scores for visual memory, BPVS and perseverative errors on the WCST are all greater than one standard deviation below the controls.

Discussion We investigated whether the cognitive deficits reported in children with AS are also found in adults, and whether these deficits exist when the AS group was compared to healthy controls rather than an autistic group. We specifically examined three hypotheses relating to previous findings, 556

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Table 2

Group means and differences on neuropsychological tests

Test

AS (n = 27) Mean (SD)

Control (n = 20) Mean (SD)

t

p

Doors and People Visual memory Verbal memory Recognition memory Recall memory Verbal forgetting Visual forgetting

8.8 (3.9) 9.9 (3.9) 9.3 (4.1) 9.3 (3.9) 10.3 (2.8) 10.9 (0.5)

10.6 (2.6) 9.8 (3.9) 9.8 (4.5) 10.7 (2.8) 10.8 (1.9) 10.4 (1.7)

2.008 –0.073 0.388 1.342 0.764 –1.169

0.05* 0.94 0.70 0.19 0.45 0.26

Wechsler Memory Scale–Revised Logical memory Verbal paired associates

22.7 (9.3) 17.7 (5.3)

23.1 (3.9) 19.0 (4.1)

0.183 0.828

0.86 0.41

Wisconsin Card Sorting Test Number of categories Perseverative errors Non-perseverative errors Conceptual-level responses

4.8 (1.6) 17.5 (20.1) 11.8 (12.8) 55.1 (14.1)

5.4 (1.3) 9.0 (6.4) 10.9 (12.3) 62.7 (12.0)

1.238 –2.064 –0.236 1.995

0.22 0.05* 0.814 0.05*

Verbal Fluency: total words produced

38.5 (11.8)

45.3 (10.0)

2.054

0.05*

Stroop Interference

96.2 (14.5)

101.7 (15.3)

1.148

0.258

146.5 (13.7)

152.6 (7.5)

1.889

0.07

17.3 (3.2) 9.5 (1.1)

18.6 (1.6) 9.7 (1.3)

1.613 0.505

0.12 0.616

BPVS VOSP Object decision Cube analysis

* Denotes significance at the 0.05 level (two-tailed).

namely: (1) that people with AS show cognitive deficits similar to those of an NVLD; (2) that people with AS tend to have a higher VIQ than PIQ; and (3) that they have deficits in executive functioning relating to cognitive flexibility but not to inhibition. Our findings supported only one of our initial hypotheses, that is, individuals with AS displayed executive function deficits on tasks of set shifting, word generation and flexibility but not on a test of response inhibition. The lack of specific impairment in visual perceptual functioning is not consistent with the hypothesis that neuropsychological deficits in AS are similar to those of an NVLD. However, the AS group were impaired on tests of visual memory. Previous studies of visual memory in ASD have 557

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PI Q

VI Q

ve se er -p on

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N

Z-score

ra tiv e Pe er rs ro ev rs er at iv e Er ro rs *

St ro op

flu en cy * al rb

Re ca ll

M em or y

BP VS Ve

–0.4

Re co gn itio n

Vi su al

–0.2

Ve rb al

M em or y

0

–0.8

–1 –1.2

–1.4 –1.6

Test

Figure 1 Z-score profile for Asperger group across neuropsychological tests * p < .01

consistently reported deficits in relation to recognition memory for faces (Boucher and Lewis, 1992). Additionally, Ameli et al. (1988) found impairments in recognition memory for abstract shapes, while Blair et al. (2002) reported intact recognition memory for leaves and buildings, but impairments for cats, horses and motorbikes. Blair et al. (2002) suggest the latter impairment relates to objects that have ‘agency’. However, the stimuli in the visual memory tests from the Doors and People memory battery do not have agency and this theory cannot therefore account for the results found in this study. Alternatively, poor visual memory could be explained as being due to loss of ‘central coherence’, hypothesized by Frith and Happé (1994) as a core cognitive deficit in ASD, and defined as a ‘lack of ability to draw together information so as to derive coherent and meaningful ideas’. Loss of central coherence could result in too much attention being paid to details of the pictures while the sense of the whole is lost, thus producing recognition and recall errors. In our study the AS group did not show a significant verbal–performance IQ discrepancy. Hence our results are not consistent with studies that have found higher VIQ than PIQ in children with AS (Klin et al., 1995; Ozonoff et al., 2000); but they were consistent with others (Manjiviona and Prior, 1999; Miller and Ozonoff, 2000) who also found no VIQ–PIQ discrepancy. However, the AS group were more likely to have a significant VIQ–PIQ discrepancy than a normal population (59% as opposed to 25%) but this could be in either direction (i.e. VIQ > PIQ or PIQ > VIQ). TagerFlusberg and Joseph (2003) also found that people with autistic disorder 558

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were more likely to have greater discrepancy scores than controls and found that the direction of the discrepancy was related to symptom severity and brain volume. Thus, future studies are required to examine the issue of VIQ–PIQ discrepancies in more detail and their relationship to anatomy and symptomatology. It has been found previously that differences between AS and HFA in language abilities decrease with age (Ozonoff et al., 2000; Szatmari et al., 1995) and this has been interpreted by Howlin (2003) as suggesting that the linguistic difficulties of AS become more apparent with age. It is possible that while VIQ and single-word comprehension was intact in our sample, more extensive investigation of language function would have revealed specific impairments. For example, Minshew et al. (1995) found that individuals with autistic disorder were able to perform adequately on tests of basic language but had deficits on more complex language tasks requiring comprehension and interpretation. Our results support other reports of EF deficits in people with ASD (Liss et al., 2001; Rumsey, 1985). Previous research using the WCST in people with ASD reported a similar pattern of results to those in our study, with increased perseverative errors as compared to controls (Liss et al., 2001; Minshew et al., 1992; Rumsey and Hamburger, 1990) and a reduced percentage of conceptual-level responses. Studies using the WCST have demonstrated that poor performance on the task occurs in young children, adolescents and adults with autistic disorders (McEvoy et al., 1993), and that the finding is cross-cultural (Shu et al., 2001). Our results show that increased perseverative errors on the WCST are also found in adults with AS. The finding of reduced conceptual-level responses indicates that the AS group demonstrated less overall understanding of the task than the control group. Studies of letter fluency in ASD have been inconsistent; some reported impaired performance in people with autistic disorder as compared to ageand ability-matched controls (Rumsey and Hamburger, 1988; Turner, 1999), whereas others found no verbal fluency deficit (Boucher et al., 2005; Manjiviona and Prior, 1999). In our sample of adults with AS we found clear evidence of a verbal fluency deficit. By contrast, the adults with AS did not show any deficits on the Stroop test of inhibition. This result supports others (Ozonoff and Strayer, 1997; Russell et al., 1999) who also found no deficits on the Stroop test in children with autistic disorder. Further, Ozonoff and Strayer (1997) found that children with autism are not impaired on tests of negative priming or on the ‘Stop–Signal’ paradigm, both of which involve inhibition. The universality of executive dysfunction has been debated in relation to autism and, in this context, it has been suggested that for this to be case 559

10(6) all patients would have to demonstrate this deficit, which has not been shown (Hill, 2004). In this study, the impairment was specific to set shifting and generativity, but not to inhibition. In autism, impairments in inhibition have been found to be a differentiating feature when compared to other disorders including ADHD (Pennington and Ozonoff, 1996; Seargent et al., 2002). Further, Boucher et al. (2005) found no deficits in their HFA group on spatial executive tasks such as the Zoo Map. Thus, the profiles may be dependent on the measures used and this highlights the need to explore the profile of EF impairment in adults with AS in more detail by using a large battery of tests. A possible explanation for the EF deficits found relates to the biological determinants of this function which in turn are thought to involve the prefrontal cortex. Other authors have drawn attention to the similarities in symptoms between people with frontal lobe lesions and those with ASD, for example, lack of initiative, lack of empathy and concreteness of thought (Damasio and Maurer, 1978). In ASD, metabolic, structural and functional abnormalities have been reported in the frontal lobes (Boddeart and Zilbovicius, 2002; Carper and Courchesne, 2000; McAlonan et al., 2005). However, Boucher et al. (2005) did not find any correlations between structural differences in the prefrontal cortex and clinical or neuropsychological measures. It is also possible that EF deficits are caused by impairments in connections between the components of the system, for example, the prefrontal-striatal loops that support executive control mechanisms. Significant differences in grey matter volume of frontal-striatal circuitry, and in white matter tracts connecting anterior and posterior (visual) brain regions (McAlonan et al., 2005) have also been reported. It is possible that the dissociations between performance on EF tests (relating to intact inhibition but impaired generativity and mental flexibility) reflect differential abnormalities in selected areas of frontal-striatal circuitry. ‘The present study used a large number of statistical tests and as such there is a risk of false positive results. The acceptance of a 0.05 level of statistical significance in this study is not conservative and many of the impairments reported would no longer be significant at a 0.01 level. Taking this into account, the areas of cognitive deficit in the AS group were not particularly severe. For example, only 11 of the 27 AS subjects performed so poorly on the WCST that their scores reached clinical significance. Thus, from a clinical/diagnostic perspective, less than half of the AS group seen would have been reported to have ‘executive deficits’. Further, on the Doors memory test, only nine of the 27 people with AS scored below the 5th percentile and only six AS subjects were below average on the shapes test. The subtlety of these deficits may be partially explained by the fact that most of the people were outpatients and had been able to pass a number AU T I S M

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of academic qualifications. However, these subtle and selective deficits do appear to affect everyday functioning. That is, while some people with AS achieved high scores on IQ tests their academic achievements were less than would be predicted. For example, subject 3 had an IQ score in the very superior range, yet is struggling to finish higher education. In addition, even those who managed to reach high academic standards have not been able to hold down jobs for significant periods and many are unemployed. For example, subject 16 had an IQ score of 120/124 and passed a science degree but is now working as a shelf stacker in a supermarket. It is likely that their poor social skills contribute significantly to explaining these findings, but subtle cognitive deficits could also account for the dislocation of IQ scores, educational achievement and career progress. In summary, we have given a preliminary assessment of overall neuropsychological functioning in adults with AS. This group of people provided a unique opportunity to investigate the cognitive deficits associated with ASD without the confounding factor of significant language delay or learning disability. We found no evidence to support the hypothesis that people with AS have an IQ differential in favour of VIQ, or that they have neuropsychological deficits that resemble those of an NVLD. However, similar to other studies in people with an autistic disorder, we found that adults with AS have deficits in some aspects of EF but not others. It is possible that within people with AS, the dissociations between deficits and preservation of some executive functions may relate to biological factors in frontal-striatal circuitry. Future studies are required of the biological basis of the cognitive variability in people with AS.

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