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Developmental Neuropsychology
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Neuropsychological Differences Among
Children With Asperger Syndrome,
Nonverbal Learning Disabilities,
Attention Deficit Disorder, and Controls
a
b
Margaret Semrud-Clikeman Ph.D. , Jenifer Walkowiak , Alison
c
Wilkinson & Gina Christopher
d
a
Departments of Psychology and Psychiatry, Michigan State
University, East Lansing, Michigan
b
Children's National Medical Center, Washington, DC
c
Children's Medical Center Dallas, Dallas, Texas
d
Department of Educational Psychology, University of Texas at
Austin, Austin, Texas
Published online: 16 Aug 2010.
To cite this article: Margaret Semrud-Clikeman Ph.D. , Jenifer Walkowiak , Alison Wilkinson
& Gina Christopher (2010) Neuropsychological Differences Among Children With Asperger
Syndrome, Nonverbal Learning Disabilities, Attention Deficit Disorder, and Controls, Developmental
Neuropsychology, 35:5, 582-600, DOI: 10.1080/87565641.2010.494747
To link to this article: http://dx.doi.org/10.1080/87565641.2010.494747
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DEVELOPMENTAL NEUROPSYCHOLOGY, 35(5), 582–600
Copyright © 2010 Taylor & Francis Group, LLC
ISSN: 8756-5641 print / 1532-6942 online
DOI: 10.1080/875656412010494747
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Neuropsychological Differences Among Children
With Asperger Syndrome, Nonverbal Learning
Disabilities, Attention Deficit Disorder, and Controls
Margaret Semrud-Clikeman
Departments of Psychology and Psychiatry, Michigan State University,
East Lansing, Michigan
Jenifer Walkowiak
Children’s National Medical Center, Washington, DC
Alison Wilkinson
Children’s Medical Center Dallas, Dallas, Texas
Gina Christopher
Department of Educational Psychology, University of Texas at Austin, Austin, Texas
Confusion is present as to possible diagnostic differences between Asperger syndrome (AS) and Nonverbal learning disabilities (NLD) and the relation of these disorders to attentional difficulties.
Three-hundred and forty-five children participated in this study in 5 groups; NLD, AS, attention deficit hyperactivity disorder (ADHD): Combined type, ADHD: Inattentive type, and controls. The NLD
group showed particular difficulty on visual-spatial, visual-motor, and fluid reasoning measures compared to the other groups. There was also a significant verbal-performance IQ split in this group related to difficulty in social functioning. This study extends the findings from previous studies and extends these findings to differences between AS and NLD groups.
Previous studies have evaluated the neuropsychological functioning of children with nonverbal
learning disabilities (NLD) (2000), Asperger disorder (AS) (Ozonoff & Griffith, 2000), or attention deficit hyperactivity disorder (ADHD) (Nigg, Blaskey, Huang-Pollock, & Rappley, 2002)
Few studies have compared the neuropsychological functioning of children across these diagnoses in the domains of intelligence, achievement, motor, perception, and fluid reasoning. The purpose of this study was to evaluate possible differences among these groups on measures of verbal
ability, fluid reasoning, and visual-motor skills.
Correspondence should be addressed to Margaret Semrud-Clikeman, Ph.D., Michigan State University, Psychology
Building, 321 A West Fee Hall, East Lansing, MI 48824. E-mail: semrudcl@msu.edu
NEUROPSYCHOLOGICAL DIFFERENCES
583
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NONVERBAL LEARNING DISABILITY
The original concept of nonverbal learning disabilities was introduced by Johnson and Myklebust
(1967) and included children who had difficulty with social perception. Subsequently Rourke and
colleagues later suggested that the combined deficits of visual-spatial learning, tactile and motor
skills, and mathematics make up a syndrome they termed a nonverbal learning disability (NLD)
(Rourke, 1989; Rourke & Tsatsanis, 1996). An area of controversy in the area of NLD has been
the definition of this disorder. Many studies utilize an approach where the child must meet a selection of symptoms from an array of possibilities in order to qualify for a diagnosis of NLD. Although the NLD subtype continues to be refined, it is currently characterized by three broad areas
of dysfunction including motoric skills, visual/spatial organizational skills, and social abilities
(Semrud-Clikeman, 2007).
Children with NLD often show excellent single word reading skills and spelling ability but
have difficulty with inferential thinking, complex reading comprehension, and mathematics
(Semrud-Clikeman & Glass, 2008). Executive functioning for these children generally may be
problematic as they often have difficulty in understanding situations that involve cause–effect
reasoning, generating solutions to problems, and learning new material that is complex or novel
(Rourke, 1995; Semrud-Clikeman, 2003).
Many clinicians and researchers suggest that children with NLD have difficulty in correctly
perceiving social relations and with social judgment (Semrud-Clikeman, 2007). Some have suggested that these social difficulties are secondary to difficulties with visual-spatial development
(Rourke, 2000) while others suggest that there are significant perceptual problems that contribute
to problems with understanding facial expressions, voice intonation, and the speaker’s intent
(Forrest, 2007; Guli, Wilkinson, & Semrud-Clikeman, 2008; Pennington, 1991, 2008; SemrudClikeman, 2007). It is unclear from the empirical literature whether this hypothesis is accurate and
further research that evaluates whether these perceptual and visual-spatial deficits underlie the social-emotional functioning of children with NLD is needed.
ASPERGER SYNDROME
A defining feature of AS is difficulty with social relationships. Particular difficulties are present in
nonverbal behaviors (eye contact, facial expression, and body gestures), successful peer relationships, and with social reciprocity. Children with AS often have interests that are circumscribed
and intense and may be inflexible in their adherence to routines. Neuropsychologically, children
with AS show strong verbal skills, poor visual-spatial ability, and problems with executive functioning (Klin, Sparrow, Cicchetti, & Rourke, 1995). As some researchers have questioned the
findings of visual-spatial difficulties in AS (Edgin & Pennington, 2005), this area of inquiry remains open.
While diagnostic criteria for AS is contained within the DSM-IV-TR (American Psychiatric
Association, 2000) structure, there is no commensurate manual for a diagnosis of NLD. There are
several similarities between AS and NLD. In both disorders, problems with social communication
and reciprocity, nonverbal communication, pragmatic language, and visual-spatial skills appear
to be present (Gunter, Ghaziuddin, & Ellis, 2002; Voeller, 1995). Stronger verbal compared to
performance skills on cognitive testing were found for children with AS or NLD (Gillberg &
584
SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
Billstedt, 2000; Klin et al., 1995). It is important to note that the many of the symptoms of NLD
may be present in children with AS. However, differences between children with AS and those
with NLD include the presence of stereotyped and restricted patterns of interest and the need to
adhere to routines present in children with AS but not NLD (Semrud-Clikeman, 2007).
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ADHD, AS, AND NLD
Of interest for this study is the co-occurrence of ADHD in children with AS and NLD (Gillberg &
Billstedt, 2000). Studies have found a high co-occurrence of ADHD in a sample of children with
AS with 33% to 50% of the samples showing significant difficulties in inattention and 7% showing problems with overactivity (Gadow, DeVincent, & Pomeroy, 2006; Ghaziuddin, WeidmerMikhail, & Ghaziuddin, 1998; Leyfer et al., 2006; Nyden, Gillberg, Hjelmquist, & Heiman,
1999). Similar to children with AS those with NLD also show a tendency to have attentional difficulties. Children with NLD are often identified as having problems with attention and tend to be
diagnosed with ADHD: Predominately Inattentive type (ADHD–PI) (Semrud-Clikeman, 2007).
Some have suggested that the attentional problems found in children with NLD are due to visual
perceptual and tactile difficulties (Rourke, 2000) while others suggest these difficulties are separate but that visual attentional issues may be related to problems with social functioning (Corbett
& Constantine, 2006; Fine, Semrud-Clikeman, Butcher, & Walkowiak, 2008). Rourke (2000)
suggested that deficits in visual perceptual skills may be related to attentional difficulty seen in
many of these children rather than a true diagnosis of ADHD. Thus, these visual attentional issues
may have a differential effect on social functioning for children with NLD apart from the difficulties found for children with ADHD; an area of inquiry that requires further research.
Given the hypothesis that children with AS or NLD may have attentional differences, it was
felt important to control for significant attentional problems for these children on the neuropsychological measures in this study. For this reason we included a group of children with
ADHD–PI and Attention Deficit Hyperactivity Disorder: Combined type (ADHD–C) to attempt
to control the effect attentional difficulties have on the ability to complete tasks that require executive functions. The main hypotheses of this study were that children with AS and NLD would
show significant problems on measures of executive functioning, visual perception, and performance abilities compared to the children with ADHD or the control group. It was also hypothesized that children with NLD would show a difference in Verbal-Performance IQ skills compared
to the other four groups as suggested by the literature. Moreover, it was hypothesized that children
with NLD would show right-sided difficulties on measures of motor dexterity while these problems would not be present in the children with AS, ADHD–C, ADHD–PI, or controls.
METHOD
Participants
Participants were children referred by parents, teachers, psychologists, psychiatrists, pediatricians,
and community organizations to a large university for participation in a larger eight-year study examining the neuropsychological functioning of children with developmental disorders. The final
sample included 345 children ranging in age from 9.1 years to 16.5 years. There were 242 males and
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NEUROPSYCHOLOGICAL DIFFERENCES
585
103 females in the sample with 18% of the sample self-identified as a minority (Hispanic, African
American, and Asian). There were five groups of children identified for the purpose of this study;
control (N = 113), AS (N = 50), NLD (N = 26), ADHD–C (N = 76), and ADHD–PI (N = 80). Reflecting the general rates of AS and ADHD comorbidity 27 of the AS group also had a secondary diagnosis of ADHD; 14 with ADHD–C and 13 with ADHD–PI. For the NLD group 22 also had a secondary diagnosis of ADHD; 6 with ADHD–C and 16 with ADHD–PI.
Doctoral-level graduate students trained in administering a comprehensive neuropsychological battery individually assessed the participants. These graduate students were blind to the diagnosis of the child. Diagnoses were determined by consensus of two independent sources; licensed psychologists within the community or university, and advanced doctoral students.
Participants for whom a diagnosis was not unanimous were not included in the study (N = 5).
Exclusionary criteria included a history of a reading disability, seizure disorder, progressive neurological problems, traumatic brain injury, or any other serious medical condition. Those with
comorbid psychopathology were also excluded from the sample, including participants with severe mood or conduct disorders. Only children with a FSIQ above 80 were included in the sample.
Children with a diagnosis of ADHD were diagnosed by either private practitioners (psychiatrists or psychologists) or through the neuropsychology clinic at the university. Our confirmation
of a diagnosis for ADHD required a T-score of 65 or higher on the Behavior Assessment Scale for
Children–2 (BASC–2)(Reynolds & Kamphaus, 2004) inattention and/or hyperactivity scale as
well as meeting criteria for DSM-IV-TR (American Psychiatric Association, 2000) diagnosis of
ADHD using a parent semi-structured interview. Children in the control group had no history of
learning, behavioral, or attentional difficulties both by parent and teacher report and an interview
completed prior to participation. No child in this group met criteria for AS, NLD, or reading disability.
The Autism Diagnostic Interview (ADI–R) (Le Couteur, Lord, & Rutter, 2003) or the Autism Diagnostic Observational System (ADOS)(Lord, Rutter, DiLavore, & Risi, 1999) were administered to
children in the AS group through a private practitioner to determine the presence of autistism spectrum
disorders (ASD). These results were not generally available for the study from these private practitioners. No child met the criteria for autism using the ADI–R. The children were diagnosed with AS
partly based on the results of one of these measures with the diagnosis of AS confirmed using
DSM-IV-TR (American Psychiatric Association, 2000) criteria for this study. An AS screener based
on DSM-IV-TR Asperger syndrome criteria developed at the clinic and completed by the child’s primary caretaker was used for tertiary confirmation. The cutoff score on this measure was 6 as defined
by DSM-IV-TR criteria. There were three children excluded from the study who did not meet all of
these criteria. Of the children with AS approximately 25% would also have met criteria for NLD.
An independent licensed psychologist evaluated approximately half of the sample of children
diagnosed with a nonverbal learning disability. This diagnosis was confirmed through review of
previous testing if current or through an updated assessment. Agreement among the two first authors and any previous diagnosis was required for inclusion in the study. There were six children
who were found to not qualify under the following criteria or who met criteria for significant depression or anxiety disorder diagnoses. Consistent with the recommendations from research criteria (Rourke & Tsatsanis, 1996), children with NLD qualified for this group if they met all of the
following criteria: (1)Scores 1 standard deviation below average on the parent form of the Social
Skills Rating Scale (SSRS) (Gresham & Elliott, 1990); (2) Math calculation skills below the 15th
percentile on the math calculation subtest of the Woodcock-Johnson Achievement Test III
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586
SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
(WJ-Ach III) (Woodcock, McGrew, & Mather, 2001b); (3) Average scores on the letter-word
identification subtest from the WJ-Ach III (Woodcock et al., 2001b); (4) Average estimated verbal IQ of at least 85 standard score points on the Wechsler Abbreviated Scale of Intelligence
(WASI) (Psychological Corporation, 1999); (5) Scores at least one standard deviation below average on the Visual Motor-Integration Test (VMI) (Beery, Buktenica, & Beery, 2006); and (6) Below average scores on the Purdue Pegboard (Tiffin, 1968). We decided to use a more conservative
approach to diagnosis and to view the disorder as a syndrome which incorporated the main areas
of visual-motor skills, motor skills, social functioning, and good verbal ability.
It is important to mention here that children with AS may have many symptoms that are consistent
with a diagnosis of NLD. For the current study, however, children with AS were selected apart from
similarities with the NLD group when one of more of the following symptoms were found during the
parent interview: a stereotyped and restricted pattern of interests, inflexible adherence to nonfunctional routines, stereotyped and repetitive motor mannerisms, preoccupation with parts of objects, and
a lack of spontaneous seeking to share enjoyment, interests, or achievements with others. The children
in the AS group also were not required to show the same symptoms as detailed above.
Inclusionary Instruments
WASI (Psychological Corporation, 1999). The WASI is an abbreviated scale of intelligence with measures of similarities, vocabulary, block design, and matrix reasoning. As discussed
earlier, there are research findings that indicate the performance IQ may be impacted in children
with NLD. For this reason, the VIQ was used as an estimate of ability.
WJ-Ach III (Woodcock et al., 2001b). Three subtests from the WJ-Ach III were administered; letter-word identification, calculation, and mathematics reasoning.
VMI (Beery et al., 2006). The VMI requires the child to copy increasingly more difficult
geometric figures within a grid. It provides a measure of visual-motor skills.
Purdue Pegboard (Tiffin, 1968). The Purdue Pegboard requires the child to place pegs in
holes as quickly as possible first with the dominant hand, then the nondominant hand, and then both
hands together for 30 seconds each. This measure has been found to be a good measure of manual dexterity but not necessarily useful for determining lateralization (Reddon, Gill, Gauk, & Maerz, 1988).
The Structured Interview for Diagnostic Assessment of Children (SIDAC) (Puig-Antich
& Chambers, 1978). The SIDAC is a formal interview based on DSM-IV diagnoses, modified and updated from the Kiddie-Schedule of Affective Disorders and Schizophrenia (K-SADS)
developed by Puig-Antich and Chambers (1978). The ADHD portion of the SIDAC interview
was used in this study to determine the presence of ADHD symptoms with severity based on the
number of symptoms reported. Symptoms related to inattention, hyperactivity, and impulsivity
were included. This measure was also used as partial confirmation of parent-reported diagnosis of
ADHD, as noted earlier.
Behavior Assessment System for Children–2 (BASC–2) (Reynolds & Kamphaus,
2004). Two subtests from the BASC–2 parent rating scale were used as a measure of attention
and hyperactivity. The BASC–2 is an omnibus behavioral rating scale that provides normative
data for specific behaviors. It has excellent psychometric properties.
NEUROPSYCHOLOGICAL DIFFERENCES
587
Social Skills Rating Scale (SSRS) (Gresham & Elliott, 1990). The SSRS is a behavioral rating scale completed by the child’s main caretaker. It measures total social skills through a
Likert scale of three options (never, sometimes, and very often).
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Study Measures
Woodcock-Johnson Cognitive Battery III (WJ-Cog III) (Woodcock, McGrew, & Mather,
2001a). Two subtests that make up the Fluid Reasoning index were utilized from the WJ-Cog
III; analysis/synthesis and concept formation. These tests require the child to look at a problem
and utilize the information present to solve the item. Analysis and synthesis requires the child to
solve picture equations while concept formation requires cognitive flexibility and skill in evaluating problems to determine what is similar between the stimuli.
Rey-Osterreith Complex Figure (Osterreith, 1944). The Rey-Osterreith complex figure
test requires the child to copy a complex figure as accurately as possible and is a measure of perceptual organization (Lezak, Howieson, & Loring, 2004). The scoring system used is the one developed by Osterreith and translated by Corwin and Bylsma (1993) involving the widely used
18-item, 36-point scoring system.
Judgment of Line Orientation (JLO) (Benton, Sivan, Hamsher, Varney, & Spreen,
2004). The JLO is a measure of spatial ability without a motor component. The child is asked to
look at an array of lines and then is shown two lines. He/she is then asked to match the two lines to
the array.
Grooved Pegboard (Klove, 1963). The grooved pegboard measures complex finger coordination. It consists of a board with slotted holes angled in various directions. Each peg has a
groove and only fits in one way in each hole. The child uses first the dominant hand and then the
nondominant hand to place the pegs as quickly as possible. It has been recommended as a good
measure of lateralized impairment (Lezak et al., 2004)
Finger Tapping Test (Reitan & Wolfson, 1985). The Finger Tapping test requires the
child to tap a key as quickly as possibly first with the dominant hand and then with the
nondominant.
Analyses
Multivariate analysis of variance (MANOVA) with multiple post-hoc comparisons was used to
determine whether there were group differences based on age or verbal IQ in the sample. The general linear model (GLM) with post-hoc comparisons was used to evaluate group differences
among the behavioral, cognitive, and neuropsychological measures.
RESULTS
Table 1 presents the group means and standard deviations for the sample age, estimated Verbal IQ
measure, and group selection measures. There were no significant differences among groups for
588
11.1
46.9
49.7
53
111.9
106.4
112.5
101.3
.04
–.24
–.11
BASC-attn9
SSRS10
VIQ11
Reading
Mathematics
Calculation
VMI12
Purdue RH13
Purdue LH14
Purdue Both
Hands
–.97
101
–1.14a
–1.3
107.8
97.1
107.3
64.7
37.1
64.1
10.6
10.3
10.2
Mean
1.9
17
1.8
1.7
17
17.4
17.6
11
11.2
13.8
4.1
28.8
2.3
SD
AS2
(N = 50)
–1.29
87.5
–1.33
–.98
102.2
90.8
109.7
65.7
38.7
64.3
10.2
11.3
5.3
Mean
1.4
11.7
1.5
1.2
15.2
19.7
16.7
8.9
8.5
12.3
3.4
26.1
2.3
SD
NLD3
(N = 26)
–.45
96.6
–.68
–.44
106.7
101.1
110
67.9
40
72
14.3
10
5.7
Mean
1.2
15.5
1.3
1.2
13.2
17.9
16.6
8.2
8.7
11.9
2.4
24.4
3.7
SD
ADHD-C4
(N = 76)
–.57
97
–.61
–.42
108.25
100
106.1
67.7
44.1
55.4
10.7
10.8
5.6
Mean
1.2
8.7
1.2
1.4
14.6
20.7
11.7
7.6
10.9
10.8
5.2
25.4
3.2
SD
ADHD-PI5
(N = 80)
N.S.
NLD < ADHD-C (p = .007), ADHD-PI (p =
.04)
C > All (p < .0001)
NLD < All (p < .02)
C < All (p < .03)
AS < C (p = .001), ADHD-C (p = .01),
ADHD-PI (p = .01)
NLD < C (p = .04)
NLD, AS < C (p < .001), NLD < ADHD-C (p =
.03)
N.S.6
AS > C (p < .0001), NLD (p < .0001) , ADHD-C
(p < .0001), ADHD-PI (p < .0001)
C < NVLD, ADHD-C, ADHD-PI (p < .0001)
AS, NLD, ADHD-PI > C (p < .0001)
ADHD-C > All (p < .0001)
ADHD-C > ADHD-PI , AS, NLD (p < .0001)
C < AS, NLD, ADHD-C, ADHD-PI (p < .0001)
C < All (p < .0001)
AS, NLD < ADHD-C (p < .022)
ADHD-PI> AS (p < .0001), NLD (p = .022),
ADHD-C (p = .014)
C < All (p < .0001)
N.S.
Group Significance
1Standard deviation; 2Asperger Syndrome; 3Nonverbal Learning Disability; 4Attention deficit hyperactivity disorder–Combined type; 5Attention deficit hyperactivity
disorder—Predominately Inattentive Type; 6Not significant; 7Structured interview; 8Social Skills Rating Scale; 9Behavior Assessment System for Children–Hyperactivity
scale; 10Behavior Assessment System for Children–Attention scale; 11Verbal IQ; 12Visual-Motor Integration Test; 13Right hand; 14Left hand.
1.04
12.5
1.04
1.3
12.3
15
14.3
9.3
10.8
3
2.7
SIDAC
Total7
BASC-hyper8
25.1
1.4
SD1
10.4
.9
Mean
Age
AS screener
Variable
Control
(N = 113)
TABLE 1
Significant Group Differences for Group Selection Measures; Means and Standard Deviations
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NEUROPSYCHOLOGICAL DIFFERENCES
589
age (p = .18). As expected due to selection criteria, there was not a significant difference in estimated Verbal IQ among the groups (p = .085, partial eta squared = .024).
Analyses of Group Selection Measures
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Membership in groups was partially determined by scores on selected psychological measures.
Preliminary analyses were conducted to determine whether the expected group differences were
present. These results are provided in Table 1.
Visual-Spatial Measures. Scores from the VMI were evaluated using a one way ANOVA.
A significant group difference was present for the VMI (F(4,290) = 5.68, p < .0001, partial eta
squared = .07). Post-hoc comparisons found that the NLD group differed from all of the other
groups (p < .02). These findings were expected for the NLD group as it was a variable involved in
the selection for the group.
A preliminary analysis of the right (RH), left (LH), and both hands results of the Purdue Pegboard found a significant main group effect difference for all conditions (F(12, 418) = 2.45, p =
.004, partial eta squared = .058). Follow-up analyses found that there were significant group differences for all conditions (p < .008). Post-hoc analysis found that Control group scored better
with the RH compared to the clinical groups (p < .03). Among the clinical groups there were no
differences for the RH. For the LH, the AS and NLD groups scored significantly worse than the
control group but not from each other (p = .44). This finding was predicted by the selection criteria
for the NLD group. This finding was not predicted for the AS group. For the both hands condition,
the AS and NLD groups were significantly less successful than the control group (p < .001) but did
not differ from each other. The NLD group also scored worse compared to the ADHD–C group
(p = .03).
Behavioral Measures
On the semi-structured interview (SIDAC) a significant main effect for group was found (F(4,
337) = 124.6, p < .0001) for total symptoms of attention/impulsivity/hyperactivity. Post-hoc comparisons found that the control group scored significantly lower than all clinical groups (p <
.0001). Clinical group comparisons found the ADHD–C group to score lower than all other clinical groups (p < .0001). There were no significant differences between the AS, NLD, or ADHD–PI
groups.
A preliminary analysis of the hyperactivity and attention scales of the BASC–2 was completed
using a 2 × 5 MANOVA. As expected significant findings were present for the main effect for
group (F(8, 656) = 47.2, p < .0001, partial eta squared = .37). Follow-up analyses found significant group differences for attention (p < .0001) and hyperactivity (p < .0001). For the hyperactivity measure, post-hoc analyses found that the ADHD–C group differed significantly from all of
the other groups (p = .005). When the clinical groups were compared, the ADHD–C showed significantly higher scores on the hyperactivity measure from all of the other clinical groups (p <
.0001) while the AS, NLD, and ADHD–PI groups did not differ from each other. For the attention
measure all clinical groups were less successful than the control group (p < .0001). No significant
differences were found among the clinical groups on the attention measure.
590
SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
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Social Skills Selection Measure
On the SSRS there was a significant main effect for group (F(4, 329) = 30.2, p < .0001)
with the control group scoring significantly higher than all of the clinical groups (p < .0001).
There were significant differences between the NLD and ADHD–C group (p = .022) with the
NLD group scoring significantly worse than the ADHD–C group. There was no significant
difference between the NLD and AS groups (p = .54). The ADHD–PI group was rated better
on this measure compared to the ADHD–C (p = .014), AS (p < .0001) and NLD (p = .022)
groups.
For the AS screener an ANOVA found a significant group difference (p < .0001). Post-hoc
analyses found that all of the clinical groups scored higher than the control group (p < .0001).
Clinical group comparisons found that the AS group scored higher than the NLD and ADHD
groups (p < .0001). No difference was found among the NLD and ADHD groups (p > .05). Table 1
provides these findings
Analysis of Measures of Interest
Evaluation of the estimated verbal and performance IQs using a 2 (verbal, performance) × 5
(group) MANOVA found a significant main effect for group (F (8, 678) = 5.769, p < .0001, partial
eta = .064). Table 2 provides these results. Follow-up analysis found no significant difference for
the verbal estimated IQ among groups (p = .085, partial eta = .024) with a significant difference
present for the performance estimated IQ among groups (p < .0001, partial eta = .095). Post-hoc
analysis found that the NLD group scored significantly worse than the control group (p < .0001),
AS group (p = .001), and both ADHD groups (p < .0001). The AS group scored worse compared
to the control group (p = .018) but not the ADHD groups.
To evaluate whether the difference between verbal and performance estimated IQ differed
among the groups, a one way ANOVA was conducted. A significant group difference was found
(F(4, 337) = 6.8, p < .0001, partial eta squared = .075). Post hoc comparisons indicated significant
differences among the NLD group and all of the other groups with the NLD group showing the
largest split (p < .006). No other group differences were found.
A significant main effect for group was found for academic achievement (F(12, 804) = 6.97, p
< .0001, partial eta squared = .084). (See Table 2.) Follow-up analysis found no significant difference for reading recognition among the groups (p = .16) while mathematics calculation (p <
.0001) and mathematics reasoning (p < .0001) were significant. Post-hoc analysis found significant differences among all of the clinical groups and the control group for mathematics calculation (p < .0001) with the control group scoring better. Analysis of the clinical groups found that
the NLD group performed significantly worse than the ADHD–C (p = .007) and ADHD–PI group
(p = .04) on mathematics calculation but not the AS group (p = .16). The ADHD groups did not
differ from each other (p = .39). The finding of differences for the NLD was not unexpected as it
was one of the criteria for selection for that group. For mathematics reasoning, the control group
performed significantly better than all of the clinical groups (p < .04). Among the clinical groups
the NLD group was less successful than the ADHD–C group (p < .0001) and the ADHD–PI group
(p = .001) but not the AS group (p = .1). The ADHD groups did not differ from each other significantly (p = .84).
591
13.7
1.5
114.0
112.6
113.8
110.1
V-P7 Split
Mathematics
Reasoning
Fluid
Reasoning
AnalysisSynthesis
Concept
Formation
.9
1.2
1.5
1.3
1.7
1.3
–.16
–.14
–.82
–.59
–.26
.2
13.7
19.2
13.5
–.8
–.7
–2.4
–.08
–1.64
–.71
102.5
104.1
100.4
3.4
103.0
103.9
Mean
1.9
1.7
2.8
1.6
2.6
.85
17.9
12.5
23.1
18.4
18.7
18.9
SD
AS2
(N = 50)
–1.4
–.8
–2.9
–1.8
–4.5
–1.7
96.4
98.5
96.7
18.8
97.4
90.9
Mean
1.7
.95
3.5
1.9
6.9
2.5
16.8
13.6
15.1
19.8
19.1
18.1
SD
NLD3
(N = 26)
.3
.34
–1.2
–.13
–.9
–.25
105.5
108.5
108
.71
108.3
109.1
Mean
1.2
1.1
1.6
1.5
1.5
.9
18.1
16.6
14.7
16
16.4
12.7
SD
ADHD-C4
(N = 76)
–.2
–.07
–1.1
–.3
–.96
–.14
106.1
105.9
107.1
–2.5
109.1
109.5
Mean
1.3
1
1.8
1.2
1.9
1.4
13.4
17.6
13.4
14.7
12.3
14.6
SD
ADHD-PI5
(N = 80)
N.S.11
N.S.
NLD < All (p < .001)
NLD < C (p = .001), ADHD-C (p = .008),
ADHD-PI (p = .004)
AS, NLD < C (p = .01)
NLD < C (p < .0001)
AS < C (p < .005)
NLD < ADHD-C, ADHD-PI (p < .01)
NLD < All (p < .01)
AS < C (p = .018)
NLD < C. ADHD groups (p < .0001)
NLD < AS (p < .001)
NLD > All (p < .006)
NVLD < ADHD-C (p < .0001), ADHD-PI (p =
.001)
C > All clinical groups (p < .04)
AS, NLD < C (p < .0001)
AS < ADHD-C (p = .01), ADHD-PI (p = .03)
NLD < ADHD-C (p .003), ADHD-PI (p =
.006)
AS, NLD, ADHD-PI <C (p < .03)
Group Significance
1Standard deviation; 2Asperger Syndrome; 3Nonverbal Learning Disability; 4Attention deficit hyperactivity disorder–Combined type; 5Attention deficit hyperactivity
disorder–Predominately Inattentive Type; 6Performance IQ; 7Verbal-Performance; 8Judgment of Line Orientation; 9Right hand; 10Left hand; 11Not significant.
Rey
Osterreith
JLO8
Grooved Peg
RH9
Grooved Peg
LH10
Tapping RH
Tapping LH
13.6
110.4
PIQ6
17.4
Mean
Measure
SD1
Control
(N = 113)
TABLE 2
Significant Group Differences on Neuropsychological Measures: Means and Standard Deviations
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SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
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Fluid Reasoning Cluster
A significant main effect for group was found on the fluid reasoning measures (F(4, 305) = 8.28, p
< .0001, partial eta squared = .1). (See Table 2.) Post-hoc analyses found that the NLD (p < .0001),
AS (p < .0001), and ADHD–PI (p = .026) performed significantly worse than the control group on
this measure. Within the clinical groups the NLD group performed significantly worse than the
ADHD–C (p = .003) and ADHD–PI (p = .006) groups but not the AS group (p = .35). In addition,
the AS group differed significantly from the ADHD–C (p = .010) and ADHD–PI (p = .03) groups.
The ADHD groups did not differ from each other (p = .72).
When the individual subtests from the fluid reasoning cluster were evaluated a significant difference was found for the analysis/synthesis subtest (p < .0001) and for the concept formation
subtest (p = .001). Post-hoc comparisons for the analysis/synthesis subtest found that the AS,
NLD, and ADHD–PI all performed significantly worse than the controls (p < .03) while the
ADHD–C group did not differ significantly from the control group (p = .06). The NLD group
scored more poorly compared to the ADHD–C group (p = .01) with no other clinical group differences found. On the concept formation subtest there was a significant difference between the AS
(p = .005) and NLD (p < .0001) groups and the control group. The NLD group scored significantly
more poorly compared to the ADHD–C (p = .01) and ADHD–PI (p = .01) but not from the AS
group (p = .12).
Visual-Spatial Abilities
To evaluate group differences on visual-motor and visual-spatial skills a 2 (JLO, Rey-Osterreith)
× 5 (group) MANOVA was conducted. A significant main effect for group was present (F(8, 308)
= 3.9, p < .0001, partial eta squared = .1). Follow-up analyses found that there was a group difference for the Rey-Osterreith (p = .001) and the JLO (p < .0001). Post-hoc analysis found that the
NLD group performed significantly worse than the control (p < .0001), AS (p = .01), and both
ADHD groups (p < .0001) on the Rey-Osterreith Complex Figure. There was no significant difference among the other groups. Similarly for the JLO the NLD group performed significantly worse
than all of the groups (p < .001) with no differences found among the other groups. These findings
indicate significantly poorer performance on all measures of visual-organization and visual-spatial skills as predicted. To evaluate the relation among the level of social skill development and
these visual-spatial abilities, a correlation was performed. There was a significant overall correlation between the JLO and the SSRS social skills rating (p = .013). Similarly there was a significant
overall correlation between the Rey-Osterreith and the SSRS (p = .017).
Motor Skills
To evaluate complex motor skills a 4 (Grooved Pegboard RH, Grooved Pegboard LH, Tapping
RH, Tapping LH) × 5 (group) MANOVA found a significant main effect for group (F(16, 336) =
2.56, p = .001, partial eta squared = .08). Follow-up analyses found significant differences present
for the Grooved Pegboard RH (p = .002), Grooved Pegboard LH (p = .002), Tapping RH (p = .05),
and Tapping LH (p =.02).
Post-hoc analyses found that for the Grooved Pegboard RH the NLD group was significantly
slower than the control group (p = .001) with no significant difference found among the ADHD
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NEUROPSYCHOLOGICAL DIFFERENCES
593
groups, AS group, and the control group (p > .3). The NLD group performed significantly worse
than the ADHD–C (p = .008) and ADHD–PI group (p = .004) with no significance difference
from the AS group (p = .056). For the Grooved Pegboard LH a significant differences was present
for the AS (p = .01) and NLD (p = .01) groups compared to the control group.
Post-hoc analysis found that for Tapping LH the AS (p = .009) and NLD (p = .027) groups performed significantly worse than the control group. No significant differences were found between
the ADHD groups and the control group (p > .4). The AS group performed significantly worse
than the ADHD–C group (p = .01) but not the ADHD–PI group (p = .1) or the NLD group (p = .9).
The NLD group performed significantly worse than the ADHD–C group (p = .03) but not the
ADHD–PI group (.13). No difference was present between the ADHD groups (p = .31).
DISCUSSION
One of the main aims of this study was to determine whether there are neuropsychological differences among children with NLD, AS, or ADHD. A main research question was to explore skills
on measures of visual-spatial, fluid reasoning, and motor skills compared to children with AS or
ADHD. It was hypothesized those children with ADHD–C and ADHD–PI would not show problems in these areas.
Cognitive Differences
The hypothesis that the NLD group would score more poorly on the Performance IQ measure
compared to the other groups was confirmed. The AS group scored more poorly than the control
group but not the ADHD groups and there was no difference among the ADHD groups and the
control groups on this measure. The NLD group also scored more poorly than the AS group on the
Performance IQ of the WASI. In addition the Verbal-Performance IQ split was found to be significantly larger only for the NLD group. No significant difference between verbal and performance
abilities was present among the other groups. These findings are consistent with those from the literature suggesting the V-P split in children with NLD.
Our study did not select subjects based on this split. We utilized this procedure in order to determine whether this split is indeed present in this population. In the NLD sample 74% of the individuals had a V > P split of more than 15 standard score points and 40% had a split of 25 standard
score points or higher (range from 15 to 55). This finding was different for the AS group where
63% showed verbal and performance IQs within 15 of each other. However, 37% showed VIQ >
PIQ in the AS group.
This finding indicates that while children with NLD are more likely to show a VIQ > PIQ split;
there is a sizable minority of children who do not. While this study does find that most children
with NLD in our sample did show such a split, this finding is not sufficient to provide a distinction
between a diagnosis of NLD and that of AS. Other researchers have reached a similar conclusion
when looking at children with NLD (Pelletier, Ahmad, & Rourke, 2001).
Conversely, for the AS group there is a sizable minority of children who also show a VIQ >
PIQ split. Recently, Black, Wallace, Sokoloff, and Kenworthy (2009) found that children with autism with a discrepantly high verbal or performance IQ showed significantly more difficulties
with social functioning. Others have found that when the nonverbal IQ was higher than the verbal
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IQ more social difficulties were present (Joseph, Tager-Flusberg, & Lord, 2002). In the current
study a discrepancy between verbal and performance IQ in children with AS was also found with
higher verbal scores related to fewer social difficulties. A future study that evaluated children with
NLD may evaluate whether less discrepant measures of ability are related to better outcomes or
severity of the disorder.
Academic findings were also similar to previous studies in that none of the children demonstrated a reading disability. Given that mathematics calculation skills were part of the inclusionary
criteria for our NLD group, it was not surprising that our NLD group scored more poorly on this
subtest (Drummond, Ahmad, & Rourke, 2005; Rourke, Ahmad, Collins, Hayman-Abello, &
Warriner, 2002). This finding was also present for the mathematics reasoning subtest and is consistent with previous research studies (Pelletier et al., 2001; Strang & Rourke, 1985).
Findings from the measure of fluid reasoning indicated that the control group scored better
than all of the clinical groups. Of more interest was the finding that both the NLD and AS groups
performed significantly more poorly compared to the ADHD groups and did not differ from each
other on this measure. Behavioral difficulties are often present for children with NLD or AS when
they are faced with a novel situation. It may well be that the deficit in fluid reasoning compromises
their already limited ability to function in unfamiliar or complex situations. Previous studies have
suggested difficulties in concept-formation and novel problem-solving skills (Rourke & Tsatsanis,
2000). Other researchers have begun to suggest that the difficulty some children with NLD have
in social functioning is due to problems with executive functioning (Forrest, 2007).
Some studies have found that children with ASD may show good to excellent abilities on a
measure of matrix reasoning (Dawson, Soulieres, Gernsbacher, & Mottron, 2007; Hayashi, Kato,
Igarashi, & Kashima, 2008). The Raven’s Standard Progressive Matrices Test (Raven, Raven, &
Court, 1993) requires the child to solve geometric designs by supplying the missing element by
choosing one of 6 to 8 alternatives that best match the design. This test differs from the WJ-Cog III
measures utilized in the current study. The fluid reasoning portion of the WJ-Cog III requires not
only solving of geometric designs but also the use of categorical reasoning, inductive and deductive logic, and the ability to shift set (Strauss, Sherman, & Spreen, 2006). In contrast the Raven’s
has been found to be a unidimensional estimate of reasoning ability (Raven, Raven, & Court,
2000). The relation of the WJ-Cog III fluid reasoning test to social functioning is likely stronger
than that found for the Raven’s because of the multidimensional nature of social reasoning.
Our findings of difficulty with fluid reasoning for both NLD and AS groups support the suggestion that these difficulties complicate the child’s ability to solve novel, visually complex problems. These difficulties may contribute to problems with perspective-taking as well as with the
ability to adapt to changing environmental demands. Children with ADHD were not found to have
significant difficulties on this task. This finding suggests that problems encoding visual stimuli
for children with AS and NLD contributes to social problems while for children with ADHD social difficulties may not be due to inaccurate perception but rather to impulsivity and inattention
(Fine et al., 2008). Further study is necessary to untangle the relation of executive functioning and
attention to social competence.
Denckla (2000) suggests that there is a “cognitive overlap zone” of executive functions in NLD
and ADHD due to overlapping neural regions. Neuroimaging provides some support for this theory. Structural and functional magnetic resonance imaging (fMRI) studies have found differences
in right hemispheric frontal and striatal networks as well as in white matter structures (i.e., corpus
callosum) in children with ADHD (Castellanos et al., 1994; Castellanos et al., 1996; Giedd et al.,
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1994; Hynd et al., 1993; Semrud-Clikeman et al., 2000). Similarly, Rourke (1995) suggested that
difficulty was present in the right-hemispheric white matter in NLD. Differences have also been
found in the smaller volume of the corpus callosum for children with AS despite control for white
matter volume (Chung, Dalton, Alexander, & Davidson, 2004), higher volumes of white matter
(Filipek, 1999), and increased volume in the caudate regions (Sears et al., 1999). While the emerging MRI research in AS suggests white matter involvement in the disorder, the findings are not
conclusive. Prospective research in imaging for children with NLD has not been published but
findings from existing neurological cases does suggest involvement of the right hemisphere and
possibly of white matter (Voeller, 1995). Further study is needed to determine the validity of the
right hemispheric white matter hypothesis in NLD.
Visual-spatial differences. The NLD group showed significantly more difficulty compared to the other groups on the Rey-Osterreith Complex Figure test. Impairment on this test is
thought to reflect problems with planning, organization, and visual-spatial reasoning as well as visual-motor skills. These findings are consistent with previous studies for children with NLD
(Wilkinson & Semrud-Clikeman, 2008; Woods, Weinborn, Ball, Tiller-Nevin, & Pickett, 2000;
Worling, Humphries, & Tannock, 1999). For the children with AS no significant differences were
found compared to the other three groups. This finding is consistent with that of Edgin and Pennington (2005) who found few problems in spatial cognition in children with AS while others
have found problems with visual organization (Kenworthy et al., 2005). These findings indicated
that copying a complex figure may be an area of specific difficulty for children with NLD. Reviewing the individual scores supports this hypothesis to some extent. In the NLD sample 63%
showed scores in the below average range while for the AS sample 39% scored in the below average range.
Similarly the JLO, a measure of spatial reasoning without a motor component, was found to
differ among the groups. The NLD group scored more poorly compared to the other groups.
Children with AS were found to show, as a group, average to above average performance on the
JLO (79% of the sample scored within the average to above average range). These visual-spatial
measures were among the few that differentiated children with NLD from those with AS.
Motor. The literature suggests that a right hemispheric deficit is present in children with
NLD and as such more difficulty would be seen with the left hand than the right hand measures. It
has also been hypothesized that children with NLD show bilateral difficulties in fine motor skills
(Rourke, 1995). We found only partial support for this hypothesis. While our findings indicated
that the NLD and AS groups performed more poorly on a measure of complex fine motor functioning compared to controls with the left hand and bilaterally for the NLD group, these measures
did not differ significantly from the scores obtained by the ADHD groups and as such may not be
specific to AS or NLD.
Limitations of the Study
There are several limitations to this study. One limitation was the lower number of children with a
diagnosis of NLD. It required several years to find sufficient numbers of children who met criteria
for NLD who did not also meet criteria for AS. The sample for this study did not include children
with genetic or other disorders that have been associated with NLD (velocardiofacial syndrome,
Williams syndrome) and these results may not be generalizable to groups of children with medical
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SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
and/or genetic disorders. An additional issue is the possible confound between the visual fluid reasoning tests of the WJ-Cog III and the visual-perceptual difficulties found in the children with
NLD and many of those with a diagnosis of AS. These results should be interpreted in light of
these problems and our findings are consistent with previous research, also using visual tasks that
find problems with concept formation and executive functioning (Fisher, DeLuca, & Rourke,
1997; Sikora, Haley, Edwards, & Butler, 2002)
Another limitation of the study was that we were not able to obtain the scores from the ADOS
or ADI–R. These measures were obtained in a private clinic setting with the results were not available to our study. In the future selection of subjects using these measures would provide for better
diagnostics and the ability to evaluate performance based on number of symptoms reported on the
ADI–R.
Finally, our sample of children with NLD did show significant difficulties on the estimated
performance test from the WASI. It was elected not to use covariate procedures to control for this
group difference. There are several articles that question the use of covariate procedures to equate
groups (Adams, Brown, & Grant, 1985; Miller & Chapman, 2001) while others suggest that
ANCOVAs are appropriate when evaluating treatment decisions (van Breukelen, 2006). In the
case of this study there were no differences in verbal estimated IQ—one of the selection criteria.
We elected not to covary for Full Scale estimated IQ which did significantly differ among the
groups due to the group differences on performance estimated IQ given the concerns voiced in
these various articles.
Conclusion
Taken together, these findings indicate that the theoretical model suggested by Rourke (1988)
provides a backdrop for our understanding of NLD. The performance deficits seen on the motor
tasks also suggest bilateral involvement of the brain with the NLD group scoring more poorly on
both right and left hands compared to the other groups. In contrast the AS group only showed differences with the LH. These findings do suggest difficulties in motor coordination for the NLD
and AS groups with poorer performance present for the right hemisphere than for the left. Some
have suggested that children with NLD may appear to be clumsy and uncoordinated (Rourke,
1988), while others have found a wide variation in bimanual motor coordination in children with
AS (Gunter et al., 2002). Our study suggests that there is a wide variation in these skills for both
groups and problems with coordination may not be an area specifically different for children with
NLD (Wilkinson & Semrud-Clikeman, 2008).
Findings of differences in visual-spatial skills were strongly present for children with NLD
even when motor disability was not present. The finding of differences in visual-spatial skills and
performance abilities implicate the posterior regions of the brain. These difficulties, however,
were present only for the NLD group. No difference was found among the AS, ADHD, or control
groups on visual-spatial ability. This finding suggests that there may be differences between the
NLD and AS groups in these areas; an issue that has been the subject of debate in the literature. It
may well be that the discriminating difference between NLD and AS is in visual-spatial ability,
thus it is strongly recommended that these measures to be included in the neuropsychological battery when evaluating these children. A comparison between children with NLD and those diagnosed with pervasive developmental disorder, not otherwise specified (PDD-NOS) has not been
conducted to determine what commonality may be present. One issue with such a comparison is
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the lack of definition for the diagnosis of PDD-NOS; basically this diagnosis is provided when the
child does not meet criteria for any other diagnosis in the autistic spectrum but has significant social difficulty.
The difference between verbal and performance abilities was found specifically for children
with NLD even though the selection criteria had not required such a split. These findings support
clinical reports of larger than expected Verbal-Performance IQ splits in children with NLD. It is
important to note that a sizable minority of children with AS also showed such a split; thus, the
split alone is not sufficient for discriminating between NLD and AS for diagnostic purposes. With
larger numbers in our study these findings may have been more robust. It is difficult, however, to
recruit sufficient numbers of well-diagnosed NLD children as it required 7 years of recruiting to
obtain our sample size in a large metropolitan region.
While attention is an important issue for children with AS or NLD, it was not strongly related to
our measures. One of the issues for our study was attempting to control for attentional problems frequently found in children with AS or NLD for which we utilized ADHD–C and ADHD–PI groups.
In the future, other studies may wish to contrast children with AS and comorbid ADHD symptoms,
those with AS without ADHD symptomatology, as well as that combination for children with NLD.
We cannot rule out that attentional issues may have played a role in some of our findings.
REFERENCES
Adams, K. M., Brown, G. G., & Grant, I. (1985). Analysis of covariance as a remedy for demographic mismatch of research subject groups: Some sobering simulations. Journal of Clinical and Experimental Neuropsychology, 7, 445–464.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.).
Washington, DC: Author.
Beery, K. E., Buktenica, N. A., & Beery, N. A. (2006). Developmental Test of Visual-Motor Integration-5. San Antonio:
Pearson.
Benton, A. L., Sivan, A. B., Hamsher, K., Varney, N. R., & Spreen, O. (2004). Contributions to neuropsychological assessment: A clinical manual (2nd ed.). New York: Oxford University Press.
Black, D. O., Wallace, G. L., Sokoloff, J. L., & Kenworthy, L. (2009). Brief report: IQ split predicts social symptoms and
communication abilities in high-functioning children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 1613–1619.
Castellanos, F. X., Giedd, J. N., Eckburg, W. L., Marsh, A. C., Kaysen, D., Hamburger, S. D., et al. (1994). Quantitative
morphology of the caudate nucleus in attention deficit hyperactivity disorder. American Journal of Psychiatry,
151(1212), 1791–1796.
Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Vaiturzis, A. C., & Dickstein, D. P. (1996). Quantitative
brain magnetic resonance imaging in attention-deficit hyperactivity disorder. Archives of General Psychiatry, 53(7),
607–616.
Chung, M. K., Dalton, K. M., Alexander, A. L., & Davidson, R. J. (2004). Less white matter concentration in autism: 2D
voxel-based morphometry. NeuroImage, 23(1), 242–251.
Corbett, B. A., & Constantine, L. J. (2006). Autism and Attention Deficit Hyperactivity Disorder: Assessing attention and
response control with the integrated visual and auditory continuous performance test. Child Neuropsychology, 12,
335–348.
Corwin, J., & Bylsma, F. W. (1993). The Clinical Neuropsychologist, 7(9–15).
Dawson, M., Soulieres, I., Gernsbacher, M. A., & Mottron, L. (2007). The level and nature of autistic intelligence. Psychological Science, 18, 657–662.
Denckla, M. B. (2000). Learning disabilities and attention-deficit/hyperactivity disorder in adults: Overlap with executive
dysfunction. In T. E. Brown (Ed.), Attention-deficit disorders and comorbidities in children, adolescents, and adults
(pp. 297–318). Washington, DC: American Psychiatric Press, Inc.
Downloaded by [University of Birmingham] at 12:47 19 September 2013
598
SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
Drummond, C. R., Ahmad, S. A., & Rourke, B. P. (2005). Rules for the classification of younger children with nonverbal
learning disabilities and basic phonological processing disabilities. Archives of Clinical Neuropsychology, 20, 171–182.
Edgin, J. O., & Pennington, B. F. (2005). Spatial cognition in Autism Spectrum Disorders: Superior, impaired, or just intact? Journal of Autism and Developmental Disorders, 35, 729–745.
Filipek, P. A. (1999). Neuroimaging in the developmental disorders: The state of the science. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 40(1), 113–128.
Fine, J. G., Semrud-Clikeman, M., Butcher, B., & Walkowiak, J. (2008). Brief report: Attention effect on a measure of social perception Journal of Autism and Developmental Disorders, 38, 1797–1802.
Fisher, N. J., DeLuca, J. W., & Rourke, B. P. (1997). Wisconsin Card Sorting Test and Halstead Category Test performances of children and adolescents who exhibit the syndrome of Nonverbal Learning Disabilities. Child Neuropsychology, 3, 61–70.
Forrest, B. (2007). Diagnosing and treating right hemisphere disorders. In S. J. Hunter & J. Donders (Eds.), Pediatric
neuropsychological intervention (pp. 175–192). Cambridge, MA: Cambridge University Press.
Gadow, K. D., DeVincent, C. J., & Pomeroy, J. (2006). ADHD symptom subtypes in children with pervasive developmental disorder. Journal of Autism and Developmental Disorders, 36(2), 271–283.
Ghaziuddin, M., Weidmer-Mikhail, E., & Ghaziuddin, N. (1998). Comorbidity of Asperger syndrome: A preliminary report. Journal of Intellectual Disability Research, 42(4), 279–283.
Giedd, J. N., Castellanos, F. X., Casey, B. J., Kozuch, P., King, A. C., Hamburger, S. D., et al. (1994). Quantitative morphology of the corpus callosum in attention deficit hyperactivity disorder. American Journal of Psychiatry, 151(5),
665–669.
Gillberg, C., & Billstedt, E. (2000). Autism and Asperger syndrome: Coexistence with other clinical disorders. Acta
Psychiatrica Scandinavica, 102(5), 321–330.
Gresham, F. M., & Elliott, S. N. (1990). Social Skills Rating System. Circle Pines, MN: American Guidance Service, Inc.
Guli, L. A., Wilkinson, A., & Semrud-Clikeman, M. (2008). Social Competence Intervention Program. Champaign, IL:
Research Press.
Gunter, H. L., Ghaziuddin, M., & Ellis, H. (2002). Asperger syndrome: Tests of right hemisphere functioning and
interhemispheric communication. Journal of Autism and Developmental Disorders, 32(4), 263–281.
Hayashi, M., Kato, M., Igarashi, K., & Kashima, H. (2008). Superior fluid intelligence in children with Asperger’s disorder. Brain and Cognition, 66, 306–310.
Hynd, G. W., Hern, K. L., Novey, E. S., Eliopulos, D., Marshall, R., Gonzalez, J. J., et al. (1993). Attention deficit-hyperactivity disorder and asymmetry of the caudate nucleus. Journal of Child Neurology, 8(4), 339–340.
Johnson, D. J., & Myklebust, H. R. (1967). Learning disablities: Educational principles and practices. New York: Grune
& Stratton.
Joseph, R. M., Tager-Flusberg, H., & Lord, C. (2002). Cognitive profiles and social-communicative functioning in children with autism spectrum disorder. Journal of Child Psychology and Psychiatry, 46, 807–821.
Kenworthy, L. E., Black, D. O., Wallace, G. L., Ahluvalia, T., Wagner, A. E., & Sirian, L. M. (2005). Disorganization: The
forgotten executive dysfunction in High-Functioning Autism (HFA) Spectrum Disorders. Developmental Neuropsychology, 28, 809–827.
Klin, A., Sparrow, S. S., Cicchetti, D. V., & Rourke, B. P. (1995). Validity and neuropsychological characterization of
Asperger syndrome: Convergence with nonverbal Learning Disabilities syndrome. Journal of Child Psychology and
Psychiatry, 36(1127–1140).
Klove, H. (1963). Clinical neuropsychology. In F. M. Forster (Ed.), The medical clinics of North America (pp.
1647–1658). New York: Saunders.
Le Couteur, A., Lord, C., & Rutter, M. (2003). Autism Diagnostic Interview-Revised. Los Angeles, CA: Western Psychological Services.
Leyfer, O. T., Folstein, S. E., Bacalman, S., Davis, N. O., Dinh, E., Morgan, J., et al. (2006). Comorbid psychiatric disorders in children with Autism: Interview development and rates of disorders. Journal of Autism and Developmental Disorders, V36(7), 849–861.
Lezak, M. D., Howieson, D. B., & Loring, D. W. (2004). Neuropsychological assessment (Fourth ed.). New York: Oxford
University Press.
Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (1999). Autism Diagnostic Observation Schedule. Los Angeles, CA:
Western Psychological Services.
Miller, G. M., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110,
40–48.
Downloaded by [University of Birmingham] at 12:47 19 September 2013
NEUROPSYCHOLOGICAL DIFFERENCES
599
Nigg, J. T., Blaskey, L. G., Huang-Pollock, C. L., & Rappley, M. D. (2002). Neuropsychological executive functions and
DSM-IV ADHD subtypes. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 59–66.
Nyden, A., Gillberg, C., Hjelmquist, E., & Heiman, M. (1999). Executive function/attention deficits in boys with Asperger
syndrome, attention disorder and reading/writing disorder. Autism, 3(3), 213–228.
Osterreith, P. A. (1944). Le test de copie d’une figure complexe. Archives de Psychologie, 30(206), 356.
Ozonoff, S., & Griffith, E. M. (2000). Neuropsychological function and the external validity of Asperger syndrome. In A.
Klin, F. R. Volkmar, & S. S. Sparrow (Eds.), Asperger syndrome (pp. 72–96). New York: Guilford Press.
Pelletier, P. M., Ahmad, S. A., & Rourke, B. P. (2001). Classification rules for basic phonological processing disabilities
and nonverbal learning disabilities: Formulation and external validity. Child Neuropsychology, 7(2), 84–98.
Pennington, B. F. (1991). Diagnosing learning disorders: A neuropsychological framework. New York: The Guilford
Press.
Pennington, B. F. (2008). Diagnosing learning disorders: A neuropsychological framework (2nd ed.). New York:
Guilford.
Psychological Corporation. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: Harcourt Assessment,
Inc.
Puig-Antich, J., & Chambers, W. J. (1978). The Schedule for Affective Disorders and Schizophrenia for School-Age
Children (K-SADS). New York: New York Psychiatric Press.
Raven, J., Raven, J. C., & Court, J. H. (1993). Raven manual: Section 1: General overview. Oxford, England: Psychologists Press.
Raven, J., Raven, J. C., & Court, J. H. (2000). Raven manual research supplement 3: American norms, neuropsychological applications. Oxford, England: Oxford Psychologists Press, Ltd.
Reddon, J. R., Gill, D. M., Gauk, S. E., & Maerz, M. D. (1988). Purdue pegboard: Test-retest estimates. Perceptual and
Motor Skills, 66, 503–506.
Reitan, R. M., & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery: Theory and Interpretation.
Tucson, AZ: Neuropsychology Press.
Reynolds, C. R., & Kamphaus, R. W. (2004). Behavior Assessment System for Children-2. Circle Pines, MN: Pearson Assessments.
Rourke, B. P. (1988). The syndrome of nonverbal learning disabilities: Developmental manifestations in neurological disease and dysfunction. The Clinical Neuropsychologist, 4, 293–330.
Rourke, B. P. (1989). Nonverbal learning disabilities: The syndrome and the model. New York: Guilford Press.
Rourke, B. P. (1995). The NLD syndrome and the white matter model. In B. P. Rourke (Ed.), Syndrome of nonverbal
learning disabilities: Neurodevelopmental manifestations (pp. 1–26). New York: Guilford Press.
Rourke, B. P. (2000). Neuropsychological and psychosocial subtyping: A review of investigations within the University
of Windsor laboratory. Canadian Psychology, 41(1), 34–51.
Rourke, B. P., Ahmad, S. A., Collins, D. W., Hayman-Abello, B. A., & Warriner, E. M. (2002). Child clinical/pediatric
neuropsychology: Some recent advances. Review of Psychology, 53, 309–339.
Rourke, B. P., & Tsatsanis, K. D. (1996). Syndrome of nonverbal learning disabilities: Psycholinguistic assets and deficits.
Topics in Language Disorders, 16(2), 30–44.
Rourke, B. P., & Tsatsanis, K. D. (2000). Nonverbal learning disabilities. In A. Klin, F. R. Volkmar, & S. S. Sparrow
(Eds.), Asperger syndrome (pp. 231–253). New York: The Guilford Press.
Sears, L. L., Vest, C., Mohamed, S., Bailey, J., Ranson, B. J., & Piven, J. (1999). An MRI study of the basal ganglia in autism. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 23, 613–624.
Semrud-Clikeman, M. (2003). Executive functions and social communication disorders. Perspectives, 29, 20–22.
Semrud-Clikeman, M. (2007). Social competence in children. New York: Springer.
Semrud-Clikeman, M., & Glass, K. L. (2008). Comprehension of humor in children with Nonverbal Learning Disabilities,
Verbal Learning Disabilities and without Learning Disabilities. Annals of Dyslexia, 58, 163–180.
Semrud-Clikeman, M., Steingard, R., Filipek, P. A., Bekken, K., Biederman, J., & Renshaw, P. F. (2000). Neuroanatomical-neuropsychological correlates of ADHD. Journal of the American Academy of Child and Adolescent Psychiatry, 39,
477–484.
Sikora, D. M., Haley, P., Edwards, J., & Butler, R. W. (2002). Tower of London test performance in children with poor
arithmetic skills. Developmental Neuropsychology, 21, 243–254.
Strang, J. D., & Rourke, B. P. (1985). Arithmetic disability subtypes: The neruopsychological significant of specific arithmetical impairment in childhood. In B. P. Rourke (Ed.), Neuropsychology of learning disabilities: Essentials of subtype
analysis (pp. 167–183). New York: Guilford Press.
Downloaded by [University of Birmingham] at 12:47 19 September 2013
600
SEMRUD-CLIKEMAN, WALKOWIAK, WILKINSON, CHRISTOPHER
Strauss, E., Sherman, E. M. S., & Spreen, O. (2006). A compendium of neuropsychological tests (Third ed.). New York:
Oxford University Press.
Tiffin, J. (1968). Purdue Pegboard: Examiner Manual. Chicago: Science Research Associates.
van Breukelen, G. J. P. (2006). ANCOVA versus change from baseline had more power in randomized studies and more
bias in nonrandomized studies. Journal of Clinical Epidemiology, 59, 920–925.
Voeller, K. K. (1995). Clinical neurological aspects of the right hemisphere deficit syndrome. Journal of Child Neurology,
10, 16–22.
Wilkinson, A., & Semrud-Clikeman, M. (2008). Motor speed in children and adolescents with nonverbal learning disabilities. Paper presented at the International Neuropsychological Society, February 2008, Waikoloa, HI.
Woodcock, R. W., McGrew, K. S., & Mather, N. (2001a). Woodcock-Johnson III Test of Cognitive Abilities. Rolling
Meadows, IL: Riverside Publishing.
Woodcock, R. W., McGrew, K. S., & Mather, N. (2001b). Woodcock-Johnson III Tests of Achievement. Itasca, IL: Riverside.
Woods, S. P., Weinborn, M., Ball, J. D., Tiller-Nevin, S., & Pickett, T. C. (2000). Periventricular leukomalacia (PVL): An
identical twin case study illustration of white matter dysfunction and nonverbal learning disability (NLD). Child
Neuropsychology, 6, 274–285.
Worling, D. E., Humphries, T., & Tannock, R. (1999). Spatial and emotional aspects of language influencing in nonverbal
learning disabilities. Brain and Language, 70, 220–239.