Social functioning using direct and indirect measures with children with High Functioning Autism, nonverbal learning disability, and typically developing children.

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Social functioning using direct and indirect measures with children with High Functioning Autism, nonverbal learning disability, and typically developing children a

b

Margaret Semrud-Clikeman , Jodene Goldenring Fine & Jesse c

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Bledsoe a

Department of Pediatrics, University of Minnesota Medical School, Minneapolis, MN, USA b

Department of Counseling, Special Education, and School Psychology, Michigan State University, East Lansing, MI, USA c

Department of Psychiatry, Children’s Hospital of Seattle, Seattle, WA, USA Published online: 25 Feb 2015.

To cite this article: Margaret Semrud-Clikeman, Jodene Goldenring Fine & Jesse Bledsoe (2015): Social functioning using direct and indirect measures with children with High Functioning Autism, nonverbal learning disability, and typically developing children, Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, DOI: 10.1080/09297049.2014.994487 To link to this article: http://dx.doi.org/10.1080/09297049.2014.994487

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Child Neuropsychology, 2015 http://dx.doi.org/10.1080/09297049.2014.994487


Social functioning using direct and indirect measures with children with High Functioning Autism, nonverbal learning disability, and typically developing children Margaret Semrud-Clikeman1, Jodene Goldenring Fine2, and Jesse Bledsoe3 1

Department of Pediatrics, University of Minnesota Medical School, Minneapolis, MN, USA Department of Counseling, Special Education, and School Psychology, Michigan State University, East Lansing, MI, USA 3 Department of Psychiatry, Children’s Hospital of Seattle, Seattle, WA, USA 2

Social perception is an important underlying foundation for emotional development and overall adaptation. The majority of studies with children with High Functioning Autism (HFA) or nonverbal learning disabilities (NLD) evaluating social functioning have used measures of parent and/or teacher ratings. The present study utilized parent and teacher ratings of behavior as well as executive functioning in addition to direct measures of social perception. Three groups participated in this study (control [n = 38] HFA [n = 36], NLD [n = 31]). Results indicated that the HFA group experienced the most difficulty understanding emotional cues on the direct measure while both the HFA and NLD groups experienced difficulty with nonverbal cues. Significant difficulties were reported on the parent rating scale for sadness and social withdrawal for both clinical groups. Executive functioning was found to be particularly problematic for the clinical groups. The direct social perception measure was highly correlated with the measures of executive functioning and reflects the contribution that executive functions have on social functioning. These findings suggest that the clinical presentation on behavior rating scales may be very similar for children with HFA and NLD. Moreover, it appears that measures of executive functioning are sensitive to the clinical difficulties these groups experience. The findings also suggest there is a commonality in these disorders that warrants further investigation. Keywords: Behavior; Social perception; High Functioning Autism; Nonverbal learning disabilities.

The ability to understand social interactions of peers is an important aspect of development that has been found to be problematic for children with High Functioning Autism (HFA) or nonverbal learning disabilities (NLD; Ozonoff & Rogers, 2003; Semrud-Clikeman, 2007). In the past assessment of social functioning has been most frequently accomplished with parent and teacher behavioral ratings and rarely with direct evaluation of the child’s social perception (Semrud-Clikeman & Fine, 2008). While parents and teachers are generally good reporters of the child’s outward behavior, it is not clear that these ratings fully capture the social experience of the child or any areas that might be most affected. Address correspondence to Margaret Semrud-Clikeman, PhD, 420 Delaware St SE, Department of Pediatrics, University of Minnesota Medical School, Box 486, Minneapolis, MN 55455, USA. E-mail: [email protected]

© 2015 Taylor & Francis


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M. SEMRUD-CLIKEMAN ET AL.

Children with Autistic Disorder by definition have difficulties with understanding social relationships (American Psychiatric Association [APA], 2000). Particular problems have been found in social reciprocity, pragmatic language, and difficulty with nonverbal cues (NV) (Klin, Volkmar, & Sparrow, 2000; Semrud-Clikeman, Walkowiak, Wilkinson, & Butcher, 2010). These social deficits are often accompanied by a stereotyped and restricted pattern of interests, difficulty with sharing enjoyment of activities or objects, and an inflexible adherence to routines or rituals (APA, 2000). A measure that is frequently utilized to characterize symptoms for children with ASD is the Autism Diagnostic Interview-Revised (ADI-R; Rutter, Le Couteur, & Lord, 2003) that has a module that particularly investigates whether stereotyped behaviors and intense interests are present. This diagnostic criterion has been retained in Diagnostic and Statistical Manual of Mental Disorders, fifth edition (DSM-5) as an integral part for the diagnosis of the new category Autism Spectrum Disorder. We are defining HFA as those children who met Diagnostic and Statistical Manual of Mental Disorders, text revision (DSM-IVTR; APA, 2000) criteria for Autistic Disorder as well as having significant stereotyped behaviors or interests as defined by the ADI-R. For our study we are utilizing the criteria from DSM-IV-TR for Autistic Disorder to define our population as our study was conducted prior to the adoption of DSM-5. It is important to note that our children were required to be high functioning and, although we did not employ DSM-5 criteria, they are similar to those children now defined as Autism Spectrum Disorder without significant impairment. Particular difficulty has been found when children with HFA are required to interpret social intent (Attwood, 1998). Understanding such intent is frequently misinterpreted leading to social misinterpretations with resulting interactions and anxiety in novel and unexpected social environments (Adolphs, Sears, & Piven, 2001). Others have found these difficulties to relate to anxiety and depression in later adolescence (Antshel & Khan, 2008; Fine, Semrud-Clikeman, & Bledsoe, 2012; Poletti, 2010). Similarly, problems with social perception are also present in children with NLD (Forrest, 2007; Myklebust, 1975). Specific deficits have been found in identifying facial expressions and gestures (Petti, Voelker, Shore, & Hayman-Abello, 2003), using emotional content to make social inferences (Fine, Semrud-Clikeman, Bledsoe, & Musielak, 2011; Worling, Humphries, & Tannock, 1999) and processing social cues (Hagberg, Nydén, Cederlund, & Gillberg, 2013; Woods, Weinborn, Ball, Tiller-Nevin, & Pickett, 2000). Some researchers have found that children with NLD are susceptible to higher levels of sadness and depression (Little, 1993; Poletti, 2010; Rourke & Tsatsanis, 2000). Diagnosis of NLD is more problematic than that for HFA as no set criteria for identification currently exists. Although some have questioned whether NLD exists due to lack of consistent research findings, it is a condition that continues to be diagnosed by clinicians (Fine, Musielak, & Semrud-Clikeman, 2014; Spreen, 2011). For that reason, it is important to try to more fully examine this issue. An early model developed by Byron Rourke and colleagues required that the child meet specific neuropsychological criteria for a diagnosis that included difficulties with motor coordination, tactile perception, visuospatial relations, language, problem solving, and academic achievement particularly in science and mathematics (Rourke & Tsatsanis, 2000). Refinement of this model has suggested inclusion of measures of executive and social functioning (Stein & Krishnan, 2007). In previous studies with a different sample, we found deficits in visual-spatial and visual-motor abilities in children with NLD but not those with Asperger Syndrome (AS) (Semrud-Clikeman, Walkowiak, Wilkinson, & Christopher, 2010). In contrast, children


DIRECT & INDIRECT MEASURES FOR SOCIAL FUNCTIONING

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with AS had more difficulty with nonverbal social cues than children with NLD. In a further study, we reported no difficulties in fine motor coordination in the NLD group (Wilkinson-Smith & Semrud-Clikeman, 2014). In another study, children with NLD were not found to have visual-spatial deficits but did show poorer gross motor skills (Miller & Ozonoff, 2000). It has not been found that children with NLD show stereotyped or restricted patterns of interest or difficulty with adherence to a schedule or ritual that are often seen in children with AS or HFA (Davis & Broitman, 2011; Palombo, 2006). These behavioral differences may separate these two disorders. A recent literature search found no articles that have contrasted groups of children with HFA or AS and those with NLD on direct or indirect social perception and functioning measures. The current study sought to evaluate the differences on direct and indirect measures of social perception and functioning, which are present between these two groups as well as a control group. Given the suggestion that HFA or AS may be a more severe form of social reciprocity difficulty than NLD (Gunter, Ghaziuddin, & Ellis, 2002), it would be expected that this group would experience more difficulty on both direct and indirect measures of social perception and functioning compared to the NLD and the control groups. The present study evaluated group differences on a direct measure of social perception and on parent and teacher and self-ratings of emotional, social, and behavioral functioning in children with HFA or NLD. The main hypothesis of the study was that children with HFA or NLD would be significantly less successful on direct measures of social understanding compared to the control group. It was also hypothesized that children with HFA would show more difficulty compared to those with NLD. The tendency to socially withdraw from peer interaction has been linked to higher rates of depression and poorer social skills. Thus, it was hypothesized that the HFA group would experience significantly more social and emotional difficulties compared to the control group with scores in the clinical range on measures of social withdrawal, anxiety, and depression on teacher and parent behavior ratings. Children with HFA were also expected to show the most difficulty compared to those with NLD.

METHOD Participants Participants were children referred by parents, teachers, psychologists, psychiatrist, and pediatricians or recruited to a large university in the Midwestern United States for participation in a larger 5-year study examining the psychological and neuropsychological functioning of children with developmental disorders. The final sample included 105 children ranging in age from 8.5 years to 16.6 years. There were 77 males and 28 females in the sample with 5% of the sample self-identified as a minority (Hispanic, African American, and Asian). There were three groups of children identified for the purpose of this study: control (n = 38), HFA (n = 36), NLD (n = 31). Doctoral-level graduate students trained in administering the social perception measure individually assessed the participants. These graduate students were blind to the diagnosis of the child. Diagnoses were determined by consensus of two independent licensed psychologists. Participants for whom a diagnosis was not unanimous were not included in the study (n = 2). Exclusionary criteria included a history of a learning disability, seizure disorder, progressive neurological problems, traumatic brain injury, or

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Table 1 Diagnostic criteria for group selection. HFA Scores on the three modules of the ADI-R above cut-off including stereotyped behaviors Four symptoms on Section C of ADI-R Met at least two of Criteria 1 of DSM-IV-TR Autistic Disorder Met at least two of Criteria 2 of DSM-IV-TR Autistic disorder Met at least two of Criteria 3 of DSM-IV-TR Autistic Disorder Verbal IQ 80 or above


Score of more than 15 on the Social Communication Questionnaire

NLD One or fewer modules above cut-off on ADI-R Two or fewer symptoms on Section C Symptoms do not meet criteria for Autistic Disorder or Asperger disorder from DSM-IV-TR Verbal IQ 80 or above Reading skills above 80 on the WJ-Ach-III Score of less than 12 on the Social Communication Questionnaire

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 verbal IQ above 80 were included for the full sample. 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. They completed all neuropsychological and emotional/behavioral measures except the ADI-R. Table 1 outlines the diagnostic criteria used to define the groups. Inclusion in the ASD group was obtained using ADI-R (Le Couteur, Lord, & Rutter, 2003) conducted by one of the authors (a licensed psychologist) and was secondarily confirmed using DSM-IV-TR (APA, 2000) criteria for this study. Each child was subsequently reviewed by the other author, also a licensed psychologist, and was included in the sample if agreement was unanimous. Both psychologists met the reliability standard for the ADI-R above the 90th percentile. There were 5 children excluded from the study who did not meet all of these criteria. Each child, prior to coming to the study, had been diagnosed with autism by outside practitioners. The parents of children with NLD also completed the ADI-R (Le Couteur et al., 2003). Consistent with the recommendations from research criteria (Rourke & Tsatsanis, 2000), children with NLD qualified for this group if they met all of the criteria listed in Table 1. In addition, to qualify for a diagnosis of NLD, 3 of the 4 criteria below also needed to be met: ● Scores on the Block Design subtest of the WASI below 40; ● Math calculation skills below the 15the percentile on the math calculation subtest of the Woodcock-Johnson Achievement Test-III (WJ-Ach-III; Woodcock, McGrew, & Mather, 2001) or scores on the calculation subtest more than 1.5 standard deviations (22 standard score points) below estimated verbal IQ; ● Scores at least one standard deviation below average on the Rey-Osterreith Complex Figure Taylor system of scoring (Osterreith, 1944); ● Scores below one standard deviation on all three scores on the Purdue Pegboard (Tiffin, 1968). These symptoms were chosen from the literature as illustrative of a nonverbal learning disability. We decided to use a more conservative approach to diagnosis and to view the disorder as a syndrome that incorporated the main areas of visual-motor skills,



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social functioning, good verbal ability, and possible right hemispheric dysfunction as suggested by previous research (Rourke & Tsatsanis, 2000). While we hypothesized that social functioning is an important part of NLD, it is not included in the classical definitions. For that reason, we did not use it as a selection measure but rather as an outcome measure to determine whether social difficulties are indeed present in this group. It is important to mention here that children with HFA may have many symptoms that are consistent with a diagnosis of NLD. For the current study, however, children with HFA 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. These are all symptoms outlined in the DSM-5 as required for a diagnosis of ASD. The children in the HFA group also were not required to show the NLD symptoms as detailed above. Instruments Inclusionary Instruments. Wechsler Abbreviated Scale of Intelligence (WASI; Psychological Corporation, 1999). The WASI is an abbreviated scale of intelligence with measures of similarities, vocabulary, block design, and matrix reasoning. It provides an estimated verbal IQ (VIQ), performance IQ (PIQ), and Full-Scale IQ (FSIQ). The Verbal IQ was used for this study. A previous study had found that children with NLD showed significant difficulties on the Performance subtests that resulted in a significant verbal/ performance split lowering the FSIQ (Semrud-Clikeman et al., 2010). Woodcock-Johnson Achievement Battery-III (WJAch-III; Woodcock et al., 2001). Three subtests from the WJ-Ach-III were administered: letter-word identification, calculation, and mathematics reasoning. Psychometric properties of this instrument are reported to be excellent. The letter-word subtest was used as a screen to rule out a verbal learning disability. A score of 16 or more standard score points is considered to be a significant deficit in learning and is used in this study to determine eligibility (Sattler, 2001). 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. The Rey Osterreith has been used with children with cognitive difficulties and has been found to be a sensitive measure for visuospatial perception as well as learning and memory (Kirkwood, Weiler, Bernstein, Forbes, & Waber, 2001; Sami, Carte, Hinshaw, & Zupan, 2004). It has been used successfully with children with significant difficulties with the visuospatial deficits seen in children with NLD (Antshel et al., 2008). Purdue Pegboard (Tiffin, 1968). The Purdue Pegboard is a measure of manual dexterity. It requires the child to place pegs in holes as quickly as possible first with the

6



dominant hand, then the nondominant hand, and then both hands together for 30 seconds each. The time it takes to place the pegs is converted to a z-score. 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). Analysis of scores indicates that, when the dominant hand exceeds the nondominant by three or more points, there is evidence for dysfunction in the contralateral hemisphere (Lezak et al., 2004). Social Communication Questionnaire (SCQ; Rutter, Bailey, Berument, Lord, & Pickeles, 2003). The SCQ is a 40-item yes/no parent-report screening measure that evaluates symptoms commonly found in children with autism and is matched to ADI-R (Rutter et al., 2003). Scores are based on behaviors that are rare in children without autism. Scores above 15 are generally considered to be consistent with a diagnosis of autism. We administered this to all groups as an additional screening measure since the ADI-R was not administered to the control group. Study Measures CASP. The Child and Adolescent Social Perception Measure (CASP; MagillEvans, Koning, Cameron-Sadava, & Manyk, 1996). The CASP was developed as a clinical tool for evaluating social perception using 10 videos. The videos show social interactions between two or more child actors or a child and an adult, with each video vignette lasting approximately 1 minute. The intonation of the voices is audible while the language is disguised by distortion. The child describes each vignette and then is asked to explain how the characters are feeling (CASPem score) and then to explain how they know what the characters felt (“mouth turned up in a smile,” or “eyebrows were raised,” or “voice went up”) (CASPnv score). The range of emotions portrayed in the vignettes is from basic emotions of happy or sad to more complex ones depicting embarrassment or frustration. More points are awarded for the awareness of the complex emotions. Raw scores are calculated by number of emotions and NV given by the child and are then converted to standardized z-scores, reflecting age differences in a normative sample. Training for scoring of the CASP was utilized and agreement among scorers was required to be at the 95th percentile prior to administering the test independently. Validation of the CASP has found good internal consistency (Cronbach’s alpha ranging from .88 for the CASPem to .92 for the CASPnv with test-retest reliability reported to range from .83 to .87; Magill-Evans, Koning, Cameron-Sadava, & Manyk, 1995). Validity for the CASP has been demonstrated in its ability to discriminate children with AS from typically developing children (C. Koning & Magill-Evans, 2001b). In addition, it has been found to correlate with the social skills rating scale at a low but significant level perhaps indicating that different areas of social functioning are being evaluated (Koning & Magill-Evans, 2001a). Behavior Assessment System for Children-2 (BASC-2; Reynolds & Kamphaus, 2004). The BASC-2 is an omnibus behavioral rating scale that provides normative data for specific behaviors. The internalizing, externalizing, behavioral symptoms index and adaptability scales from the teacher and parent versions are reported in the Table 2 for clarity but are not the main focus of this article. The main interest was whether children with HFA or NLD would show higher scores on the subscales of anxiety,


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Table 2 Selection measures. Control


Measure

Mean

HFA SD

NLD

Mean

SD

Mean

SD

Age (months) 156.7 31.1 154.4 CASP EM −0.7 1.3 −1.6 NV −1.0 1.4 −2.1 WASI Verbal IQ 111.4 13.1 105.9 Performance IQ 110.9 9.8 97.1 Full-Scale IQ 113.0 10.9 102.3 Woodcock-Johnson Achievement Battery–III Letter-Word ID 107.0 12.8 102.4 Calculation 108.0 14.4 94.7 Rey-Osterreith −0.3 1.0 −2.0 Purdue Pegboard Dominant Hand −0.6 1.2 −1.5 Nondominant Hand −0.5 1.4 −1.5 Both Hands −0.1 2.2 −1.8 SCQ 5.8 6.4 18.5

31.5

154.2

29.1

1.2 1.0

−1.1 −1.9

0.9 0.9

15.9 14.4 16.3

113.1 100.8 104.0

15.1 16.5 14.5

ns C > HFA, NLD C < HFA, NLD

12.9 16.1 2.0

102.4 82.2 −2.0

9.3 13.4 1.5

ns C> HFA, NLD; HFA>NLD C > HFA, NLD

1.6 1.4 1.5 7.8

−1.8 −1.7 −1.2 10.1

1.5 1.5 1.8 5.5

C > HFA, NLD C> HFA, NLD C > HFA, NLD C < HFA, NLD NLD < HFA

6.2 5.5 3.9 3.1

7.1 4.2 1.6 1.5

4.4 2.2 1.4 1.3

HFA HFA HFA HFA

Autism Diagnostic Interview-Revised Part A NA Part B-verbal NA Part B-nonverbal NA Part C NA

17.3 11.1 5.6 7.3

Significance ns C > HFA; NLD > HFA C > HFA, NLD

> > > >

NLD NLD NLD NLD

Note. EM = Emotion Cues; HFA = High Functioning Autism; NLD = Nonverbal Learning Disability; SD = Standard Deviation; ns = nonsignificant; C = control; ID = identification; SCQ = Social Communication Questionnaire; NA = nonapplicable.

depression, withdrawal, and social skills. Similarly, the Self-Report version of the BASC2 was also used with particular attention to the locus of control, self-esteem, and selfreliance scales.

Behavior Rating Inventory of Executive Functions (BRIEF; Gioia, Isquith, Guy, & Kenworthy, 2000). The BRIEF is a behavior rating scale with two forms: teacher and parent. It provides T-scores on measures of inhibition, emotional control, initiation, working memory for example as well as overall scores for behavioral regulation (BRI), metacognition (MI), and a global executive composite (GEC). Behavioral and Emotional Rating Scale-2 (BERS-2; Epstein, 2004). The BERS-2 is a parent-completed rating scale of the child’s emotional and behavioral strengths. Higher scores are generally considered to indicate better functioning. There are five scales: interpersonal strength, family involvement, intrapersonal strength, school functioning, and affective strength as well as an overall score for the BERS-2 Strength Index. Children are rated on a 0–3 scale with 3 being most like the child and 0 being less like the child. Psychometric properties are acceptable.

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Analyses Initial analyses were conducted using a multivariate analysis of variance (MANOVA) for the main indices for the BASC-2, BRIEF, and BERS-2. A follow-up general linear model (GLM) including univariate analyses of variance (ANOVAs) and pairwise for selected post hoc comparisons based on the hypotheses was used to evaluate group differences. Post hoc comparisons were conducted among the clinical groups to determine what group differences were present. Given that there are several subscales for each of these measures, profile analysis was used to determine which subscales were most appropriate for further analysis using the group patterns and effects.


RESULTS Preliminary Measures Preliminary measures were administered determining group selection as outlined above. The measures are discussed below for each of the groups for which they were used to determine eligibility for the study. There were no significant differences among groups for age (p = .93) or for verbal IQ (p = .06). Table 2 provides the findings for all preliminary measures. Main Analyses The first hypothesis of this study stated that there would be group differences on the direct measure of social perception with the children with HFA or NLD scoring worse than the other groups. It was expected that children with HFA would score lower than those with NLD on both indices of the CASP. These hypotheses were partially confirmed by a 2 (CASPem, CASPnv) x 5 (Group) MANOVA. Findings indicated a significant Group effect was present, F(4, 172) = 4.996, p = .001, ηp2 = .104. See Table 2. Follow-up analyses found a significant Group effect for CASPem, F(2, 87) = 7.13, p = .006, ηp2 = .11, and for CASPnv, F(2, 87) = 11.2, p < .0001, ηp2 = .17. Post hoc analysis found that the HFA group scored lower than the control group (p = .002) and the NLD group (p = .04) on the CASPem. On the CASPnv, the control group scored significantly better compared to the HFA group (p < .0001) and NLD group (p = .002). However, there was no difference among the clinical groups on this measure contrary to our hypothesis. Table 3 provides the results for the study measures and Figure 1 illustrates these findings. We also compared the HFA and NLD groups to the control groups on the BASC-2 Parent overall scales. A 2 (Group) x 4 (Externalizing, Internalizing, Behavioral Symptoms Index [BSI] and Adaptability) MANOVA found a significant Group effect, F(8, 198) = 16.03, p < .0001, ηp2 = .39. Follow-up analyses found significant differences for Externalizing (p = .0001, ηp2 = .14), Internalizing (p = .001, ηp2 = .14), BSI (p < .0001, ηp2 = .43), and Adaptability (p < .0001, ηp2 < .0001). Post hoc analyses found that in all cases the control group scored significantly lower (better) than either of the clinical groups (see Table 3). Looking at the means for the externalizing scale all groups were within the average range. For the internalizing and adaptability scales, the NLD and HFA groups were within the at-risk rank. On the overall internalizing scale, the HFA group scored the highest (poorest). A profile analysis of the individual subscales found that the withdrawal (p < .0001), social skills (p = .001), and depression (p = .001) subscales were the most highly significant comparison. Figure 2 illustrates this finding.


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Table 3 Behavior Rating Scales for the three groups. Control Measure

NVLD

Mean

SD

Mean

SD

Mean

SD

Significance

−0.7

1.3

−1.6

1.2

−1.1

0.9

NV BASC-2 Parent Externalizing Internalizing BSI5 Adaptability1 Social Skills1 Anxiety Depression Withdrawal BASC-2 Teacher Externalizing Internalizing BSI Adaptability1 Depression Withdrawal BASC-2 Self-Report Internalizing School Performance Inattention ESI8 Depression Inadequacy BRIEF-Parent BRI9

−1.0

1.4

−2.1

1.0

−1.9

0.9

C > HFA; NLD > HFA C > HFA, NLD

48.3 50.7 49.1 54.5 53.0 52.0 51.3 50.6

7.2 10.8 8.4 8.9 11.1 13.5 10.0 10.1

57.5 61.3 61.3 33.4 36.6 60.5 64.1 73.9

11.7 14.4 14.4 8.4 9.1 15.4 15.7 12.5

55.4 61.2 61.2 35.5 40.0 58.9 64.3 69.5

11.3 13.2 13.2 6.7 8.8 13.4 13.9 13.0

C C C C C C C C

< < < > > < <
C< C
HFA, NLD NLD > HFA C > HFA, NLD C > HFA, NLD C > HFA, NLD C > HFA, NLD

20.0 2.9 2.5 2.3 2.5 3.2

92.2 10.5 9.5 8.8 9.5 8.2

16.0 2.6 3.3 2.8 2.4 3.2

Family Involvement 11.6 2.8 8.2 Intrapersonal Strength 11.5 3.4 6.1 School Functioning 11.6 3.2 7.7 Affective Strength 11.8 2.9 7.5 Behavioral and Emotional Rating Scale-Teacher Strength Index 114.0 17.3 95.2 Interpersonal Strength 12.1 2.9 10.5 Family Involvement 12.4 2.7 10.2 Intrapersonal Strength 12.0 3.23 8.7 School Functioning 12.4 2.6 9.9 Affective Strength 11.4 3.5 9.4

C> ns C> C> C> C>

HFA, NLD HFA, NLD HFA, NLD HFA, NLD NLD

Note. HFA = High Functioning Autism; NLD = Nonverbal Learning Disability; SD = Standard Deviation; C = Control; BSI = Behavioral Symptoms Index; ns = Nonsignificant; ESI = Emotional Symptoms Index; BRI = Behavioral Regulation Index; MI = Metacognition Index; GEC = General Executive Composite. 1 Higher scores are desirable.

Figure 1 CASP Results.

The teacher BASC-2 was completed by fewer teachers. For this measure, we were able to obtain information for 25 typically developing, 20 NLD, and 20 HFA participants. A 2 (Group) x 4 (BASC-2 Indices) MANOVA yielded a significant group effect, F(8, 118) = 5.64, p < .0001, ηp2 = .28. Post hoc analyses found a significant Group effect for Internalizing (p = .001, ηp2 = .21), BSI (p < .0001, ηp2 = .25), and Adaptability (p < .0001, ηp2 = .33). A review of the means for all of these scales indicated that, for the most part, the means are well within expectations for age and are not in the clinically



11

Figure 2 BASC-2 parent scores.

significant range. Profile analysis found two main significant comparisons. The HFA group scored significantly poorer on the depression scale compared to the control group (p < .0001) thus confirming one of our hypotheses. Both clinical groups scored poorer on the withdrawal scale (p < .001). The BASC-2 self-report was also administered to the full sample. There was a significant Group difference for the main scores, F(8, 192) = 3.03, p = .003, ηp2 = .11. Profile analysis indicated that only the attention, depression, and inadequacy scales were of interest. Pairwise comparisons indicated that both clinical groups were significantly different from the control group on the attention scale (NLD p < .0001; HFA, p = .03). The NLD group scored significantly higher (poorer) than the control group on the depression scale (p = .008) and inadequacy (p < .0001). The NLD group also scored significantly higher (poorer) than the HFA group on attention (p = .01) and inadequacy (p = .008). The BRIEF-Parent (BRIEF-P) was also administered to the main caregiver of the child to determine whether difficulties were present in regulation of emotions and executive functioning. A 3 (Group) x 3 (Behavioral Regulation Index [BRI], metacognition, General Executive Functioning) MANOVA yielded a significant Group effect, F(6, 188) = 22.74, p < .0001, ηp2 = .42. Follow-up ANOVAs found significant Group effects for BRI (p < .0001, ηp2 = .501), metacognitive index (p < .0001, ηp2 = .595), and general executive functioning (p < .0001, ηp = .64). In all cases, there is a moderate effect for these three main indices. A profile analysis of the BRIEF-P subscales indicated a significant interaction effect, F(14, 174) = 5.6, p < .0001, ηp2 = .31. Follow-up comparisons found clinically significant results present for the shift, emotional control, working memory, and planning/ organization scales. On all scales, there was a significant difference for the clinical groups from the typically developing children (p < .0001). For the shift scale, the HFA group scored worse than the NLD group (p = .009) as well as on the emotional control scale (p = .026). Sixty-five teachers completed the teacher form of the BRIEF. There were completed forms for 25 children in the control group, 20 in the NLD group, and 20 in the HFA group. A 3 (Group) x 3 (BRI, Metacognition Index, General Executive Functioning


12


Index) MANOVA resulted in a significant Group effect, F(6, 120) = 6.92, p < .0001, ηp2 = .26. Post hoc analyses found the control group scoring significantly better than both clinical groups (p < .0001) on all main indices. The clinical groups differed from each other on the BRI index with the HFA group scoring significantly poorer than the NLD group (p = .035). Follow-up post hoc ANOVAs found a significant effect for all indices (p < .0001). To determine which subtests were the most important to evaluate, a profile analysis was conducted that resulted in a significant Group finding, F(7, 54) = 5.6, p < .0001, ηp2 = .42, but not a significant interaction effect (p = .06). Profile analysis found that shift, working memory, planning/organization, and organization of materials differed among the groups. For these scales, post hoc analysis found the HFA group differed significantly from the control group on the following scales: shift (p < .0001) and working memory (p < .0001). The NLD group differed from the control group on shift (p = .001), and working memory (p < .0001). The HFA group was rated poorer than the NLD group on shift (p = .008). Twenty-five children in the control group and 24 in each of the NLD and HFA groups completed the self-report form of the BRIEF. A 3 (Group) x 3 (BRIEF Main Indices) MANOVA resulted in a significant Group effect, F(6, 136) = 2.97, p = .009, ηp2 = .12. While the findings were significant, the means are all in the average range. This was true also for the individual scales. No further analysis was conducted. Finally the caregivers for all groups completed the BERS-2. The parent-completed BERS-2 resulted in a significant Group finding, F(12, 194) = 7.96, p < .0001, ηp2 = .33, for a moderate effect. Profile analysis found a significant interaction effect, F(10, 104) = 2.58, p = .008, ηp2 = .2. Follow-up analysis indicated that the main contributors to this significance were lower scores on the scales of intrapersonal strength and school functioning (p < .001) for both clinical groups with no difference between the clinical groups. The teacher form of the BERS-2 resulted in significant Group finding, F(4, 55) = 2.6, p = .008, ηp2 = .2). While profile analysis did not find a significant interaction effect, F(3.6, 78) = 0.89, p = .51, ηp2 = .03, a significant Group effect was found, F(3.6, 78) = 4.71, p = .002, ηp2 = .03. Follow-up analyses found that this was due to significant group differences on the subscales of intrapersonal strength and school functioning. Pairwise comparisons of these two subscales found that there was a significant difference on both of these scales (p < .0001) with the control group scoring better than either clinical group with no significant difference found between the clinical groups. While these findings are significant, they are not necessarily clinically important as all groups scored well within the average range. For the self-report form of the BERS-2, a 3 (Group) x 5 (Main Indices) MANOVA did not result in a significant Group effect. F(12, 190) = 1.68, p = .07, ηp2 = .096. Selected subtests of the BRIEF and BASC-2 were correlated to the CASP. As can be seen in Table 4, the CASP significantly correlated with several indices of the BRIEF and BASC-2. Particular relation was found between the CASP and the main indices of the BRIEF measuring metacognition. DISCUSSION The purpose of this study was to utilize direct and indirect measures of social and emotional functioning with children with HFA and NLD as well as typically developing children. Most previous studies have solely utilized behavioral ratings


13

Table 4 Correlation matrix of CASP, BASC-2, and BRIEF. CASPem CASPnv CASPem CASPnv Dep With


BRI MI GEC SHIFT INIT WM PPO MON

.623 .000

Dep

With

BRI

MI

WM

PPO

MON

EMO Con

GEC

SHIFT

INIT

−.073 −.209 −.220 −.198 −.228 .463 .035 .031 .051 .025 −.206 −.275 −.439 −.442 .038 .005 .000 .000 .545 .706 .551 .647 .000 .000 .000 .000 .569 .609 .646 .000 .000 .000 .737 .893 .000 .000 .959 .000

−.275 .006 −.275 .005 .616 .000 .689 .000 .882 .000 .701 .000 .825 .000

−.188 −.201 −.188 −.213 −.175 .07 .048 .066 .036 .089 −.417 −.399 −.437 −.456 −.289 .000 .000 .000 .000 .004 .570 .480 .334 −.456 .681 .000 .000 .001 .000 .000 .668 .554 .575 .549 .454 .000 .000 .000 .000 .000 .714 .691 .690 .764 .901 .000 .000 .000 .000 .000 .912 .943 .964 .910 .580 .000 .000 .000 .000 .000 .898 .905 .916 .913 .746 .000 .000 .000 .000 .000 .718 .662 .659 .690 .751 .000 .000 .000 .000 .000 .842 .863 .820 .567 .000 .000 .000 .000 .888 .808 .525 .000 .000 .000 .858 .550 .000 .000 .820 .000

Note. CASPem = CASP Emotional cues; CASPnv = CASP Nonverbal Cues; Dep = BASC- 2 Parent Depression; With = BASC-2 Parent Withdrawal; BRI = BRIEF-P Behavioral Regulation Index; MI = BRIEF—P Metacognition Index; GEC = BRIEF-P General Executive Composite; INIT = BRIEF-P Initiate; WM = BRIEF-P Working Memory; PPO = BRIEF—P Planning and organization; MON = BRIEF-P Monitor; EMO Con = BRIEF-P Emotional Control.

completed by caregivers to determine how children with developmental disorders function in social settings. A literature search found no studies that compare children with HFA with those with NLD on a measure of social perception or social performance. The main finding of this study was that children with HFA and children with NLD had difficulty evaluating the EM and NV on a measure of direct social perception. Both groups showed much poorer understanding of social exchanges compared to the control group on both scales (EM and NV). For the present study, it had been expected that children with HFA would show more difficulty on the direct measure of social perception compared to the NLD group. This finding was not present. The findings from the current study are consistent with our previous study that found that children with AS and those with NLD were more similar than different in their ability to understanding social interactions (Semrud-Clikeman et al., 2010). Other than our previous work cited above, there are no studies that we could identify in a literature search contrasting HFA and NLD on these measures. Previous findings regarding the similarities between AS and HFA groups have found qualitative rather than quantitative differences. The current findings continue to highlight the difficulties with social perception experienced by children with HFA and NLD. These findings are also similar to the differences we previously found in children with AS.


14


The teacher (TRS) and parent (PRS) behavioral ratings were fairly consistent for the groups. As expected the control group showed better behavioral functioning in all areas compared to the clinical groups. For the PRS measure, children in both clinical groups showed significantly more behavioral symptoms on the BSI particularly in the area of withdrawal and sadness compared to the control group. Overall, the self-report BASC-2 (SRP) showed no clinically significant findings, which may indicate that children with these disorders either are not aware of the level of distress present or were not willing to report it on a behavioral rating scale. Previous studies have indicated that children with HFA or NLD show signs of sadness particularly as they became older (Ozonoff & Rogers, 2003; Rourke, 2000; Semrud-Clikeman, Walkowiak, Wilkinson, & Minne, 2010). In contrast, one study did not find significant difficulties with depression in children with NLD (Forrest, 2004). While the depression and anxiety scale (as well as the internalizing scale) on the BASC2 were in the at-risk range for both the HFA and NLD groups, the HFA showed a clinically significant finding on withdrawal with the NLD group just slightly below clinically significant on the withdrawal scale (69.5). Children who are withdrawn frequently do not interact with others and do not then practice the skills that lead to additional social interactions (Semrud-Clikeman, 2007; Semrud-Clikeman & Glass, 2010). Clinically these findings are important because children with HFA and NLD may not only inaccurately interpret social interactions but also may withdraw from social interactions following several negative experiences. Perceptive parents and teachers become aware of these difficulties and need to provide support so that these children do not withdraw from social interactions. On a measure purported to distinguish children with behavioral and emotional difficulties (BERS-2), the scores were generally within the average range for all groups. This measure was not helpful for use to discriminate children with HFA from NLD and did not add to the diagnosis. There is a strong relation between the CASP Nonverbal scores and all of the BRIEF parent scores and the depression and withdrawal scales of the parent BASC-2. This is the first published study that has compared CASP scores with executive functioning scores on the BRIEF. Those children with higher scores on depression and withdrawal and the BRIEF scores performed poorer on the nonverbal scale. This finding is significant as difficulties with emotional modulation and/or depressed mood were significantly related to the child’s ability to recognize NV. It is not clear from our data if there is a cause-and-effect relation. However, if a child has difficulty with NV and misidentifies these and acts accordingly to the mistaken perception, it is not unlikely that the child will feel sad and may withdraw from further social interactions particularly if there is a negative outcome. This difficulty may be bidirectional and should be further studied. While children with HFA or NLD do differ in some dimensions, there appears to be more similarity than difference on the behavioral and executive functioning behavior rating scale. Both groups had difficulty on day-to-day executive functioning as measured by the BRIEF as well as with a tendency to withdraw from social situations. These measures are not significantly sensitive enough to differentiate between these clinical groups. While the CASP did show differences on the ability to recognize EM between the two clinical groups, the differences were not substantial. These findings suggest that these two disorders may reflect different degrees of difficulty in social perception rather than a quantitative difference.


15


We recently published an article about differences we found in the corpus callosum area with smaller splenial measures only for children with NLD (Fine et al., 2014). Similarly, we found differences in amygdaloid volume with the HFA group showing larger volumes than the NLD and control groups (Semrud-Clikeman, Fine, Bledsoe, & Zhu, 2013). Such amygdaloid volume differences may underlie some of the difficulties with executive functioning seen in the present study. As noted by the findings of the current study where the neuropsychological measures are similar between the HFA and NLD groups, behavioral performance may result from a different underlying pathoneuroanatomical basis. Connecting the neuroanatomical/neurofunctional data with behavioral data will be an important next step for our understanding of these disorders. LIMITATIONS OF THE STUDY A limitation of this study is the difficulty in diagnosing NLD. We chose to use a very conservative method that combined a previous diagnosis with selected measures gleaned from the literature. It is not clear how representative our selection process would be compared to the literature as selection varies widely across researchers (Forrest, 2007). Finally, the findings from the behavioral ratings need to be considered carefully. In most cases, all groups were rated within the clinically acceptable range and did not qualify for diagnoses of anxiety and/or depression. We also did not administer direct measures of executive functioning for this particular study. There was less compliance by teachers in completing many of the instruments. Due to age restrictions for the self-report of the BRIEF, the number of self-reports was also lower. These lower numbers of reports that were completed may have affected the generalizability of these findings to the larger population. Thus, the teacher scores should be viewed cautiously. CONCLUSION In conclusion, our study indicated that children with HFA or NLD experience difficulty understanding NV in social interactions with children with HFA experiencing additional difficulty with interpreting EM. Children with HFA or NLD were also shown to show more clinically significant difficulty in the area of social withdrawal compared to the typically developing children. This tendency coupled with difficulty interpreting social interactions as demonstrated on the CASP may contribute to further feelings of isolation and withdrawal. It is important to note that there were few significant differences on behavioral rating scales between the two clinical groups with slightly more elevation on the withdrawal scale for the HFA group. It is also important to note that, on several of the indices, both clinical groups were functioning quite well and were particularly noted on the teacher rating scales. The most difficulty was found in the ratings of executive functioning for both clinical groups. These difficulties likely impact adaptive skills as well as social functioning and should be carefully evaluated for children with these difficulties. Clinicians need to be particularly sensitive to these tendencies and to provide additional resources and interventions. Of significant concern is the general finding of children with NLD being identified at older ages and showing more sadness compared to their peers (Fine et al., 2012; Poletti, 2010). Without early identification, these children

16


may go on to develop significant mental health issues that are frequently unaddressed until they are adults (Davis & Broitman, 2011). Children with both types of disorders were found to either not report concerns or to not be aware of such concerns. Qualitative clinical interviews would be an important method for evaluating the emotional functioning of these children. Original manuscript received April 22, 2014 Revised manuscript accepted November 29, 2014 First published online February 20, 2015


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