J Abnorm Child Psychol DOI 10.1007/s10802-014-9902-9

Attention-Deficit/Hyperactivity Disorder Symptoms Mediate the Association between Deficits in Executive Functioning and Social Impairment in Children Nora Bunford & Nicole Evangelista Brandt & Catherine Golden & Jana B. Dykstra & Julie A. Suhr & Julie Sarno Owens

# Springer Science+Business Media New York 2014

Abstract We investigated whether symptoms of attentiondeficit/hyperactivity disorder (ADHD) are pathways through which deficits in inhibition and working memory are associated with teacher- and parent-rated social impairment in children. Participants were 64 children (55 % males; 53 % with ADHD) in grades 3–6. Consistent with our hypotheses, the association between inhibition and social impairment was mediated by hyperactivity/impulsivity and the association between working memory and social impairment was mediated by inattention. Support was not obtained for alternative models wherein the association between inhibition and social impairment was mediated by inattention, and the association between working memory and social impairment was mediated by hyperactivity/impulsivity. Further, tests of hierarchical models suggest that neither inhibition nor working memory is primary but, rather, that these cognitive processes are related to one another and that they collectively (but not uniquely) contribute to hyperactivity/impulsivity and inattention. These findings have implications for conceptual models of ADHD, for understanding factors that influence and sustain social

Electronic supplementary material The online version of this article (doi:10.1007/s10802-014-9902-9) contains supplementary material, which is available to authorized users. N. Bunford (*) : J. B. Dykstra : J. A. Suhr : J. S. Owens Department of Psychology, Ohio University, Athens, OH 45701, USA e-mail: [email protected] N. E. Brandt University of Maryland School of Medicine, 685 W Baltimore St #480, Baltimore, MD 21201, USA C. Golden Louis Stokes Cleveland VA Medical Center, 10701 East Blvd, Cleveland, OH 44106, USA

impairment among youth with symptoms of the disorder, and for interventions aimed to addressing such impairment. Keywords ADHD . Executive functioning . Hyperactivity/ impulsivity . Inattention . Social impairment . Children Attention-deficit/hyperactivity disorder (ADHD) is a prevalent and impairing disorder (American Psychiatric Association 2013) that typically first manifests during the preschool years and persists through adulthood (Barkley et al. 2008). Of the impairments commonly associated with ADHD, social impairment is particularly pervasive and intractable (McQuade and Hoza 2008). Given the negative impact of childhood social impairment on later social adjustment (Parker and Asher 1987), it is important to understand factors that contribute to and sustain social impairment among youth with ADHD. Executive functions, including inhibition and working memory, are important for competent social functioning among youth with ADHD (Huang-Pollock et al. 2009; Kofler et al. 2011; Rinsky and Hinshaw 2011). There is evidence of positive bivariate associations between poor performance on measures of executive functioning (relative to non-ADHD controls) and ADHD symptoms (Halperin et al. 2008), executive deficits and social impairment (Diamantopoulou et al. 2007), and ADHD symptoms and social impairment (McQuade and Hoza 2008). Yet, there is limited understanding of mechanisms involved in these associations, a better understanding of which has implications for (a) conceptualizing ADHD and the factors that lead to and sustain social impairment in this population and (b) developing or refining interventions for social impairment. The aim of this study was to examine mechanism(s) that underlie these bivariate effects; specifically, whether ADHD symptoms mediate the effects of executive deficits on social impairment in children.

J Abnorm Child Psychol

Executive Dysfunction is Associated with ADHD Although not all children with ADHD demonstrate executive deficits, early-appearing and enduring deficits in inhibition, working memory, set shifting, and planning are positively associated with ADHD (Halperin et al. 2008). Specifically, the severity of executive deficits is linearly associated with the severity of ADHD symptoms (Depue et al. 2010), the presence of executive deficits distinguishes individuals whose ADHD symptoms remit from those whose symptoms persist (Halperin et al. 2008), and improvements in executive functioning are associated with declines in ADHD symptoms over time (Miller et al. 2013). Neuropsychological theories of ADHD illuminate deficits that underlie symptomatic behavior (Nigg et al. 2002). The implications of two widely cited neuropsychological models of ADHD (Barkley 1997; Sonuga-Barke 2002) are that disinhibition is primarily associated with hyperactivity/impulsivity symptoms (H/I), whereas a deficit in working memory is mainly associated with inattention symptoms (IA). Barkley’s (1997) model of ADHD is hierarchical and posits that deficits in four executive functions, including working memory, are secondary to a deficit in inhibition. Thus, in Barkley’s model, an inhibitory deficit underlies both H/I and IA. That is, any behavioral expression that is a result of impaired working memory is also a result of disinhibition, because the former depends on the latter, but the latter does not necessarily depend on the former. Championing a competing model, Sonuga-Barke (2002; 2003) proposes a dual pathway model of ADHD wherein executive functions associated with high affective involvement such as the self-regulation of affect, motivation, and arousal, are distinguished from purely cognitive executive functions such as working memory. In contrast to Barkley’s model, Sonuga-Barke’s model does not place any of the executive systems implicated in ADHD into a hierarchical relation with the other (s), but rather indicates unique associations between inhibition and H/I, and working memory and IA. Empirical findings pertinent to these models are inconsistent. Some indicate that children with ADHD Combined Type demonstrate different executive deficits than those with ADHD Inattentive Type (e.g., Lockwood et al. 2001; Nigg et al. 2002, among boys only), indicating that H/I combined with IA is neuropsychologically distinct from IA alone. Conversely, other investigators have not found support for this pattern (e.g., Chhabildas et al. 2001; Faraone et al. 1998; Nigg et al. 2002, among girls only), indicating that the ADHD subtypes may not be distinguishable on the basis of neuropsychological measures. (Note: most studies focus on the Combined and Inattentive types and exclude the Hyperactive/ Impulsive Type). Because executive deficits may play a role in social impairment, this inconsistency has implications for conceptualizing not only the etiological relationship of the

symptom-dimensions (Nigg et al. 2004), but also for identifying a parsimonious set of variables that contribute to social impairment in ADHD.

ADHD is Associated with Social Impairment Children with ADHD experience significant impairment in social functioning (e.g., McQuade and Hoza 2008). Most are rejected by their peers (Hoza 2007) and, relative to typically developing peers, are less likely to have close dyadic friendships (Hoza et al. 2005). These impairments confer incremental risk for academic failure and school dropout, above and beyond the risk conferred by ADHD symptoms alone (Mikami and Hinshaw 2006). Further, social problems may result in youth with ADHD associating with deviant peers (Hoza 2007) and using substances (Greene et al. 1999), potentially contributing to further negative outcomes throughout the life span. Thus, it is important to understand mechanisms underlying social problems among youth with ADHD. Executive functioning may be one such mechanism in that it may predict social problems directly as well as indirectly, through ADHD symptoms.

Executive Dysfunction is Associated with Social Impairment Per social information processing theory (Crick and Dodge 1994), intact executive functioning is essential for social competence. For example, deficits in working memory processes responsible for processing and coordinating stored information are associated with impaired conflict resolution skills, peer rejection, and poor social competence among typicallydeveloping youth (McQuade et al. 2013). Deficits in inhibition, verbal and non-verbal working memory, and verbal fluency are associated with impaired adaptive behavior, communication, and socialization among youth with ADHD (Clark et al. 2002; Happe et al. 2006) (but see Biederman et al. 2004 for an exception) and with negative peer nominations (Diamantopoulou et al. 2007) among youth who exhibit symptoms of the disorder (but are undiagnosed).

ADHD Symptoms May Mediate the Association between Executive and Social Deficits As reviewed hitherto, it has been established that there are associations between executive deficits, ADHD symptoms, and social impairment. There is less research on specific mechanisms at play among these variables (Huang-Pollock et al. 2009; Kofler et al. 2011; Rinsky and Hinshaw 2011; Tseng and Gau 2013) and the available studies have

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limitations. For example, although the findings of both Huang-Pollock et al. and Kofler et al. indicate that ADHD symptoms mediate the association between executive deficits and social impairment, these authors either examined a single executive function (Kofler et al. 2011) or tested models only in the hypothesized direction, but not the reverse (Huang-Pollock et al. 2009; Kofler et al. 2011; Tseng and Gau 2013). Further, to our knowledge, no studies to date have examined the hierarchical relationships among executive deficits proposed by Barkley (1997). Thus, questions regarding executive functions other than working memory, the direction of causality (e.g., see Tseng and Gau 2013), and the relations among executive deficits remain unaddressed. Given heterogeneity within the ADHD population, the theories examined herein may only apply to those with executive deficits (Nigg et al. 2005). However, in light of the sophisticated evolution of these theories and the mounting empirical support for the associations described above, we argue that an enhanced understanding of these issues will contribute to the refinement of conceptualizations of the disorder and facilitate identification of factors that contribute to and perhaps sustain social impairment in this population. To examine such factors in the context of a theoretically-informed methodology, it is important to consider neuropsychological models specific to ADHD. As previously discussed, the relationships in Barkley’s (1997) model are hierarchical; whereas, the relationships in Sonuga-Barke’s model (2002) are linear. In the present study, we examined both hierarchical and linear models.

associated with H/I and IA (i.e., inhibition and working memory, respectively). Per Barkley’s conceptualization, we also tested hierarchical models (see Figs. 3 and 4) wherein deficits in one executive function (i.e., inhibition vs. working memory) are associated with deficits in another (i.e., working memory vs. inhibition), which are, in turn, associated with symptoms and result in social impairment. Accordingly, our second hypothesis was that inhibition would be primary to working memory (H2a), but working memory would not be primary to inhibition (H2b). Due to a paucity of research, we did not pose hypotheses regarding specific areas of social impairment.

Method Participants In the context of a larger study (Golden 2009), participants were recruited from elementary schools, mental health clinics, and a university listserv in rural Midwestern communities. Participants were 64 children in third to sixth grade (see Table 1 for participant characteristics). Although ADHD status is not used as a variable in any analyses, we report data on subsamples that meet/do not meet DSM-IV-TR criteria for ADHD, per evidence-based assessment guidelines (Pelham et al. 2005), to document that our sample has sufficient ADHD symptom and impairment variability to examine the stated research questions. Measures

The Present Study The aim of the present study was to examine the relationships among executive deficits, ADHD symptoms, and social impairment by exploring specific pathways through which these associations operate. Per Sonuga-Barke’s model, we first hypothesized that performance on measures of executive functioning previously identified as most closely linked to H/I (i.e., inhibition) would be associated with social impairment through H/I (H1a; see Fig. 1, Domain-Specific Linear Model). In addition, we hypothesized that performance on measures of executive functioning previously identified as most closely linked to IA (i.e., working memory) would be associated with social impairment through IA (H1b; see Fig. 2, DomainSpecific Linear Model). Given theoretical disagreement and the above-described mixed research findings, we also conducted exploratory analyses with domain-crossed models, wherein inhibition was paired with IA (see Fig. 1, DomainCrossed Linear Model) and working memory with H/I (see Fig. 2, Domain-Crossed Linear Model). Although a number of executive deficits are linked to ADHD, for purposes of parsimony, we focused on the two deficits most consistently

Wechsler Abbreviated Scale of Intelligence– Second Edition (WASI-II; Wechsler 1999). The WASI-II provides an estimate of cognitive ability in individuals 6 to 89 years. The 2-subtest score, tested in this study as a covariate, is highly correlated with the Wechsler Intelligence Scale for Children-Fourth Edition FSIQ (r=0.83; Homack and Reynolds 2007). Disruptive Behavior Disorders Rating Scale (DBD; Pelham et al. 1992). The DBD Rating Scale is a 45-item measure of the presence and severity of DSM-IV-TR symptoms of ADHD (IA and H/I), ODD, and CD. For this study, each child was rated by one parent and one teacher using a 4-point scale ranging from 0 (“not at all” present) to 3 (“very much” present), with higher scores indicating more severe symptoms. The ADHD subscales have adequate convergent validity when compared to classroom observations of distractibility, fidgeting, and academic accuracy (DuPaul et al. 1998). For the present sample, internal reliability for the four subscales ranged from 0.83 to 0.96 (parent) and 0.95 to 0.96 (teacher). To capture the full range of symptoms, the sum of parent and

J Abnorm Child Psychol

Fig. 1 Domain-specific and domain-crossed simple mediational models with response inhibition as the predictor

teacher ratings on the H/I and IA subscales was used in the analyses. Impairment Rating Scale (IRS; Fabiano et al. 2006). The IRS is a measure of parent and teacher perceptions of child impairment across a variety of domains (e.g., relationships with peers, siblings, and adults; family functioning; academic progress; self-esteem), as well as global impairment. Parents and teachers rate children’s functioning (one item per domain) along a 6-point continuum ranging from 0 (“Not a problem at all/Definitely does not need treatment or special services”) to 6 (“Extreme problem/Definitely needs treatment and special services”), with higher scores indicating more impairment and need for treatment. Strong internal consistency across domains (parent 0.95; teacher 0.97) and moderate to high convergent validity with other measures of impairment (e.g., r=0.77 between ratings of overall impairment on the IRS and on the Children’s Global Assessment Scale) has been demonstrated (Fabiano et al. 2006). In the present study, only the items assessing social impairment were used (i.e., parent-rated relationships with peers, parents, and overall family functioning; and teacher-rated relationships with peers and teacher). Teacher Rating Scale of Child’s Actual Behavior (TRS; Harter 1985). The TRS is a measure of teacher perceptions of a child’s competency across multiple domains (scholastic competence, social acceptance, athletic competence, behavioral conduct, global self-worth). Convergent and divergent validity of this measure have been demonstrated across several studies that included children with and without ADHD (e.g., Hoza et al. 2004; Hoza et al. 2010). In the present study, the social acceptance subscale (α=0.92) was utilized as a measure of social impairment. Higher scores indicate greater perceived competence.

Delis-Kaplan Executive Function System (D-KEFS) ColorWord Interference Test (Delis et al. 2001). Condition three of the D-KEFS Color-Word (CW) Interference Test was used as a measure of inhibition. In this condition words describing colors are printed in a color that is incongruent with the word (e.g., the word “green” printed in red ink). Participants must inhibit reading the word and instead say the color of the ink. The total time to complete Condition three was used as the measure of inhibition and was converted to age-scaled scores (M=10; SD=3), with higher scores indicating better inhibition. Test-retest reliability for Condition three across 25 days was excellent (r=0.90) in a sample of 8–19 year olds (Delis et al. 2001). Stop-Signal Task The Stop-Signal Task (SST) is a computerized task that measures inhibition. Participants respond to two different target stimuli by pressing different keys. Neuroimaging studies confirm that the process of stopping on the SST activates brain regions implicated in motor inhibition (e.g., inferior frontal cortex, subthalamic nucleus, premotor supplemental area) (Chambers et al. 2007). Children with ADHD are consistently found to demonstrate worse performance on this measure compared to typically-developing children (Alderson et al. 2007). The Stop Signal Reaction Time (SSRT), an estimate of the time needed for successful inhibition of response, was utilized in the present study. Longer reaction times (i.e., higher scores) indicate increased difficulty with inhibition. Stanford-Binet Intelligence Scales– Fifth Edition (SB5) Spatial Working Memory Test (Roid 2003). The SB5 Spatial Working Memory Test (WM) was utilized as a test of nonverbal working memory. This task is one of two subtests that comprise the Working Memory Index of the SB5, which has

Fig. 2 Domain-specific and domain-crossed simple mediational models with working memory as the predictor

J Abnorm Child Psychol

Deficits in Working Memory (Mediator #1)

H/I or IA symptoms (Mediator #2)

Social Impairment (Outcome)

Deficits in Inhibition (Predictor)

Fig. 3 Hierarchical model in which deficits in inhibition are primary to deficits in working memory

demonstrated good criterion validity (r=0.61 with the Working Memory Index of the Woodcock-Johnson Scales of Cognitive Ability, 3rd Edition) (Roid 2003). The Spatial WM subtest has high concurrent validity with the Verbal WM subtest of the SB5 (r=0.47) (Roid 2003). In addition, the Spatial WM subtest correlates higher with measures of nonverbal (r=0.43) and spatial memory (r=0.45) (Pomplun and Custer 2005) compared to the Verbal WM subtest. Higher scores represent better nonverbal working memory. Wechsler Intelligence Scale for Children, Fourth Edition (WISC-IV)– Digit Span (Wechsler 2003). The Digit Span (DS) subtest was used as a test of verbal working memory. Convergent and divergent validity are evidenced by a high correlation with the Working Memory Index (r=0.86), moderate correlation with Full Scale IQ (r=0.62), and low correlations with the Verbal Comprehension (r=0.44), Perceptual Reasoning (r=0.42), and Processing Speed (r=0.30; Sattler and Dumont 2004) indices. For this study, the total age-scaled score (M=10; SD=3) was utilized. Higher scores indicate better verbal working memory. Procedure All procedures were approved by the University Institutional Review Board. Following informed consent and assent procedures, parents and teachers completed ratings scales, and children completed the neuropsychological tests in a randomized, counterbalanced order during an individual session. Parents and teachers were instructed to complete all rating scales based on the child’s behavior when not medicated.1 Families were paid $15.00 and given a small toy, and teachers were paid $10.00. Because research suggests that individuals with ADHD who take stimulant medication perform better on tests of executive functioning than those who do not (e.g., Chow and Cummings 2007), 22 children who were prescribed

1 Although teachers were specifically instructed to rate children when not medicated, it should be noted as a limitation that we cannot be certain that this was the case. As such, the number of teacher-rated symptoms may be an underestimate.

a central nervous system stimulant were required to take a 12 h stimulant hiatus prior to participating.

Results Data Preparation and Analytic Plan Independent variables were inhibition on the CW and SSRT, and working memory on the WM and DS. Mediator variables were H/I and IA, indexed by the sum of parent and teacher ratings on the H/I and IA subscales of the DBD Rating Scale. Outcome variables were teacher- and parent-rated social impairment on the IRS and the social acceptance subscale of the TRS. Exploratory Factor Analysis We conducted an exploratory factor analysis (EFA) to determine whether the teacher- and parent-rated IRS items and social acceptance subscale of the TRS were measuring one construct (e.g., social functioning) or independent constructs (e.g., teacher- and parent-rated social functioning). Using the principal axis factoring method of extraction and direct oblique rotation, obtained eigenvalues (>1.0) as well as the scree test indicated that two factors produced the best fit. Based on item loadings, the factors involved teacher-rated (i.e., peer relationships = 0.94; teacher-child relationships = 0.89; TRS social acceptance = 0.74) and parent-rated (i.e., peer relationships = 0.90 parent–child relationships = 0.96; family functioning = 0.96) social functioning. We thus created two latent variables (teacher- and parent-rated social functioning) to index social functioning in all subsequent analyses. Simple Correlations To determine which independent variables were related to the putative mediator and outcome variables, simple correlations were computed among all variables of interest (see Table 2). Correlations indicated that DS was not significantly related to either of the outcome variables; therefore, it was dropped from the analyses while SSRT, CW, and WM served as the predictor variables in the ensuing analyses.

J Abnorm Child Psychol

H/I or IA symptoms (Mediator #2)

Deficits in Inhibition (Mediator #1)

Social Impairment (Outcome)

Deficits in Working Memory (Predictor)

Fig. 4 Hierarchical model in which deficits in working memory are primary to deficits in inhibition

Mediational Analyses of Domain-Specific Linear Models To test whether impairment on the independent variables is associated with social impairment through ADHD symptoms, a series of simple mediational analyses were conducted. We tested two models with SSRT as the predictor, H/I as the mediator, and two latent social functioning variables as the outcomes. We tested two models with CW as the predictor, H/I

as the mediator, and two latent social functioning variables as the outcomes (see Fig. 1, Domain-Specific Linear Model). Next, we tested two models with WM as the predictor, IA as the mediator, and two latent social functioning variables as the outcomes (see Fig. 2, Domain-Specific Linear Model). We first tested our models without controlling for the other ADHD symptom dimension, then repeated these analyses

Table 1 Descriptive Characteristics of Sample Variable

Total Sample (n=64)

ADHD Group (n=34)

Non-ADHD Group (n=30)

Age (M, SD) Gender (Percent Male) Caucasian SES (M, SD)a* Has Repeated a Grade* WASI- II Two Subtest Score (M, SD)b* Meets Criteria for ADHD Combined Typec Meets Criteria for ADHD Inattentive Typec On Medication for ADHDd* Parent DBD Inattention (M, SD)e Teacher DBD Inattention (M, SD) e Parent DBD Hyperactivity/Impulsivity (M, SD)e Teacher DBD Hyperactivity/Impulsivity (M, SD)e Parent Impairment Rating Scale – Peers (M, SD)* Parent Impairment Rating Scale – Parents (M, SD)* Parent Impairment Rating Scale –Family (M, SD)*

9.64 (1.15) 35 (54.7 %) 60 (93.8 %) 32.25 (14.53) 8 (12.5 %) 95.97 (16.03) 28 (43.8 %) 6 (9.4 %) 22 (34.4 %) 1.16 (0.91) 1.01 (0.76) 0.93 (0.96) 0.73 (0.83) 1.24 (1.84) 1.5 (1.98) 1.64 (1.95)

9.65 (1.18) 20 (58.8 %) 30 (88.2) 27.0 (13.38) 7 (20.6 %) 91.15 (14.69) 28 (82.4 %) 6 (17.6 %) 22 (64.7 %) 1.73 (0.81) 1.51 (0.68) 1.46 (0.98) 1.20 (0.88) 2.50 (2.04) 2.82 (2.09) 2.88 (2.03)

9.63 (1.13) 15 (50 %) 30 (100 %) 38.18 (13.64) 1 (3.3 %) 101.43 (15.96) 0 (0 %) 0 (0 %) 0 (0 %) 0.53 (0.56) 0.45 (0.34) 0.34 (0.50) 0.25 (0.36) 0.18 (0.51) 0.35 (0.86) 0.57 (1.05)

Teacher Impairment Rating Scale – Peers (M, SD)* Teacher Impairment Rating Scale – Teacher (M, SD)* Teacher Harter Social Acceptance (M, SD)f D-KEFS Color-Word Interference Test (M, SD)g* Stop Signal Reaction Time (M, SD)* SB5 Spatial Working Memory (M, SD)h* WISC-IV Digit Span (M, SD)i

1.58 (1.86) 1.3 (1.78) 2.77 (0.84) 9.22 (3.48) 367.46 (148.43) 8.55 (2.88) 8.50 (2.50)

2.41 (2.07) 2.20 (1.92) 2.40 (0.81) 7.70 (3.11) 423.34 (167.12) 7.53 (2.61) 8.06 (2.60)

0.91 (1.34) 0.58 (1.27) 3.06 (0.76) 10.90 (3.11) 307.86 (96.78) 9.70 (2.77) 9.00 (2.32)

To provide a comprehensive clinical diagnosis and classify children into the ADHD or non-ADHD group, the DBD and P-ChIPS were used to determine if children met DSM-IV-TR criteria for ADHD. *p

hyperactivity disorder symptoms mediate the association between deficits in executive functioning and social impairment in children.

We investigated whether symptoms of attention-deficit/hyperactivity disorder (ADHD) are pathways through which deficits in inhibition and working memo...
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