Executive Function and ADHD -Single Space Version

Executive Function and ADHD: Exploration through Children’s Everyday Behaviors

Gerard A. Gioia1,2 & Peter K. Isquith3 1

Mt. Washington Pediatric Hospital

2

Dept. of Psychiatry & Behavioral Sciences, Johns Hopkins School of Medicine 3

Dept. of Psychiatry, Dartmouth Hitchcock Medical Center

Accepted for publication in Clinical Neuropsychological Assessment

Executive Function and ADHD

2

Abstract Recent re-examination of Attention-Deficit/Hyperactivity Disorder (ADHD) in terms of the neuropsychological construct of executive function (Pennington & Ozonoff, 1996; Barkley, 1997) provided impetus to explore this relationship using the Behavior Rating Inventory of Executive Function (BRIEF; Gioia, Isquith, Guy & Kenworthy, 2000). The BRIEF assesses the behavioral manifestations of eight subdomains of executive functions in children aged 5 to 18 years via standardized parent and teacher ratings. The diagnostic utility of the BRIEF for identifying subtypes of childhood ADHD was examined. Two of the eight BRIEF scales Working Memory and Inhibit - were examined via logistic regression analyses for their predictive validity in identifying clinically referred children with ADHD subtypes versus children with no diagnosis. The Working Memory scale discriminated between children with no ADHD diagnosis and those with either the Inattentive or Combined subtypes, while the Inhibit scale further distinguished between children with the Combined subtype of ADHD and those with the Inattentive subtype or no diagnosis. Additionally, the relationship of the broader construct of executive function to ADHD was examined via factor analysis of the BRIEF with the ADHD Rating Scale-IV (DuPaul, Power, Anastopoulos & Reid, 1998). Specific subscales of the BRIEF were more highly associated with the Inattention syndrome of the ADHD Rating Scale whereas other subscales were associated with the Hyperactive/ Impulsive syndrome. The findings underscore the importance of executive functions as critical components in the functional definition of ADHD. The underlying functional components of the Inattention subtype include not simply a sustain factor but other metacognitive functions including the ability to initiate, organize and plan an action sequence, as well as to maintain a problem-solving set in active working memory. Similarly, the functional definition of the ADHD Combined subtype includes not only the executive function subdomain of inhibit but also the regulatory functions of flexibility and appropriate emotional control. These findings provide evidence for the strong relationship between executive function and the clinical diagnosis of ADHD. The multi-dimensional neuropsychological construct of executive function is both more specific and comprehensive in highlighting the critical functional aspects of ADHD beyond the traditional triad of symptoms.

Executive Function and ADHD

3

Executive Functions and ADHD: Exploration through Children’s Everyday Behaviors The syndrome of Attention-Deficit/Hyperactivity Disorder (ADHD) has traditionally been defined by three aspects of disordered functioning including sustained attention, impulsivity, and high activity level (DSM-IV, American Psychiatric Association, 1994). The definition of ADHD has been evolving over the last thirty years (Barkley, 1997). More recently, the nature of the disorder has been re-examined and is undergoing further redefinition in terms of a disorder of the executive functions (e.g., Barkley, 1997, 2000; Brown, 1999; Denckla, 1996, 1989; Pennington & Ozonoff, 1996). Various authors have argued that the syndrome of ADHD might better be viewed in terms of the construct of executive function than the traditional triad of symptoms reflected in current diagnostic criteria. Many agree that ADHD is not a unitary disorder, and that difficulties with sustained attention, impulsivity and hyperactivity are not the sole characteristics or areas of difficulty. A model of “attentional” disorders defined by executive function may be both more specific and more inclusive in identifying problematic areas of functioning. Further, viewing the behavioral symptoms of ADHD as ramifications of deficits in executive function provides a more useful neuropsychological model, as executive functions are one step closer to neural substrate than the ADHD diagnosis and provide a more functional framework for research (Barkley, 2000). We propose further that a comprehensive understanding of ADHD requires explicit inclusion of the executive functions in clinical assessment and intervention, as well as in research. At the outset, it is essential to appreciate the distinction between executive functions and the diagnosis of ADHD: Executive function is a neuropsychological construct inferred from observed behavior, whereas ADHD is a medical diagnosis based on a cluster of observed symptoms (APA, 1994). Although executive functions underlie the symptoms of ADHD, they are not synonymous with a diagnosis of ADHD. The relationships are not yet entirely clear; however, there is general agreement that different aspects of executive dysfunction contribute to the three ADHD subtypes: Predominantly Inattentive Type (ADHD-I), Predominantly Hyperactive-Impulsive Type (ADHD-H), and Combined Type (ADHD-C). Indeed, several authors have recently focused on the relationship between executive function, attention, and the diagnosis of ADHD and its subtypes (Barkley, 1990, 1996; Brown, 1999; Isquith & Gioia, 1999; Pennington and Ozonoff, 1996). As can be presumed from the nature of executive function, there is a close link with attentional functioning (Barkley, 1997; Mirsky, 1989). Indeed, executive function deficits may be most noticeable, and perhaps most measurable, as expressed via the attentional system. An intact executive system is necessary to support the ability to initiate, sustain, inhibit, shift and direct the child’s attention (Denckla, 1989). A child who cannot initiate attention or is slow to do so may never manage to focus on what someone is saying or on what he, himself, is doing. Disorders of sustaining attention and performance are characteristic of the inattentive type of ADHD (APA, 1994). Isquith and Gioia (1999) recently demonstrated that initiating, sustaining, planning, organization and working memory are likely functional underpinnings of the inattentive subtype of ADHD, while inhibiting, shifting, self-monitoring and emotional control are strongly related to the combined subtype of ADHD. Barkley (1990, 1997) gives thorough consideration to inhibitory control as a central problem in ADHD, particularly the Combined Type. While many have explored the relationship between executive function and ADHD (e.g., Barkley 1997; Bayliss & Roodenrys, 2000; Pennington & Ozonoff, 1996), the relationship

Executive Function and ADHD

4

remains elusive for several reasons, including both definitional and measurement problems with executive functions (Rabbit, 1997). While behavioral criteria are well established for diagnosing ADHD (DSM-IV, American Psychiatric Association, 1994), the same cannot be said for executive function. Definitions and models of executive function abound in the literature (e.g., Barkley, 2000; Brown, 1999; Denckla, 1994; Fuster, 1989; Goldman-Rakic, 1987; Levin et al., 1991; Stuss, 1986; Welsh & Pennington, 1988), with varying degrees of overlap and consensus as to the overall nature of executive function and specific subdomains. Some authors argue, in fact, that it may not be possible to segment the central executive beyond the molar level (Burgess, 1997; Goldman-Rakic 1987). To date, attempts to operationalize models of executive function have focused on laboratory or clinical performance tests (Welsh & Pennington, 1988; Welsh, Pennington & Grossier, 1991; Kelly, 2000), although such measures contain inherent problems (Pennington et al., 1996; Rabbit, 1997). For example, Burgess (1997) suggests that most neuropsychological tests alone are inadequate in assessing the executive functions because they attempt to separate integrated functions. Yet executive functions are typically measured by performance on clinical and experimental tests. Indeed, many consider the Wisconsin Card Sorting Task (Heaton, Chelune, Talley, Kay & Curtiss, 1993) the prototypical executive function test, despite the inherently limited focus and scope of any single performance measure. In their comprehensive review of executive function and ADHD studies, Pennington and Ozonoff (1996) cite only a few performance tests that are consistently impaired across studies and note that the Wisconsin Card Sorting Test is not among them. Assessment of Attention-Deficit/Hyperactivity Disorder The assessment of Attention-Deficit/Hyperactivity Disorder is a complex process given the genetic, neurological, neuropsychological, developmental, behavioral, familial, and social aspects of the disorder (Shelton & Barkley, 1990). Several levels of assessment are recommended in considering these factors, including a medical examination, clinical interviews, and careful behavioral assessment (Goldstein & Goldstein, 1990). The behavioral assessment can be accomplished via direct observational methods and the collection of ratings of the child’s behavior via standardized behavior rating scales. The administration of tests has proven less useful for the specific diagnosis of ADHD (Barkley & Grodzinsky, 1994; Pennington & Ozonoff, 1996) although it can be critically important for examining underlying executive deficits (Pennington et al., 1996) and comorbid cognitive or social-emotional conditions (Shelton & Barkley, 1990). A medical examination should be considered given the underlying neurobiological basis of ADHD and the various conditions that can contribute to poor attention, impulse control, and high activity level (e.g., prenatal alcohol/ drug exposure, exposure to neurotoxins, perinatal or postnatal hypoxia, traumatic brain injury) or co-exist with ADHD (e.g., motor incoordination, enuresis/ encopresis, allergies). Careful clinical interview of the parent and child seeks to understand factors associated with the child’s birth and developmental history; genetic history of psychiatric, medical or developmental disorders; social and family factors that may contribute positively or negatively to the child’s adaptive functioning; and school performance and functioning. Finally, the use of well-standardized and validated child behavior rating scales in the assessment of ADHD has become an essential component in order to measure the degree to which the problematic behavior falls outside of the norm for children of the same age and gender (Barkley, 1990; American Academy of Child and Adolescent Psychiatry, 1997; American Academy of Pediatrics, 2000). Such information is typically gathered from parents and

Executive Function and ADHD

5

teachers in order to understand the child’s behavioral functioning in the home and school settings, respectively. Many different behavior rating scales are now available including those that assess the broad spectrum of behavioral, social, emotional and attentional functioning (e.g., Child Behavior Checklist, Achenbach, 1991; Behavior Assessment System for Children (BASC), Reynolds & Kamphaus, 1994), as well as those that assess specific behaviors associated with ADHD (e.g., ADHD Rating Scale - IV, DuPaul, Power, Anastopoulos & Reid, 1998; Brown Attention Deficit Disorder Scales, 1996; SNAP-IV, Swanson, Nolan & Pelham, 2000). Assessment of Executive Function The assessment of the executive functions is equally as complex as the assessment of ADHD (Anderson, 1998). The clinical assessment of the executive functions is quite challenging given their dynamic essence (Denckla, 1994). Any assumption that the executive functions are a static set of abilities simply amenable to traditional testing is false. The fluid strategic, goal-oriented problem-solving involved in the executive functions is not as amenable to a paper-and-pencil assessment model as are the more domain-specific functions of language, motor, and visual/nonverbal abilities (Gioia, Isquith & Guy, 2001). Furthermore, the structured nature of the typical assessment situation often does not place a high demand on the executive functions, reducing the opportunity for observing this important domain (Bernstein and Waber, 1990). In considering whether or not a child has difficulty in the executive domain, suspected executive difficulties need to be viewed within the larger context of a neuropsychological framework (Bernstein and Waber, 1990). That is, in many testing situations, the examiner provides the structure, organization, guidance, and plan, as well as cueing and monitoring necessary for optimal performance by the child, thus serving as that child’s external executive control (Stuss & Benson, 1986; Kaplan, 1988). A child with significant executive dysfunction can perform appropriately on well-structured tasks of knowledge where the examiner is allowed to cue and probe for more information, thus relieving the child of the need to be strategic and goal-directed. Comprehensive assessment of executive function should include information gathered from testing, focused observations, standardized behavioral ratings, and clinical interview. In addition, problems in other domain-specific functions such as attention, language, visual/nonverbal processing, sensory inputs, motor outputs, and learning and memory must be understood. A clear understanding of the differences between assessment of the “basic” domain-specific content areas of cognition (e.g., memory, language, visuospatial) and the domain general or “control” aspects of cognition and behavior is essential. By necessity, there is always a “domain-specific” content area regulated by the executive control process. Teasing apart executive functions from domain-specific functions is part of the challenge of the neuropsychological assessment (Gioia et al., 2001). A paradox in the assessment of the executive functions is that some individuals with significant deficits in specific executive function subdomains may, in fact, perform appropriately on many purported "tests of executive function" yet have significant problems making simple real-life decisions (Stuss and Buckle, 1992). All tests are multi-factorial, with greater or lesser degrees of domain-specific content knowledge and thereby demanding varying degrees of organization, planning, inhibitory control, or flexibility. For example, a child may be able to perform appropriately on the Wisconsin Card Sorting Test (Heaton et al. 1993), which requires flexibility in problem-solving, yet fail miserably in strategically modifying his/her approach to completing a set of math problems in the classroom or in solving social problems. In a formal

Executive Function and ADHD

6

testing situation, one may not be collecting the relevant data to document the full essence of strengths and weaknesses in the array of executive functions. Assessment of the executive functions requires a multi-modal approach to characterize fully the child’s profile. The examiner must (1) obtain systematic observations of ways the child manages task demands within the context of the assessment situation, (2) recruit reliable reports of critical problem-solving behaviors in the child’s “real world”, and (3) provide psychometrically and developmentally appropriate tests for direct observation of executive problem-solving performance. The notion of ecological validity is particularly relevant in the assessment of the executive functions (Burgess, Alderman, Evans, Emslie & Wilson, 1998). In this context, ecological validity is defined as the ability of an assessment instrument to validly measure a behavior, function or process that is representative of the functioning of the individual in their everyday world. In addition to discussions regarding the ecological validity of tests, the artificial nature of the test environment has been questioned in terms of its ability to reflect the test-takers natural environment (Burgess, 1997). Efforts to better tap real-world environments and behaviors in the assessment of executive function have been made by various authors (e.g., Shallice & Burgess, 1991; Wilson, 1996; Burgess et al., 1996). We believe the everyday environment of the child at home and school serves as an important venue for observing the essence of the executive functions in children. Parents and teachers possess a wealth of information about the child’s behavior in these settings that is directly relevant to an understanding of his executive function. As previously noted, a rich tradition exists in utilizing structured behavior rating systems in the assessment of psychological and neuropsychological constructs (Achenbach, 1991; Conners, 1989; Reynolds & Kamphaus, 1994). Given the difficulties and complexities involved in test-based assessment of executive function, an ecologically valid system of assessing the everyday self-regulatory behaviors of children serves as an important adjunct to the clinical evaluation and treatment of executive dysfunction. One such measure, the Behavior Rating Inventory of Executive Function (BRIEF), was designed to assess the behavioral manifestations of executive functions in children aged 5 to 18 years (Gioia, Isquith, Guy & Kenworthy, 2000). The BRIEF assesses 8 interrelated subdomains of executive function within two general domains - Behavioral Regulation (Inhibit, Shift (Flexibility), Emotional Control) and Metacognitive problem-solving (Initiation, Task Organization/Planning, Environmental Organization, Self-Monitoring, Working Memory). Items were generated primarily from parent and teacher behavioral descriptions of executive difficulties, ensuring good ecological validity. The BRIEF demonstrates appropriate internal consistency and test-retest reliability, a consistent factor structure, convergent and discriminant validity with other behavior rating scales, and different profiles of dysfunction with a variety of populations (Gioia et al., 2000). In relying upon more ecologically valid parent and teacher ratings of children’s everyday executive and attentional behavior, we offer a different perspective of the relationship between executive function and ADHD. The present studies focus on two aspects of the relationship between ADHD and executive function. First, we explore the relative predictive value of parent and teacher ratings of inhibitory control and working memory in detecting the diagnosis of ADHD subtypes via logistic regression. Second, we examine the relationship between subdomains of executive function and the traditional symptomatology of ADHD through factor analysis of parent ratings. Both studies offer a different methodology than those of many previous reports by relying on observed behaviors presumed to reflect executive function. An ecologically-sensitive assessment of the everyday self-regulatory behaviors in children with the

Executive Function and ADHD

7

diagnosis of Attention-Deficit/ Hyperactivity Disorder (ADHD) can contribute significantly to the clinical evaluation and treatment process. Study 1. Working Memory and Inhibit as Predictors of ADHD Subtypes In the first study, parent and teacher ratings of everyday executive behaviors in separate samples of clinically referred children with ADHD subtypes were compared with parent and teacher ratings for matched groups of non-referred children. Theoretically, working memory deficits contribute substantially to the primarily inattentive subtype of ADHD, while inhibitory control deficits account for the cluster of symptoms comprising the hyperactive/impulsive subtype (Barkley, 1996; Isquith & Gioia, 1999; Pennington & Ozonoff, 1996). While children with ADHD may exhibit problems in several areas of executive function (e.g., planning, organization, self-monitoring), we focused on the most direct theoretical relationships. We hypothesized that children with the inattentive subtype of ADHD and those with the combined type of ADHD would show marked problems with working memory, but that only the latter type would show significant problems with inhibitory control. Methods Participants Children referred to a hospital-based outpatient pediatric neuropsychology practice who met DSM-IV criteria for either ADHD, Predominantly Inattentive Type (ADHD-I) or ADHD Combined Type (ADHD-C) participated in the study. ADHD diagnosis was based on interview, observation, parent and teacher ADHD-specific and broad behavior rating scales (e.g., CBCL, BASC) and neuropsychological evaluation as per clinical routine. No ADHD, Predominantly Hyperactive-Impulsive Type, diagnostic group was included because this diagnosis occurs infrequently in our clinical practice in school-age children. Most children who meet the hyperactivity and/or impulsivity criteria for the ADHD diagnosis also meet the inattention criteria, warranting the diagnosis of ADHD, Combined Type. Children with comorbid diagnoses (e.g., Conduct Disorder, Oppositional Defiant Disorder, Reading Disorder) were excluded from the study. The control groups were comprised of children selected from original standardization samples of the Behavior Rating Inventory of Executive Function (BRIEF; Gioia, Isquith, Guy & Kenworthy, 2000) without identified attentional, learning, or behavioral concerns and matched for age, gender, ethnicity and parental education to the clinical groups. The standardization samples were collected from a broad range of schools in terms of socioeconomic and geographic variables. Separate clinical and control groups were recruited for parent and teacher ratings on the BRIEF. Table 1 presents sample sizes and essential demographics for the parent and teacher samples. Insert Table 1 about here Procedures Parents and teachers completed the BRIEF as part of either the standardization sample via schools or as part of a clinical evaluation. The BRIEF is an 86-item questionnaire designed to assess executive functions via ratings of children’s everyday behaviors. Of the eight nonoverlapping BRIEF scales, two- Working Memory and Inhibit -served as the dependent measures. While the remaining six scales may be of interest in this population (i.e., Initiate, Plan/Organize, Organization of Materials, Monitor, Emotional Control, and Shift), for the

Executive Function and ADHD

8

purposes of this study we focused on Working Memory and Inhibit for the strong theoretical relationship to ADHD symptoms (Barkley, 1997). The BRIEF Working Memory and Inhibit scales have demonstrated strong psychometric properties: internal consistency, stability over short periods of time, and interrater (teacher-parent) agreement in the appropriate range. The Working Memory scale correlates in a logical fashion with a variety of attention scales, such as those included within the BASC (Reynolds & Kamphaus, 1994), CBCL/TRF (Achenbach, 1991), Conners’ Rating Scales (Conners, 1989), and the ADHD Rating Scale IV (DuPaul, Power, Anastopoulos & Reid, 1998), providing evidence for convergent validity. The Inhibit scale correlates strongly with measures of restlessness, impulsivity, overactivity, behavior problems, and aggression, and demonstrates secondary correlations with attention problem scales. Both the Working Memory and Inhibit scales correlate moderately with scales reflecting social difficulties, consistent with the observation that children who have attention and, in particular, impulse control problems, also have social difficulties. Equally important are the low correlations with a variety of scales that reflect behavioral and emotional difficulties that should not be related to inattention, impulsivity, and hyperactivity. The pattern of low correlations with scales measuring somatic complaints, anxiety, and depression provide evidence of discriminant validity for the Working Memory and Inhibit scales. RESULTS Group Differences Parent and teacher ratings on the BRIEF Working Memory and Inhibit scales were submitted to two separate (parent, teacher) one-way (Control, ADHD-I, ADHD-C) multivariate analyses of variance. Tables 2 and 3 present mean scale T scores for ADHD-I, ADHD-C, and matched control groups on the parent and teacher forms, respectively. The T scores have a mean of 50 and a standard deviation of 10. Of interest, both samples of control groups were above the mean of 50 but within one standard deviation. This likely reflects sampling error and causes the significance tests to be more conservative. Still, the omnibus multivariate analyses of variance were significant for each form, indicating large overall effects of diagnostic group membership. The Working Memory and Inhibit scale univariate between-groups tests were significant for the parent ratings with large effect sizes as reported in Table 2: Working Memory F(2, 127) = 50.9, p < .001, Eta2 = .45; Inhibit F(2, 127) = 31.2, p < .001, Eta2 = .33. Results of the teacher ratings analysis, reported in Table 3, were similar: Working Memory F(2, 218) = 75.1, p < .001, Eta2 = . 41; Inhibit F(2, 218) = 45.1, p < .001, Eta2 = .29. Insert Table 2 about here Insert Table 3 about here Post-hoc comparisons (Scheffe, p < .05) between diagnostic groups for the parent and teacher samples revealed similar patterns for each form. Children with both subtypes of ADHD (i.e., ADHD-I and ADHD-C) were rated by teachers and parents as significantly higher (i.e., more impaired) on the Working Memory scale than controls. There was no significant difference between ADHD-I and ADHD-C groups on Working Memory. Children diagnosed with ADHD-C were rated significantly higher by parents and teachers on the Inhibit scale than children in the ADHD-I and control groups. The ADHD-I group was somewhat elevated on the

Executive Function and ADHD

9

Inhibit scale, but significantly less elevated than the ADHD-C group. [see tables 2 and 3] Predicting Diagnosis Prediction of diagnostic group membership for the BRIEF Working Memory and Inhibit scales was then examined via logistic regression. Parent ratings on the BRIEF Working Memory and Inhibit scales were entered separately as predictor variables in logistic regression equations with diagnostic group membership as the criterion variable. Data were examined for the ADHDI versus control groups, separately for the ADHD-C versus control groups, and finally for the ADHD-I versus ADHD-C groups. The same analyses were conducted for teacher BRIEF ratings. Table 4 presents results of the logistic regression analyses predicting ADHD-I versus control group membership for the parent and teacher Working Memory and Inhibit scales. Parent ratings on the Working Memory scale predicted 81% of diagnostic group membership correctly, whereas ratings on the Inhibit scale correctly predicted 78%. Group membership was similarly predicted by teacher ratings: Working Memory correctly predicted 83% and Inhibit correctly predicted 70%. Insert Table 4 about here Table 5 shows the same analyses conducted with the ADHD-C diagnostic group versus matched controls for the Working Memory and Inhibit scales. Again, the percentage of correctly predicted group membership was acceptable: Parent ratings on the Working Memory scale predicted 84% and ratings on the Inhibit scale predicted 85% of group membership accurately. Teacher ratings on the Working Memory scale predicted 80% and ratings on the Inhibit scale predicted 79% correctly. Insert Table 5 about here The Working Memory scale was not helpful in distinguishing between ADHD-I and ADHD-C diagnostic groups, either in isolation or in concert with the Inhibit scale. Recall that both groups demonstrated elevated scores on the Working Memory Scale. The Working Memory scale was not predictive of ADHD-I vs ADHD-C group membership, and did not add significantly to the predictive power when included with the Inhibit scale. The Inhibit scale in isolation, however, was useful in distinguishing children diagnosed with ADHD-C from children diagnosed with ADHD-I, such that 68% of group membership was accurately predicted. Teacher ratings predicted 65% of group membership. Table 6 shows the logistic regression analyses for Working Memory and Inhibit scales for the ADHD-I and ADHD-C groups. Insert Table 6 about here Discussion In essence, children with either Inattentive or Combined types of ADHD were rated by parents and teachers significantly, indeed substantially, higher than children without an ADHD diagnosis on the BRIEF Working Memory scale. Parents and teachers also rated children with the combined type of ADHD significantly higher on the Inhibit scale than children with the inattentive type of ADHD, who were in turn rated higher on the same scale than children with no

Executive Function and ADHD

10

diagnosis. Both BRIEF forms predicted ADHD-I and ADHD-C group membership (vs. no diagnosis) adequately. The Working Memory scale did not distinguish between subtypes of ADHD, whereas the Inhibit scale distinguished some 65% to 68% of cases. This study supports the notion that deficits in domains of executive function underlie the behavioral symptom clusters that characterize the diagnosis of ADHD. Specifically, working memory deficits are characteristic of attention problems in both subtypes of ADHD, however failure of inhibitory control was a stronger contributor to the hyperactive/impulsive symptoms of ADHD, Combined Type. Study 2. Factor Analysis of ADHD Rating Scale and BRIEF Next, we examined the relationship between the broader neuropsychological construct of executive function and aspects of the clinical syndrome of ADHD by comparing the BRIEF scales with a published measure of ADHD symptoms based on the DSM-IV diagnostic criteria, the ADHD Rating Scale-IV (DuPaul et al., 1998). The ADHD Rating Scale-IV is a behavior rating questionnaire, with separate home and school versions, that consists of 18 items reflecting the nine DSM-IV Inattention criteria and the nine Hyperactivity/ Impulsivity criteria of the diagnosis of ADHD. The respondent is asked to indicate the frequency of the behavior on a 4-point Likert scale (ranging from “Never or rarely” to “Very Often”). The home and teacher versions of the scale have high internal consistency, good test-retest and inter-rater reliability, and demonstrated criterion validity and clinical utility. We hypothesized that the subdomains of executive function, as measured by the BRIEF, would be associated with ADHD symptomatology in specific and differential ways based on earlier work (Isquith & Gioia, 1999). More specifically, we predicted that difficulties with sustained attention and performance would be associated with difficulties initiating problem-solving activity, organization, planning and working memory. These metacognitive functions would, therefore, load more significantly with the “cognitive”/ inattention symptoms than the impulsive and hyperactive behaviors. In contrast, we predicted that hyperactive/ impulsive behaviors would be associated with greater difficulties regulating behavior including inhibiting and shifting behavior, as well as emotional control and self-monitoring. Method Participants Parents of 81 clinically referred children completed the BRIEF along with the ADHD Rating Scale –IV: Home Version as a routine part of a neuropsychological evaluation. Responses were collected for 51 boys and 30 girls with the DSM-IV diagnosis of ADHD, aged 5 to 17 years (M = 9.2, SD = 2.8). The sample was subdivided into diagnostic subtype groups as follows: Attention-Deficit/Hyperactivity Disorder, Predominantly Inattentive Type (n=50; 30 boys, 20 girls) and Attention-Deficit/Hyperactivity Disorder, Combined Type (n=31; 21 boys, 10 girls. Overall intellectual functioning of the sample was at the lower end of the Average range (Mean Full Scale IQ = 91.3, SD = 16.6). There were no differences between the diagnostic groups for age or IQ. Results Raw total score ratings for each of the eight BRIEF scales were correlated with raw total scores for the Inattention and Hyperactivity/Impulsivity scales of the ADHD Rating Scale-IV (Table 7). Inattention was most strongly related to Initiate, Plan/Organize, Working Memory, and Monitor. Hyperactivity/Impulsivity was most strongly related to Inhibit, Shift, and Emotional Control.

Executive Function and ADHD

11

Insert Table 7 about here In order to clarify the relationships between the various scales in Table 7, the correlation matrix was submitted to exploratory principal factor analysis (PFA) with oblique rotation to allow for the intercorrelation of factors. Factor loadings greater than .40 were retained on a factor. Two-, three- and four-factor solutions were examined. A two-factor solution was determined to be the most parsimonious based on the analysis of the scree plot and the clinical/ theoretical meaningfulness of the solution. Table 8 presents the rotated pattern matrix. The factor structure of the BRIEF scales was identical to the structure found in the normative sample (Gioia et al., 2000). Factor 1 was defined by the five BRIEF Metacognition scales (Initiate, Plan/Organize, Working Memory, Organization of Materials, and Monitor) loading with the ADHD Rating Scale-IV Inattention scale, accounting for 59% of the variance. Factor 2 was defined by the three BRIEF Behavioral Regulation scales (Emotional Control, Inhibit, and Shift) loading with the ADHD Rating Scale-IV Hyperactive/Impulsivity scale, accounting for an additional 13% of the variance. The two factors were moderately correlated (r = -.53). _____________________ Insert Table 8 about here _____________________ Discussion The findings of the factor analysis highlight the relationship between eight subdomains of executive function, as measured by the BRIEF, and the symptom components of the ADHD syndrome. Specific scales of the BRIEF were associated more highly with Inattention symptoms whereas other scales were associated with Hyperactive/ Impulsive symptoms. The Inattention symptoms were highly related to the metacognitive domains of task initiation, organization and planning, working memory, monitoring, and organizing one’s materials. The Hyperactive/ Impulsive symptoms were more highly related to the behavioral regulation aspects of executive function including inhibitory control, emotional control, and problem-solving flexibility. These findings extend the viewpoint of executive function as a critical component, together with inattention and hyperactivity/ impulsivity, of the ADHD diagnosis. These findings suggest that executive functions, as a neuropsychological construct, are a set of regulatory subdomains that characterize the functional components underlying the clinical syndrome of ADHD. The present results suggest the underlying functional elements of the Inattention subtype include not simply inattention behaviors in the narrow sense but also the executive ability to initiate, organize, plan, and monitor an action sequence and to maintain this problem-solving set in active working memory. Similarly, the behaviors within the ADHD Combined subtype would include the executive function subdomain of inhibit, consistent with Barkley’s (1997) model, as well as the ability to flexibly shift problem-solving set, and maintain appropriate emotional control. Conclusions The findings of these two studies provide evidence for the strong relationship between the neuropsychological construct of executive function and the clinical diagnosis of AttentionDeficit/Hyperactivity Disorder, consistent with the viewpoints expressed by Barkley (2000), Brown (1999), and Denckla (1996). Additionally, specific relationships between the traditional symptoms of ADHD and subdomains of executive function are suggested. We concur that executive function is a more useful framework for understanding the behavioral characteristics

Executive Function and ADHD

12

captured as the triad of ADHD symptoms. The multi-dimensional construct of executive function is both more specific in highlighting the multiple functional components within the subtypes of ADHD and more comprehensive in expanding the critical behavioral symptoms beyond the traditional triad. The first study highlights the relevance and utility of the specific executive function behaviors of inhibitory control and working memory in the diagnosis of the subtypes of ADHD. These two executive function domains, as assessed by the BRIEF, demonstrate good ability to detect the ADHD subtypes of Predominantly Inattentive Type and Combined Type. The second study supports the “redefinition” of the ADHD diagnostic components within an executive function framework. Barkley (1994) and others (Conners & Wells, 1986; Douglas, 1999) have long held inhibitory self-control as the fundamental symptom of ADHD. Redefining the critical diagnostic behaviors in terms of the neuropsychological construct of inhibition is supported. The construct of working memory has also been proposed as a possible underlying element of ADHD (Barkley, 1997). In fact, the “attention” in ADHD has been questioned as a discriminating aspect of ADHD (Gordon, 1995) and suggested to be the secondary consequence of other more primary underlying functions (e.g., inhibition). Thus, the present redefinition of attention in the ADHD symptom complex in terms of executive function has prior support. Not only do specific components of executive function serve to redefine the diagnosis of ADHD but we also demonstrate the importance of considering the broader metacognitive and behavioral/ emotional regulatory aspects of executive function as well. We believe this inclusive application of the executive function construct to ADHD has clinical support when one considers the types of everyday problems that are often reported by parents and teachers. Although “not paying attention” and “not thinking before he acts” are frequent concerns, reports of “disorganized thinking and performance”, “poor planning”, “not checking his work”, and “difficulty accepting other strategies” are also expressed quite frequently. The formal assessment of these critical aspects of executive function is necessary in functional diagnosis and treatment planning for children with ADHD symptoms. Articulating the particular behavioral subdomains of executive function allows for a more specific targeting of behavioral and cognitive/ academic treatment methods toward those deficient areas. Following an executive function rubric, the clinician would not be asking questions only about the inattention of the child but would also be formally inquiring about the child’s ability to initiate, plan, organize, and monitor task and social behavior, as well as hold the information actively in working memory. Furthermore, rather than pursuing information primarily in terms of overactive or impulsive behavior, assessment questions regarding the broader aspects of inhibitory control (including cognitive inhibition), as well as problem-solving flexibility and control of emotional responses, would be addressed. An ecologically relevant method of assessing the executive functions in children suspected of ADHD is consistent with the current approach to assessing this behavioral diagnosis. This paper demonstrates a reliable and valid method, via standardized parent and teacher behavior ratings, of assessing these critical component behaviors. The studies presented in this article are only a first step in the re-examination of ADHD as a disorder of the executive functions. As suggested by Barkley (2000), this reformulation may prove particularly useful in further research and clinical model development. For example, he speculates that an executive function model of ADHD would predict secondary executive function deficits due to the primary deficit in response inhibition. Attention deficits are also redefined as “intention deficits” (p. 1067) from an executive function perspective. The relationship between executive function and ADHD as demonstrated by the current set of studies

Executive Function and ADHD

13

provides support for future model-building. We advocate a behavioral phenotype paradigm with an executive function model at its core to further specify the full nature of the regulatory disorder now known as Attention-Deficit/Hyperactivity Disorder. The causal relationships among the subdomains of the executive functions, as posited by Barkley, could be investigated further with structural equation modeling. Preliminary support for the primary underlying role of inhibitory control with respect to the other executive functions has been reported in a sample of children with ADHD (Gioia, Isquith, Retzlaff & Pratt, 2000). Finally, the redefinition and refinement of our understanding of ADHD may promote better clinical treatment of individuals with this disorder. A more specific executive function model of ADHD would be useful for targeting appropriate cognitive/ academic, social, and behavioral treatments. References Achenbach, T. (1991) Manual for the Child Behavior Checklist/4-18 and 1991 profile. Burlington, VT: University of Vermont Department of Psychiatry. American Academy of Pediatrics (2000). Clinical practice guideline: Diagnosis and evaluation of the child with Attention-Deficit/Hyperactivity Disorder, Pediatrics, 105, 11581170. American Academy of Child and Adolescent Psychiatry: Practice parameters for the assessment and treatment of children, adolescents and adults with attention-deficit/hyperactivity disorder (1997). Journal of the American Academy of Child and Adolescent Psychiatry, 36, 85s121s. American Psychiatric Association (1994). Diagnostic and statistical manual of mental disorders (4th Edition). Washington, DC: American Psychiatric Association. Anderson, V. (1998) Assessing executive functions in children: Biological, psychological and developmental considerations. Neuropsychological Rehabilitation, 8, 319349. Barkley, R.A. (1990) Attention deficit hyperactivity disorder: A handbook for diagnosis and treatment. New York, NY: The Guilford Press. Barkley, R.A. (1994) Impaired delayed responding: A unified theory of attention deficit hyperactivity disorder. In D.K. Routh (Ed.) Disruptive behavior disorders in childhood: Essays honoring Herbert C. Quay (pp.11-57). New York: Plenum. Barkley, R.A.& Grodzinsky, G.M. (1994) Are tests of frontal lobe functions useful in the diagnosis of attention deficit disorders? Clinical Neuropsychologist, 8, 121-139 Barkley, R.A. (1996). Linkages between attention and executive functions. In G. R. Lyon & N. A. Krasnegor (Eds.), Attention, memory and executive function (pp. 307-326). Baltimore: Paul H. Brookes. Barkley, R.A. (1997) ADHD and the Nature of Self-Control. New York: Guilford Press. Barkley, R.A. (2000) Genetics of Childhood Disorders: XVII. ADHD, Part 1: The executive functions and ADHD. Journal of American Academy of Child and Adolescent Psychiatry, 39, 1064-1068. Bayliss, D.M. and Roodenrys, S. (2000) Executive processing and attention deficit hyperactivity disorder: An application of the supervisory attentional system. Developmental Neuropsychology, 17, 161-180.

Executive Function and ADHD

14

Bernstein, J.H. & Waber, D.P. (1990) Developmental neuropsychological assessment: The systemic approach. In A.A. Boulton, G.B. Baker & M. Hiscock (Eds.) Neuromethods: Vol. 17 Neuropsychology (pp. 311-371). Clifton, N.J.: Humana. Brown, T.E. (1996) Brown Attention Deficit Disorder Scales. San Antonio, TX: The Psychological Corporation. Brown, T.E. (1999) Does ADHD Diagnosis require impulsivity-hyperactivity?: A response to Gordon & Barkley. ADHD Report, 7, 1-7. Burgess, P.W. (1997) Theory and methodology in executive function and research. In P. Rabbitt (Ed.) Methodology of frontal and executive function. (pp.81-116). Hove, U.K.: Psychology Press. Burgess, P.W., Alderman, N., Evans, J., Emslie, H., & Wilson, B.A. (1998) The ecological validity of tests of executive function. Journal of the International Neuropsychological Society, 4, 547-558. Conners, C.K. (1989) Manual for Conners’ Rating Scales. North Towanda, NY: MultiHealth Systems, Inc. Conners, C.K., & Wells, K.C. (1986). Hyperkinetic children: A neuropsycholosocial approach. Beverly Hills: Sage Publications. Denckla, M.B. (1989) Executive function, the overlap zone between attention deficit hyperactivity disorder and learning disabilities. International Pediatrics, 4, 155-160. Denckla, M.B. (1994) Measurement of executive function. In G.R. Lyon (Ed.) Frames of reference for the assessment of learning disabilities: New views on measurement issues (pp.117142). Baltimore: Paul Brookes Publishing Co. Denckla, M.B. (1996) A theory and model of executive function: A neuropsychological perspective. In G.R. Lyon & N.A. Krasnegor (Eds.) Attention, memory and executive function (pp. 263-278). Baltimore, Md: Paul H. Brookes Publishing Co. Douglas, V.I. (1999) Cognitive control processes in attention-deficit/hyperactivity disorder. In H.C. Quay and A. Horgan (Eds.), Handbook of Disruptive Behavior Disorders (pp. 105-138). New York: Plenum Press. DuPaul, G.J., Power, T.J., Anastopolous, A.D., & Reid, R. (1998). ADHD Rating Scale IV: Checklist, norms and clinical interpretation. New York, Guilford Press. Fuster, J.M. (1989) The prefrontal cortex: Anatomy, physiology, and neurophysiology of the frontal lobe. New York: Raven Press. Gioia, G.A., Isquith, P.K. & Guy, S.C. (2001) Assessment of executive functions in children with neurological impairment. In R.S. Simeonsson & S. Rosenthal (Eds.) Psychological and Developmental Assessment. New York: Guilford Press. Gioia, G.A., Isquith, P.K., Retzlaff, P.D., & Pratt, B.M. (2000) Modeling Executive Functions with Everyday Behaviors: A Unitary or Fractionated System? Paper presented at the 10th Annual Rotman Institute Conference, Toronto, Ontario. Gioia, G.A., Isquith, P.K. & Guy, S.C. (1998) The regulatory role of executive control processes in children’s behavioral, social, and emotional functioning. The Journal of Neuropsychiatry and Clinical Neurosciences, 9, 663. Gioia, G. A., Isquith, P. K., Guy, S. C., & Kenworthy, L. (2000). Behavior Rating Inventory of Executive Function. Lutz, FL: Psychological Assessment Resources, Inc. Gordon, M. (1995) How to operate an ADHD clinic or subspecialty practice. Syracuse, NY: GSI Publications.

Executive Function and ADHD

15

Goldman-Rakic, P. (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In F. Plum (Ed.), Handbook of Physiology: The Nervous System (pp. 373-417). NY: Oxford University Press. Goldstein, S. and Goldstein, M. (1998) Managing attention deficit hyperactivity disorder in children: A guide for practitioners (2nd ed.). New York: John Wiley & Sons. Heaton, R., Chelune, G., Talley, J., Kay, G., and Curtiss, G. (1993). Wisconsin Card Sorting Test Manual. Lutz, FL: Psychological Assessment Resources. Isquith, P. K., & Gioia, G. A. (1999). The nature of executive function in ADHD [Abstract]. The Clinical Neuropsychologist, 13, 222. Isquith, P.K., Guy, S., Pratt, B., & Gioia, G. (1999). Initial clinical validity of the Behavior Rating Inventory of Executive Function. Journal of the International Neuropsychological Society, 5, 117. Kaplan, E. (1988) A process approach to neuropsychological assessment. In T. Boll and B.K. Bryant (Eds.) Clinical Neuropsychology and Brain Function: Research, Measurement and Practice (pp. 125-167). Washington, D.C.: American Psychological Association. Kelly, T.P. (2000) The development of executive function in school-aged children. Clinical Neuropsychological Assessment, 1, 38-55. Levin, H. S., Culhane, K. A., Hartmann, J., Evankovich, K., Mattson, A. J., Harward, H., Ringholz, G., Ewing-Cobbs, L., & Fletcher, J. M. (1991). Developmental changes in performance on tests of purported frontal lobe functioning. Developmental Neuropsychology, 7, 377-395. Lyon, R. & Krasnegor, N. (1996). Attention, Memory and Executive Function. Baltimore: Paul H. Brookes Publishing Co. Mirsky, A.F. (1989) The neuropsychology of attention: Elements of a complex behavior. In E. Perecman (Ed.) Integrating Theory and Practice in Clinical Neuropsychology (pp. 75-91). Hillsdale, NJ: Lawrence Erlbaum Associates. Passler, M.A., Isaac, W., and Hynd, G.W. (1985) Neuropsychological development of behavior attributed to frontal lobe functioning in children. Developmental Neuropsychology, 1, 349-370. Pennington, B.F. & Ozonoff, S. (1996) Executive functions and developmental psychopathology. Journal of Child Psychology and Psychiatry, 37, 51-87. Pennington, B.F., Bennetto, L., McAleer,O.K. and Roberts, R.J. (1996) Executive functions and working memory: Theoretical and measurement issues. In G.R. Lyon and N.A. Krasnegor (Eds.) Attention, Memory and Executive Function (pp. 327-348). Baltimore: Paul H. Brookes Publishing Co. Rabbitt, P. (1997). Introduction: Methodologies and models in the study of executive function. In P. Rabbitt (Ed.), Methodology of frontal executive function (pp. 1-38). East Sussex, UK: Psychology Press. Reynolds, C.R. and Kamphaus, R.W. (1994) Behavior Assessment System for Children. Circle Pines, MN: American Guidance Service, Inc. Shallice, T. & Burgess, P.W. (1991) Deficits in strategy application following frontal lobe damage in man. Brain, 114, 727-741. Shelton, T. & Barkley, R.A. (1990) Clinical, developmental, and biospychosocial considerations. In R.A. Barkley (Ed.) Attention Deficit Hyperactivity Disorder: A Handbook for Diagnosis and Treatment (pp. 209-231). New York: Guilford Press. Stuss, D.T. & Benson, D.F. (1986) The frontal lobes. New York: Raven.

Executive Function and ADHD

16

Stuss, D.T. and Buckle, L. (1992) Traumatic brain injury: Neuropsychological deficits and evaluation at different stages of recovery and in different pathologic subtypes. Journal of Head Trauma Rehabilitation, 7, 40-49. Swanson, J.M., Nolan, W., Pelham, W.E. (2000). The Swanson, Nolan and Pelham (SNAP) Rating Scales. (Web: WWW.ADHD.net). Welsh, M.C., Pennington, B.F., and Grossier, D.B. (1991) A normative-developmental study of executive function: A window on prefrontal function in children. Developmental Neuropsychology, 7, 131-149. Welsh, M.C. and Pennington, B.F. (1988) Assessing frontal lobe functioning in children: Views from developmental psychology. Developmental Neuropsychology, 4, 199-230. B.A. Wilson, N. Alderman, P.W. Burgess, H. Emslie, & J.J. Evans (Eds.) Behavioural assessment of the dysexecutive syndrome. Bury St. Edmunds, U.K.: Thames Valley Test Company.

Executive Function and ADHD

17

Table 1 Demographic Data by Diagnostic Group Diagnostic Group Parent Ratings ADHD-I ADHD-C Controls Teacher Ratings ADHD-I ADHD-C Controls

N

Gender % Boys % Girls

Age SD

M

27 26 77

63 58 58

37 42 42

8.7 8.1 8.3

(1.8) (1.8) (1.5)

42 78 101

69 65 70

31 35 30

9.3 8.7 8.9

(2.5) (2.4) (2.5)

Table 2 Mean T Scores on Parent Form Working Memory and Inhibit Scales Participant Group Control ADHD-I Scale M SD M SD Working Memory 56.1a 12.1 76.3b 9.5 Inhibit 56.9a 12.3 67.1b 15.3

ADHD-C M SD 75.8b 9.4 80.3c 13.9

Note. Row Means sharing a subscript are not significantly different at p < .05. Table 3 Mean T Scores on Teacher Form Working Memory and Inhibit Scales Participant Group Control ADHD-I Scale M SD M SD Working Memory 59.9a 15.2 82.6b 17.5 Inhibit 59.1a 12.3 75.6b 23.0

ADHD-C M SD 84.2b 16.7 89.9c 23.6

Note. Row Means sharing a subscript are not significantly different at p < .05.

Executive Function and ADHD

18

Table 4 Logistic Regression Analyses Predicting ADHD, Predominantly Inattentive Type β

SE

Odds Rati o

Working Memory

3.62

.74

Inhibit

1.53

Working Memory Inhibit

Wald Statistic

p

R

% Predicted a

37.44

24.25

.001

.43

81

.49

4.61

16.5

.001

.25

78

2.55

.42

12.76

35.9

.001

.44

83

1.16

.30

3.18

15.34

.001

.28

70

Parent Form

Teacher Form

Note. Statistics are for scales entered independently as predictors of diagnostic group. a Refers to the number of cases accurately classified, or hit rate, for children with a diagnosis of ADHD, Predominantly Inattentive Type versus Controls (no ADHD diagnosis). Table 5 Logistic Regression Analyses Predicting ADHD, Combined Type β

SE

Odds Rati o

Working Memory

3.65

.76

Inhibit

3.24

Working Memory Inhibit

Wald Statistic

p

R

% Predicted a

38.7

22.8

.001

.43

84

.65

25.58

25.4

.001

.45

85

2.82

.39

16.8

53.09

.001

.46

80

3.6

.51

6.46

49.57

.001

.43

79

Parent Form

Teacher Form

Note. Statistics are for scales entered independently as predictors of diagnostic group. a Refers to the number of cases accurately classified, or hit rate, for children with a diagnosis of ADHD, Combined Type versus Controls (no ADHD diagnosis).

Executive Function and ADHD

19

Table 6 Logistic Regression Analyses Predicting ADHD, Predominantly Inattentive Type Versus ADHD, Combined Type Odds Rati o

Wald Statistic

p

R

% Predicted a

β

SE

Working Memory

-.15

.76

.86

.04

.84

.01

49

Inhibit

-1.75

.62

5.74

8.05

.01

.29

68

Working Memory

-.18

.37

.83

.25

.62

.01

0

Inhibit

-.85

.42

2.43

9.04

.01

.21

65

Parent Form

Teacher Form

Note. Statistics are for scales entered independently as predictors of diagnostic group. a Refers to the number of cases accurately classified, or hit rate, for children with a diagnosis of ADHD, Predominantly Inattentive Type versus ADHD, Combined Type. Table 7 BRIEF Scale Correlations with the ADHD Rating Scale IV Working Plan/ Org. of Scale Initiate Memory Organize Materials Monitor Inattention .56* .65* .62* .40* .65* HyperImpulsive N= 81

.34*

.49*

*p < .001

.30*

.08

.49*

Emotional Control .43*

Inhibit .46*

Shift .40*

.55*

.76*

.55*

Executive Function and ADHD

Table 8 Principal Factor Analysis of BRIEF and ADHD Rating Scale IV with Oblique Rotation Factor 1 Factor 2 57.6% 14.0% Inattention .58 Initiate .71 Working Memory .72 Plan/ Organize .87 Org. of Materials .67 Monitor .64 Hyper/Impulsivity -.84 Inhibit -.91 Shift -.66 Emotional Control -.66 N=81 Note. Scales of the ADHD Rating Scale IV are italicized for clarity.

20