J Abnorm Child Psychol DOl 10. 1007/sl0802-010-9449-3
Executive Functioning Characteristics Associated with ADHD Comorbidity in Adolescents with Disruptive Behavior Disorders Tom A. Hummer · William G. Kronenberger · Yang Wang • David W. Dunn • Kristine M. Mosier • Andrew J. Kalnin • Vincent P. Mathews
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Springer Science toBusiness Media, LLC 2010
Abstr act The nature of executive dysfunction in youth with disruptive behavior disorders (DBD) remains unclear, despite extensive research in samples of children with attention-deficit hyperactivity disorder (ADHD). To determine the relationship between DBD, ADHD, and executive function deficits in aggressive teens. adolescents with DBO and comorbid ADHD (DBD+ AOHO; n=25), DBD without AOHD (DBO-ADHD; n=- 23), and healthy controls (HC; n ~ 25) were compared on ncurocognitivc lests and questionnaires measuring executive functioning. Teens wilb DBD+ ADHD pcrfonned worse on both neurocognitivc and questionnaire measures of executive function than the OBD-ADHD and HC groups. Results suggest that subgroups of DBD may exist depending on the presence or absence of comorbid ADHD, which may have implications for the selection and efficacy of treatment strategies. Keywords Oppositional-defiant disorder· Conduct disorder· Attention-deficit hyperactivity disorder· Comorbidity ·Aggression ·Executive function
T. A. Hummer· Y. Wang· K. M. Mosier· A. J. Kalnin · V. P. Mathews Department of Radiology and Imaging Sciences. Indiana University School of Medicine, Indianapolis, TN, USA
T. A. Hummer· W. G. Kronenberger· D. W. Dunn Department of Psychiatry, Indiana University School of Medicine. Indianapolis, IN, USA
T. A. Hummer(~) Indiana University Center for Neuroimagmg. 950 West Walnut Street E124. Indianapolis. II\ 46202. USA e-mail:
[email protected] Published online: 06 August 20 I 0
Oppositional defiant disorder (ODD) and conduct disorder (CD) are among the most commonly diagnosed mental disorders of children and adolescents. ODD and CD, collectively referred to as disruptive behavior disorders (DBD), are defined by a variety of behavioral symptoms that cause significant disruptions in functioning. Adolescents with 080 demonstrate defiant, disobedient, aggressive and hostile behavior, particularly towards authority figures. This consi:stt:nt bt:havior pattern results in behaviors such as arguing. rulebreaking and, in more extreme forms, aggressive criminal acts (American Psychiatric Association 1994; Kronenberger and Meyer 200 I). Environmental and behavioral influences on symptoms of DBD are well-documented (Cadoret et at. 1995; Dodge 1993; Frick et at. 1'192), and most of the widely used and validated treatments for DBD involve bchavioml modification (Brcstan and Eyberg 1998). Additionally, individuals with DBD make distorted cognitive attributions. and treatments to modify such attributions can reduce symptoms (Kazdin et at. 1989; Lochman L992; Lochman et a!. 1993). In addition to these cognitive and behavioral components of DBO, there has been some question about whether neurocognitivc processes involving executive functioning (specifically manifest by impulsivity and poorly developed self-regulation) contribute to these disorders. Executive function refers to a collective set of processes that encompasses planning, cognitive flexibility, working memory, organization, inhibition and problem solving (see Miyake ct al. 2000). Research has been mixed on whether individuals with DBD demonstrate poor executive functioning. Studies on delinquent or aggressive individuals (Giancola and Zeichner 1994; Moflitt 1993; Moffitt and ~Springer
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Silva 1988; Seguin et al. 1999) or specifically on those with conduct disorder (Toupin et al. 2000) have reported deficits in neuropsychological pedormancc on executive function measures, although the intervening ro le of comorbid disorders is not always fully examined (Barkley et al. 2001; Kim et al. 200 I). On the other hand. several metaanalytic reviews have reported no connection between conduct disorder or delinquency and poor executive functioning (Pennington and Ozonoff 1996}, particularly when accounting for comorbidity with attention disorders (Moffitt and Henry 1989). Attention deficit-hyperactivity disorder (ADHD) is commonly comorbid with DBD, although comorbidity estimates range widely (Biedennan ct al. 1991; Jensen ct al. 1997). ADHD is characterized by inattention, disorganization, impulsivity and hyperactivity, which disrupt the child's functional and adaptive behaviors (Barkley 2006). A considerable amount of research bas demonstrated that deficits in behavioral manifestations of executive functioning are a core feature of ADHD (Barkley 1997), and treatments targeting executive functioning deficits in daily behavior are an important option for children with ADHD (Kempton et al. 1999; Klingberg ct al. 2005). However, individual perfonnancc on neuropsychological measures of executive function can be an inconsistent indicator of ADHD (Doyle et al. Wahlstedt et al. 2009), given the heterogeneity of neurocognitive abilities of children diagnosed with the disorder. Children with DBD who also have comorbid AOHD demonstrate a high level of impulsivity and poor selfregulatory processes in their defiant, angry, and rulebreaking behavior (Kronenberger and Meyer I). A potentially important characteristic within the DBD group, therefore, is the presence or absence of comorbid ADHD symptoms, which may indicate distinct etiologies and, relatedly, differences in optimal treatment strategies. Because treatment of disorders involving executive dysfunction differs in some ways from that of disorders involving predominantly behavioral-environmental contingencies (Barkley 2006; McMahon and Forehand 2003). understanding of the role of executive functioning in DBDs may be valuable for guiding treatment options and decisions. Several studies have examined executive performance in DBD samples with and without ADHD. Adolescents diagnosed with CD and ADIID demonstrated impairments on aspects of the Ncimark Memorization Strategies Test and the Wisconsin Card Sorting Test relative to those diagnosed with only conduct disorder, albeit in a study with small san1ple sizes (Aronowitz et al. 1994). Similarly, Clark et al. (2000) found that teens with ADHD perfonncd significantly worse on executive function test-;, with DBD playing no role in this effect. Conversely, other studies report that adolescents with DBD show no difference on a
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battery of executive functioning tests when compared to a similar DBD group that is comorbid for ADHD (DBD+ AD HD; Oery et a!. 1999), or demonstrate impairments on tests of working memory and association even when statistically controlling for the number of ADHD symptoms (Seguin et al. J999; Toupin et al. 2000). More recently, children aged 7-12 with ADHD alone, ODD or CD alone or with both disorders were tested on the Self-Ordered Pointing Task and the Tower of London (Oosterlaan et al. 2005). Results showed an association of executive impairment with ADHD symptoms, with no such relationship with DBD diagnosis. Furthennorc, detriments in verbal fluency were unrelated to either CD or ADHD diagnosis, contrary to previous research (e.g. Dery et a!. 1999). The disparities in these studies may be due to several factors, including age and culture of participants, how executive function was defined and measured, and the manner in which AOHD or DBD symptoms were identified. Thus. questions remain regarding how executive functioning may differ between DBD youths with and without a comorbid diagnosis of ADHD. To address this question. we investigated neurocognitive differences between groups of adolescents with DBD alone (DBDADHD), DBD comorbid with AOHD (DBD+ADHD), and no diagnosis (healthy controls; HC), in order to better understand the relationship between executive functioning and DBD diagnoses. Unlike prior research, this study incorporated a comprehensive set of executive functioning measures based on both questionnaire and neuropsychological tests in wellmatched samples of adolescents. Using both such measures enabled examination of behavioral and neurocognitivc characteristics of these samples using multiple testing techniques. Notably, an important focus in this study were measures of inhibition and interference control, executive function measures largely ignored in prior research in similar samples, despite their importance in DBD and ADHD. Furthermore, the focus in this study was on adolescents with a history of aggressive behavior as a part of their DBD diagnosis, in order to obtain a more homogeneous sample of teens with the most debilitating types of symptoms (American Psychiatric Association 19Q4; Kronenberger and Meyer 200 I). Finally, diagnosis in this investigation was based on a "gold-standard" !'cmistructured clinical interview, rather than parent- or teacher-reports as employed in prior studies (e.g. Clark et al. 2000; Oosterlaan et al. 2005). The goal of this study was to examine executive functioning in well-defined and well-matched samples of adolescents who have histories of aggression and DBD diagnosis, with and wit11out comorbid ADHD, using a broad set of behavioral and ncurocognitive measures. Specifically, we aimed to test the hypothesis that teens
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with DBDs and aggressive behavior would demonstrate executive functioning deficits only when ADHD was present; otherwise, we expected performance on tests of executive functioning to be similar to that of controls.
Methods Participants Participants were obtained from a larger group of adolescents, aged 13- 17 years (Table I), who participated in two studies of aggressive-disruptive behavior and media exposure (Kronenberger ct al. 2005). Adolescents were recruited via informational flyers at pediatric settings, a psychiatry clinic, community organizations, and schools. Diagnoses were made based on the Schedule for Affective Disorders and Schizophrenia for School-Aged Children, Present and Lifetime Version (K-SADS; Kaufman ct at. 1996) Semistructured Diagnostic Interview (Behavior Disorders Module), performed by trained psychology graduate students under the supervision of a licensed clinical psychologist. Three subgroups of participants were derived from the larger subject pool of the two studies. Based on the K-SADS interview, participants in the disruptive behavior disorder alone subgroup (DBDADHD; n= 23) were required to meet DSM-IV criteria for CD or ODD with at least one recurrent CD symptom of aggressive behavior towards people or animals within the past 6 months; to have three or fewer inattentive ADITD symptoms; and to have three or fewer hyperactive-impulsive ADHD symptoms. Participants in the DBD and comorbid ADHD subgroup (DBD+ADHD; n =25) met the same DSM-TV criteria for CD or ODD with aggressive features and also met criteria for ADIJD (8 Inattentive, 17 Combined subtype), based on the K-SADS interview. The ratio of participants qualifying for CD diagnosis did not differ between DBD-ADHD and DBD ... ADHD groups (X 2 (1, N=48)=2.25, p=O.l9;
Table 1 Demographics
Demogrnph1c data includes mean (standard deviation) for adolescents with DBD and comorbid ADHD (OBOi ADIID), DBD
without ADHO (080-ADHD) and healthy controls. Symbols indicate group means significantly differ from • control or h DB DAD l-iD group ntp: 6/(6), 725-737. doi: I 0.1 002/jclp.200:!2. Lachar. D .. & Gruber. C. P. (1995). Personality Inventory for Youth (PlY) manual. Los Angeles: Western Psychological Services. Lochman. l E. (I 992). Cognitive-behavioral intervention with aggressive boys: three-year follow-up nnd preventive effects. Joumol of Consulting and Clinical Psychology. 60(3), 426-432. doi: 10.1 037/0022-006X.60.3.426. Lochman. J. E., Coie, J. D., Underwood, M. K.. & Terry, R. (1993). Effectiveness of a social relations intervention program for aggressive and nonaggrcssivc. rejected children. Journal of Consulting Clinic:al Pl'yr:ho/og,: 6/(6). I 053-1058. doi: I 0.1037 00~-006X.6J.6. 1 05:t. MacLeod. D .. & Prior. M. (1996). Attention deficits in adolescents with ADHD and other clinical groups. Child Neuropsyf'hology. 2 (I), 1- 10. doi: 10.1 080109297049608-tO13-t5.
1 Abnorm Chi ld Psycho! McMahon. R. J.. & Forehand, R. L. (2003). Helping the noncompliant child: Family-based treaime/11 for oppositional behavior (2nd cd.). New York: Gui lford. Miyake, A., Friedman. N. P.. Emerson, M. J.• Witzki, A. H .. Howcncr, A., & Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex ''Frontal Lobe" tasks: a latent variable analysis. Cognitive Psychology, 4/(1), 49100. doi: 10 . l 006/cogp.l999 .0734. Moffitt, T. E. (1993). The ncuropsycholOf.'Y of conduct disorder. Development and Psychopathology, 5. 135- 151. doi:l0.1017/ S0954579400004302. Moffitt, T. E., & Silva. P. A. (1988). Self-reponed delinquency. neuropsychological deficit, and h istory of anention deficit disorder. Journal of Abnormal Child Psychology. 16(5), 553569. doi:IO. l007/BF00914266. MoffitL T. E., & Henry, B. ( 1989). Neuropsychological a~sessmcnt of executive functions in self-reponed delinquents. Developmental P~:vchopathoiog)\ I, 105- 118. doi: 10. 10 17/S095457940000029K Nigg. J. T.. Blaskey. L. G., Huang-Pollock, C. L. , & Rappley, M. D. (2002). Neuropsychological executive functions and DSM-lV ADHD subtypes. Journal of the American Academy of Child and Adolescent Psychiatry, 41(1 ), 59-66. doi: I 0. 1097/0U004583200201000-00012. Oosterlaan. J.. Scheres, A.. & Sergeant, J. A. (2005). Which executive functioning deficits are associated with AD/ HD, ODD/CD and comorbid AD/IID1 ODD/CD? Journal of Abnormal Child Psychology. 33(1), 69- 85. doi: 10. 1007/s I OR02-005-0935-y. Patterson. G. R. ( 1982). Coercive family processes. Eugene: Castalia. Pennington, B. F., & Ozonoff. S. ( 1996). Executive functions and developmental psychopathology. Jouma/ of Child Psychology and Psychiat1y. 37(1), 51-87. doi:IO. Illl /j. l469-7610. 1996.tb01380.x.
Reynolds. C. R.. & Kamphaus, R. W. (1992). Behavior assessment system for children manual. Circle Pines: American Guidance Service. Seguin, J. R.. Boulerice, B., Harden, P. W., Tremblay, R. E., & Pihl, R. 0. (1999). Executive functions and physical aggression after controlling for attention deficit hyperactivity disorder, general memory. and lQ. Joumal ofChild Psychology and Psychiatry. 40 (8). 1197-1208. doi:IO.llll/1~69-7610.00536. Snyder, J., Schrcpfcrman, L., & St Peter, C. ( 1997). Origins of antisocial behavior. Negative reinforcement and affect dysregu lation of behavior as socialization mechanisms in family interaction. Behavior Modification, 2/(2). 187- 215. doi:\0. 1177101454455970212004. Stroop, J. R. ( 1935). Studies of interference in serial verbal reactions. Journal of Experimental Psycholog}; 18, 643--662. doi:l0.1037/ h0054651. Toupin. J., Dcry. M .. Pauze. R.. Mercier, H .. & Fortin, L. (2000). Cognitive and familial contributions to conduct disorder in children . .Journal of Child Psychology and Psychiatry, 4/(3), 333- 344. doi:JO. l l ll/ 1469-7610.00617. Wahlstcdt, C., Thorell, L. B., & Bohlin. G. (2009). Heterogeneity in ADHD. Neuropsychological pathways, comorbidity and symptom domains. Journal of Abnormal Child Psyhcology. 37(4). 551-564. doi:l0. 1007/sl0802-008-9286-9. Wechsler, D. ( 1999). Wechsler abbreviated scale of intelligence. San Antonio: The Psychological Corporation. Willcutt, E. G., Doyle, A . E., Nigg, J. T., Faraone. S. V., & Pennington, B. F. (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biological Psyc:hiarry, 57(11), 1336-1346. doi:IO.l016/j . hiopsych.::W05.02.006.
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