Sage Journals: Discover world-class research

Abstract

Objective: The aim of the present study was to examine the effect of comorbid oppositional defiant disorder (ODD) and conduct disorder (CD) on (i) symptom levels in attention-deficit–hyperactivity disorder (ADHD) and (ii) the relationship between neurocognitive impairment and ADHD symptom severity.

Method: A total of 200 6–12-year-old children with DSM-IV ADHD, combined type (ADHD-CT) were identified in a specialist ADHD clinic in metropolitan Melbourne. From this initial group, 23 were identified with ADHD without ODD/CD (ADHD alone), 22 had ADHD and ODD and 20 had ADHD and CD. All the children were medication naïve. Twenty-five healthy control children were also recruited from local primary schools. The four groups did not differ in age, gender or full-scale IQ. A cross-sectional study of parent- and teacher-reported ADHD and externalizing symptoms, spatial span, spatial working memory, visuospatial memory, spatial recognition, spatial planning and behavioural inhibition was completed.

Results: Parent-reported externalizing symptoms were higher in the ADHD + CD and ADHD + ODD groups compared to the ADHD alone group. There were no differences in neurocognitive function between children with ADHD-CT with and without ODD or CD. All the ADHD groups, however, performed worse than the healthy control group. Further, worse spatial span, spatial working memory and delayed matching to sample performance were associated with increased teacher-reported ADHD symptoms in the ADHD alone group. Also, worse spatial working memory performance was associated with increased teacher-reported ADHD symptoms in the ADHD + CD group.

Conclusions: ADHD symptom severity is associated with the magnitude of impairment in executive functions in children with ADHD alone, but these relationships can be obscured by the presence of comorbid disruptive disorders. Children with ADHD + CD may demonstrate similar associations to children with ADHD alone, suggesting a similar underlying dysfunction. ADHD + ODD, however, may be better understood as a maladaptive response to the abnormal behaviours and neurocognitive functions in ADHD.

Keywords

attention-deficit–hyperactivity disorder conduct disorder oppositional defiant disorder response inhibition spatial memory working memory

Attention-deficit–hyperactivity disorder (ADHD) is a common childhood psychiatric disorder characterized by developmentally inappropriate levels of hyperactivity, inattention and impulsivity (DSM-IV) [1, 2]. The majority of neuropsychological deficits associated with ADHD involve the executive functions (EFs), such as response inhibition, planning and organization, problem solving and working memory 3–8. Contemporary brain–behaviour models of ADHD integrate the neurocognitive and behavioural impairments with neurobiological data and hypothesize that ADHD arises from disruption to neural networks that involve the prefrontal cortex, basal ganglia and their dopaminergically modulated interconnections 9–14. In contrast to such hypotheses, however, neuropsychological studies generally find no reliable association between the magnitude of impairment on tasks of EF and the severity of behavioural disturbance in ADHD [3, 6, 7], 15–20. Consequently, debate continues regarding the nature of any relationship between neurocognitive impairments and symptoms in ADHD.

One complication when examining relationships between neurocognitive function and symptom levels in ADHD is the high prevalence (40–90%) of comorbid oppositional defiant disorder (ODD) and conduct disorder (CD) in samples recruited from child psychiatry clinics and, to a lesser degree, in samples recruited from the community 21–24. Both ODD and CD are associated with poor neurocognitive performance independent of an ADHD diagnosis [3], 25–27 and many studies report more severe hyperactive, impulsive or inattentive symptoms in ADHD with comorbid ODD or CD [22], 28–30. It is unclear, however, whether the presence of comorbid ODD or CD also increases the magnitude of the EF impairment in ADHD. Some studies report that impairments in EF are greater in children with ADHD and ODD or CD than in children with ADHD without ODD or CD 31–33. Other studies find no additional impairment in EF in children with ADHD and comorbid ODD or CD [4, 29], 34–37. If ODD or CD were associated with more severe impairment in EF in addition to their more severe symptoms, then reliable robust associations between symptom severity and EF are likely to be observed in samples of ADHD + ODD/CD. If, however, the magnitude of impairment in EF in ADHD + ODD/CD is equivalent to that for ADHD alone, but symptom severity is greater, any associations between symptoms and EF function would be weakened. Given this uncertainty, the association between symptom severity and neurocognitive function should be investigated in samples of ADHD that do not contain comorbid ODD or CD.

Studying children with ADHD without cormorbid disruptive disorders is more difficult when attempting to control for DSM-IV subtype [38]. CD and ODD are less prevalent in children with the ADHD-inattentive (ADHD-I) subtype than the ADHD-combined (ADHD-CT) subtype [24, 39]. Therefore, in studies in which ADHD subtype has not been controlled or determined, it is possible that ADHD-I is overrepresented in experimental groups classified as having no comorbid ODD or CD (i.e. pure ADHD). Conversely, children with ADHD-CT may be overrepresented in ADHD + ODD/CD groups. Because ADHD-I may be associated with a less severe profile of neurocognitive impairment than ADHD-CT, researchers may in fact be measuring differences between ADHD subtypes rather than determining the effects of comorbid disruptive disorders on EF 40–43. It is therefore important to control ADHD subtype in neuropsychological studies that seek to determine the effect of ODD or CD on cognitive function in ADHD.

As part of our ongoing research into neurocognitive function in ADHD, we have now recruited enough children with ADHD-CT to obtain estimates of neurocognitive function and symptom levels in groups with (i) ADHD alone, (ii) ADHD with CD, and (iii) ADHD with ODD. Therefore, the first aim of the study was to measure the effect of comorbid ODD and CD on symptom levels in ADHD. It was hypothesized that children with ADHD and comorbid disruptive behaviour disorders would be rated higher on measures of ADHD symptoms than children with ADHD alone. The second aim was to determine the relationship between neurocognitive impairment and symptom severity in the different groups of children with ADHD-CT with or without a cormorbid disruptive behaviour disorder. We hypothesized that ADHD children with comorbid disruptive behaviour disorders would show greater impairment on the neurocognitive tests than children with ADHD alone.

Methods

Participants

The current sample was selected from a database of 200 children with ADHD-CT, who had undergone a comprehensive assessment of behavioural symptoms, neurocognitive function, intellectual functions and academic performance. All children were recruited from referrals to a specialist ADHD clinic in metropolitan Melbourne, Australia [44] and were aged between 6 and 12 years old. All were living with at least one biological parent and were attending general primary schools. All children had a full-scale IQ (FSIQ) score >75, and were excluded if they had any neurological and/or endocrine conditions, bipolar or psychotic disorders as established through parental interview. All diagnoses were confirmed by a consultant psychiatrist and administration of the IQ, academic and neuropsychological tests were performed by registered or trainee clinical psychologists. To be classified as ADHD, children were required to meet DSM-IV criteria for ADHD-CT based on diagnostic DSM-IV semi-structured interview administered to at least one parent to establish diagnoses of ADHD and other existing disorders including ODD, CD. The Child Behaviour Checklist (CBCL; parent and teacher forms) and the Conners’ Global Index (CGI; parent and teacher forms) were obtained to confirm pervasive impairment and to rate the severity of the disorder.

To be included in the current study, all children with ADHD were required to be medication naïve. Twenty-three children who did not meet the DSM-IV criteria for ODD or CD were identified (ADHD only). Twenty children who met the clinical criteria for ADHD and CD were identified (ADHD/CD). Twenty-two children were randomly selected from the remainder of the sample, all of whom met the clinical criteria for ADHD and ODD (ADHD/ODD). Twenty-five children who were healthy control participants were recruited from local primary schools. They did not manifest any medical and psychiatric disorders, via the same structured clinical interview and parent/teacher questionnaires used to define the three ADHD groups. The demographic characteristics of these four groups were inspected to determine whether there were any differences in age, gender distribution or intelligence between the groups (Table 1).

Measures

The Anxiety Disorders Interview Schedule for DSM-IV (ADIS-parent form) is a semi-structured interview designed for the diagnosis of psychiatric disorders in children and adolescents. Symptoms are judged by the parent as present or absent and the total number of affirmative responses is calculated to obtain a symptom score. If the number of symptoms present meets DSM-IV criteria, the parent is asked the extent to which the symptoms cause impairment or interference for the child. Impairment ratings are made using an 8-point scale, and must be ≥4 to be diagnostically relevant [45].

The CBCL is a widely used standardized instrument for the assessment of behavioural problems and competencies. The questionnaire consists of 118 behaviour problem items rated on a 3-point scale (0 = not true to 2 = very true) as to how well each describes the child over the past 6 months. An externalizing subscale, composed mainly of ODD/CD symptoms, and an ADHD subscale are generated from parent (CBCL) and teacher (Teacher Report Form (TRF)) ratings. T scores (norms) are provided for children aged 4–5, 6–11 and 12–16 by gender [46].

The CGI is a 10-item questionnaire particularly useful for screening for the core symptoms of ADHD [47]. Items are rated on a 4-point scale (0 = not at all to 3 = very much) indicating the extent to which the child has been affected by the problem (e.g. constantly fidgeting) during the past month [47].

The Wechsler Intelligence Scale for Children–third Edition was used to provide FSIQ scores. Eleven of the 13 WISC-III subtests were administered, with the exception of Symbol Search and Mazes [48].

Computerized neuropsychological tasks

Cognitive function was assessed using tests from the (Cambridge Neuropsychologist Test Automated Battery (CANTAB)). The CANTAB is a series of computerized tests presented to subjects on a high-resolution IBM colour monitor with a touch-sensitive screen. The six subtests used in this study were mostly administered in one testing session lasting no more than 70 min. Participants were seated approximately 50 cm from the monitor with the instruction that they were required to respond to stimuli by touching the screen. The tests have been described extensively in the literature and will be outlined only briefly here. Based on findings from past studies using the same neurocognitive tests in children with ADHD, only tasks that previously demonstrated impairment in ADHD were included here [8, 49, 50], or those that demonstrated a large effect between control and ADHD groups.

The Spatial Span task is a computerized version of the Corsi Block Tapping Test that measures the subject's ability to remember a sequence of squares presented on the screen. After an incorrect attempt at choosing the squares in sequence, the next trial remained at the same difficulty level. The spatial short-term memory span was calculated at the highest level at which the subject successfully remembered at least one sequence of boxes [51].

The Spatial Working Memory task is a self-ordered searching task that measures working memory for spatial stimuli and requires the subject to use mnemonic information to work towards a goal. Subjects were required to search through boxes that appeared on the screen with the aim of finding the blue tokens hidden inside. Returning to an empty box already targeted (and hence emptied of its blue token) on a particular search constituted a ‘forgetting’ or ‘between search’ error (BSE). After two practice trials with two boxes, there were four test trials with each of two, three, four, six and eight boxes [52].

The Delayed Matching to Sample (DMTS) task assessed the ability to recall a complex target stimulus (an abstract pattern), which was presented on the screen for 4 s. In the simultaneous trials, the target stimulus remained on the screen with the choice stimuli. In the delayed matching trials, the target stimulus was removed followed by a 0, 4 or 12 s delay before the choice stimuli was presented. In all trials, subjects were required to choose the target stimulus in a four-alternative forced choice procedure. Performance was measured according to the percentage of correct responses at the simultaneous and each of the delay levels [53].

The spatial recognition task assessed the ability to recognize spatial locations of target stimuli. Four sets, each with five stimuli, were presented, and performance was defined as the percentage of correct responses for the 20 trials [51].

The Tower of London task (TOL) assessed spatial planning and behavioural inhibition. Subjects were required to rearrange their set of coloured balls so that their positions match a goal arrangement in the other half of the screen. The copying trials are scored by (i) the number of test trials completed within the minimum number of moves and (ii) the total number of moves in excess of the minimum. These provide scores of accuracy. The following trials provide a yoked control condition to measure motor initiation and execution times, independent of thinking times [54].

Procedure

The CBCL and CGI parent and teacher forms were generally completed before the assessment sessions began. The child was given the WISC-III and the academic achievement tests. For younger children, sometimes the academic achievement tests were administered in a separate session. The neurocognitive battery of tests was administered using standard instructions and equipment, and generally took no longer than 70 min to complete. The parents were given the diagnostic interview in a separate session.

Statistical analysis

Performance on the spatial span, spatial recognition, DMTS and TOL was compared between groups using a series of one-way ANOVAs. On the spatial working memory task that contained varying levels of difficulty, performance between groups was compared using a group×level of difficulty repeated measures ANOVA. To investigate any differences between groups in the relationship between scores on the CBCL and the CGI and performance on the neurocognitive tests, Pearson product moment correlation coefficients were calculated. This is appropriate rather than using Spearman's rho because the ordinal variables of the CBCL and CGI are effectively rank transformed. Therefore, Pearson product moment correlation between the ordinal variables (CBCL/CGI) and the continuous neurocognitive variables is appropriate. Significance level was set at p < 0.05. Significant correlations were compared with others using the method described by Crawford et al.[55]: ‘both correlations were converted to Fisher's z and the difference between them divided by the standard error of the difference to yield a normal curve deviate (z)’.

Results

Demographic and clinical characteristics of the sample

Table 1 describes the demographic characteristics of the sample. The ADHD groups did not differ from the healthy control group in age, gender or FSIQ. The ADHD groups had higher parent and teacher CGI scores and parent and teacher externalizing subscale scores than the healthy control group. In addition, the ADHD only group had significantly lower scores than the ADHD + CD and ADHD + ODD groups on the parent externalizing subscale, while the three groups did not differ on the externalizing subscale.

Table 1.

Sample characteristics and symptom scores

	1 ADHD only (mean±SD) n = 23	2 ADHD + ODD (mean±SD) n = 22	3 ADHD + CD (mean±SD) n = 20	4 Control n = 25	p
N (male/female)	17/6	19/3	16/4	18/7	NS
Age (years)	8.23±1.94	9.02±2.11	8.24±1.64	8.81±1.48	NS
CGIp	19.08±5.96	22.95±5.77	23.40±4.40	4.22±4.08	1,2,3 > 4∗
CGIt	18.92±9.42	16.82±6.60	19.20±5.39	1.71±1.74	1,2,3 > 4∗
Parent-ext	62.75±10.15	73.77±8.50	75.53±6.53	52.09(2.99	4 < 1<2,3∗
Teacher-ext	66.58±12.76	62.64±10.95	70.60±7.92	51.00(2.10	1,2,3 > 4∗
Full-scale IQ	98.67±12.64	98.91±15.04	97.80±10.96	99.27±9.88	NS

ADHD, attention-deficit–hyperactivity disorder; CD, conduct disorder; CGIp, Conners’ Global Index parent's form; CGIt, Conners’ Global Index teacher's form; ODD, oppositional defiant disorder; Parent-ext, Child Behaviour Checklist (CBCL) externalizing subscale parent form; Teacher-ext, CBCL externalizing subscale teacher form. Full-scale IQ estimated from the Wechsler Intelligence Scale for Children. ∗p < 0.0005.

Neurocognitive performance

Table 2 shows the group means for each of the neurocognitive measures. The three ADHD groups had worse spatial span, spatial working memory, DMTS and TOL performance than the healthy control group. The groups did not differ on the spatial recognition task. To determine whether there was any effect of level of difficulty on performance on the spatial working memory task, scores on each level of difficulty were submitted to a 4 (group)×4 (difficulty) repeated measures MANOVA. There was a significant main effect for level of difficulty (Wilk's λ = 0.10, F(3,84) = 834.53, p < 0.0005, partial η²=0.90), group (F(3,86) = 5.85, p = 0.001, partial η²=0.12) and a group×difficulty interaction (Wilk's? λ = 0.77, F(9,195) = 3.94, p < 0.0005, partial η²=0.08). Post-hoc analysis showed that the three ADHD groups performed worse than the healthy control group.

Table 2.

Group comparisons on neurocognitive tasks

	ADHD only (mean±SD) n = 23	ADHD + ODD (mean±SD) n = 22	ADHD + CD (mean±SD) n = 20	Control (mean±SD) n = 25	Group comparison
Spatial Span	4.08±1.67	4.09±1.37	3.46±1.06	5.06±1.09	F = 8.10∗∗
					4 > 1,2,3

SWM Total BSE	57.50±17.89	50.27±16.83	56.06±17.46	42.48±19.85	F = 5.90∗
					1,2,3 > 4

DMTS (% correct)
Simultaneous	75.83±31.17	82.27±18.23	81.33±15.05	93.65±8.86	F = 6.91∗∗
					4 > 1
Total across delay trials	49.72±19.41	54.09±17.84	52.44±20.21	68.59±15.33	F = 9.75∗∗
					4 > 1,2,3
Total responses	56.25±19.84	61.13±16.39	58.00±18.27	73.89±15.43	F = 9.33∗∗
					4 > 1,2,3

Spatial Recognition (% correct)	70.83±14.74	62.95±14.36	62.00±14.97	72.50±15.61	F = 2.56

Tower of London
No. minimum move solutions	4.75±2.00	6.50±1.89	5.93±2.08	7.73±1.93	F = 7.25∗∗
					4 > 1,2,3

Total in excess of the minimum	26.25±14.51	21.45±9.70	19.66±8.96	12.54±8.85	F = 9.86∗∗
					4 < 1,2,3

ADHD, attention-deficit–hyperactivity disorder; CD, conduct disorder; DMTS, Delayed Matching to Sample task; ODD, oppositional defiant disorder; SWM Total BSE, Spatial Working Memory task, total between-search error score.

Table 3 lists the relationship between scores on the parent and teacher CBCL ADHD subscale, the parent and teacher CGI and the neurocognitive measures for each group. In the ADHD only group, the parent and teacher CBCL ADHD subscales had a large positive correlation, as did the parent ADHD subscale and the teacher CGI. These correlations differed from the healthy control and ADHD and CD groups, respectively. For parent ratings, the parent CBCL ADHD subscale had a medium positive correlation with spatial working memory errors and a medium negative correlation with spatial span in the ADHD only group. Also, the parent CGI had a medium negative correlation with spatial span and visuospatial memory performance in the ADHD and CD group. These correlations did not significantly differ from those in the other diagnostic groups. In contrast, the teacher CBCL ADHD subscale had a large positive correlation with spatial working memory errors, and large negative correlations with spatial span and visuospatial memory performance in the ADHD only group. There was also a large positive correlation between this teacher report and spatial working memory errors in the ADHD and CD group and a medium positive correlation in the healthy control group. The ADHD only and ADHD and CD group correlations differed significantly from that in the ADHD and ODD group. Further, the ADHD only spatial span and visuospatial memory correlations differed from those in the other three groups. In addition, the teacher CGI had a large positive correlation with spatial working memory errors in the ADHD and CD group that differed from correlations in the other three diagnostic groups. Further, the teacher CGI had a medium positive correlation with spatial working memory errors and medium negative correlations with spatial span and visuospatial memory performance in the ADHD only group.

Table 3.

Correlations between neurocognitive measures and severity of symptoms

	1 ADHD only n = 23	2 ADHD + ODD n = 22	3 ADHD + CD n = 20	4 Control n = 25	Correlations Comparison Fisher's z
Parent/BSE	0.45 0.03∗	0.18 0.28	0.45 0.06	0.17 0.29
Parent/SS	–0.46 0.03∗	–0.29 0.08	–0.27 0.32	–0.26 0.09
Parent/DMTS	–0.27 0.22	–0.05 0.77	–0.26 0.30	–0.19 0.45
Teacher/BSE	0.63 0.03∗	0.14 0.53^#	0.64 0.01∗	0.49∗ 0.03	1,3 > 2
Teacher/SS	–0.73 0.007∗	–0.007 0.97^#	–0.12 0.67^#	–0.07 0.78^##	1 > 2,3,4
Teacher/DMTS	–0.63 0.02∗	–0.14 0.62^#	–0.16 0.46^#	–0.39 0.09	1 > 2,3
CGIp/BSE	0.10 0.68	0.01 0.98	0.09 0.72	0.01 0.97
CGIp/SS	–0.08 0.73	–0.31 0.07	–0.52 0.02	–0.06 0.83
CGIp/DMTS	–0.16 0.48	–0.15 0.36	–0.43 0.04	–0.15 0.55
CGIt/BSE	0.38 0.04∗^#	0.12 0.51^##	0.80 0.001∗	0.08 0.70^##	3 > 1,2,4
CGIt/SS	–0.50 0.02∗	–0.06 0.76	0.01 0.96	–0.09 0.64
CGIt/DMTS	–0.43 0.04∗	–0.04 0.82	–0.15 0.57	–0.08 0.69
Parent/Teacher	0.64 0.002∗∗	0.29 0.08	0.36 0.16	0.06 0.81^#	1 > 4
CGIp/CGIt	0.17 0.59	0.04 0.86	0.19 0.50	0.50∗ 0.04
Parent/CGIt	0.59 0.003∗∗	0.20 0.28	0.01 0.99^#	0.18 0.35	1 > 3
Teacher/CGIp	0.43 0.07	0.15 0.37	0.46 0.04	0.23 0.61

ADHD, attention-deficit–hyperactivity disorder; BSE, between-search errors total; CBCL, Child Behaviour Checklist; CD, conduct disorder; CGIp, Conners’ Global Index parent's form; CGIt: Conners’ Global Index teacher's form; DMTS, delayed matching to sample total; ODD, oppositional defiant disorder; Parent, CBCL ADHD subscale parent form; SS, spatial span total; Teacher, CBCL ADHD subscale teacher form. Significant correlations: ∗p < 0.05; ∗∗p < 0.005; comparison of correlations: ^#p < 0.05; ^##p < 0.01.

Discussion

In the current study we observed no differences in neurocognitive function between children with ADHD-CT with and without ODD or CD. In contrast to this, the severity of externalizing symptoms rated by parents on the CBCL was higher in children with ADHD/CD and ADHD/ODD than in children with ADHD alone. When rated by teachers, children with ADHD/CD were rated as having more severe symptoms than children with ADHD alone, but this was not significant. This trend in mean scores was expected given the selection bias inherent in the current sample, because all children were recruited from a specialist ADHD clinic in a child mental health service.

The strongest associations between teacher symptom ratings and neurocognitive function were identified for the relationships between symptom severity and spatial span, spatial working memory and DMTS in the ADHD alone group. Associations of a similar magnitude were observed between teacher symptom severity and the number of between search errors in the ADHD/CD group. In both groups, these relationships were detected at a significant level (z) only for symptoms rated by teachers.

Taken together, these results suggest that the severity of symptoms is associated with the magnitude of impairment in EF in children with ADHD alone, but that these relationships can be obscured by the presence of comorbid disruptive disorders. If a relationship between ADHD symptoms and impaired EF exists, this lends support to recent neurobiological models that assume that abnormal behaviours and neurocognitive functions in ADHD arise from disruption to the same neural networks or neurobiological systems [10], 56–58. It is unclear whether models such as these can be applied to all children with ADHD, due to the heterogenous nature of the disorder. Taylor highlighted various sources of heterogeneity in ADHD and the various predominant types of symptoms and subtypes that are emerging in the literature examining the cognitive and behavioural symptoms of ADHD [59]. Therefore, children with ADHD and comorbid CD may demonstrate impairments in behaviour and neurocognitive measures likely to have stemmed from a similar underlying dysfunction [60, 61]. ADHD/ODD, however, may be better understood as a maladaptive response to the abnormal behaviours and neurocognitive functions in ADHD [25, 59].

The neurocognitive measures used in the current study were selected on the basis of their demonstrated sensitivity to ADHD in our previous studies [8, 49, 50], and because they have been used successfully with normally developing children in past research [62]. Furthermore, impairments in aspects of EF such as the ability to hold information ‘online’, as is required in the spatial working memory, spatial span and DMTS, have been well documented in ADHD [6]. In our previous studies we found that performance on the measures used here differentiated between unmedicated children with ADHD and healthy controls, with approximately a 44–52% overlap between the two distributions (i.e. effect sizes range between 0.8 and 1.0) [63]. Importantly, the performance of each of the three ADHD-CT subgroups on the EF were impaired, similar to our previous published data [8, 49, 50].

Despite the modest sample sizes in the current study, the magnitude of the relationships between symptom severity and measures of memory and EF detected in the ADHD alone group was larger than any observed in our previous studies (highest correlation: r = 0.31) [8]. Further, the relationships between performance on neuropsychological tests and symptom severity detected in the current study were stronger than in many past neuropsychological studies of ADHD. When detected, most relationships were of low to moderate strength [23, 64]. Many past studies, however, may have included children with comorbid CD or ODD in their ADHD groups. To the best of our knowledge, the contribution of comorbid disorders to the relationship between symptom severity and EF performance has not been examined directly. When considered with the current results, the lack of associations, or small associations observed in previous studies, is not surprising because perhaps the relationship between symptoms and neurocognitive impairment became evident in the current group due to the ADHD subtype and comorbid disruptive behaviour disorders being controlled.

When compared to a normally developing control group, children with ADHD consistently demonstrate impairment on the same EF tasks that were used in the present study [8, 49, 50]. The present study demonstrated that comorbid disruptive behaviour disorders do not necessarily alter the performance of children with ADHD on tasks of EF, despite differing levels of behavioural symptoms. This finding lends support to the premise that ADHD and other disruptive behaviour disorders may reflect a common underlying deficit, and suggests that children with ADHD and comorbid CD may present a more severe form of ADHD [23, 60, 61]. Alternatively, the finding of similar EF impairment in children with ADHD and ADHD with CD and ODD may merely reflect the large overlap in symptoms observed in these childhood disorders. Groups of children who meet the clinical criteria for CD or ODD without ADHD are necessary to investigate the question of whether the EF impairments observed in ADHD are specific to the disorder or reflect a general deficit found in children with any attentional disorder.

Interestingly, no statistically significant relationship (z) was found between parent ratings of behaviour and performance on any EF task. Parent–teacher agreement regarding symptomatology is reportedly low [65, 66], and teachers have been found to rate children's behaviour as less severe than parents, and distinguish less between the subtypes compared with parent ratings [67]. The reliability of parents more than teachers in rating ADHD behaviour has been questioned due to artefactual factors, such as maternal education or single-parent households. In addition, recall biases or halo effects may interfere with objective reporting of parents and/or teachers [22], or the intensity of ADHD symptoms may fluctuate [68]. Therefore, most researchers consider teacher ratings of symptoms to be more reliable than parent ratings.

The present results must be interpreted with caution due to the small sample sizes used. In addition, a selection bias may exist in the current sample, because the children with ADHD were recruited from a hospital outpatient clinic. The current findings need further support by future studies that examine the proposal that relationships between symptom severity and EF impairment are most apparent in children with ADHD-CT without comorbid disruptive disorders and are therefore specific to children with ADHD-CT. In our entire sample of unmedicated children with ADHD-CT, 60% had comorbid ODD and 11% had comorbid CD [8]. High prevalence rates of disruptive disorders are common in clinic-referred samples of ADHD, as was found in the current group [29]. Therefore, ADHD without comorbid disruptive disorders may be relatively rare, especially in groups of children referred to hospital child psychiatry clinics. If this is the case, then the current finding that ADHD symptom level and neurocognitive performance are strongly related in children with ADHD without ODD/CD will apply to a relatively small group of children with ADHD. The present findings may therefore be of greater importance to brain–behaviour models of ADHD than to the management of the disorder itself. Nonetheless, in most cases parents and teachers of children with ADHD-CT could be informed that the severity of a child's symptoms do not predict a great deal about their cognitive function.

In summary, a question of considerable importance in the present study was whether the neurocognitive and behavioural symptoms that characterize ADHD are related, as would be expected given the cotemporary neurocognitive models currently underpinning much of the research into ADHD. In our previous study we found no relationship between symptoms and performance on EF tests. When comorbidity in the sample was controlled for, however, the relationship between teacher-rated symptoms and neurocognitive impairment was strong in the ADHD alone group. The pattern of relationships differed for the comorbid groups, because only the comorbid CD group showed a relationship between teacher ratings of symptoms and the number of between-search errors.

References

1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 4th edn. Washington, DC: American Psychiatric Association, 1994.

2. Rapport

Scanlan

Denney

. Attention deficit hyperactivity disorder and scholastic achievement: a model of dual developmental pathways. J Child Psychol Psychiatry 1999; 40: 1169–1183.

3. Oosterlaan

Sergeant

. Response inhibition and response re-engagement in attention-deficit-hyperactivity disorder, disruptive, anxious and normal children. Behav Brain Res 1998; 94: 33–43.

4. Murphy

Barkley

Bush

. Executive functioning and olfactory identification in young adults with attention deficit hyperactivity disorder. Neuropsychology 2001; 15: 211–220.

5. Seidman

Biederman

Monuteaux

Doyle

Faraone

. Learning disabilities and executive dysfunction in boys with attention-deficit/hyperactivity disorder. Neuropsychology 2001; 15: 544–556.

6. Martinussen

Hayden

Hogg-Johnson

Tannock

. A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2005; 44: 337–384.

7. Willcutt

Doyle

Nigg

Faraone

Pennington

. Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 2005; 57: 1336–1346.

8. Vance

Maruff

Barnett

. Attention deficit hyperactivity disorder, combined type (ADHD-CT): better executive function performance with longer-term psychostimulant medication. Aust N Z J Psychiatry 2003; 37: 570–576.

9. Arnsten

AFT

Steere

Hunt

. The contribution of alpha-2 noradrenergic mechanisms to prefrontal cortical cognitive function. Arch Gen Psychiatry 1996; 3: 448–455.

10.

10. Barkley

. Behavioural inhibition, sustained attention and executive functions: constructing a unifying theory of ADHD. Psychol Bull 1997; 121: 65–94.

11.

11. Barnett

Maruff

Vance

. An investigation of visuospatial memory impairment in children with ADHD, combined type. Psychol Med 2005; 35: 1433–1443.

12.

12. Pennington

Ozonoff

. Executive functions and developmental psychopathology. J Child Psychol Psychiatry 1996; 37: 51–87.

13.

13. Pliszka

McCracken

Maas

. Catecholamines in ADHD: current perspectives. J Am Acad Child Adolesc Psychiatry 1996; 35: 264–272.

14.

14. Vance

Silk

Casey

. Right parietal dysfunction in children with attention deficit hyperactivity disorder, combined type: a functional MRI study. Mol Psychiatry 2007; 12: 826–832.

15.

15. Barkley

Fischer

Edelbrock

Smallish

. The adolescent outcome of hyperactive children diagnosed by research criteria: 1. An 8-year prospective follow-up study. J Am Acad Child Adolesc Psychiatry 1990; 29: 546–557.

16.

16. Chelune

Ferguson

Koon

Dickey

. Frontal lobe disinhibition in attention deficit disorder. Child Psychiatry Hum Dev 1986; 16: 221–234.

17.

17. Muir-Broaddus

Rosenstein

Medina

Soderberg

. Neuropsychological test performance of children with ADHD relative to test norms and parent behavioural ratings. Arch Clin Neuropsychol 2002; 17: 671–689.

18.

18. Paternite

Loney

Roberts

. A preliminary validation of subtypes of DSM-IV attention deficit/hyperactivity disorder. J Atten Disord 1996; 1: 70–86.

19.

19. Reader

Harris

Schuerholz

Denkla

. Attention deficit hyperactivity disorder and executive dysfunction. Dev Neuropsychol 1994; 19: 493–512.

20.

20. Seguin

Boulerice

Harden

Tremblay

Pihl

. Executive functions and physical aggression after controlling for attention deficit hyperactivity disorder, general memory and IQ. J Child Psychol Psychiatry 1999; 40: 1197–1208.

21.

21. Biederman

Newcorn

Sprich

. Comorbidity of attention deficit hyperactivity disorder with conduct, depressive, anxiety and other disorders. Am J Psychiatry 1991; 148: 564–577.

22.

22. Clark

Prior

Kinsella

. Do executive function deficits differentiate between adolescents with ADHD and oppositional defiant/conduct disorder? A neuropsychological study using the Six Elements test and Hayling Sentence Completion test. J Abnorm Child Psychol 2000; 28: 403–414.

23.

23. Schachar

Tannock

Marriott

Logan

. Deficient inhibitory control in attention deficit hyperactivity disorder. J Abnorm Child Psychol 1995; 23: 411–437.

24.

24. Vance

ALA

Luk

ESL

. Heart of the matter review: attention deficit hyperactivity disorder: progress and controversies. Aust N Z J Psychiatry 2000; 34: 719–730.

25.

25. Baving

Rellum

Laucht

Schmidt

. Children with oppositional-defiant disorder deviant attentional processing independent of ADHD symptoms. J Neural Transm 2006; 113: 685–693.

26.

26. Pajer

Chung

Leininger

Wang

Gardner

Yeates

. Neuropsychological function in adolescent girls with conduct disorder. J Am Acad Child Adolesc Psychiatry 2008; 47: 416–425.

27.

27. Sergeant

Geurts

Oosterlaan

. How specific is a deficit of executive functioning for attention-deficit/hyperactivity disorder?. Behav Brain Res 2002; 130: 3–28.

28.

28. Nigg

Carte

Hinshaw

Treuting

. Neuropsychological correlates of childhood attention deficit hyperactivity disorder: explainable by comorbid disruptive behaviour or reading problems?. J Abnorm Psychol 1998; 107: 468–480.

29.

29. Schachar

Mota

Logan

Tannock

Klim

. Confirmation of an inhibitory control deficit in attention deficit hyperactivity disorder. J Abnorm Child Psychol 2000; 28: 227–235.

30.

30. Scheres

Oosterlaan

Sergeant

. Response inhibition in children with DMS-IV subtypes of AD/HD and related disruptive disorders: the role of the reward. Child Neuropsychol 2001; 7: 172–189.

31.

31. Rothenberger

Banaschewski

Heinrich

Moll

Schmidt

van Klooster

. Comorbidity in ADHD-children: effects of coexisting conduct disorder or tic disorder on event-related brain potentials in an auditory selective attention task. Eur Arch Psychiatry Clin Neurosci 2000; 250: 101–110.

32.

32. Ackerman

Anhalt

Dykman

. Arithmetic automatization failure in children with attention and reading disorders: associations and sequela. J Learn Disabil 1986; 19: 222–232.

33.

33. Jensen

Hinshaw

Kraemer

. ADHD comorbidity findings from the MTA study: comparing comorbid subgroups. J Am Acad Child Adolesc Psychiatry 2001; 40: 147–158.

34.

34. Barkley

Edwards

Laneri

Fletcher

Metevia

. Executive functioning, temporal discounting, and sense of time in adolescents with attention deficit hyperactivity disorder (ADHD) and oppositional defiant disorder (ODD). J Abnorm Child Psychol 2001; 29: 541–556.

35.

35. Oosterlaan

Scheres

Sergeant

. Which executive functioning deficits are associated with AD/HD, ODD/CD and comorbid AD/HD + ODD/CD?. J Abnorm Child Psychol 2005; 33: 69–85.

36.

36. Sarkis

Sarkis

Marshall

Archer

. Self-regulation and inhibition in comorbid ADHD children: an evaluation of executive functions. J Atten Disord 2005; 8: 96–108.

37.

37. Van Goozen

Cohen-Kettenis

Snoek

Matthys

Swaab-Barneveld

van Engeland

. Executive functioning in children: a comparison of hospitalised ODD and ODD/ADHD children and normal controls. J Child Psychol Psychiatry 2004; 45: 284–292.

38.

38. Vance

ALA

Luk

Costin

Tonge

Pantelis

. Attention deficit hyperactivity disorder (ADHD): anxiety phenomena in children with treated psychostimulant medication for six months or more. Aust N Z J Psychiatry 1999; 33: 399–406.

39.

39. Eiraldi

Power

Nezu

. Patterns of comorbidity associated with subtypes of attention deficit hyperactivity disorder among 6 to 12 year old children. J Am Acad Child Adolesc Psychiatry 1997; 36: 503–514.

40.

40. Brown

. ADD/ADHD and impaired executive function in clinical practice. Curr Psychiatry Rep 2008; 10: 407–411.

41.

41. Chhabildas

Pennington

Willcutt

. A comparison of the neuropsychological profiles of the DSM-IV subtypes of ADHD. J Abnorm Child Psychol 2001; 29: 529–540.

42.

42. Geurts

Verte

Oosterlaan

Roeyers

Sergeant

. ADHD subtypes: do they differ in their executive functioning profile?. Arch Clin Neuropsychol 2005; 20: 457–477.

43.

43. Nigg

Blaskey

Huang-Pollock

Rappley

. Neuropsychological executive functions and DSM-IV ADHD subtypes. J Am Acad Child Adolesc Psychiatry 2002; 41: 59–66.

44.

44. Vance

ALA

Costin

Birleson

Tonge

Luk

ESL

Maruff

. A specialist clinic for primary school age children with disruptive behaviour disorders who are not responding to conventional psychological and medication treatments. Australas Psychiatry 2001; 9: 36–40.

45.

45. Silverman

Albano

. anxiety disorders interview schedule for DSM-IV. Graywind, Texas 1996.

46.

46. Achenbach

. Manual for the Child Behavior Checklist/4-18 and profile. University of Vermont, Department of Psychiatry, Burlington, VT 1991; 1991.

47.

47. Conners

. Conners’ rating scales, revised. Multi-Health Systems, New York 1997.

48.

48. Wechsler

. Wechsler Intelligence Scale for Children3rd edn. Psychological Corporation, Texas 1991.

49.

49. Barnett

Maruff

Vance

Luk

Costin

. Abnormal executive function in attention deficit hyperactivity disorder: The effect of stimulant medication and age on spatial working memory. Psychol Med 2001; 31: 1107–1115.

50.

50. Kempton

Vance

Maruff

Luk

Costin

. Executive function and attention deficit hyperactivity disorder: stimulant medication and better executive function performance in children. Psychol Med 1999; 29: 527–538.

51.

51. Owen

James

Leigh

. Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 1992; 115: 1727–1751.

52.

52. Owen

Downes

Sahakian

Polkey

Robbins

. Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia 1990; 28: 1021–1034.

53.

53. Elliott

Dolan

. The neural response in short-term visual recognition memory for perceptual conjunctions. Neuroimage 1998; 7: 14–22.

54.

54. Shallice

. Specific impairments in planning. Phil Trans R Soc Lond 1982; 298: 199–209.

55.

55. Crawford

Blackmore

Lamb

Simpson

. Is there a differential deficit in fronto-executive functioning in Huntington's disease?. Clin Neuropsychol Assess 2000; 1: 3–19.

56.

56. Denney

Rapport

. Cognitive pharmacology of stimulants in children with ADHD. Stimulant drugs and ADHD, Solanto

Arnsten

AFT

Castellanos

. Oxford University Press, Oxford 2001; 283–302.

57.

57. Vance

ALA

Luk

. Attention deficit hyperactivity disorder and anxiety: is there an association with neurodevelopmental deficits?. Aust N Z J Psychiatry 1998; 32: 650–657.

58.

58. Castellanos

Tannock

. Neuroscience of ADHD: the search for endophenotypes. Nat Rev Neurosci 2002; 3: 617–628.

59.

59. Taylor

. Clinical foundations of hyperactivity research. Behav Brain Res 1998; 94: 11–24.

60.

60. Jain

Palacio

Castellanos

. Attention-deficit/hyperactivity disorder and comorbid disruptive behaviour disorders: evidence of pleiotropy and new susceptibility loci. Biol Psychiatry 2007; 61: 1329–1339.

61.

61. Rhee

Willcutt

Hartman

Pennington

DeFries

. Test of alternative hypotheses explaining the comorbidity between attention-deficit/hyperactivity disorder and conduct disorder. J Abnorm Child Psychol 2008; 36: 29–40.

62.

62. Luciana

Nelson

C A

. The functional emergence of prefrontally guided working memory systems in four-to-eight year old children. Neuropsycholgia 1998; 36: 273–293.

63.

63. Zakzanis

. Statistics to tell the truth, the whole truth and nothing but the truth: formulae, illustrative numerical examples, and heuristic interpretation of effect size analyses for neuropsychological researchers. Arch Clin Neuropsychol 2001; 16: 653–667.

64.

64. McGee

Clark

Symons

. Does the Connors’ Continuous Performance Test aid in ADHD diagnosis?. J Abnorm Child Psychol 2000; 28: 415–424.

65.

65. Gomez

Harvey

Quick

Scharer

Harris

. DSM-IV AD/HD: confirmatory factor models, prevalence, and gender and age differences based on parent and teacher ratings of Australian primary school children. J Child Psychol Psychiatry 1999; 40: 265–274.

66.

66. Mitsis

McKay

Schulz

Newcorn

Halperin

. Parent-teacher concordance for DSM–IV ADHD in a clinic-referred sample. J Am Acad Child Adolesc Psychiatry 2000; 39: 308–313.

67.

67. Crystal

Ostrander

Chen

August

. Multimethod assessment of psychopathology among DS subtypes of children with attention deficit hyperactivity disorder: self-, parent and teacher reports. J Abnorm Child Psychol 2001; 29: 189–205.

68.

68. Swanson

Kraemer

Hinshaw

. Clinical relevance of the primary findings of the MTA: success rates based on severity of ADHD and ODD symptoms at the end of treatment. J Am Acad Child Adolesc Psychiatry 2001; 40: 168–179.

Neurocognitive Function in Attention-Deficit–Hyperactivity Disorder with and Without Comorbid Disruptive Behaviour Disorders

Abstract

Keywords

Methods

Participants

Measures

Computerized neuropsychological tasks

Procedure

Statistical analysis

Results

Demographic and clinical characteristics of the sample

Neurocognitive performance

Discussion

References