Introduction
Attention-deficit/ hyperactivity disorder (ADHD) in children is a chronic childhood developmental disorder expressed in symptoms of inattention, hyperactivity, and impulsivity (APA
2000). There is large phenomenological overlap between ADHD and oppositional defiant disorder (ODD) with comorbidity rates of 30–90% (Angold et al.
1999; Pliszka
2000). ODD is expressed as refusing to comply with rules, deliberately annoying others, and a frequent loss of temper. Several researchers have suggested common etiological factors that add to the development of ADHD and ODD. In particular, neurocognitive impairments may be a key route for the development of both disorders through the expression of genetic, perinatal and psychosocial influences (Barkley
1997; Castellanos and Tannock
2002; Loeber et al.
2000). Although many studies have investigated neurocognitive functions in ADHD and ODD (see meta-analyses Willcutt et al.
2008), studies into neurocognitive impairments in children with comorbid ADHD and ODD are scarce. Thus, it remains controversial whether the co-occurrence of ADHD and ODD represents a combination of both disorders, or a separate entity with a distinct neurocognitive functioning profile. Knowledge on comorbid ADHD and ODD has important clinical implications, since this comorbidity is associated with increased morbidity and disability in terms of psychiatric, family and social functioning as compared to ADHD alone, even in the absence of conduct problems (Biederman et al.
1996).
Executive functioning (EF) is a well studied domain of neurocognitive functioning in ADHD and ODD (e.g., Barkley
1997; Morgan and Lilienfeld
2000; Oosterlaan et al.
2005; Pennington and Ozonoff
1996). EF comprises a set of higher order cognitive abilities that enable goal directed behavior and problem solving (Pennington and Ozonoff
1996), subserved by the prefrontal cortex and its subcortical connections (Casey et al.
2007; Semrud-Clikeman et al.
2000). In particular, inhibitory control is thought to be a key function, fundamental for the later emergence of other aspects of EF (Barkley
1997). The Stop Task allows measurement of the latency of the covert inhibitory response (Logan et al.
1984) and several studies reported on impaired Stop Task performance in children with ADHD and children with ODD (Albrecht et al.
2005; Alderson et al.
2007; Logan et al.
1997; Scheres et al.
2001). In a meta-analysis of the Stop Task, Oosterlaan et al. (
1998) concluded that both disorders are associated with inhibitory deficits, although the evidence for ADHD is stronger than for ODD. In contrast, a recent meta-analysis of EF functions such as inhibitory control revealed that ADHD, not ODD is associated with EF problems (Willcutt et al.
2008). Thus, whether ADHD and ODD contribute jointly or independently to these problems is unclear. There are two studies comparing children with ADHD-only and ADHD+ODD on the Stop Task with conflicting results: One study reported intact inhibitory control in both clinical groups (Scheres et al.
2001), while the other reported problems in children with ADHD-only, but not in children with ADHD+ODD (e.g., Albrecht et al.
2005).
In addition to EF, researchers have related ADHD and ODD to a motivational deficit (Newman and Wallace
1993; Quay
1997; Raine
1993; Sergeant et al.
1999; Sonuga-Barke
2002). An unusual sensitivity to motivational incentives is suggested to result in excessive reward-seeking behavior and impulsive tendencies in the presence of reward, as well as a decreased sensitivity to penalty. In ADHD there are reports of a strong preference for immediate over delayed reward, even when the delayed reward is larger (see for review Luman et al.
2005). This is explained by an aversion for waiting and a decreased sensitivity to cues that predict rewards (Sagvolden et al.
2005; Sonuga-Barke
2002; Tripp and Wickens
2008). Aggressive and delinquent youngsters are found to search for reward, irrespective of decreased total gain and increasing penalty (Daugherty and Quay
1991; Fonseca and Yule
1995; Matthys et al.
1998; O’Brien and Frick
1996). This is explained by a decreased emotional reactivity to the negative consequences of reward-searching behavior (Raine
1993), and researchers argue that, due to comorbid ODD, similar processes explain reward-searching behavior in ADHD (e.g., Daugherty and Quay
1991). Indeed, there is some evidence of decreased sensitivity to aversive stimuli in ADHD+ODD (Herpertz et al.
2001); a reward-immediacy effect in ODD is not supported so far (Van Goozen et al.
2004).
A third potentially underlying neurocognitive deficit in ADHD and ODD is a deficit in temporal information processing (Castellanos and Tannock
2002; Dougherty et al.
2007). Temporal information processing is the ability to order sequential events in time and the ability to create rhythms; skills that depend on intact time perception, time discrimination and time (re)production (Ivry
1996). There is evidence of temporal information processing impairments in children with ADHD and adolescents with anti-social behavior in terms of an internal clock that runs too fast (Barratt and Patton
1983; Dougherty et al.
2007; Toplak et al.
2006), and a decreased stability of time estimation output (Dougherty et al.
2007; Luman et al.
2008). Thus, in these groups time seems to elapse too quickly and too variably, which may explain their problems with waiting and planning (APA
2000). Whether problems with temporal information processing are more related to ADHD or ODD is unclear, since studies comparing children with (ADHD+) ODD and ADHD-only are absent so far.
In sum, studies strongly suggest neurocognitive impairments in ADHD compared to typical development, but it is unclear whether children with ADHD+ODD are impaired and to what extent. Thus, the aim of this study was twofold: (a) to investigate neurocognitive impairments in ADHD-only and ADHD+ODD by assessing three key neurocognitive functions: response inhibition, reinforcement sensitivity, and temporal information processing, and (b) to test whether ADHD+ODD is a more severe from of ADHD in terms of neurocognitive performance, in line with observed increased disability in ADHD+ODD at other levels of performance (Biederman et al.
1996). In Experiment 1, inhibition abilities were measured using the Stop Task. In Experiment 2, groups were compared in terms of time production abilities and reinforcement sensitivity using a Time Production Task that was administered under a reward and penalty condition (Luman et al.
2008). If comorbid ADHD+ODD constitutes of a more severe form of ADHD, we expect impaired performance in both clinical groups compared to controls (e.g., Dougherty et al.
2007; Logan et al.
1997; Newman and Wallace
1993; Sonuga-Barke
2002; Toplak et al.
2006), but with a more deviant pattern of deficits observed in ADHD+ODD than the ADHD-only group. The unique contribution of this study is that it directly compares ADHD and ADHD+ODD on three key neurocognitive functions that have not been investigated in concert so far.
Discussion Experiment 1
The results demonstrated inhibition problems (slower SSRT) in ADHD-only, but not in ADHD+ODD. Impaired inhibition performance in the ADHD-only group replicates earlier findings (Oosterlaan et al.
1998; Willcutt et al.
2008), and confirms inhibition problems as an important neurocognitive disability in ADHD. This difficulty with inhibiting an initiated motor response, may partly explain the behavioral symptoms of impulse control (APA
2000). Imaging data of the Stop Task in children with ADHD (Rubia et al.
2008) suggest that children with ADHD-only show underactivation of the dorsolateral prefrontal cortex during inhibition, a brain area that is found to play a major role in explaining impulsive and hyperactive behavior in ADHD (Bush et al.
2005; Seidman et al.
2005). The difficulties with inhibiting a motor response in the ADHD-only group may have been caused by ‘poor motor control’, since their responses to go trials were slower and more variable than those in the TD group. However, also children with ADHD+ODD showed poor motor control, while showing intact SSRT.
Intact inhibition in the ADHD+ODD group in contrast to the ADHD-only group implies that this function is more related to ADHD than ODD, which is reported in earlier studies (Alderson et al.
2007; Logan et al.
1997; Scheres et al.
2001). Results of a recent meta-analysis suggest that EF impairments in ODD, thus not only inhibition, are related to comorbid ADHD (Willcutt et al.
2008), which argues against the hypothesis that the variance in EF is more related to aggression than hyperactivity (Séguin et al.
2004). The difference in inhibition performance between the ADHD-only and ADHD+ODD group suggests that comorbid ADHD+ODD is not a more severe form of ADHD. As the data show, children with comorbid ADHD+ODD had larger error-rates than children with ADHD-only and controls, while showing similar SSRT. Possibly, children with ADHD+ODD used a different strategy than children with ADHD-only, such as not responding to go-signals (increasing the error-rate) in favor of accurate inhibitions. MRI studies using the Stop Task, report that ADHD and CD children differ in brain activation during inhibitions: while CD was more related to attention allocation problems as a result of deficits in the temporal-parietal lobe, ADHD was more related to inhibition problems as a result of deficits in the prefrontal cortex (Rubia et al.
2008). Although imaging studies in children with (ADHD+)ODD are missing so far, differences in brain activity between ADHD-only and ADHD+ODD may explain the observed differences in performance.
Reports on a lack of differentiation on stop task performance between ADHD and ADHD+ODD (see Scheres et al.
2001), could be related to differences in the Stop Task used. In the study by Scheres et al. (
2001) the event rate manipulations may have ‘activated children to perform well’, which resulted in a lack of performance differences between the ADHD groups and the TD group.
Discussion Experiment 2
According to the model of Wing and Kristofferson (
1973) intact time production requires an accurate internal clock and intact execution of motor responses. The internal clock includes the actual internal representation of time, and motor execution includes all that happens between the clock trigger and the response being executed. The findings show that, compared to TD children, (1) both clinical groups showed a faster internal clock, as indicated by greater underestimations of time, and (2) children with ADHD+ODD showed impaired execution of motor responses, as indicated by more variable time productions. The findings confirm that time passes faster in children with ADHD (comorbid with ODD) than controls (Dougherty et al.
2007; Toplak et al.
2006). Such an abnormally fast internal clock could explain overactive and impulsive behavior (acting ‘too fast’) in ADHD (comorbid with ODD) and the problems with waiting and planning (Oosterlaan et al.
2005; Sergeant et al.
2002). A faster execution of movements in children with ADHD (comorbid with ODD) is observed in difficulties with hand-motor coordination in sports or writing, which is often described as ‘clumsy’ behavior (Karatekin et al.
2003). The observation that time estimations of children with ADHD+ODD fell in-between those of children with ADHD-only and controls, suggests that comorbid ADHD+ODD is not a more severe form of ADHD in terms of timing performance. Increased variability in motor timing execution has been observed in many patient groups (see Stuss et al.
2003), including anti-social adolescents (Dougherty et al.
2007). This is the first study that demonstrates these problems in children with ODD (comorbid with ADHD). Many experimental studies on response variability have focused only on ADHD (e.g., Leth-Steensen et al.
2000; Russell et al.
2006), but our findings stress the importance of investigating the role of comorbid ODD.
Children with ADHD-only responded differently to reinforcement than children with ADHD+ODD, at least when the median time production was considered. Children with ADHD+ODD and controls decreased their tendency to underestimate time in the face of reward and penalty (median time production closer to 1,000 ms), suggesting an increase in motivation to perform well. Children with ADHD-only, on the other hand, pressed the button too early in the prospect of winning and also in the prospect of loosing money, possibly because they were distracted by reinforcement stimuli (see Douglas
1989) or tried to avoid reward delay (see Sonuga-Barke
2002). The results suggest that children with ADHD+ODD and not children with ADHD-only are reward maximizers (the positive effect of reward was larger for children with ADHD+ODD than for controls) at least as measured in an experimental setting. In the face of penalty, children with ADHD+ODD performed similarly to controls. Thus, no evidence was revealed that children with ADHD+ODD are less sensitive to penalty as observed in children with CD. Children with CD are thought to show a smaller emotional response to threat-related stimuli (Raine
1993), which may explain their diminished attention to penalty. This ‘lack of fear’ would not apply for children with ADHD+ODD in our study. Otherwise, a decreased sensitivity to penalty in children with (ADHD+)ODD may occur only in conflicting situations were both reward and penalty are available (Raine
1993). If replicated using ecological valid paradigms, these findings have important clinical implications for behavioral interventions that use reinforcement to shape behavior (see Clinical Implications).
Taken together, children with ADHD-only seem distracted by reward and penalty, while children with ADHD+ODD seem to profit from reinforcement. Again, these findings argue against the idea that ADHD+ODD can be considered a more severe form of ADHD.
General Discussion
The goal of this study was twofold: (a) to investigate neurocognitive impairments in children with ADHD and children with ADHD+ODD and (b) to test whether ADHD+ODD is a more severe from of ADHD in terms of neurocognitive performance. Since studies of neurocognitive functioning in children with ADHD+ODD are currently lacking, the second aim of this study was of specific importance (Willcutt et al.
2008). The findings suggest that children with ADHD-only showed difficulties on all three neurocognitive functions: inhibition, timing (internal clock functioning) and reinforcement sensitivity. Children with ADHD+ODD were less impaired on inhibition and reinforcement sensitivity than children with ADHD-only, and were unique in their pattern of increased timing variability. Thus, the findings suggest that comorbid ADHD+ODD is a substantially different entity in terms of neurocognitive problems, and not a separate subgroup of ADHD with equal or more severe neurocognitive problems as compared to ADHD-only (Biederman et al.
1996). These findings stress the importance of investigating the role of comorbid ODD when studying these neurocognitive functions in ADHD.
The idea that comorbid ADHD+ODD is a different entity than ADHD-only is supported by electrophysiological studies that show different brain abnormalities in children with ADHD+ODD compared to children with ADHD-only or ODD-only (Banaschewski et al.
2003; Clarke et al.
2002). Children with ADHD-only, in contrast to the ADHD+ODD group, demonstrated attenuated electrophysiological responses (less P3 activation to cues) during a Continuous Performance Task (CPT; Banaschewski et al.
2003). These findings suggest problems with anticipation and preparation of responses in ADHD-only that are not observed in children with ADHD+ODD. Impaired anticipation and preparation of responses in ADHD-only may explain problems with response inhibition such as observed in the Stop Task.
Our findings have implications for the theories on the possible mechanisms of comorbidity between ADHD and ODD (see Rutter
1997). According to Rutter (
1997) the first possibility is that the diagnostic distinction between ADHD and ODD is artefactual. In other words, both forms of psychopathology represent varied manifestations of the same general syndrome of disruptive behaviour, possibly with different peak ages of manifestation. Another option is that symptoms associated with ADHD provoke environmental factors that predisposes to ODD. For example, ADHD behaviour may provoke negative reactions from other people, that may lead to ODD symptoms. Our finding that ADHD+ODD is a less severe form of ADHD in terms of the three key neurocognitive functions studied here, may suggest the development of ADHD in children with ADHD+ODD differs from the development of ADHD in children with ADHD-only. The common etiological model for ADHD is that the disorder develops through heritable risk factors, which lead to neurocognitive dysfunctions which in turn lead to the symptoms of ADHD (Doyle et al.
2005). This model might not hold for comorbid ADHD+ODD. Possibly the development of ADHD in children with ADHD+ODD is the result of (negative) environmental factors, rather than neurocognitive deficiencies that result from risk genes for ADHD. This hypotheses is supported by lower heritability estimates for ADHD+ODD than for ADHD (Eaves et al.
1997; Thapar et al.
1999). This would argue for multiple developmental pathways for ADHD as has been suggested by others (Castellanos and Tannock
2002).
This study has some limitations. Firstly, the inclusion of a group of children with ODD-only would have enabled us to investigate whether ADHD+ODD is a separate entity, that differs from both ADHD and ODD (such as observed by Banaschewski et al.
2003). Secondly, in both Experiments groups differed in IQ, especially the group with ADHD+ODD showed a lower IQ than the TD group. A review of 27 studies (Hogan
1999) showed that 60% of the studies into IQ in relation to ADHD and ODD reported a significant negative relation between IQ and ADHD and IQ and ODD. Importantly, inserting IQ as a covariate in our analyses resulted in similar results as ANOVAs without IQ as covariate, indicating that the neurocognitive problems are robust and independent of IQ. A similar limitation is the difference in age in Experiment 1: Children with ADHD were almost a year younger than children with ADHD+ODD. Both groups were recruited from our outpatient clinic, where ADHD is usually diagnosed in development earlier than ODD. Despite the positive relation between age and SSRT, covarying for age left the findings unchanged. Finally, one may question whether the differences between ADHD-only and ADHD+ODD relate to differences in ADHD subtypes. In Experiment 1, children with ADHD-only showed higher (parent) ratings of inattention and lower ratings of hyperactivity/impulsivity than children with ADHD+ODD. Future studies should reveal whether problems with the response inhibition are more related to inattention than hyperactivity/impulsivity. And although no differences in ADHD-ratings were observed between the clinical groups in Experiment 2, recent findings suggest that altered reinforcement sensitivity is related to hyperactivity/impulsivity, rather than inattention (Scheres et al.
2007).
Clinical implications
Although confirmation of our findings is necessary in a community sample of children with ADHD (not only including children with ADHD symptoms above a certain cutt-off), the findings suggest that ADHD+ODD is not a more severe form of ADHD in terms of impairments in neurocognitive functioning. Since neurocognitive functions are of great importance for daily life functioning, affecting academic (e.g., Geary
1993), and social performance (Lezak
2004), assessing comorbid ODD in ADHD seems highly significant. Therefore, interventions that focus on training these neurocognitive abilities (e.g., Klingberg et al.
2005) seem particularly relevant for children with ADHD-only. Otherwise, the observation that children with ADHD+ODD profit more from reward and penalty than children with ADHD-only suggest that behavioral interventions that make use of rewards and penalties to shape behavior (mediation therapy) may be especially effective in the comorbid group. Rewards may have a distracting impact on performance of children with ADHD, especially when they try to work ‘as quickly as possible’ to obtain a reward.