Matthys2012 Article ImpairedNeurocognitiveFunction PDF
Matthys2012 Article ImpairedNeurocognitiveFunction PDF
Matthys2012 Article ImpairedNeurocognitiveFunction PDF
DOI 10.1007/s10567-012-0118-7
Abstract In this review, a conceptualization of opposi- Likewise, problem solving is impaired due to deficiencies
tional defiant (ODD) and conduct disorder (CD) is pre- in inhibition, attention, cognitive flexibility, and decision
sented according to which social learning processes in making. Consequently, children and adolescents with ODD
these disorders are affected by neurocognitive dysfunc- and CD may have difficulty learning to optimize their
tions. Neurobiological studies in ODD and CD suggest that behavior in changeable environments. This conceptualiza-
the ability to make associations between behaviors and tion of ODD and CD is relevant for the improvement of the
negative and positive consequences is compromised in effect of psychological treatments. Behavioral and cogni-
children and adolescents with these disorders due to tive-behavioral interventions that have been shown to be
reduced sensitivity to punishment and to reward. As a modestly effective in ODD and CD are based on social
result, both learning of appropriate behavior and learning to learning. Limited effectiveness of these interventions may
refrain from inappropriate behavior may be affected. be caused by difficulties in social learning in children and
adolescents with ODD and CD. However, although these
impairments have been observed at a group level, the
W. Matthys
Department of Child and Adolescent Psychiatry, Rudolf Magnus deficits in reward processing, punishment processing, and
Institute of Neuroscience, University Medical Centre Utrecht, cognitive control mentioned above may not be present to
Heidelberglaan 100, 3584 CX Utrecht, The Netherlands the same extent in each individual with ODD and CD.
e-mail: w.matthys@uu.nl
Therefore, the neurocognitive characteristics in children
W. Matthys and adolescents with ODD and CD should be assessed
Department of Child and Adolescent Studies, Utrecht University, individually. Thus, instead of delivering interventions in a
Utrecht, The Netherlands standardized way, these programs may benefit from an
individualized approach that depends on the weaknesses
L. J. M. J. Vanderschuren
Department of Neuroscience and Pharmacology, Rudolf Magnus and strengths of the neurocognitive characteristics of the
Institute of Neuroscience, University Medical Centre Utrecht, child and the adolescent.
Utrecht, The Netherlands
Keywords Oppositional defiant disorder
L. J. M. J. Vanderschuren
Division of Behavioural Neuroscience, Department of Animals Conduct disorder Neurocognitive dysfunctions
in Science and Society, Faculty of Veterinary Medicine, Utrecht Social learning processes
University, Utrecht, The Netherlands
D. J. L. G. Schutter
Department of Experimental Psychology, Utrecht University, Introduction
Utrecht, The Netherlands
The characteristic features of oppositional defiant disorder
J. E. Lochman (&)
(ODD) and conduct disorder (CD) (American Psychiatric
Department of Psychology, University of Alabama, Tuscaloosa,
AL, USA Association 2000) are oppositional, aggressive, and anti-
e-mail: jlochman@as.ua.edu social behaviors. ODD and CD are among the most
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prevalent psychiatric disorders in children and adolescents, environments, adequate cognitive control of emotions,
with percentages of 3.2 for ODD and 2.0 for CD (Lahey thought, and behavior is necessary.
et al. 1999). In addition to the negative developmental The present conceptualization is based on our recent
consequences of ODD and CD for the individual, such as review in which we provide a coherent picture of the
poor interpersonal and school adjustment, delinquency, neurobiology of ODD and CD within the framework of
substance use disorders, and other psychiatric disorders these three interrelated mental domains (Matthys et al.
(Kim-Cohen et al. 2003; Maughan and Rutter 2001), these 2012). In extension of this review, here we discuss the
disorders also incur high costs to society (Raaijmakers main findings of this review from the perspective of social
et al. 2011; Scott et al. 2001). Conceptual developmental learning processes that are impeded in ODD and CD by
models are needed as they can identify active mechanisms, impairments in the three mental domains. Thus, in the
which can be targets of preventive and treatment inter- present paper, we first give a concise overview of the neu-
ventions for ODD and CD youth (Matthys and Lochman robiology of ODD and CD from the perspective of the
2010). three mental domains. We then conceptualize ODD and
While some models focus on environmental factors such CD as disorders in which social learning processes are
as coercive parent–child interactions (Reid et al. 2002), affected by impairments in the three mental domains.
others also target individual psychological factors such as Finally, we provide suggestions for improving learning-
in the contextual social cognitive model (Lochman and based interventions to prevent and treat ODD and CD.
Wells 2002). Such models describe the development of In the neurobiological overview, we primarily focus on
oppositional, aggressive, and antisocial behaviors from the studies including clinical samples of children and adoles-
perspective of deviances in social learning based on oper- cents with ODD and CD, and children and adolescents with
ant conditioning, that is, the contingencies of reinforcement these disorders and/or psychopathic or callous–unemo-
(Kazdin 2005), and of observational learning, that is, tional (CU) traits, that is, the affective factor of psychop-
observing another individual engage in behavior without athy (Frick and White 2008). The samples of many studies
performing the behavior oneself (Bandura 1973). Likewise, consist of both children and adolescents with ODD and
these models serve as a foundation for learning-based children and adolescents with CD, here referred to as dis-
interventions, that is, behavioral parent training and cog- ruptive behavior disorders (DBDs). In order to better
nitive behavior therapy, with small-to-medium effect sizes understand the development of ODD and CD, we also
(McCart et al. 2006). Although individual biologically discuss several subclinical community studies that classify
based factors such as temperamental characteristics are subject groups on the basis of aggressive behavior, anti-
acknowledged in these social learning models (e.g., Patt- social behavior, and delinquent behavior.
erson 2002), in our view, the specific role of neurobio-
logical factors involved in the learning processes resulting Punishment Processing
in ODD and CD symptoms has been neglected. Here, we
present a conceptualization of ODD and CD according to Young children learn to make associations between inap-
which social learning processes in ODD and CD are propriate behaviors and (threats of) punishment. Yet,
affected by neurobiological factors. children need to be sensitive to punishment cues in order to
Our conceptual framework consists of three interrelated learn refraining from inappropriate behaviors. Learning to
mental domains: punishment processing, reward process- refrain from inappropriate behaviors is indeed based on
ing, and cognitive control (for similar models, see Ernst classical (aversive) conditioning. For example, aversive
and Fudge 2009; van Honk et al. 2010). The mental conditioning involves learning to associate hitting another
domains in this framework are defined in terms of their child with subsequent punishment or the perception of the
functions (e.g., the processing of punishment cues) that are distress of the victim. Lack of fear in children can explain
physically realized by the various neurobiological systems poor socialization because low fear of punishment would
(e.g., the amygdala, the autonomic nervous system, and the reduce the effectiveness of classical conditioning (Lykken
hypothalamus–pituitary–adrenal axis). According to this 1957). Aversive conditioning is crucial for children as it
conceptual framework presented here, adequate function- results in anticipatory fear whenever children consider
ing of the three mental domains is necessary for the behaving inappropriately as well as in discomfort (e.g.,
occurrence of appropriate social learning processes. guilt and remorse) occasioned by committed antisocial
Indeed, children need to be sensitive to punishment cues in behavior (Kochanska 1993). The neurobiological system
order to learn refraining from inappropriate behaviors. involved in punishment processing consists of the amyg-
Likewise, normative sensitivity to reward cues is a pre- dala, the sympathic nervous system, and the hypothala-
requisite condition for learning appropriate behaviors. mus–pituitary–adrenal axis. The amygdala has been widely
Finally, in order to adapt behavior in changeable implicated in learning and expressing the association of
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certain undesirable behaviors with punishment, as shown levels of CU traits who also had ADHD symptoms showed
by studies on classical (fear) conditioning and operant less right amygdala activity to fearful faces compared with
conditioning (e.g., passive avoidance learning) (Davis and healthy controls; these differences remained after control-
Whalen 2001; Cardinal et al. 2002; Maren and Quirk 2004; ling for ADHD symptoms (Jones et al. 2009). In summary,
Balleine and Killcross 2006; Phelps and Ledoux 2005). these studies reveal evidence of deficits in amygdala
Thus, impaired functioning of the amygdala associated function in children and adolescents with DBDs or conduct
with decreased aversive stimulus–reinforcement associa- problems with or without psychopathic or CU traits. The
tions is thought to be the characteristic of psychopathic above-mentioned studies all are cross-sectional. Thus,
individuals (Blair 2007). The amygdala has projections although these studies may help explain the occurrence of
to the hypothalamus, midbrain reticular formation, and ODD and CD symptoms in elementary school children and
brainstem, areas that are associated with autonomic adolescents, they are not informative about the develop-
responses. ment of these symptoms in young children.
A number of studies on structure and function of the The neural circuit network involved in responsiveness to
amygdala have been performed in children and adolescents aversive stimuli also comprises the sympathetic branches
with CD or conduct problems with or without psychopathic of the autonomic nervous system. In a prospective study,
characteristics. In adolescents with early-onset CD, most of fear conditioning using electrodermal responsivity was
whom were comorbid with attention deficit hyperactivity assessed in children at ages 3, 4, 5, 6, and 8. It was shown
disorder (ADHD), reduced gray matter volumes were that poor fear conditioning from ages 3–8 years is associ-
found in a variety of brain regions, including the amygdala ated with aggression at age 8 (Gao et al. 2010a). Further-
relative to healthy controls. Regression analyses indicated more, it appeared that poor fear conditioning at age 3
that CD symptoms were primarily correlated with gray predisposes to crime at age 23 (Gao et al. 2010b).
matter reductions in temporal lobes, including the amyg- Besides this important series of studies that demonstrate
dala, as well as the prefrontal cortex (Huebner et al. 2008). poor fear conditioning in young children as a risk factor for
In addition, reduced gray matter volumes in the left developing aggressive and criminal behavior, psychopathy-
amygdala have been found in adolescents with CD, relative prone adolescent boys, relative to healthy controls, have
to healthy controls (Sterzer et al. 2007). Likewise, gray also been found to display reduced sympathetic electro-
matter volume reductions in the bilateral amygdala have dermal activity in anticipation of and in response to an
been found in adolescents with CD, relative to healthy aversive stimulus (Fung et al. 2005). Importantly, no dif-
comparison subjects (Fairchild et al. 2011). In contrast, one ferences were found between antisocial non-psychopathic
study failed to find structural deviances of the amygdala in boys and antisocial psychopathy-prone boys. Thus, the
boys with CU traits (De Brito et al. 2009). Although the antisocial component of psychopathy may be associated
boys in this study had conduct problems, the presence of with electrodermal hyporesponsivity. In another study,
ODD or CD was not assessed, however. Thus, the negative children and adolescents with CD comorbid with ADHD
findings could have been due to the presence of a less showed low skin conductance responses to aversive stimuli
severe form of psychopathology in these boys. as well as to (positive and negative) emotional stimuli and
Findings from a functional magnetic resonance imaging to neutral pictures, compared to children and adolescents
(fMRI) study suggest left amygdala hyporeactivity to with ADHD-only and healthy controls (Herpertz et al.
negative emotional stimuli in children and adolescents 2005). The authors concluded that this general autonomic
aged 9–15 years with CD (Sterzer et al. 2005). Likewise, in hyporeactivity may reflect a deficit in associative infor-
an fMRI study, DBD children and adolescents (aged mation-processing systems that normally produce adaptive
10–17 years) with CU traits, many of whom also had cognitive-emotional reactions.
comorbid ADHD, were found to have reduced amygdala
responsiveness during the presentation of fearful facial Hypothalamus–Pituitary–Adrenal Axis
expressions in comparison with healthy controls and youth
with ADHD. Interestingly, in this study, functional con- The neural circuit network involved in responsiveness to
nectivity analyses demonstrated greater correlations aversive stimuli and stress also comprises the hypothala-
between the amygdala and ventromedial prefrontal cortex mus–pituitary–adrenal axis (LeDoux 2002). Cortisol
in healthy controls and youth with ADHD relative to those secretion by the adrenal cortex is controlled by adreno-
with DBDs and CU traits (Marsh et al. 2008). In another corticotropic hormone released from the pituitary, which is
fMRI study, boys with conduct problems and elevated regulated by corticotrophin-releasing hormone from the
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hypothalamus. Corticotrophin-releasing hormone is sensitivity may also result in reduced motivation to obtain
released in response to stress and subsequent activation of natural rewards. The associated unpleasant effect may
the amygdala and prefrontal cortex. Reduced cortisol incite children and adolescents to sensation-seeking, which
reactivity to stress has been found in children with DBDs, may manifest in antisocial behavior and in searching
many of whom had comorbid ADHD (van Goozen et al. unnaturally strong rewards such as drugs of abuse. The
1998, 2000). Importantly, low cortisol responsivity during neurobiological system involved in reward processing
stress appears to be specific to DBDs. In a study that consists of the amygdala, the orbitofrontal cortex, and the
examined children with DBDs, children with ADHD, and striatum (Cardinal et al. 2002; Balleine and Killcross 2006;
healthy controls, only children with DBDs showed a Blair 2007; Schoenbaum and Roesch 2005). The amygdala
blunted cortisol response (Snoek et al. 2004). is thought to subserve the formation of stimulus-outcome
associations based on reward, and the amygdala closely
Neurochemistry interacts with the orbitofrontal cortex, which has been
implicated in the generation of reinforcement expectations.
On the neurochemical level, studies examining serotoner- The orbitofrontal cortex and striatum also play a role in
gic (5-HT) and noradrenergic neurotransmission in the error prediction, thus facilitating learning of reward
central nervous system are particularly relevant. 5-HT (O’Doherty et al. 2006).
neurotransmission has, among other functions, been
implicated in the sensitivity to punishment and aversive Amygdala, Orbitofrontal Cortex, and Striatum
signals (Cools et al. 2008). There is support for an inverse
relationship between 5-HT measures and aggressive Reduced gray matter volumes in the amygdala in adoles-
behavior in children and adolescents with ODD and CD, cents with CD discussed above (Fairchild et al. 2011;
although this relationship is less clear than in adults (for an Huebner et al. 2008; Sterzer et al. 2007) may result in
extensive review, see Matthys et al. 2012). Noradrenergic altered reward processing. With respect to the functioning
neurotransmission may also play an important role in of the amygdala, the orbitofrontal cortex and the caudate
behavioral arousal associated with punishment (Berridge nucleus (i.e., part of the dorsal striatum), an fMRI study
and Waterhouse 2003). That is, if signals associated with using a passive avoidance task in adolescents with DBDs
punishment do not lead to the noradrenergically driven and psychopathic traits is relevant here (Finger et al. 2011).
increase of attention and change in emotional state, these In this task, participants learned to respond to stimuli that
signals become less meaningful. There is some evidence to engender reward and to refrain from responding to stimuli
suggest decreased noradrenergic functioning in the DBDs that engender punishment. First, amygdala responsiveness
(for an extensive review, see Matthys et al. 2012). throughout the learning task was lower in adolescents with
DBDs than in controls associated with an impairment in
Summary making stimulus-reinforcement associations. Second, while
performing the task, less orbitofrontal and caudate nucleus
Studies on amygdala function, electrodermal fear condi- responsiveness to early exposure in the task was shown in
tioning, cortisol reactivity to stress, and serotonergic and adolescents with DBDs relative to comparison youths,
noradrenergic neurotransmission indicate that reduced resulting in disrupted prediction error signaling. Third, less
sensitivity to punishment and aversive cues plays a role in orbitofrontal responsiveness to rewards was shown, asso-
ODD and CD symptoms. Children and adolescents with ciated with decreased representation of reward expectancy
ODD and CD thus may have difficulties in learning to values. Thus, the integrated functioning of the amygdala,
refrain from inappropriate behaviors. caudate nucleus, and orbitofrontal cortex seems to be dis-
rupted in adolescents with DBDs and psychopathic traits.
Reward Processing More evidence for orbitofrontal dysfunction in CD comes
from an fMRI study that assessed brain activation during a
In young children, newly acquired behaviors are likely to continuous performance task measuring sustained attention
become part of their behavioral repertoire when these and the effects of reward on performance. Children and
behaviors are rewarded. Indeed, according to operant adolescents with CD without ADHD showed underactiva-
conditioning principles, behaviors that are rewarded are tion in the right orbitofrontal cortex during the reward
more likely to be repeated. In learning new behaviors, condition relative to healthy comparison subjects and
classical conditioning is also thought to be involved, that is, children and adolescents with ADHD without CD (Rubia
in making the association between behaviors and reward- et al. 2009a). These studies suggest that compromised
ing stimuli. Thus, low sensitivity to reward will reduce the processing of reward cues may result in impaired rein-
learning of appropriate behaviors. Besides, low reward forcement processing.
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Heart Rate et al. 2001; Taylor et al. 1987) and in one meta-analysis
(Connor et al. 2002); in the latter study, the overall
Heart rate has been linked to reward processing (Fowles weighted mean effect size was 0.84 for overt and 0.69 for
1980) whereby low resting heart rate may reflect reduced covert aggression-related behaviors in ADHD. Together,
reactivity to rewarding stimuli associated with an these studies suggest that improved dopaminergic function
unpleasant state. In support of this interpretation, preschool results in a reduction of ODD and CD symptoms.
boys who chose to watch videotapes of intense anger had With respect to the behavioral mechanism of action
lower basal heart rates than boys who chose to watch of psychostimulants, methylphenidate has been shown to
videotapes of mild anger. Thus, boys with a lower heart exert positive effects on cognitive performance by
rate level might have sought a higher level of stimulation to increasing task salience (Volkow et al. 2004). As incentive
experience a pleasant emotional state (El-Sheikh et al. salience or ‘‘wanting’’ is particularly influenced by dopa-
1994). A longitudinal general population study found that minergic neurotransmission (Berridge 2007), an increase in
sensation-seeking, but not behavioral disinhibition, in boys incentive salience by psychostimulants might explain why
at age 13.5 and 16 mediated the relationship between low parents of children and adolescents with DBDs treated with
resting heart rate at age 11 and rule breaking at age 16 methylphenidate report improvement in their children’s
(Sijtsema et al. 2010). This study supports sensation- attention, motivation to comply, and to engage more pos-
seeking theory, which states that rule breaking in adoles- itively in social interactions. Indeed, evidence from animal
cence serves to alleviate the unpleasant state of stimulus studies indicates that treatment with psychostimulant drugs
hyporeactivity associated with low resting heart rate, to enhances the influence of salient, reward-, or punishment-
experience a pleasant level of emotional stimulation. associated cues on behavior (Robbins et al. 1983; Killcross
et al. 1997; Wyvell and Berridge 2000) and can also
Neurochemistry enhance reward- and punishment-driven learning processes
(Carr and White 1984; Hitchcott et al. 1997; Phillips et al.
Dopamine is an important neurotransmitter involved in 2003; Tye et al. 2010). Finally, an increase in dopami-
several aspects of reward processing. For example, dopa- nergic functioning by psychostimulants may also facili-
mine has been implicated in reward-related learning tate appropriate reward expectations (Berridge 2007;
processes, reward expectation, incentive salience, and Bromberg-Martin et al. 2010; Cardinal et al. 2002; Kelley
incentive motivation (Berridge 2007; Bromberg-Martin 2004; Robbins and Everitt 2007; Schultz 2007).
et al. 2010; Cardinal et al. 2002; Kelley 2004; Robbins and
Everitt 2007; Schultz 2007). Lower activity of brain Summary
dopamine systems could therefore result in reduced sal-
ience of positive emotional stimuli in the environment, lack Studies on the amygdala, orbitofrontal cortex, and caudate
of motivation to exert effort to obtain rewards, impaired nucleus, on heart rate, and on dopaminergic functioning
learning of stimulus-reward associations or reduced influ- indicate that reduced reward sensitivity plays a role in
ence of reward-associated stimuli on positive emotions. ODD and CD symptoms. Children and adolescents with
Both genetic studies (e.g., of catechol-O-methyltransferase; ODD and CD may therefore have difficulties in learning
COMT) and studies of the metabolite of dopamine suggest appropriate behaviors.
decreased dopaminergic functioning in ODD and CD (for
an extensive review, see Matthys et al. 2012). Furthermore, Cognitive Control
studies of the effectiveness of psychostimulants, which
enhance dopaminergic neurotransmission by blocking the In everyday situations, children are continuously faced
reuptake and/or enhancing the release of dopamine (Fone with problems they need to solve. Various cognitive con-
and Nutt 2005), may give insight into the neurochemical trol or executive functions are involved in problem solving,
mechanisms of ODD and CD. These studies have been such as planning, working memory, inhibition of inappro-
conducted primarily in ADHD, but in view of the sub- priate responses, flexibility in adaptation to environmental
stantial comorbidity of the DBDs with ADHD (Angold changes, and decision making (Nigg 2006). These func-
et al. 1999), it is no surprise that many studies have tions are subserved by the frontal cortex. Specifically, the
investigated the effect of psychostimulant drugs, such as paralimbic system comprising orbitofrontal, superior tem-
methylphenidate and amphetamine, in subjects with poral, cingulate cortices, and limbic brain regions mediates
ADHD with or without DBD or DBD symptoms. The the cognitive control of emotion and motivation (Blair
effect of psychostimulants on disruptive behaviors has been 2004). Due to maturation of the frontal cortex with age
shown convincingly in a number of studies (Ghuman et al., (Durston et al. 2001), cognitive control over behavior
2007; Greenhill et al. 2006; Klein et al. 1997; Swanson increases in children and adolescents.
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According to a meta-analysis of studies in school-aged A number of studies on structure and function of the
children, adolescents, and adults with externalizing dis- paralimbic system have been performed in children and
orders, the average mean effect size (Cohen’s d) of a adolescents with ODD and CD or conduct problems with or
variety of executive measures for the groups with anti- without psychopathic characteristics (for extensive
social behavior (criminality, delinquency, CD, psychopa- reviews, see Rubia 2011, and Matthys et al. 2012). For
thy, antisocial personality disorder) was 0.62, whereas the example, in a study with early-onset adolescents with CD
effect size for CD was 0.36 (Morgan and Lilienfeld (most of whom were comorbid with ADHD), whole brain
2000). However, the possible role of ADHD comorbidity volume analysis showed reduced gray matter volumes in
in executive functions impairments in CD was not the left orbitofrontal region, bilaterally in the temporal
examined in this study, while another meta-analysis lobes, and in the amygdala and hippocampus on the left
revealed that deficits in executive functions in CD are side compared with healthy controls. Mean total gray
likely due to the presence of comorbid ADHD matter volume was 6 % smaller in the clinical group.
(Pennington and Ozonoff 1996). On the other hand, it was Regression analyses indicated that CD symptoms were
shown in a further meta-analysis that deficits in response correlated primarily with gray matter reductions in limbic
inhibition are not only found in elementary school chil- brain structures including the amygdala and the prefrontal
dren with ADHD, but also in children with DBD without areas, whereas hyperactive/impulsive symptoms were
comorbid ADHD (Oosterlaan et al. 1998). Likewise, correlated with gray matter abnormalities in the frontopa-
impairments in inhibition have been found in preschool rietal and temporal cortices (Huebner et al. 2008).
children with aggressive behavior when compared with With respect to the functioning of the prefrontal cortex,
non-aggressive preschoolers, and these impairments were children and adolescents with CD and children and adoles-
maintained after controlling for attention problems cents with ADHD performing an inhibition task showed
(Raaijmakers et al. 2008). Impairments in inhibition were reduced activation in the posterior cingulate compared to
also found in preschool children with DBDs without healthy controls in an fMRI study. Children and adolescents
ADHD comorbidity relative to normal controls (Schoemaker with CD showed reduced activation in temporal-parietal
et al. 2012). Impaired executive functioning capacities regions during failed inhibition when compared with the
such as planning ability and inhibitory control have other groups. Since participants obtained feedback about
been linked specifically to reactive aggression (Ellis et al. their inhibition failures, the results suggest that performance
2009). monitoring networks are dysfunctional in CD when com-
Results of studies in ODD and CD are even more con- pared to ADHD and healthy controls (Rubia et al. 2008).
sistent when motivational factors are involved in executive Consistent with this notion is the observation that adoles-
functions. In this respect, the distinction has been made cents with psychopathic traits and ODD or CD, the majority
between ‘‘cool’’ executive functions and ‘‘hot’’ executive of whom also had comorbid ADHD, showed abnormal
functions that involve reward and punishment (Rubia responses of the ventromedial prefrontal cortex during
2011). For example, the tendency to continue a previously punished errors in a reversal learning task, as compared to
rewarded response that is now punished, that is, response adolescents with ADHD and healthy controls (Finger et al.
perseveration, has been demonstrated in children and 2008a, b). According to Rubia et al. (2008), this could mean
adolescents with DBDs (Daugherty and Quay 1991; that adolescents with CD care less about their mistakes than
Matthys et al. 1998, 2004; van Goozen et al. 2004). adolescents with ADHD and healthy controls, which is in
Response perseveration may contribute to impairments in line with evidence that children with DBDs are undermoti-
decision making rendering individuals unable to shift their vated and respond less to negative feedback than controls
behavior away from immediate rewards that are associated (Matthys et al. 2004; van Goozen et al. 2004).
with even larger punishments. Disadvantageous decision As already discussed in the section on reward processing,
making indicating favoring immediate rewards despite lower responsiveness to reward outcome information within
long-term punishments has been shown in children and the orbitofrontal cortex has been shown in children and ado-
adolescents with psychopathic tendencies (Blair et al. lescents with CD (Rubia et al. 2009a, b). Blair (2004) has
2001), adolescents with ADHD or CD (Ernst et al. 2003), argued that orbitofrontal cortex dysfunctioning is involved in
children with ODD most of whom were comorbid with the modulation of reactive aggression. Executive functioning
ADHD (Luman et al. 2010), adolescents with CD some of capacities such as planning ability and inhibitory control have
who had comorbid ADHD (Fairchild et al. 2009), and been specifically linked to reactive aggression (Ellis et al.
adolescents with both DBDs and substance dependence 2009). As the orbitofrontal cortex is involved in the compu-
(Schutter et al. 2011). tations of expectation of reward and violations of expected
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240 Clin Child Fam Psychol Rev (2012) 15:234–246
reward result in frustration, orbitofrontal dysfunction as necessary for the occurrence of appropriate social learning
shown in the studies by Finger et al. (2011), and by Rubia et al. processes. Results of neurobiological studies in ODD and
(2009a) may indeed be associated with reactive aggression. CD suggest that impaired neurocognitive functions, that is,
During interference inhibition and attention allocation, boys the functions exerted by the three mental domains, affect
with CD only showed reduced activation in right middle and the social learning processes in these disorders. First, the
superior temporal and parietal regions compared to controls. ability to make associations between behaviors and posi-
Impaired function of these areas possibly accounts for atten- tive or negative consequences is compromised. As a result,
tional deficits in CD, causing more errors (Rubia et al. 2009b). both learning of appropriate behavior and learning to
The anterior cingulate cortex, which is involved in refrain from inappropriate behavior may be affected. Sec-
emotion processing and social functioning (Bush et al. ond, problem solving is impaired due to deficiencies in
2000), has also been studied in children and adolescents inhibition, attention, cognitive flexibility, and decision
with DBDs. In an fMRI study by Stadler et al. (2007), making. As a result, children and adolescents may have
children aged 9–15 years with CD, the majority of who difficulty learning to optimize their behavior in changeable
also had comorbid ADHD, viewed negative pictures, and environments. Prospective studies, however, are needed to
showed reduced activation in the dorsal part of the anterior further clarify the role of impaired neurocognitive func-
cingulate cortex, that is, the part believed to be involved in tions in the development and in the maintenance of ODD
the cognitive control of emotional behavior, as compared and CD. Importantly, it should be excluded that the social
to healthy controls. This abnormal suppression of neural learning difficulties in ODD and CD are exclusively due to
activity may result in a failure to cognitively control general deficits of learning.
emotional behavior. Similarly, abnormal right anterior The conceptualization of the neurobiological systems in
cingulate cortex activation during the presentation of terms of functions allows for the inclusion of environ-
images with negative valence was shown in children and mental factors to better understand social learning diffi-
adolescents aged 9–15 years with CD most of whom also culties in ODD and CD. For example, as children learn to
had comorbid ADHD relative to healthy controls (Sterzer refrain from inappropriate behaviors based on aversive
et al. 2005). Impaired functioning of the anterior cingulate conditioning, difficulties in the processing of punishment
cortex associated with the cognitive control of emotions cues resulting in fewer associations between inappropriate
may thus be involved in DBD. Finally, during cognitive behaviors and punishment may put children at risk of
flexibility, brain dysfunctions in left superior temporal, developing ODD and CD symptoms, especially in families
bilateral parietal, and occipital regions were observed in with inconsistent discipline. Similarly, difficulties in the
CD boys relative to healthy controls (Rubia et al. 2010). processing of reward cues may result in compromised
learning of appropriate behaviors. This is an important
Summary issue that has often been overlooked and that may help
answer the question of why some children with ODD and
Impairments in executive or cognitive control functions have CD do not learn to substitute inappropriate behaviors with
been shown, that is, in inhibition and decision making, appropriate behaviors, as children typically do. To more
especially when motivational factors (reward and punish- fully understand this social learning difficulty, we need to
ment) are involved. Likewise, ODD and CD have been account for the parenting characteristics in the families of
associated with structural deficits and impaired functioning these children, such as the amount and quality of praising
of the paralimbic system comprising the orbitofrontal cortex, children’s appropriate behaviors. Finally, decreased cog-
superior temporal lobes, and cingulate cortices. Children and nitive control in children and adolescents may result in
adolescents with ODD and CD thus are less likely to learn reactive aggression and risk-taking behavior, maybe espe-
from their mistakes. Consequently, they may not learn to cially when parents of these children and adolescents do not
make appropriate decisions in the context of punishment and present appropriate models of coping in situations of frus-
reward. Impaired attention and cognitive flexibility also have tration because of difficulties in self-control themselves.
been shown in ODD and CD. Finally, problems in the
computations of expectation of reward and violations of
expected reward may result in reactive aggression. Improving the Tailoring of Psychological Treatments
Impaired Neurocognitive Functions Affect Social The role of impaired neurocognitive functions in the social
Learning Processes learning processes of ODD and CD has consequences for
the deployment of interventions with specific children.
According to the conceptual framework presented here, Over the years, behavioral and cognitive-behavioral inter-
adequate functioning of the three mental domains is ventions based on social learning have been developed,
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adapted, and tested. On the one hand, there is evidence of anxiety and mood disorders (Stringaris and Goodman
effectiveness of interventions in ODD and CD: the mean 2009b). Thus, the neurocognitive characteristics and asso-
effect size of behavioral parent training is 0.47 (range from ciated social learning difficulties in ODD may in part differ
1.68 to -0.06) and the mean effect size of cognitive from those in CD, and even among CD children and ODD
behavior therapy is 0.35 (range from 1.87 to -1.04) children, there are likely to be variations in the degree of
(McCart et al. 2006). These mean effect sizes, however, are neurocognitive difficulties evident.
not large. Furthermore, these effect sizes are based on We here suggest that for clinical purposes, the neuro-
studies conducted in highly controlled research settings in cognitive characteristics in children and adolescents with
which, for example, therapists are specifically trained to ODD and CD need to be assessed individually. This clin-
conduct the intervention and treatment fidelity is checked. ical assessment may consist of a mixture of assessment
Dissemination research does suggest that these interven- procedures such as standardized behavioral observation of
tions can be implemented effectively in real-world settings response to reward and punishment cues, neuropsycho-
when intensive training is provided to clinicians (Lochman logical tests of responsivity to reward and punishment,
et al. 2009) but it remains unclear whether the effect sizes neuropsychological tests of executive functions, and
obtained in everyday clinical practice would be as large as judgements of children’s and adolescents’ neurocognitive
evident in the clinical trials. functioning by parents and teachers. Instead of delivering
One may question why, despite intense efforts for five intervention programs in a standardized way, these pro-
decades to develop behavior parent training programs and grams should be individualized depending on the weak-
for four decades to develop cognitive behavior therapy nesses and strengths of the neurocognitive characteristics
programs, effects of these interventions still are small to of the child and the adolescent associated with their social
moderate, at best. Based on the evidence of impaired learning difficulties. We now discuss this individualization
neurocognitive functions in ODD and CD, limited effec- of psychological interventions indicating how the three
tiveness of these learning-based interventions may be mental domains could relate to intervention elements.
caused by difficulties in social learning by children and Evidence-based interventions for children with ODD and
adolescents with ODD and CD. The neurocognitive char- CD often include behavioral parent training (BPT) with
acteristics mentioned above, resulting in difficulty to parents, school-based behavioral consultation with teachers,
refrain from inappropriate behaviors due to low punish- and cognitive-behavioral intervention (CBI) with the chil-
ment sensitivity, however, refer to characteristics that have dren. CBI often becomes an increasingly important inter-
been found in groups of children and adolescents with vention component from middle childhood through
ODD and CD. This also applies to difficulties in learning to adolescence, while BPT is important at all ages. Typical, or
behave appropriately due to low reward sensitivity and to common, elements of evidence-based interventions for
difficulties in learning to optimize behavior in changeable children with ODD and CD have been described in recent
environments due to impaired cognitive control of behavior years (e.g., Matthys and Lochman 2010). Evidence-based
and emotions. Thus, at an individual level children and intervention work with parents in the home context, and also
adolescents with ODD or CD may differ in these neuro- with teachers and other personnel in the school context,
cognitive characteristics and associated learning difficul- typically includes: (1) increase of positive attention, social
ties, as ODD and CD are heterogeneous disorders reinforcement, and rewards, (2) enhanced antecedent control
depending on, i.a., comorbidity with ADHD, association through clarification of instructions and commands, (3)
with CU traits and anxiety symptoms. Importantly, recent improved consistency of clearly defined (and non-harsh)
research suggests that ODD is a separate disorder to be discipline methods, and (4) improved monitoring and
distinguished from CD both in symptomatology, comor- supervision of children’s behavior. Both BPT and CBI often
bidity, and development (Rowe et al. 2010; Nock et al. include a focus on (5) enhanced stress management and
2007; Stringaris and Goodman 2009a, b). Indeed, with emotional regulation (anger management) skills. Other
respect to ODD symptomatology, a defiant/headstrong typical elements of CBI with children include: (6) enhanced
behavior cluster (argues with adults, defies adults’ requests, goal setting and behavioral goal completion abilities, (7)
deliberately annoys people, blames others) can be differ- enhanced perspective taking and abilities to accurately per-
entiated from an irritability cluster (temper tantrums, ceive the intentions of others, (8) improved social problem-
touchy or easily annoyed, angry, and resentful) (Stringaris and solving skills, and (9) improved social skills and abilities to
Goodman 2009a; Rowe et al. 2010). ODD may therefore become more engaged with less-deviant peer groups. This
be considered a mixed disorder of behavior and emotion. listing of typical common elements is not totally compre-
The defiant/headstrong behavior cluster is associated spe- hensive but does address primary targets of intervention.
cifically with the development of CD, while the irritability So, while all of these domains are conceptualized as key
factor is associated specifically with the development of mechanisms of action in intervention with ODD and CD
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242 Clin Child Fam Psychol Rev (2012) 15:234–246
children, how would relative emphasis on these typical may be adequate when used selectively. Because children
common elements shift if children had difficulties in a and adolescents with deficient punishment processing
specific mental domain? If a child had relative deficits in characteristics probably are at risk for escalating cycles of
the mental domain of reward processing, the first two of the punishment as milder forms of punishment may not
common elements noted, in work with parents and teach- ‘‘work’’ for them (see also Dadds and Salmon 2003), it is
ers, would be of special value. Thus, more time would be also important to emphasize the first typical element above
spent with parents and teachers than would typically be the by relabeling inappropriate behaviors into positive oppo-
case on parent–child special time, use of praise and point sites. It is particularly critical to positively reinforce the
systems with rewards, and focus on how clearly stated appropriate behaviors using praise and token economy
instructions to children is more likely to lead to compliant rewards for these children and adolescents. In CBI work
behaviors and then to positive reinforcement. Importantly, with children with deficient punishment processing, it is
BPT and behavioral school consultation in general assist especially important to assist children to experience clear
parents and teachers to relabel inappropriate behaviors consequences for their behaviors and to more accurately
such as fighting with siblings or defiance toward parents expect negative outcomes, or consequences, for their
into ‘‘positive opposites’’ (Kazdin 2005) or ‘‘prosocial behavior. CBI elements that appear to be especially critical
opposites’’ (Wells et al. 2008) such as cooperative play for enhancing children’s outcome expectations for their
with siblings and compliance toward parents. Adults, then, behaviors are short- and long-term goal setting activities
learn how to use labeled praise appropriately (e.g., having (typical element 6 above) and a highly detailed and com-
eye contact with the child, praising the child with enthu- prehensive approach to considering consequences for
siasm, and describing the particular behavior that is possible problem solutions during social problem-solving
praised; Webster-Stratton 2001; Wells et al. 2008). activities (typical element 8 above).
Individualization of use of rewards and praising may While children with a weak cognitive control domain
help increase the efficiency of these parenting skills; for can benefit from the BPT typical elements (1–4), some of
example, if it is demonstrated that the processing of reward the CBI activities are likely to be particularly relevant.
cues in a child with ODD/CD comorbid with ADHD is Failures to inhibit one’s behavior appropriately can be
severely impaired, then parents and teachers can practice associated with poor self and emotional regulation skills.
getting the attention of the child by touching and holding Thus, CBI elements designed to assist with emotional
the child’s attention by using eye contact. Likewise, if the regulation could be an area of particular emphasis. As
emotional significance of the positive message of praise is children develop better perspective taking skills (typical
less well processed, both verbal and nonverbal enthusiasm element 7 above), they can be less prone to impulsively and
would be particular relevant. In children with borderline erroneously misinterpret the intentions of others (thus
intelligence and deficient reward processing, adults need to reducing hostile attributional biases). Children’s develop-
be extremely clear in specifying the behavior that is ment of improved anger management skills (typical ele-
expected for the child to understand what behavior is being ment 5 above) and deliberate social problem-solving skills
praised. Enhanced focus on rewards within the CBI would (‘‘stop-think-what should I do?’’ typical element 8 above)
also be useful for children with deficient reward process- can also assist children’s inhibitory abilities, and these
ing. To increase children’s attention to rewards, shorter typical elements can thus receive greater emphasis with
behavioral monitoring intervals should be used during these children. Decision making is a key aspect of one of
intervention sessions and in children’s weekly behavioral the last steps of the problem-solving model and can be an
goals in school or home settings, and more frequent and important area of emphasis for children with cognitive
more salient rewards should be used as consequences for control problems. Addressing children’s expectations of
children accomplishing behavioral goals during interven- long-term consequences and outcomes of behaviors can
tion and in real-world class and home settings (e.g., assist children to reduce inappropriate decision making,
Lochman et al. 2008). which favors immediate rewards despite long-term pun-
With regard to the mental domain of punishment pro- ishments and results in risky decisions.
cessing, relatively greater emphasis in work with parents In conclusion, in the etiology of ODD and CD, more
and teachers can be placed on clarifying antecedent control attention should be paid to neurobiological factors involved
and monitoring of children, and use of more consistent and in the social learning processes that play a role in the ini-
less harsh discipline methods (e.g., withdrawal of privi- tiation and maintenance of these disorders. Likewise, the
leges, work chores, and time-out) (typical elements 2–4 assessment of the neurocognitive characteristics associated
above). It is clear that punishment as the presentation of an with the social learning processes may help individualize
aversive stimulus such as slapping is inappropriate while interventions. As a result, the effectiveness of learning-
the removal of a positive stimulus such as losing privileges based interventions may increase.
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