EDITORIALS
The Neurobiology of Disruptive Behavior Disorder
James R. Blair, Ph.D.
Disruptive behavior disorder comprises conduct disorder,
defined as the persistent violation of the rights of others and
of age-appropriate norms, and oppositional defiant disorder,
characterized by angry or irritable mood, argumentative or
defiant behavior, or vindictiveness. Conduct disorder and
oppositional defiant disorder are two of the most prevalent
child psychiatric disorders. They confer considerable costs
to society and are associated with relatively poor long-term
prognoses. The meta-analytic review published in this issue
(1) summarizes the findings of 24 functional magnetic reso-
nance imaging (fMRI) studies of patients with these disorders
and provides useful information regarding the pathophysi-
ology of the disorders. The authors conducted several meta-
analyses of these studies: one omnibus analysis contrasting
youths with disruptive behavior disorder or conduct prob-
lems across all tasks and then several sub-meta-analyses that
examined group differences on tasks grouped according to
whether they involved “hot” executive functioning, “cool”
executive functioning, or emotion processing. Core findings
of the omnibus meta-analysis are that, across tasks, youths with
disruptive behavior disorder or conduct problems showed
underactivation in the rostral and dorsal anterior cingulate and
in the medial prefrontal cortex and ventral caudate. However,
the sub-meta-analyses revealed that these results were primarily
driven by the hot executive function fMRI studies. It is perhaps
worth considering here what hot executive functioning is. As the
authors point out, previous work has distinguished between hot
and cool executive functions as motivationally and emotionally
significant tasks compared with more abstract tasks (2). How-
ever, it is important to note that almost all of the hot executive
functioning tasks were reinforcement-based decision-making
tasks (participants are choosing whether to respond to objects
based on whether their choices are likely to engender reward or
punishment). Indeed, as the authors state, this dysfunction “may
represent the neural underpinning for evidence that perturbed
reward-based decision making is key to conduct disorder” (1).
The other two sub-meta-analyses examining the cool executive
function and emotion processing tasks both revealed temporal
abnormalities with emotion processing tasks also linked to con-
sistent underresponsiveness in the prefrontal cortex.
This review is important both for identifying consistent
regions of dysfunction in patients with conduct disorder or
oppositional defiant disorder and for concentrating attention
on the neurodevelopmental nature of such disorders. Re-
views such as this stress the importance of neurobiology in
the early development of these pernicious disorders.
Am J Psychiatry 173:11, November 2016
It is interesting to consider the present findings in the
context of the ongoing discussion about how we should ap-
proach the definition of psychiatric disorders. Should psy-
chiatric disorders be considered categorically distinct entities
with separable forms of pathophysiology? Alternatively, should
we adopt a more dimensional approach as envisaged by the
Research Domain Criteria (RDoC) (3); that is, should we
consider neural systems and their associated functions and
how these, when compromised, give rise to specific symptom
sets (i.e., clusters of behaviors that appear to occur together)
that may be shared across disorders? The authors argue that
the hot executive function decision-making deficits may
be “key to conduct disorder” (1), potentially implying a
more categorical view. But decision-making deficits, or at
least reduced reward re-
sponsiveness, are seen not Previous work has
only in conduct disorder distinguished between
but also in several other hot and cool executive
psychiatric conditions,
functions as motivationally
including attention defi-
and emotionally significant
cit hyperactivity disorder
(ADHD) and depression tasks compared with more
(4, 5). As such, we might abstract tasks.
want to consider these
findings from an RDoC perspective. The difficulty here,
however, is that the symptom sets associated with reduced
reward responsiveness remain unclear. Reduced reward re-
sponsiveness has been linked to impulsiveness in patients
with ADHD (4) and to anhedonia in patients with de-
pression (5). Moreover, there are other forms of decision-
making deficits that may be more directly related to the
expression of conduct problems. Specifically, there is evi-
dence that the relative inability to recruit regions involved
in avoidance behavior as a function of expected value re-
lates to level of conduct problems (6, 7). In other words,
while healthy youths recruit regions such as the dorso-
medial frontal and, particularly, the inferior frontal and
anterior insula cortices as they are attempting to avoid a
poor choice as a function of how poor the choice is, youths
with conduct problems do this to a significantly reduced
extent. Moreover, the level of impairment in youths is
positively related to their level of conduct problems. In
short, further work is necessary to identify the symptom
sets associated with specific forms of dysfunction in the
neurocognitive systems involved in reward-punishment
decision making and to determine the extent to which
ajp.psychiatryonline.org 1073
EDITORIALS
these forms of dysfunction, and associated symptom sets,
are seen across disorders.
The cool executive function and emotion processing sub-
meta-analyses both revealed temporal cortex dysfunction in
the disruptive/conduct problems group, albeit in different
temporal regions. This is interesting because, as the authors
note, structural imaging studies have relatively consistently
identified structural deficits in these regions (8). However,
while these findings, consistent within both structural and
functional studies, stress the neurodevelopmental nature of
the disorder, their functional significance remains elusive.
The authors suggest that temporal lobe dysfunction might
reflect attention problems. However, it should be noted that
regions classically implicated in either top-down attention or
endogenous orientation (e.g., frontal and parietal regions)
were not seen to be dysfunctional in the youths with conduct
problems in this meta-analysis. One possible explanation is
that these regions reflect atypical development within the
temporal cortex as a secondary consequence of dysfunction
in other structures that more directly incur risk for conduct
problem symptom sets. As such, they would reflect the neu-
rodevelopmental nature of the disorder without incurring a
risk for a specific symptom set. Alternatively, or additionally,
these forms of temporal lobe dysfunction may incur a risk for
a specific symptom set that has yet to be specified.
The sub-meta-analysis of emotion processing tasks also
revealed decreased right dorsolateral prefrontal activation in
the youths with conduct problems. The authors suggest that
this implies that youths with conduct problems show poor
frontal top-down cognitive control over emotion processing.
This may be correct. There is an argument that at least some
youths with conduct problems show overly responsive emo-
tional responses that would be consistent with poor frontal
top-down control (9). However, most studies find reduced
emotional responsiveness in youths with conduct problems,
and it is worth noting that this sub-meta-analysis also revealed
reduced activity in the left temporal pole. Reduced temporal
pole activity during emotion processing tasks does not sug-
gest disinhibited responding but rather reduced responding.
Reduced emotional responding is unlikely to reflect reduced
top-down control. Importantly, the flow of information be-
tween the frontal and temporal cortices is not one way but is
interactive. Activity in the dorsolateral prefrontal cortex can
be stimulated by salient visual stimuli represented in more
posterior regions (10). As such, it is perhaps more likely that
the decreased right dorsolateral prefrontal activation reflects
1074 ajp.psychiatryonline.org
reduced attention toward the underprocessed emotional
features.
In conclusion, this meta-analytic review stresses the
neurodevelopmental nature of disruptive behavior disorder.
It strongly suggests that attention to the neurocognitive sys-
tems underpinning reward- and punishment-based decision
making is critical. Moreover, it reminds us that, as the field
progresses, we concentrate on the functional implications of
specific forms of dysfunction and the incurred risk for specific
forms of symptom sets.
AUTHOR AND ARTICLE INFORMATION
From the Section of Affective and Cognitive Neuroscience, NIH,
Bethesda, Md.
Address correspondence to Dr. Blair (jamesblair@mail.nih.gov).
The author reports no financial relationships with commercial interests.
Accepted August 2016.
Am J Psychiatry 2016; 173:1073–1074; doi: 10.1176/appi.ajp.2016.16080971
REFERENCES
1. Alegria AA, Radua J, Rubia K: Meta-analysis of fMRI studies of
disruptive behavior disorders. Am J Psychiatry 2016; 173:1119–1130
2. Zelazo P, Muller U: Executive function in typical and atypical de-
velopment, in Handbook of Childhood Cognitive Development.
Edited by Goswasmi U. Oxford, England, Blackwell, 2004
3. Insel T, Cuthbert B, Garvey M, et al: Research domain criteria
(RDoC): toward a new classification framework for research on
mental disorders. Am J Psychiatry 2010; 167:748–751
4. Plichta MM, Scheres A: Ventral-striatal responsiveness during re-
ward anticipation in ADHD and its relation to trait impulsivity in the
healthy population: a meta-analytic review of the fMRI literature.
Neurosci Biobehav Rev 2014; 38:125–134
5. Stringaris A, Vidal-Ribas Belil P, Artiges E, et al: The brain’s response
to reward anticipation and depression in adolescence: dimensionality,
specificity, and longitudinal predictions in a community-based sample.
Am J Psychiatry 2015; 172:1215–1223
6. White SF, Tyler PM, Erway AK, et al: Dysfunctional representation
of expected value is associated with reinforcement-based decision-
making deficits in adolescents with conduct problems. J Child Psychol
Psychiatry 2016; 57:938–946
7. White SF, Pope K, Sinclair S, et al: Disrupted expected value and
prediction error signaling in youths with disruptive behavior dis-
orders during a passive avoidance task. Am J Psychiatry 2013; 170:
315–323
8. Rogers JC, De Brito SA: Cortical and subcortical gray matter volume
in youths with conduct problems: a meta-analysis. JAMA Psychiatry
2016; 73:64–72
9. Blair RJ, Leibenluft E, Pine DS: Conduct disorder and callous-
unemotional traits in youth. N Engl J Med 2015; 372:784
10. Miller EK, Buschman TJ: Cortical circuits for the control of attention.
Curr Opin Neurobiol 2013; 23:216–222
Am J Psychiatry 173:11, November 2016