We contrasted 2 hypotheses regarding the neural basis of the reversal learning deficit typically found in children and adults with psychopathic traits. Specifically, we predicted that children with psychopathic traits would demonstrate dysfunction in either regions of the vl and dmPFC associated with processing response conflict and implementing alternative responses or, alternatively, regions of the vmPFC associated with reinforcement processing. Consistent with the latter hypothesis, we found that children with psychopathic traits displayed abnormal activity in the vmPFC (BA 10) during punished reversal errors. There were no indications of atypical activity in the vl and dmPFC in the children with psychopathic traits.
Reversal learning impairments have been repeatedly reported in children and adults with psychopathic traits.18,19,23
On the basis of the early human neuroimaging literature, which stressed the importance of the vlPFC in reversal learning,24,28,58
it was initially assumed that the reversal impairment in persons with psychopathic traits was due to dys-function in the vlPFC.16,19,23
However, the current data do not support this theory. As can be seen in , the children with psychopathic traits showed appropriate increases in vlPFC activation during punished reversal errors.
Recent neuroimaging data highlighting the importance of the vmPFC in reversal learning suggested that dys-function in this region may account for the impairment in individuals with psychopathic traits.27
In line with this hypothesis, we found that children with psychopathic traits displayed abnormal activity in the vmPFC during punished reversal errors. To our knowledge, this is the first report of abnormal vmPFC activation in children with severe disruptive behaviors and high psychopathic traits. This finding is consistent with neuropsychological work in adults that has associated orbital and vmPFC dysfunction with individuals with developmental psychopathy.16,18,59
Furthermore, fMRI studies of adults with high psychopathic traits have demonstrated functional abnormalities in the ventromedial cortex during aversive conditioning60
and a correlation with the vmPFC (BA 10) and psychopathy scores during a prisoner's dilemma task.61
The high prevalence of substance abuse in adults with psychopathic traits has been an important caveat in prior studies,16,18
as exposure to illicit drugs, such as cocaine, can impair orbitofrontal cortex function and reversal learning.62-65
Herein, this potential confound was reduced by studying children and young adolescents who have not had significant exposure to illicit substances, further strengthening the evidence for vmPFC abnormality in individuals with psychopathic traits.
A critical role of the vmPFC in reversal learning appears to be its role in processing reinforcement expectations and information. Studies across species support the role of the orbital and vmPFC in the generation and representation of reinforcement expectations.24,31,32,35,38,64,66
Consistent with these studies and replicating the findings of this reversal task in healthy adults,27
our comparison groups demonstrated decreased BOLD signal responses in the vmPFC during punished reversal errors compared with correct rewarded responses. In contrast, children with psychopathic traits did not show a decrease in vmPFC BOLD signal during punished reversal errors but instead demonstrated increased BOLD signal compared with correct rewarded responses. The lack of the typical reduction in activity in this region during punished reversal errors indicates children with psychopathic traits may not be appropriately processing the violation of reinforcement expectations. Failure to appropriately process this violation may impair their ability to detect the contingency change.
A similar pattern was observed in the caudate. As in the vmPFC, healthy children showed decreased BOLD responses during punished reversal errors. This is in line with recent work implicating the caudate in addition to the medial PFC in prediction error signaling.67,68
In contrast, children with psychopathic traits showed an increase in caudate BOLD signal during punished reversal errors in comparison with correct control responses. This atypical caudate responding in the children with psychopathic traits may be due to abnormal input from the vmPFC or may reflect a more general impairment in prediction error signaling. The current result must be interpreted with caution, however, as activity in the caudate in children with ADHD alone was not significantly different from the control or psychopathic traits groups.
Given the high prevalence of comorbid ADHD and psychopathic traits, it is notable that we did not observe the abnormalities in the vmPFC in children with ADHD only. In the vmPFC, activity in children with ADHD only did not differ from that of healthy comparison children. This suggests that vmPFC dysfunction is specific to the group with psychopathic traits and is not likely attributable to comorbid ADHD. Many early studies implicating ADHD with increased criminality did not assess for comorbid CD,69
and fewer assessed for the presence of psychopathic traits.4,70
Interestingly, a recent prospective longitudinal study of hyperactive children that did assess for the presence of childhood conduct problems found that while adult recidivism rates for hyperactive children with early conduct problems were significantly elevated, rates for hyperactive children without childhood conduct problems were no higher than control children.69
The appropriate pattern of vmPFC activity observed in our ADHD-only group offers some of the first neural-level evidence of how children with ADHD plus psychopathic traits differ from those with ADHD only. However, the present study does not distinguish whether the vmPFC abnormality is specific to children high in psychopathic traits or whether such dysfunction would be also observed in children with severe conduct problems but low in psychopathic traits.
Additional caveats to the present study should be mentioned. The first is that the behavioral performance of children with psychopathic traits did not significantly differ from that of either comparison group. The relatively preserved reversal performance in children with psychopathic traits contrasts with data from previous studies18,19,23
and likely reflects task differences between the current fMRI study and previous behavioral work. In particular, this study used serial presentation of the stimulus pairs during the imaging runs unlike previous behavioral studies where the participants learned about several pairs simultaneously. This reduced task difficulty and thus also reduced the likelihood of confounds introduced by large performance differences. The presence of vmPFC dysfunction in this psychopathic traits cohort, despite comparable task performance, indicates that group differences in this region stem from neural abnormalities rather than performance differences. A second potential limitation is the inclusion of children with psychopathic traits and ADHD with medication histories. While simple stimulant medications were held in all children with psychopathic traits and ADHD for 48 hours prior to the scanning session, the long-term effects of these medications may have impacted the current results. While no orbitofrontal cortex dysfunction was observed in this study, this does not imply that the orbitofrontal cortex, a region previously causally related to psychopathy, is intact in children high in psychopathic traits. The absence of dysfunction may reflect a lack of involvement of this region in this form of reversal task or signal loss in the inferior orbitofrontal cortex.
Models of developmental psychopathic traits have postulated functional abnormalities in the amygdala,71,72
The vmPFC and amygdala are reciprocally connected75
and the interaction of these 2 structures is important in stimulus-reinforcement learning.76,77
It is possible that the aberrant signal in the vmPFC in children with psychopathic traits arises from abnormal inputs from the amygdala. However, recent nonhuman primate studies demonstrate that amygdala lesions alone do not impair reversal learning.78
We therefore propose that the altered signal in the present study represents dysfunction within the vmPFC. Whether vmPFC dysfunction occurs independently, or as a developmental consequence of abnormal inputs from the amygdala, remains to be determined. In conclusion, this study provides one of the first confirmations at the neural level of dysfunction specific to the vmPFC in children with high psychopathic traits and disruptive behavioral disorders. The functional specificity indicated by the current study suggests that impairments in the processing of reinforcement information and expectations in the vmPFC may predispose these individuals to impaired decision making, leading to increased frustration and reactive aggression.