Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning

Abstract

Context: Children and adults with psychopathic traits and conduct or oppositional defiant disorder demonstrate poor decision making and are impaired in reversal learning. However, the neural basis of this impairment has not previously been investigated. Furthermore, despite high comorbidity of psychopathic traits and attention-deficit/hyperactivity disorder, to our knowledge, no research has attempted to distinguish neural correlates of childhood psychopathic traits and attention-deficit/hyperactivity disorder.

Objective: To determine the neural regions that underlie the reversal learning impairments in children with psychopathic traits plus conduct or oppositional defiant disorder.

Design: Case-control study.

Setting: Government clinical research institute.

Participants: Forty-two adolescents aged 10 to 17 years: 14 with psychopathic traits and oppositional defiant disorder or conduct disorder, 14 with attention-deficit/hyperactivity disorder only, and 14 healthy controls.

Main outcome measure: Blood oxygenation level-dependent signal as measured via functional magnetic resonance imaging during a probabilistic reversal task.

Results: Children with psychopathic traits showed abnormal responses within the ventromedial prefrontal cortex (Brodmann area 10) during punished reversal errors compared with children with attention-deficit/hyperactivity disorder and healthy children (P < .05 corrected for multiple comparisons).

Conclusions: To our knowledge, this study provides the first evidence of abnormal ventromedial prefrontal cortex responsiveness in children with psychopathic traits and demonstrates this dysfunction was not attributable to comorbid attention-deficit/hyperactivity disorder. These findings suggest that reversal learning impairments in patients with developmental psychopathic traits relate to abnormal processing of reinforcement information.

Figure 1

Probabilistic reversal task. Participants made button-press responses to select one of the pair images and received positive or negative feedback. After 20 or 25 acquisition trials, the contingency was reversed for the next 20 or 25 trials so that selection of the previously “good” image now resulted in loss of points. Participants then learned to reverse their response and select the alternate image to gain points.

Figure 2

Diagnosis×response type interaction. In the left (A) and right (B) ventromedial prefrontal cortex/Brodmann area (BA) 10, healthy children and children with attention-deficit/hyperactivity disorder (ADHD) demonstrated decreased blood oxygenation level–dependent (BOLD) responses during punished reversal errors compared with correct rewarded responses. In contrast, patients with psychopathic traits showed increased BOLD responses during punished reversal errors in this region. Error bars represent standard errors.

Figure 3

Main effect of response type. Blood oxygenation level–dependent (BOLD) responses in the ventrolateral prefrontal cortex (A) and dorsomedial prefrontal cortex (B) were significantly greater during punished reversal errors compared with correct rewarded responses in all 3 groups: psychopathic traits, attention-deficit/hyperactivity disorder (ADHD), and healthy controls. Error bars represent standard errors.