The neurobiology of psychopathic traits in youths

Abstract

Conduct disorder is a childhood behaviour disorder that is characterized by persistent aggressive or antisocial behaviour that disrupts the child's environment and impairs his or her functioning. A proportion of children with conduct disorder have psychopathic traits. Psychopathic traits consist of a callous-unemotional component and an impulsive-antisocial component, which are associated with two core impairments. The first is a reduced empathic response to the distress of other individuals, which primarily reflects reduced amygdala responsiveness to distress cues; the second is deficits in decision making and in reinforcement learning, which reflects dysfunction in the ventromedial prefrontal cortex and striatum. Genetic and prenatal factors contribute to the abnormal development of these neural systems, and social-environmental variables that affect motivation influence the probability that antisocial behaviour will be subsequently displayed.

Figure 1. Core regions implicated in, and functions disrupted by, psychopathic traits

a | Core regions implicated in psychopathic traits: the amygdala, the caudate (which is part of the striatum) and the ventromedial prefrontal cortex (vmPFC). In addition to these core regions, the anterior insular cortex (AIC) and the dorsomedial PFC (dmPFC) may also be implicated. b | Functional impairments associated with psychopathic traits. In individuals with psychopathic traits, impaired processing of distress cues results in impaired learning about actions that harm others (stimulus-reinforcement learning), which involves the amygdala. In addition, impaired prediction error signalling in these individuals, which involves the striatum, causes impairments in both stimulus-reinforcement and response–outcome learning. As a result, the expected value of objects, cues and responses are poorly learnt and represented (in the vmPFC), and decision making is impaired. Response conflict resolution (which involves the dmPFC), initiation of response change (which involves the AIC) and response implementation (caudate) — functions implicated in guiding an individual away from suboptimal behavioural choices — are thought to be generally intact in individuals with psychopathic traits. These regions are also recruited to guide an individual away from suboptimal behavioural choices based on expected value information, that is, because the response about to be made is associated with punishment. Individuals with psychopathic traits show reduced recruitment of these areas on the basis of expected value information.

Figure 2. A framework for understanding conduct disorder

This model shows the aetiological (genetic and environmental), neural, cognitive and behavioural aspects of conduct disorder. Genetic factors reduce amygdala activation, specifically in response to distress cues, and consequently reduce emotional empathy. Genetic factors may also influence striatal and ventromedial prefrontal cortex (vmPFC) responsiveness to prediction error and expected value information and thereby lead to impaired decision making, but this has yet to be empirically demonstrated. Owing to the extensive interconnections between the amygdala, striatum and vmPFC, early dysfunction in one area is likely to be associated with dysfunction in the others. Perinatal factors, such as maternal substance abuse during pregnancy, can affect the functional integrity of these regions. All of these factors may lead to similar dysfunction at the cognitive level and may result in callous–unemotional traits and in increased antisocial behaviour and instrumental aggression. Impairments in decision making increase the risk that these individuals fail to achieve their goals, become frustrated and demonstrate frustration-based reactive aggression. Specific genetic polymorphisms as well as exposure to trauma, violence and neglect can result in increased amygdala responsiveness, specifically to threat cues. Such increased responsiveness increases threat sensitivity and the likelihood that a threat triggers reactive aggression (as opposed to freezing or escape behaviour). Increased amygdala responsiveness is also associated with an increased risk for anxiety disorders. Thus, patients meeting criteria for conduct disorder can have callous–unemotional traits or high levels of anxiety: callous–unemotional traits are associated with reduced amygdala responses to threat, whereas anxiety is associated with increased amygdala responses to threat. This suggests that there are at least two forms of conduct disorder. The first is referred to here as ‘conduct disorder with psychopathic traits’ and includes behaviours marked in red. The second is known as ‘conduct disorder associated with anxiety and emotional lability’ and includes the behaviours marked in blue (also see BOX 1). Both forms are likely to show under-regulated responses to social provocation (marked in green).