Reward-Related Neural Correlates of Antisocial Behavior and Callous-Unemotional Traits in Young Men

Abstract

Background: Individuals involved in antisocial behavior often engage in excessive reward-driven behavior even in the face of severe punishments including incarceration. However, the neural mechanisms of reward processing in antisocial behavior have not been examined while considering the heterogeneity of antisocial behavior and specific phases of reward and loss processing. In this study, we investigate the relationship between antisocial behavior, callous-unemotional traits, and neural activity during the anticipation and receipt of rewards and losses.

Methods: A community sample of 144 low income, racially diverse, urban males at risk for antisocial behavior completed self-report measures, a clinical interview, and an fMRI scan at age 20. Neural response during the anticipation and receipt of monetary rewards and losses was linked to antisocial behavior and callous-unemotional traits using a priori ventral striatum region of interest analyses and exploratory whole brain analyses.

Results: Antisocial behavior, but not callous-unemotional traits, was related to less ventral striatum response during reward anticipation. There were no significant relationships between neural reactivity and antisocial behavior or callous-unemotional traits during reward or loss outcomes. Antisocial behavior was also related to less ventrolateral prefrontal cortex reactivity during reward and loss anticipation.

Conclusions: These findings support a hypo-reactivity model of reward and loss anticipation in antisocial behavior. Lower striatal reactivity to cues of reward and lower prefrontal-regulatory recruitment during reward and loss anticipation may contribute to maladaptive reward-related behavior found in antisocial behavior.

Keywords: Antisocial Behavior; Callous-Unemotional; Loss; Reward; Ventral Striatum; fMRI.

Figure 1. Self-reported antisocial behavior (AB) predicts less ventral striatum and vlPFC reactivity during the anticipation of rewards

(A) Self-reported AB is negatively correlated with ventral striatum reactivity in the right ventral striatum region of interest (centered at the peak voxel, MNI: 10, 14, -6, t=−2.73, k=164). This finding emerges across multiple measures of AB and when controlling for CU traits and other psychiatric diagnoses. (B) Scatterplot of Self-Reported AB and ventral striatum reactivity during anticipation of rewards. (C) Self-reported AB is negatively correlated with activity in the left middle frontal gyrus (ventrolateral prefrontal cortex) and activity in a cluster extending from the right VS into the broader caudate during anticipation of rewards (centered at the second peak voxel, MNI: 10 14 −6; t = 3.06, k=625). The VS/caudate cluster remains (and demonstrated suppression effects) when controlling for CU traits and other psychiatric diagnoses. The left middle frontal gyrus cluster was only significant when partialling out variance of CU traits and other psychiatric diagnoses (centered at the peak voxel, MNI: −32, 60, −2; t = −3.36, k =601). (D) Scatterplot of Self-Reported AB and middle frontal gyrus (ventrolateral prefrontal cortex) reactivity during anticipation of rewards

Figure 2. Self-reported antisocial behavior (AB) predicts less middle frontal gyrus reactivity during loss anticipation (versus baseline)

(A) Self-report AB is negatively correlated with left middle frontal gyrus (lateral prefrontal cortex) reactivity (centered at the peak voxel, MNI: −42, 48, 2, t=−3.32, k=531) during anticipation of loss. This cluster remains (and demonstrated suppression effects) when controlling for CU traits and other psychiatric diagnoses. (B) Scatterplot of Self-Reported AB and middle frontal gyrus (ventrolateral prefrontal cortex) reactivity during anticipation of loss.