Limbic responses to reward cues correlate with antisocial trait density in heavy drinkers

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2012-03, Vol.60 (1), p.644-652
• Main Authors: Oberlin, Brandon G., Dzemidzic, Mario, Bragulat, Veronique, Lehigh, Cari A., Talavage, Thomas, O'Connor, Sean J., Kareken, David A.
• Format: Article
• Language: English
• Subjects: Alcohol use; Alcohol use disorder; Alcoholism; Alcoholism - physiopathology; Alcoholism - psychology; Antisocial personality disorder; Antisocial Personality Disorder - physiopathology; Behavior; Cues; Ethanol; Humans; Limbic System - physiopathology; Magnetic Resonance Imaging; Odors; Olfaction; Orbital; Personality disorder; Prefrontal; Retrospective Studies; Reward; Studies; Young Adult
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2011.12.043

Antisocial traits are common among alcoholics— particularly in certain subtypes. Although people with antisocial tendencies show atypical brain activation in some emotion and reward paradigms, how the brain reward systems of heavy drinkers (HD) are influenced by antisocial traits remains unclear. We used subjects' preferred alcohol drink odors (AO), appetitive (ApCO) and non-appetitive (NApO) control odors in functional magnetic resonance imaging (fMRI) to determine if reward system responses varied as a function of antisocial trait density (ASD). In this retrospective analysis, we examined 30 HD who had participated in imaging twice: once while exposed to clamped intravenous alcohol infusion targeted to 50mg%, and once during placebo saline infusion. Under placebo, there were positive correlations between ASD and blood oxygenation level dependent (BOLD) activation in the [AO>ApCO] contrast in the left dorsal putamen, while negative correlations were present in medial orbitofrontal cortex (OFC) and the bilateral amygdala. A similar pattern was observed in the correlation with the [AO>NApO] contrast. This inverse relationship between ASD and activation in OFC and amygdala was specific to AO. However, negative correlations between ASD and the [ApCO>NApO] contrast were also present in the insula, putamen, and medial frontal cortex. These data suggest that frontal and limbic reward circuits of those with significant ASD are less responsive to reward cues in general, and particularly to alcohol cues in medial OFC and amygdala. These findings are broadly consistent with the reward deficiency syndrome hypothesis, although positive correlation in the striatum suggests regional variability. ► fMRI measured responses to aromas of heavy drinkers' individually preferred drinks. ► We measured correlations between this activation and density of antisocial traits. ► Antisocial traits correlated positively with activation in the putamen. ► But activation correlated negatively in medial orbitofrontal cortex and amygdala. ► Antisocial traits may mediate responses to alcohol odor cues in heavy drinkers.