Adolescent-onset regular cannabis use is associated with altered neural and behavioural responses during anticipation and feedback of monetary reward and loss

Abstract Rationale Regular cannabis use has been associated with alterations in reward-related neural processes, yet findings remain inconsistent and the relationship between neural activity and behavioural performance is not fully understood. Objectives The present study aimed to characterise neural and behavioural correlates of reward processing in regular cannabis users (CU) compared with matched non-users (NU) using the Monetary Incentive Delay Task (MIDT). Methods Twenty adolescent-onset regular cannabis users (CU; ≥4 days/week for 2 years, with regular use initiated before age 18) and twenty age- and sex-matched non-users (NU) completed the Monetary Incentive Delay Task during functional MRI. Firstly, we assessed behavioural performance through reaction times, accuracy and monetary earnings to determine whether potential neural alterations were reflected in task performance. Secondly, focusing on reward-related brain regions, we examined group differences in BOLD functional MRI activity during anticipation and outcome phases separately for monetary win and loss conditions. Finally, we explored the association between behavioural performance and neural activation. Results Our findings provide preliminary evidence that adolescent-onset regular cannabis use is associated with altered engagement of key nodes within the mesocorticolimbic circuit accompanied by impaired behavioural performance. Particularly, compared with NU, CU showed (I) lower striatal activity during anticipation of monetary win and higher ventral striatum and frontal pole activity during anticipation of monetary loss; (II) different VTA BOLD contrast estimates during outcome of successful monetary win and loss avoidance, and lower frontal pole activity during outcome of unsuccessful loss avoidance; (III) lower monetary rewards and a trend towards slower reaction times and reduced accuracy; (IV) disrupted brain-behaviour coupling. Conclusions Results from this study may help inform future research on the neurobiological mechanisms underlying changes in reward function and the resultant behavioural consequences of adolescent-onset cannabis use.