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Neural responses to reward anticipation and feedback in adult and adolescent cannabis users and controls

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Martine Skumlien, Claire Mokrysz, Tom P Freeman, Matthew B Wall, Michael Bloomfield, Rachel Lees, Anna Borissova, Kat Petrilli, James Carson, Tiernan Coughlan, Shelan Ofori, Christelle Langley, Barbara J Sahakian, H Valerie Curran, Will Lawn

Original languageEnglish
Pages (from-to)1976-1983
Number of pages8
JournalNeuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
Volume47
Issue number11
DOIs
Published31 Oct 2022

Bibliographical note

Funding Information: This study was funded by a grant from the Medical Research Council, MR/P012728/1, to HVC and TPF. MS is funded by an Aker Scholarship from the Aker Foundation. AB was funded by a fellowship from the National Institute for Health Research (NIHR) UCLH Biomedical Research Centre. BJS receives funding from the Wallitt Foundation, Eton College, and a Wellcome Trust Collaborative Award 200181/Z//15/Z, CL is funded by a Wellcome Trust Collaborative Award 200181/Z//15/Z, and their research is conducted within the NIHR Cambridge Biomedical Research Centre (Mental Health Theme and Neurodegeneration Theme) and the NIHR Brain Injury MedTech and in vitro diagnostics Co-operative (MIC), Cambridge. HVC is supported by grants from the UK MRC (MR/P012728/1) UK Department of Health, and by the NIHR UCLH Biomedical Research Centre. Publisher Copyright: © 2022, The Author(s).

King's Authors

Abstract

Chronic use of drugs may alter the brain's reward system, though the extant literature concerning long-term cannabis use and neural correlates of reward processing has shown mixed results. Adolescents may be more vulnerable to the adverse effects of cannabis than adults; however, this has not been investigated for reward processing. As part of the 'CannTeen' study, in the largest functional magnetic resonance imaging study of reward processing and cannabis use to date, we investigated reward anticipation and feedback in 125 adult (26-29 years) and adolescent (16-17 years) cannabis users (1-7 days/week cannabis use) and gender- and age-matched controls, using the Monetary Incentive Delay task. Blood-oxygen-level-dependent responses were examined using region of interest (ROI) analyses in the bilateral ventral striatum for reward anticipation and right ventral striatum and left ventromedial prefrontal cortex for feedback, and exploratory whole-brain analyses. Results showed no User-Group or User-Group × Age-Group effects during reward anticipation or feedback in pre-defined ROIs. These null findings were supported by post hoc Bayesian analyses. However, in the whole-brain analysis, cannabis users had greater feedback activity in the prefrontal and inferior parietal cortex compared to controls. In conclusion, cannabis users and controls had similar neural responses during reward anticipation and in hypothesised reward-related regions during reward feedback. The whole-brain analysis revealed tentative evidence of greater fronto-parietal activity in cannabis users during feedback. Adolescents showed no increased vulnerability compared with adults. Overall, reward anticipation and feedback processing appear spared in adolescent and adult cannabis users, but future longitudinal studies are needed to corroborate this.

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