The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents

Martine Skumlien; Tom P. Freeman; Daniel Hall; Claire Mokrysz; Matthew B. Wall; Shelan Ofori; Kat Petrilli; Katie Trinci; Anna Borissova; Natalia Fernandez-Vinson; Christelle Langley; Barbara J. Sahakian; H. Valerie Curran; Will Lawn

doi:10.1016/j.bpsc.2022.10.004

The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents

Martine Skumlien^*, Tom P. Freeman, Daniel Hall, Claire Mokrysz, Matthew B. Wall, Shelan Ofori, Kat Petrilli, Katie Trinci, Anna Borissova, Natalia Fernandez-Vinson, Christelle Langley, Barbara J. Sahakian, H. Valerie Curran, Will Lawn

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

Abstract

Background: Adolescents may respond differently to cannabis than adults, yet no previous functional magnetic resonance imaging study has examined acute cannabis effects in this age group. In this study, we investigated the neural correlates of reward anticipation after acute exposure to cannabis in adolescents and adults. Methods: This was a double-blind, placebo-controlled, randomized, crossover experiment. Forty-seven adolescents (n = 24, 12 females, ages 16–17 years) and adults (n = 23, 11 females, ages 26–29 years) matched on cannabis use frequency (0.5–3 days/week) completed the Monetary Incentive Delay task during functional magnetic resonance imaging after inhaling cannabis with 0.107 mg/kg Δ⁹-tetrahydrocannabinol (“THC”) (8 mg THC for a 75-kg person) or with THC plus 0.320 mg/kg cannabidiol (“THC+CBD”) (24 mg CBD for a 75-kg person), or placebo cannabis. We investigated reward anticipation activity with whole-brain analyses and region of interest analyses in the right and left ventral striatum, right and left anterior cingulate cortex, and right insula. Results: THC reduced anticipation activity compared with placebo in the right (p = .005, d = 0.49) and left (p = .003, d = 0.50) ventral striatum and the right insula (p = .01, d = 0.42). THC+CBD reduced activity compared with placebo in the right ventral striatum (p = .01, d = 0.41) and right insula (p = .002, d = 0.49). There were no differences between “THC” and “THC+CBD” conditions and no significant drug by age group interaction effect, supported by Bayesian analyses. There were no significant effects in the whole-brain analyses. Conclusions: In weekly cannabis users, cannabis suppresses the brain's anticipatory reward response to money, and CBD does not modulate this effect. Furthermore, the adolescent reward circuitry is not differentially sensitive to acute effects of cannabis on reward anticipation.

Original language	English
Pages (from-to)	219-229
Number of pages	11
Journal	Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume	8
Issue number	2
DOIs	https://doi.org/10.1016/j.bpsc.2022.10.004
Publication status	Published - Feb 2023

Keywords

Adolescents
Cannabis
CBD
fMRI
Reward
THC

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10.1016/j.bpsc.2022.10.004

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Skumlien, M., Freeman, T. P., Hall, D., Mokrysz, C., Wall, M. B., Ofori, S., Petrilli, K., Trinci, K., Borissova, A., Fernandez-Vinson, N., Langley, C., Sahakian, B. J., Curran, H. V., & Lawn, W. (2023). The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 8(2), 219-229. https://doi.org/10.1016/j.bpsc.2022.10.004

@article{aa9317b248de4967b796efd8b1945c47,

title = "The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents",

abstract = "Background: Adolescents may respond differently to cannabis than adults, yet no previous functional magnetic resonance imaging study has examined acute cannabis effects in this age group. In this study, we investigated the neural correlates of reward anticipation after acute exposure to cannabis in adolescents and adults. Methods: This was a double-blind, placebo-controlled, randomized, crossover experiment. Forty-seven adolescents (n = 24, 12 females, ages 16–17 years) and adults (n = 23, 11 females, ages 26–29 years) matched on cannabis use frequency (0.5–3 days/week) completed the Monetary Incentive Delay task during functional magnetic resonance imaging after inhaling cannabis with 0.107 mg/kg Δ⁹-tetrahydrocannabinol (“THC”) (8 mg THC for a 75-kg person) or with THC plus 0.320 mg/kg cannabidiol (“THC+CBD”) (24 mg CBD for a 75-kg person), or placebo cannabis. We investigated reward anticipation activity with whole-brain analyses and region of interest analyses in the right and left ventral striatum, right and left anterior cingulate cortex, and right insula. Results: THC reduced anticipation activity compared with placebo in the right (p = .005, d = 0.49) and left (p = .003, d = 0.50) ventral striatum and the right insula (p = .01, d = 0.42). THC+CBD reduced activity compared with placebo in the right ventral striatum (p = .01, d = 0.41) and right insula (p = .002, d = 0.49). There were no differences between “THC” and “THC+CBD” conditions and no significant drug by age group interaction effect, supported by Bayesian analyses. There were no significant effects in the whole-brain analyses. Conclusions: In weekly cannabis users, cannabis suppresses the brain's anticipatory reward response to money, and CBD does not modulate this effect. Furthermore, the adolescent reward circuitry is not differentially sensitive to acute effects of cannabis on reward anticipation.",

keywords = "Adolescents, Cannabis, CBD, fMRI, Reward, THC",

author = "Martine Skumlien and Freeman, {Tom P.} and Daniel Hall and Claire Mokrysz and Wall, {Matthew B.} and Shelan Ofori and Kat Petrilli and Katie Trinci and Anna Borissova and Natalia Fernandez-Vinson and Christelle Langley and Sahakian, {Barbara J.} and Curran, {H. Valerie} and Will Lawn",

note = "Publisher Copyright: {\textcopyright} 2022 Society of Biological Psychiatry",

year = "2023",

month = feb,

doi = "10.1016/j.bpsc.2022.10.004",

language = "English",

volume = "8",

pages = "219--229",

journal = "Biological Psychiatry: Cognitive Neuroscience and Neuroimaging",

issn = "2451-9022",

publisher = "Elsevier Inc.",

number = "2",

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Skumlien, M , Freeman, TP, Hall, D, Mokrysz, C, Wall, MB, Ofori, S, Petrilli, K, Trinci, K, Borissova, A, Fernandez-Vinson, N, Langley, C, Sahakian, BJ, Curran, HV & Lawn, W 2023, 'The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents', Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, vol. 8, no. 2, pp. 219-229. https://doi.org/10.1016/j.bpsc.2022.10.004

TY - JOUR

T1 - The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents

AU - Skumlien, Martine

AU - Freeman, Tom P.

AU - Hall, Daniel

AU - Mokrysz, Claire

AU - Wall, Matthew B.

AU - Ofori, Shelan

AU - Petrilli, Kat

AU - Trinci, Katie

AU - Borissova, Anna

AU - Fernandez-Vinson, Natalia

AU - Langley, Christelle

AU - Sahakian, Barbara J.

AU - Curran, H. Valerie

AU - Lawn, Will

PY - 2023/2

Y1 - 2023/2

N2 - Background: Adolescents may respond differently to cannabis than adults, yet no previous functional magnetic resonance imaging study has examined acute cannabis effects in this age group. In this study, we investigated the neural correlates of reward anticipation after acute exposure to cannabis in adolescents and adults. Methods: This was a double-blind, placebo-controlled, randomized, crossover experiment. Forty-seven adolescents (n = 24, 12 females, ages 16–17 years) and adults (n = 23, 11 females, ages 26–29 years) matched on cannabis use frequency (0.5–3 days/week) completed the Monetary Incentive Delay task during functional magnetic resonance imaging after inhaling cannabis with 0.107 mg/kg Δ⁹-tetrahydrocannabinol (“THC”) (8 mg THC for a 75-kg person) or with THC plus 0.320 mg/kg cannabidiol (“THC+CBD”) (24 mg CBD for a 75-kg person), or placebo cannabis. We investigated reward anticipation activity with whole-brain analyses and region of interest analyses in the right and left ventral striatum, right and left anterior cingulate cortex, and right insula. Results: THC reduced anticipation activity compared with placebo in the right (p = .005, d = 0.49) and left (p = .003, d = 0.50) ventral striatum and the right insula (p = .01, d = 0.42). THC+CBD reduced activity compared with placebo in the right ventral striatum (p = .01, d = 0.41) and right insula (p = .002, d = 0.49). There were no differences between “THC” and “THC+CBD” conditions and no significant drug by age group interaction effect, supported by Bayesian analyses. There were no significant effects in the whole-brain analyses. Conclusions: In weekly cannabis users, cannabis suppresses the brain's anticipatory reward response to money, and CBD does not modulate this effect. Furthermore, the adolescent reward circuitry is not differentially sensitive to acute effects of cannabis on reward anticipation.

AB - Background: Adolescents may respond differently to cannabis than adults, yet no previous functional magnetic resonance imaging study has examined acute cannabis effects in this age group. In this study, we investigated the neural correlates of reward anticipation after acute exposure to cannabis in adolescents and adults. Methods: This was a double-blind, placebo-controlled, randomized, crossover experiment. Forty-seven adolescents (n = 24, 12 females, ages 16–17 years) and adults (n = 23, 11 females, ages 26–29 years) matched on cannabis use frequency (0.5–3 days/week) completed the Monetary Incentive Delay task during functional magnetic resonance imaging after inhaling cannabis with 0.107 mg/kg Δ⁹-tetrahydrocannabinol (“THC”) (8 mg THC for a 75-kg person) or with THC plus 0.320 mg/kg cannabidiol (“THC+CBD”) (24 mg CBD for a 75-kg person), or placebo cannabis. We investigated reward anticipation activity with whole-brain analyses and region of interest analyses in the right and left ventral striatum, right and left anterior cingulate cortex, and right insula. Results: THC reduced anticipation activity compared with placebo in the right (p = .005, d = 0.49) and left (p = .003, d = 0.50) ventral striatum and the right insula (p = .01, d = 0.42). THC+CBD reduced activity compared with placebo in the right ventral striatum (p = .01, d = 0.41) and right insula (p = .002, d = 0.49). There were no differences between “THC” and “THC+CBD” conditions and no significant drug by age group interaction effect, supported by Bayesian analyses. There were no significant effects in the whole-brain analyses. Conclusions: In weekly cannabis users, cannabis suppresses the brain's anticipatory reward response to money, and CBD does not modulate this effect. Furthermore, the adolescent reward circuitry is not differentially sensitive to acute effects of cannabis on reward anticipation.

KW - Adolescents

KW - Cannabis

KW - CBD

KW - fMRI

KW - Reward

KW - THC

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U2 - 10.1016/j.bpsc.2022.10.004

DO - 10.1016/j.bpsc.2022.10.004

M3 - Article

C2 - 36642667

AN - SCOPUS:85146453151

SN - 2451-9022

VL - 8

SP - 219

EP - 229

JO - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

JF - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

IS - 2

ER -

The Effects of Acute Cannabis With and Without Cannabidiol on Neural Reward Anticipation in Adults and Adolescents

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