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Original Investigation |

Association of Marijuana Use With Blunted Nucleus Accumbens Response to Reward Anticipation

Meghan E. Martz, MS1,2; Elisa M. Trucco, PhD1,3; Lora M. Cope, PhD1; Jillian E. Hardee, PhD1; Jennifer M. Jester, PhD1; Robert A. Zucker, PhD1,2; Mary M. Heitzeg, PhD1
[+] Author Affiliations
1Addiction Research Center, Department of Psychiatry, University of Michigan, Ann Arbor
2Department of Psychology, University of Michigan, Ann Arbor
3Center for Children and Families, Department of Psychology, Florida International University, Miami
JAMA Psychiatry. 2016;73(8):838-844. doi:10.1001/jamapsychiatry.2016.1161.
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Importance  Marijuana use may alter ventral striatal response to reward, which might heighten susceptibility to substance use disorder. Longitudinal research is needed to determine the effects of marijuana use on neural function involved in reward response.

Objective  To determine whether marijuana use among young adults prospectively affects nucleus accumbens (NAcc) activation during reward anticipation.

Design, Setting, and Participants  One hundred eight young adults were recruited from the Michigan Longitudinal Study, an ongoing study of youth at high risk for substance use disorder and a contrast sample of control families. Participants underwent 3 consecutive functional magnetic resonance imaging scans at approximate ages of 20 (time 1), 22 (time 2), and 24 (time 3) years. Self-report data on marijuana and other drug use occasions were collected annually since age 11 years.

Main Outcomes and Measures  Cross-lagged models were used to test the association of marijuana use with neural response in the NAcc to reward anticipation during a monetary incentive delay task controlling for sex, age, other substance use, and family history of substance use disorder.

Results  Of 108 participants, 39 (36.1%) were female and mean (SD) age at baseline was 20.1 (1.4) years. Greater marijuana use was associated with later blunted activation in the NAcc during reward anticipation (time 1 to time 2: β = −0.26, P = .04; time 2 to time 3: β = −0.25, P = .01). When the cross-lagged model was tested with the inclusion of previous and concurrent cigarette use, the effect of marijuana use from time 2 to time 3 remained significant (β = −0.29; P = .005) and the effect of cigarette use was nonsignificant.

Conclusions and Relevance  The findings of this study indicate that marijuana use is associated with decreased neural response in the NAcc during the anticipation of nondrug rewards. Over time, marijuana use may alter anticipatory reward processing in the NAcc, which may increase the risk for continued drug use and later addiction.

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Figure 1.
Longitudinal Cross-lagged Associations Between Marijuana Use and Nucleus Accumbens (NAcc) Activation During Reward Anticipation

Results are shown from cross-lagged analysis of past-year marijuana use at each scan date and NAcc activation during reward anticipation. The coefficients indicated are standardized path coefficients with covariates of sex, age at time 1, parental history of substance use disorder, previous marijuana use and binge drinking up to 12 months before time 1, and past-year binge drinking corresponding to each time (covariances of exogenous variables are not depicted). Straight arrows represent causal paths; curved arrows, covariances. Indices of model fit are χ2 = 8.94; P = .35; root mean square error of approximation, 0.03; comparative fit index, 0.99; and Tucker-Lewis Index, 0.97.

aP < .001.

bP < .05.

cP < .01.

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Figure 2.
Prospective Associations Between Marijuana Use and Nucleus Accumbens (NAcc) Activation During Reward Anticipation

A, Past-year marijuana use at age 20 years (time 1) and NAcc activation during reward anticipation at 22 years (time 2). B, Past-year marijuana use at 22 years (time 2) and NAcc activation during reward anticipation at 24 years (time 3). Both partial regression plots controlled for all covariates included in cross-lagged analyses. Circles indicate data points for each participant; horizontal line, coefficient line.

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