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Official websites use. Share sensitive information only on official, secure websites. Address correspondence to Mary M. Heitzeg, Ph. Marijuana use may alter ventral striatal response to reward, which may heighten susceptibility to substance use disorder SUD. Cross-sectional studies have reported either increased ventral striatal response to reward or no difference in marijuana users compared with controls. Longitudinal research is needed to resolve the inconsistencies and disentangle preexisting susceptibility from the effects of marijuana use on neural function involved in reward responding. To determine whether marijuana use among young adults prospectively impacts nucleus accumbens NAcc activation during reward anticipation. Longitudinal study of self-report marijuana use and brain function using functional magnetic resonance imaging fMRI at three consecutive time points. Data were obtained from young adult participants in the Michigan Longitudinal Study, an ongoing, prospective study of youth at high risk for SUD and a contrast sample of control families. We investigated the impact of marijuana use on neural response in the NAcc to reward anticipation during a monetary incentive delay task MIDT using a cross-lagged model. Covariates for analyses included sex, age at first scan, family history of SUD, prior marijuana use, and binge drinking prior and concurrent. This model was also tested separately with the inclusion of cigarette smoking. When we tested the cross-lagged model with the inclusion of prior and concurrent cigarette use, the impact of marijuana use from time 2 to time 3 remained significant and the effect of cigarette use was non-significant. Our findings indicate that marijuana use is associated with decreased neural response in the NAcc during the anticipation of non-drug rewards. Over time, marijuana use may alter anticipatory reward processing in the NAcc, which may increase risk for continued drug use and later addiction. Marijuana is the most commonly used illicit substance in the United States, with use especially prevalent among young adults 1. This pervasiveness may be due to low perceptions of harm 2 , despite the short- and long-term negative consequences 3 of marijuana. Short-term consequences may include acute anxiety, paranoia, and altered perception 4 , as well as impaired motor coordination while driving 5. Deficits in academic achievement 6 and disrupted brain structure and function 7 — 10 suggest long-term negative consequences of marijuana use. Of particular relevance to this study is evidence that earlier marijuana use onset leads to a faster transition to marijuana dependence 11 and increases risk of developing other substance use disorders SUDs THC binds to CB1 cannabinoid neural receptors and stimulates the transmission of dopamine from the ventral tegmental area VTA to the nucleus accumbens NAcc in the ventral striatum VS , a region involved in reward-driven behavior, including substance use 13 — A recent positron emission tomography PET study demonstrated reduced reactivity of this system in chronic marijuana users during extracellular dopamine stimulation, which was correlated with greater addiction severity and craving This is consistent with theories positing that with chronic use, the incentive salience of cues that predict receipt of the drug strengthens, likely at the expense of rewards not associated with that drug—an effect believed to contribute to the development and maintenance of problematic substance use 17 — Thus, marijuana use may cause a perturbation of the dopaminergic reward system, thereby increasing risk for developing marijuana and other SUDs. A number of cross-sectional studies have investigated the impact of marijuana use on non-drug reward responding during functional magnetic resonance imaging fMRI using the monetary incentive delay task MIDT 20 — Some studies report that marijuana users show increased activation of the VS to monetary reward anticipation compared to non-users 23 , 24 , whereas others have found no differences 25 — Cross-sectional studies, however, may be unable to disentangle differences in activation due to preexisting neural susceptibilities compared to altered neural function as a result of marijuana use. Increased NAcc activation to reward anticipation has been linked to behavioral traits associated with substance use risk 22 , 28 — 30 and prospectively associated with later substance use problems Thus, longitudinal studies that account for preexisting susceptibilities are needed to more clearly identify the cumulative impact of marijuana use on neural mechanisms underlying reward responsivity. To address this gap, the present study examined cross-lagged, prospective associations between marijuana use and NAcc activation to monetary reward anticipation. Consistent with prior evidence supporting attenuated dopamine release in the VS among heavy marijuana users 16 and reduced incentive salience for non-drug rewards 17 , 18 in chronic substance users, we hypothesized that greater marijuana use would be associated with later decreases in NAcc activation to monetary reward anticipation, beyond possible cofounding influences. Participants were young adults recruited from the Michigan Longitudinal Study, an ongoing, prospective study of youth from families with high levels of SUD and a contrast sample of families without SUD Exclusionary criteria are in eMethods of the Supplement. No minimum levels of marijuana use were required for inclusion in the present study. All eligible participants were assessed for psychosocial functioning at 3-year intervals and substance use and problems beginning annually at age Additional details on MLS assessment and data collection protocol are provided elsewhere 31 , Participants completed three consecutive scans at approximately 2-year intervals. The present study was reviewed and approved by the University of Michigan Medical School Institutional Review Board, and all participants provided written informed consent. Prior use was measured by use days from age 11 through the year prior to time 1. Substance use was assessed annually using the Drinking and Drug History questionnaire Past year marijuana use was measured by the number of days during the past year that participants reported using marijuana or hashish. Past year cigarette use was measured by the number of days participants reported smoking cigarettes during the past year. For each substance, 'prior' use was the number of days of use from age 11 through the year prior to time 1. Substance use means and percentages are shown in Table 1. To assess neural response during anticipation of monetary reward, participants performed a modified version of the MIDT 20 — A fixation cross then appeared anticipation , followed by a variable-duration target. Pressing the button while the target was on the screen signified a correct response. After each trial, participants were shown feedback indicating whether they pressed the button quickly enough outcome. Additional details are provided in eMethods of the Supplement. Whole-brain blood oxygen level-dependent BOLD images were acquired on a 3. Image processing and individual-level analyses are described in eMethods of the Supplement. The present report focuses on the contrast between anticipation during monetary gain trials and neutral trials i. Contrasts for small and large gains were estimated separately. Contrasts for small and large gains were then linearly combined and averaged across hemispheres. Associations between incentive amount and hemisphere in NAcc volume are described in eMethods of the Supplement. We previously reported acceptable reliability of NAcc activation across sessions To examine longitudinal associations between marijuana use and NAcc activation during monetary reward anticipation, cross-lagged analyses were conducted using robust maximum likelihood estimation in Mplus version 7. Cross-lagged analyses included across-time stability coefficients for marijuana use and NAcc activation, within-time associations between marijuana use and NAcc activation, and across-time cross-lagged paths between marijuana use and NAcc activation. Covariates were sex, age at time 1, parental history of SUD, prior marijuana use and binge drinking, and past year binge drinking. Age at time 1 was included to control for the range in ages 18—24 years old at the initial scan. Parental history of SUD was included to control for heightened substance use risk Due to evidence suggesting an impact of onset and duration of marijuana use on brain structure and function 3 , 7 , we accounted for prior marijuana use. We also accounted for prior and past year binge drinking, given the high comorbidity between marijuana and alcohol use 40 — Because marijuana use is also comorbid with cigarette smoking 41 and some studies suggest that nicotine use may reduce the impact of THC on NAcc response to non-drug reward anticipation 43 , 44 , we tested an additional analytic model that included prior and past year cigarette use as covariates. The following parameters determined adequate model fit: non-significant chi-square, a root mean square error of approximation RMSEA below 0. To allow comparison with prior cross-sectional studies 23 — 25 , 27 , we also investigated associations between Time 1 NAcc activation and prior marijuana use and age at first use using partial correlations, controlling for prior binge drinking and cigarette use. Reaction times and accuracy data are provided in eResults and eTable 1 of the Supplement. Partial correlations were conducted to test associations between marijuana use and task performance, controlling for sex, age at time 1, parental history of SUD, prior marijuana use and binge drinking, and co-occurring past year binge drinking. Participants showed robust VS activation at each time during reward anticipation eFigure 2. The cross-lagged model showed excellent model fit and significant cross-lagged paths between marijuana use and blunted NAcc activation during monetary reward anticipation Figure 1. Past year marijuana use at time 1 negatively predicted NAcc activation at time 2, with no covariates reaching significance. A graphical representation of cross-lagged results is shown in Figure 2. Testing positive for marijuana use but reporting abstinence within 48 hours prior to each scan did not greatly impact findings eResults. Results are shown from cross-lagged analysis of past year marijuana use at each scan date and NAcc activation during reward anticipation. Coefficients are standardized path coefficients, with covariates of sex, age at time 1, parental history of substance use disorder, prior marijuana use and binge drinking up to 12 months prior to time 1, and past year binge drinking corresponding to each time covariances of exogenous variables are not depicted to improve readability. Straight single-headed arrows represent causal paths; Curved double-headed arrows represent covariances. Partial regression plots for A. Both partial regression plots control for all covariates included in cross-lagged analyses. Pearson correlations were examined between marijuana use and other substances of interest included in cross-lagged analyses eTable 3. The present study is the first to report longitudinal associations between marijuana use and NAcc activation during a non-drug reward anticipation task. We found a significant, prospective relationship between marijuana use and decreased NAcc activation to monetary reward anticipation. Our findings indicate that continued marijuana use may result in a blunted NAcc response to non-drug rewards, even when controlling for prior and co-occuring substance use. Importantly, the model also controlled for potential risk factors, such as familial risk for SUD and baseline differences in NAcc activation. This work provides robust evidence that marijuana use has long-term associations with anticipatory reward processing. While existing studies have shown increased NAcc activation to monetary reward anticipation among marijuana users 23 , 24 or no significant differences from controls 25 — 27 , we found decreased NAcc activation over time. Prior cross-sectional studies may not have been able to account for preexisting differences in NAcc activation that predisposed certain individuals toward engaging in reward seeking behavior, such as substance use. At time 1, we found a trend for an association between greater NAcc activation and earlier age of use onset, but no association with amount of use, supporting the view that heightened reward system activation represents a risk factor for use rather than a consequence. Using prospective, cross-lagged analyses, we isolated the relation between marijuana use and later NAcc function more directly, while accounting for baseline NAcc activation at time 1. Findings indicate that continued marijuana use impacts anticipatory reward processing, while preexisting differences in NAcc function were not associated with later marijuana use. Given that the baseline measurement in this study was conducted in young adulthood, future prospective studies at earlier ages may more clearly detect preexisting striatal risk related to continued marijuana use on reward responsivity. Finding a prospective relationship between marijuana use and decreased NAcc activation to monetary reward supports a mechanism through which marijuana use may lead to enhanced vulnerability to SUD. Although early substance use involves voluntary decisions to use, our findings support the view that repeated consumption produces long-term alterations in neural circuits involved in reward processing, which may in turn contribute to drug seeking behavior and compulsive use One possibility is that effects of chronic marijuana use on these neural systems results in a general blunting of reward responding. This may lead to further drug use in an attempt to counteract insufficient reward responsivity, consistent with the reward deficiency theory of addiction We did not observe an association between NAcc response to monetary reward and later marijuana use. While a direct, robust association may not exist between these factors, repeated marijuana use may result in a bias toward marijuana and marijuana-associated cues relative to non-marijuana cues. Repeated stimulation of mesolimbic neural circuits during marijuana use may sensitize this circuitry to attribute greater salience to stimuli paired with marijuana use This bias toward marijuana cues may contribute to repeated marijuana use and an increased risk for addiction. To test this theory, it will be necessary for future studies to prospectively examine neural response to both marijuana-associated and non-drug reward cues over time. An additional possibility is that blunted reward system responding in marijuana users is associated with general anhedonia, which may maintain substance use. This may be a more marijuana-specific association, given that endogenous cannabinoids have been shown to be involved in regulating emotional responses 48 , and animal work has demonstrated a link between exposure to exogenous cannabinoids and depressive phenotypes 49 , Marijuana may be used to cope with dysregulated mood, and continued marijuana use may alter neural systems involved in mood and emotion e. Attenuated striatal reactivity to dopamine stimulation in marijuana abusers has been shown to correlate with negative emotionality 16 , which is also supported by our prior work demonstrating a prospective relationship between marijuana use and greater negative emotionality Given the high incidence of polysubstance use 41 and that all drugs of abuse impact dopamine levels in the NAcc 13 — 15 , we accounted for potentially confounding substance use. For example, there is evidence that heavy alcohol use may blunt NAcc activation to reward anticipation 52 , We found an impact of chronic marijuana use on anticipatory reward processing when controlling for potential effects of prior and co-occuring binge drinking. Thus, marijuana use may have a specific influence on NAcc response above and beyond that of heavy alcohol use. Interestingly, cumulative marijuana use and binge drinking prior to time 1 had a significant impact on NAcc activation at time 3 but not at time 2. This was likely due to the more proximal influence of marijuana use at time 1 accounting for a large degree of the variance of time 2 NAcc activation, resulting in less unexplained variance to be accounted for by prior marijuana use and binge drinking. In contrast, there may have been more unexplained variance to be accounted for by prior marijuana use and binge drinking at time 2 given the weaker correlation see eTable 3. Due to prior work showing blunted NAcc during monetary reward anticipation among marijuana users who also use cigarettes 43 , 44 , we tested a cross-lagged model that included cigarette use. The association between marijuana use at Time 1 and later NAcc activation was reduced to trend-level, whereas the association between marijuana use at Time 2 and later NAcc activation remained significant. However, no significant effects of prior or co-occuring cigarette use on NAcc activation were observed at any time point. Our findings suggest that reduced NAcc activation was not being driven by nicotine effects on endocannabinoid modulation of the NAcc More specific cross-lagged, group comparisons between marijuana, cigarette, and combined marijuana and cigarette users may further disentangle the relation between marijuana and nicotine on anticipatory reward processing. Our findings may also have limited generalizability to other groups, given that our sample consisted predominately of White and high-risk defined by family history of SUD youth. Yet, in many ways this was an appropriate sample, given that both White youth 2 and youth with a family history of SUD 39 tend to show high levels of substance use. Finally, early versus late marijuana use onset could be an important moderator, but we did not have an adequate number of early onset marijuana users to test for such differences. Future studies with larger sample sizes should examine whether these associations differ across age of marijuana use onset. The present study provides evidence for the longitudinal impact of marijuana use on NAcc functioning during monetary reward anticipation. In light of the rise in marijuana use rates coupled with decreasing perceptions of harm 2 , this study provides important and novel information pertaining to the long-term influence of marijuana use on brain mechanisms underlying addiction. Educating youth about the impact of marijuana on this neural circuitry and its potential downstream consequences on addiction vulnerability may help improve efforts to prevent the initiation and escalation of marijuana use. Such efforts may dispel the notion that marijuana use produces no lasting neural influences and may elucidate the potential harms associated with this substance. Heitzeg and R. Zucker; T32 DA to P. Gnegy; T32 DA to J. Zucker and M. Heitzeg; R01 AA to R. Heitzeg; T32AA to F. Blow; K08 AA to E. Author Contributions: Dr. Heitzeg had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis; Study concept and design: Heitzeg, Martz; Acquisition, analysis, or interpretation of data : All authors; Drafting of the manuscript: Martz, Heitzeg, Trucco, Cope, Hardee; Critical revision of the manuscript for important intellectual content: All authors; Statistical analysis: Martz, Trucco; Obtained funding: Zucker, Heitzeg; Administrative, technical, or material support: All authors; Study supervision: Heitzeg. Conflict of Interest Disclosures: All authors are free of any actual or potential conflict of interest including any financial, personal, or other relationships with other people or organizations within three years of beginning the submitted work that would inappropriately influence, or be perceived to influence, their worWord Count: 2, Revision Date: April 15, This section collects any data citations, data availability statements, or supplementary materials included in this article. As a library, NLM provides access to scientific literature. JAMA Psychiatry. Find articles by Meghan E Martz. Find articles by Elisa M Trucco. Find articles by Lora M Cope. Find articles by Jillian E Hardee. Find articles by Jennifer M Jester. Find articles by Robert A Zucker. Find articles by Mary M Heitzeg. PMC Copyright notice. N White a Open in a new tab. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel. Family History SUD b. Mean prior marijuana use days c. Mean prior binge drinking days c. Mean prior cigarette use days c.

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