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. Author manuscript; available in PMC: 2020 Oct 15.
Published in final edited form as: Birth Defects Res. 2019 Aug 5;111(17):1302–1307. doi: 10.1002/bdr2.1572

Cannabis and the Developing Brain: What Does the Evidence Say?

Joanna Jacobus 1, Kelly E Courtney 1, Elizabeth A Hodgdon 1, Rachel Baca 1
PMCID: PMC7239321  NIHMSID: NIHMS1588981  PMID: 31385460

Abstract

Cannabis use during adolescence has been linked to deleterious effects on brain integrity. This article summarizes findings from two prospective investigations (3 years and 6-years, on average) on adolescent cannabis use from our laboratory that utilize structural neuroimaging and neurocognitive assessment approaches. Across most studies, findings suggest recency, frequency, and age of onset of cannabis use are likely key variables in predicting poorer neural health outcomes. There is some evidence that pre-existing differences in brain architecture may also contribute to vulnerability and outcome differences. Ongoing large-scale prospective studies of youth will be able to disentangle how both cannabis use as well as pre- and post-exposure differences play a role in divergent outcomes among youth who use cannabis.

Background.

Adolescent brain development is dynamic, with changes in gray and white matter tissue and structural integration occurring well into young adulthood (Gonzalez, Pacheco-Colon, Duperrouzel, & Hawes, 2017; Stiles & Jernigan, 2010). There is a growing need to better understand how cannabis use impacts brain integrity throughout neurodevelopment, particularly as legalization of cannabis use increases throughout the United States and perception of cannabis-related harm declines among youth (Johnston et al., 2019; Lubman, Cheetham, & Yucel, 2015; Volkow et al., 2016). A clearer understanding of the neurobiological, environmental, and cannabis-related risk factors that contribute to health-related outcomes among adolescent cannabis users will help inform public health policy on cannabis as it pertains to youth.

Few prospective studies have followed adolescent cannabis users and assessed them at multiple independent time points, and/or assessed adolescents pre- and post-cannabis initiation (Gonzalez et al., 2017). Evidence that cannabis use may have deleterious effects on neurodevelopment and result in poorer neural health outcomes is mixed (Meier et al., 2012; Meier et al., 2017), particularly for neurocognitive outcomes (Jackson et al., 2016). For example, studies find heavier use patterns associated with poorer performance on tests of attention, learning and memory, and executive functioning (Gonzalez et al., 2017). However the relationship between cannabis and neural outcomes is often quite attenuated after accounting for recency effects and confounding sociodemographic factors (Scott et al., 2018). Systematic reviews suggest restored functioning with abstinence, poorer outcomes for those with more severe use histories, and shared risk factors (e.g., mental health, psychosocial factors) associated with cannabis initiation and brain-behavior based outcomes (Gonzalez et al., 2017; Scott et al., 2018).

Similarly, neuroimaging studies find structural and functional differences between adolescents reporting a history of cannabis use and those with minimal to no use histories, including differences in microstructural and macrostructural neural tissue indices (Baker, Yucel, Fornito, Allen, & Lubman, 2013; Orr et al., 2019), blood-oxygen level dependent signal responses and neural network integration (Lichenstein, Musselman, Shaw, Sitnick, & Forbes, 2017; Yanes et al., 2018), cerebral blood flow (Filbey, Aslan, Lu, & Peng, 2018; Jacobus et al., 2012), as well as behavioral and emotional functioning (Griffith-Lendering, Huijbregts, Mooijaart, Vollebergh, & Swaab, 2011; Moitra, Anderson, & Stein, 2016). Nevertheless, some studies find no association between cannabis use and brain integrity (Thayer et al., 2017; Weiland et al., 2015). There is strong research to suggest early brain-based vulnerabilities contribute to substance use initiation (Loeber et al., 2018; Spechler et al., 2018), leaving some individuals even more vulnerable to cannabis-related effects than others. Cannabis-related risk is likely moderated by many neural and environmental factors.

To date, our laboratory has conducted a series of prospective investigations that find evidence for both pre-existing brain differences as well as cannabis-related deleterious effects on neurostructural and neurocognitive development in youth. All participants (spanning ages 12–26) in the studies discussed below were recruited from San Diego area schools and screened for exclusion criteria that included major medical and/or mental health problems (e.g., Axis I DSM-IV diagnosis excluding substance use disorders).

Findings from two independent study designs are presented and include: (1) a three year investigation that identified cannabis users at baseline enrollment (>200 lifetime cannabis use episodes at baseline, on average) and demographically matched (e.g., age, socioeconomic status) non-cannabis using controls (< 10 lifetime cannabis use episodes at baseline, on average) and followed them every 18-months for 3 years (ages 17 at enrollment and 20 by last follow-up, on average; N=175 in cohort); and (2) a six-year investigation (on average) of youth at risk of substance initiation at baseline (pre-initiation, average age 13 at enrollment) and followed for 6–14 years (N=296 in cohort). Minimal illicit drug use and tobacco use was reported in both samples, however groups differed on lifetime alcohol use and therefore alcohol use was included as a covariate and/or subgroup analysis as appropriate. Comprehensive neurocognitive, neuroimaging, and substance use assessment was administered at all in-person visits for both studies. The following brief overview of our prospective work over the past decade focuses on associations between cannabis use, neurocognition, and structural brain integrity.

3-Year Investigation.

Two cross-sectional studies of the first time point in this investigation found group differences between adolescent cannabis users and matched non-cannabis using controls (average age 17) in neurocognition and white matter fiber integrity. Poorer performance on tests of processing speed, attention, memory, and sequencing was observed in the cannabis group (Medina et al., 2007). Greater estimates of white matter fiber integrity were found for controls as compared to cannabis users in widespread bilateral white matter regions that included association and projection fiber tracts (Jacobus et al., 2009). Adolescents from this initial study were prospectively followed and assessed at independent time points 18 and 36-months later (average age 20 by last follow-up) to determine if those remaining cannabis users continued to show evidence of poorer white matter health. We found that controls consistently showed values reflective of better white matter integrity compared to cannabis users who continued to use cannabis over time, and that indices of poorer white matter health were related to poorer global cognitive status by 36-month follow-up (Jacobus, Squeglia, Bava, & Tapert, 2013).

Similarly, we investigated cortical thickness and neuropsychological performance to determine if gray matter refinement (i.e., cortical thinning) was impacted by cannabis use and to identify neurocognitive domains that may be more sensitive to frequent cannabis use. We found adolescents that continued to use cannabis from ages 17 to 20 had thicker cerebral cortices compared to matched controls across both hemispheres, but particularly in frontal and parietal regions. Dose-dependent associations were identified, as more cannabis use was associated with thicker cortices by age 20 (Jacobus, Squeglia, Meruelo, et al., 2015). Neurocognitive domains assessed included attention, learning and memory, processing speed, spatial functioning and executive functioning. Between-group differences between controls and cannabis users were observed across domains, as better cognitive performance was observed by controls over all three years of independent assessment. The largest average effect sizes were observed in attention and memory, as non-cannabis using controls performed substantially better on subtests in this domain over three years as compared to cannabis users (Cohen’s ds > 0.5). We saw positive associations between age of onset and performance on several tasks, particularly processing speed (Jacobus, Squeglia, Infante, et al., 2015), suggesting early age of regular use initiation is likely an important factor in predicting poorer outcomes.

To understand if neural health differences observed in this investigation were cannabis-related vs. pre-existing vulnerabilities, we examined neural tissue integrity and neurocognitive functioning among youth pre- and post-cannabis initiation. In a study conducted by our group in 2013, we observed equal to or greater white matter integrity estimates among cannabis initiators at baseline (pre-initiation, average age 17) compared to those who did not later initiate cannabis use. However, decreasing white matter integrity estimates were observed over time (ages 17–20) in cannabis initiators compared to those who did not initiate cannabis use. The data provide support for a deleterious effect of cannabis on white matter tissue development (Jacobus, Squeglia, Infante, Bava, & Tapert, 2013) independent of possible pre-existing vulnerabilities (see Table 1).

Table 1.

Summary of findings from our laboratory that includes primary results for each study, average age across time points, stage of cannabis initiation across time points, and methods (*= longitudinal analysis).

3-Year Investigation
Author (Year) Average Age Cannabis Initiation Method/Analysis Primary Result
Medina et al. (2007) 17 Post Initiation Comprehensive assessment of 8 neurocognitive domains ↓ Attention and memory performance (cannabis)
Jacobus et al. (2009) 17 Post Initiation Diffusion tensor imaging; Whole brain white matter tissue voxelwise analysis ↓ White matter integrity (cannabis)
Jacobus et al. (2013)* 17–20 Post Initiation Diffusion tensor imaging; Whole brain voxelwise white matter analysis ↓ White matter integrity (cannabis)
Jacobus, Squeglia, Infante et al. (2013)* 17–20 Pre to Post Initiation Diffusion tensor imaging; Whole brain white matter tissue voxelwise analysis ↓ White matter integrity (cannabis)
Jacobus, Sqeuglia, Meruelo et al. (2015)* 17–20 Post Initiation 3T MRI; 34 Cortical regions of interest ↑ Cortical thickness (cannabis)
Jacobus, Squeglia, Infante et al. (2015)* 17–20 Post Initiation Comprehensive assessment of 5 neurocognitive domains ↓ Attention and memory performance; earlier age of onset= ↓ performance (cannabis)
6+ Year Investigation
Author (Year) Average Age Cannabis Initiation Method/Analysis Primary Result
Nguyen-Louie et al. (2015)* 13–17 Pre to Post Initiation Comprehensive assessment of 5 neurocognitive domains ↓ Psychomotor speed
Jacobus et al. (2016)* 13–19 Pre to Post Initiation 3T MRI; 34 Cortical regions of interest ↓ Cortical thinning trajectory (cannabis)
Nguyen-Louie et al. (2017)* 13–20 Pre to Post Initiation Comprehensive assessment of 6 neurocognitive domains ↓ Cognitive inhibition and memory performance
Infante et al. (2018)* 13–19 Pre to Post Initiation 3T MRI; 34 Cortical regions of interest ↓ Cortical surface reduction (cannabis)
Wade et al. (2019)* 13–22 Pre to Post Initiation 3T MRI; Orbitofrontal cortex region of interest ↑ Left lateral orbitofrontal cortex volume prior to cannabis use linked to cannabis use in young adulthood
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6+ Year Investigation.

Several studies conducted from 2016 to 2019 using structural imaging and neurocognitive assessment over a longer follow-up period (6+ years) captured cannabis users prior to initiation (age 13) to better disentangle the contribution of pre-existing differences on neural and behavioral outcomes by young adulthood. Findings suggest a more substantial decrease in cortical thickness (i.e., cortical thinning) and surface area (i.e., gray matter reduction) over time (ages 13–19) for individuals who remained abstinent from cannabis use by young adulthood (Infante, Courtney, Castro, Squeglia, & Jacobus, 2018; Jacobus et al., 2016). Notably, larger left lateral orbitofrontal cortex volume measured from ages 12–15 (prior to cannabis initiation) was linked to greater reward responsiveness and predicted classification as a regular cannabis user by age 22. (Wade et al., 2019). Hence, there is evidence to suggest that pre-existing differences are likely present prior to initiation, but that cannabis use during neuromaturation may also interfere with thinning and gray matter reduction trajectories that contribute to morphological differences by young adulthood (Infante et al., 2018; Jacobus et al., 2016). Nguyen-Louie and colleagues (2015, 2017) found that more recent cannabis use (e.g., past year use) was associated with worse neurocognitive performance during young adulthood after controlling for pre-initiation baseline differences in the sample (see Table 1.) Several associations between neurocognitive test performance and estimates of white and gray matter tissue integrity have been observed, such as increased white matter integrity and more substantial reductions in thickness (i.e., thinning) correlated with better cognitive performance by later follow-up time points (ages 17+) in widespread brain regions (Jacobus et al., 2016). Hence, characterizing early risk-related vulnerabilities and cannabis-related effects on the neural level are important to fully understand potential mechanisms of cannabis-related adverse behavioral outcomes.

Discussion.

In summary of this brief review of our work, the findings represent a scientific basis that suggests the risks of adolescent cannabis use outweigh any potential benefit during typical development. As only few longitudinal studies outside of our laboratory have examined cannabis users pre- and post-initiation (Jackson et al., 2016; Meier et al., 2012; Meier et al., 2017; Mokrysz et al., 2016), our laboratory will continue to study how pre-existing vulnerabilities and cannabis-related brain changes interact and influence healthy outcomes. Currently, we have evidence to suggest recency, frequency, and age of onset of cannabis are likely key variables in predicting not only poor neural health and cognitive functioning, but emotional functioning as well (e.g., depression) (Jacobus et al., 2017). Larger prospective studies such as the newly launched Adolescent Brain Cognitive Development (ABCD) study will help us better understand the role of pre-existing childhood brain differences that contribute to substance use initiation and progression to problematic use, and ultimately poorer health outcomes for adolescents and young adults (Garavan et al., 2018; Lisdahl et al., 2018).

Acknowledgements

We would like to thank the National Institute on Alcohol Abuse and Alcoholism (R01 AA013419); the National Institute on Drug Abuse (R01 DA021182; U01 DA041089; R21 DA047953); and the California Tobacco-Related Disease Research Grants Program Office of the University of California Grant 580264. The authors would like to thank participating schools in the San Diego Unified School District and participating families.

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