Longitudinal Changes in Cognition in Young Adult Cannabis Users
Mary Becker, Paul F. Collins, Ashley Schultz, Snežana Urošević, Brittany Schmaling, and Monica Luciana
The Journal of Clinical and Experimental Neuropsychology, 2018, 40, (6), 529–543.
doi : 10.1080/13803395.2017.1385729
Introduction : Adolescent cannabis use (CU) is associated with impaired attention, executive function, and verbal learning/memory. These associations are generally observed in cross-sectional studies. Longitudinal studies of cannabis users are lacking.
Method : The present study examines associations between CU and cognition over time in chronic daily adolescent-onset CUs, as compared to non-using controls. Both groups completed a neuropsychological battery at study intake and again two years later.
Results : Baseline group differences have been published (Becker, Collins, & Luciana, 2014) and indicated deficits in verbal learning and memory, motivated decision-making, planning and working memory in CUs. In this follow-up report, the longitudinal performance of users is compared to that of sustained non-users using the same battery. At follow-up, the majority of CUs continued to report regular and heavy cannabis use. Relative impairments in the domains of working memory, planning and verbal memory remained stable, suggesting that these are enduring vulnerabilities associated with continued CU during young adulthood. Improvements in motivated decision-making were evident in both groups. In addition, CUs demonstrated relatively better performance on short-duration speeded tasks. An earlier age of CU onset was associated with poorer verbal learning and memory and planning performance over time.
Conclusions : Verbal learning and memory and planning processes, as well as their neural correlates, merit further scrutiny within etiological models of cannabis-induced cognitive impairments.
Keywords : Cannabis; adolescence; neurocognition; memory; executive function
Adolescent cannabis use (CU) is associated with cognitive disruptions based on cross-sectional research. Longitudinal studies are rare but permit consideration of dose-response associations, whether impairments exist before use onset, and whether they persist with continued use. This study follows a college-aged sample of adolescent-onset cannabis users (CUs) and comprehensively examines neurocognition over time.
It is well established that adolescent and young adult CUs demonstrate cognitive deficits that cut across domains of function. Among these are deficits in sustained attention (Dougherty et al., 2013; Jacobsen, Mencl, Westerveld, & Pugh, 2004), processing speed (Fried, Watkinson, & Gray, 2005; Lisdahl & Price, 2012; Medina et al., 2007) and complex attention (Bolla, Brown, Eldreth, Tate, & Cadet, 2002; Fontes et al., 2011; Lisdahl & Price, 2012 ). Relative deficits in executive functions have been reported across a number of paradigms and processes. For instance, inhibitory control is impaired in CU adolescents (Lisdahl & Price, 2012), adults (Bolla et al., 2002; Gruber & Yurgelun-Todd, 2012; Pope & Yurgelun-Todd, 1996), and early-onset users (Battisti, Roodenrys, Johnstone, Pesa et al., 2010; Fontes et al., 2011; Gruber et al., 2012). In addition, CUs demonstrate poor set-shifting performance (Gruber, Dahlgren, Sagar, Gonenc, & Killgore 2012; Lane, Cherek, Tcheremissine, Steinberg, & Sharon, 2007), which is worse with early onset use (Fontes et al., 2011; Gruber et al., 2012).
Studies that have focused on executive functions in the context of motivations to attain rewards have shown that adult CUs show decision-making deficits (Ernst et al., 2003; Verdejo-García, Rivas-Pérez, Vilar-López, & Pérez-García, 2007; Whitlow et al., 2004), which have been linked to increased CU disorder symptoms (Gonzalez, Schuster, Mermelstein, & Diviak, 2015). Younger CUs, as well as those with longer CU durations, are prone to impulsive choices (Clark, Roiser, Robbins, & Sahakian, 2009; Dougherty et al., 2013; Solowij et al., 2012).
Mnemonic function is variable depending on the domain of memory that is assessed. Consistent with deficits in executive function, prospective memory appears to be impaired in CUs (Bartholomew, Holroyd, & Heffernan, 2010; McHale & Hunt, 2008; Montgomery, Seddon, Fisk, Murphy, & Jansari, 2012). Findings for spatial memory are inconsistent, depending on the task. For instance, studies have found no evidence for deficits in spatial span (Harvey, Sellman, Porter, & Frampton, 2007) or visual n-back performance (Ehrenreich et al., 1999). In contrast, it was found in one study that CUs were impaired on a complex spatial self-ordered search task that involved both spatial memory and spatial monitoring (Harvey et al., 2007). In one study, male young adult heavy CUs demonstrated poorer delayed visuospatial memory as a function of amounts used (Pope & Yurgelun-Todd, 1996). Many labs have examined spatial memory performance and report no deficits (Bolla et al., 2002; Macher & Earleywine, 2012; Mahmood, Jacobus, Bava, Scarlett, & Tapert, 2010; McHale & Hunt, 2008; Medina et al., 2007).
A more robust finding is that performance during the encoding stage of verbal list-learning tasks is deficient in CU adolescents and adults (Gonzalez et al., 2012; Hanson et al., 2010; Harvey et al., 2007; Solowij et al., 2011) and that this deficit persists after abstinence (Bolla et al., 2002; Cuttler, McLaughlin, & Graf, 2012; Gonzalez et al., 2012; Hanson et al., 2010; Pope & Yurgelun-Todd, 1996; Solowij et al., 2011; Takagi et al., 2011). Similarly, CUs demonstrate impaired story learning following brief abstinence periods (Medina et al., 2007; Schwartz, Gruenewald, Klitzner, & Fedio, 1989). A meta-analysis that focused on cognitive disruptions in the context of cannabis use (Grant, Gonzalez, Carey, Natarajan, & Wolfson, 2003) reported a reliable impairment across studies in verbal learning and recall. Motivation may play an important role in CU’s verbal learning performance given that motivational interventions have been shown to improve performance in CU but not in controls (Macher & Earleywine, 2012).
Most of these neurocognitive findings stem from cross-sectional research. Four studies have assessed CUs at multiple time points over years (Jacobus, Squeglia, Sorg, Nguyen-Louie, & Tapert, 2014; Jackson et al., 2016; Meier et al., 2012; Tait, Mackinnon, & Christensen, 2011). Meier et al. (2012) utilized a large birth cohort to prospectively assess cognition beginning before use initiation and extending into adulthood. Those who abstained from cannabis use had stable IQs over time, while decreases were observed among those who developed cannabis dependence. Adolescent-onset use was specifically associated with IQ declines. Jackson et al. (2016) used a behavior genetics approach to examine a large sample of adolescent twins as they transitioned into substance use. A major finding from this study was that CU twins failed to show significantly greater IQ declines over time relative to their abstinent siblings, suggesting that the cognitive changes observed by Meier et al. (2012) might be attributable to premorbid factors.Tait et al. (2011) followed young adult CUs at four-year intervals for two assessments of cognition. Persistent heavy CUs demonstrated poorer immediate verbal recall while former users were unimpaired. The groups were otherwise equivalent, suggesting that verbal memory is selectively diminished with regular use but with potential for recovery after abstinence.
Another longitudinal study followed 16–19 year old alcohol+cannabis users over 3 years (Jacobus et al., 2015). Participants were assessed at baseline, after 18 months, and after 3 years. A global neuropsychological composite derived from numerous measures of cognition was equivalent between users and non- using controls at the first and third assessments, but it was lower among users at the second assessment. Verbal memory deficits were consistently found.