Abstract
Introduction:
Theories of relative deprivation suggest African Americans in disadvantaged communities are at increased risk for drug use. This increased risk may be due, in part, to exposure to drugs and drug subcultures. Given the significance of the prefrontal cortex (PFC) functioning in yielding behavior that is strategically guided rather than reactive to environmental demands, it is important to examine the relationship between PFC functioning, neighborhood drug activity and substance use among African Americans residing in high risk communities.
Methods:
A sample of 120 young adult African American females was recruited from high-risk neighborhoods. Each completed a modified version of neighborhood environment scale, a neurobehavioral assessment designed to measure apathy, behavioral disinhibition and executive dysfunction, and provided a urine sample that was tested for the presence of psychoactive drugs.
Results:
Logistic regression analyses indicated females with higher scores on behavioral disinhibition were 2.6 times more likely to test positive for marijuana (95%CI = 1.02, 6.57). Neither apathy nor executive dysfunction was related to marijuana use. No relationship emerged between neighborhood drug activity and marijuana use.
Conclusions:
Among the neurobehavioral traits considered only behavioral disinhibition was associated with marijuana use, suggesting different neurobehavioral domains may be uniquely related to marijuana use. For females living in high risk environments, the extent to which that they are able to control impulses may provide some protection against marijuana use. Future studies focused on the moderating effects of behavioral disinhibition on the association of exposure to risk environments and marijuana use may prove beneficial. Further, the study adds to the small base of literature supporting the Frontal Systems Behavior Scale as a brief assessment to evaluate frontally-mediated neurobehavioral traits relevant to substance use in community samples. However, future studies aimed at examining the influence of neighborhood drug activity might benefit from more precise measures of exposure to neighborhood drug activity. More research to replicate and expand on the present findings is warranted.
Keywords: marijuana, Frontal System Behavior Scale, behavioral disinhibition, neighborhood drug activity, African Americans, females
INTRODUCTION
National data indicate marijuana is the most commonly consumed illicit drug and current trends suggest both marijuana use and cannabis use disorders are increasing in African Americans (Chen & Jacobson, 2012; Compton, Grant, Colliver, Glantz, & Stinson, 2004; Johnston, O’Malley, Miech, Bachman, & Schulenberg, 2014). Despite the recent push for the legalization of marijuana, a substantial base of research has linked marijuana use to a range of adverse outcomes, including criminal activity, poor employment and high-risk sexual behaviors (Green, Doherty, Stuart, & Ensminger, 2010; Shook, Vaughn, Goodkind, & Johnson, 2011). Consequently, there remains a need to identify factors that are associated with or indicate risk for marijuana use among those at greatest risk for suffering these adverse outcomes (i.e., African Americans) (Zapolski, Pedersen, McCarthy, & Smith, 2014; Green et al., 2010 Kakade et al., 2012; Des Jarlais, McCarty, Vega, & Bramson, 2013).
According to the Social Cognitive Theory (SCT) (Bandura, 1986), human behavior results from the dynamic and ongoing interaction of personal, environmental and behavioral factors. In the field of substance abuse, intra- person factors, such as behavioral under-control (impulsivity), emotional dysregulation and deficits in executive functioning, have been linked to substance use disorders (Ridenour et al., 2009; Tarter et al., 2003; Verdejo-Garcia, Bechara, Recknor, & Perez-Garcia, 2006). Furthermore, neuroimaging and neuropsychological studies have identified several frontal lobe functional systems underlying behavioral regulation and executive control believed to be impaired in substance users (e.g., the medial prefrontal cortex (PFC), anterior cingulate cortex (ACC), the orbitofrontal cortex (OFC) and dorsolateral PFC) (Verdejo-Garcia, Bechara, Recknor, & Perez-Garcia, 2006; Ersche et al., 2005; Fishbein et al., 2005). For example, damage to the ACC, a frontal lobe region highly innervated with medial PFC connections, results in apathy and low motivation for natural reinforcers (Verdejo-Garcia, Bechara, Recknor, & Perez-Garcia, 2006). OFC dysfunction increases impulsive behavior (Everitt et al., 2007; Schoenbaum & Shaham, 2008; Wrase et al., 2007), and impairment of the dorsolateral PFC is associated poor planning, organization and working memory (Boeka & Lokken, 2011; Verdejo-Garcia, Bechara, Recknor, & Perez-Garcia, 2006). Frontal cortical dysfunction in these areas are thought to mediate substance use vulnerability (Ersche et al., 2005; Fishbein et al., 2005).
At the level of the environment, neighborhood factors have been shown to influence substance use and poor outcomes associated with use. One unique characteristic of economically disadvantaged African American neighborhoods that is conceptualized as a risk factor for substance use is visible drug market activity (Wallace & Muroff, 2002; Saxe et al., 2001; Crum, Lillie-Blanton, & Anthony, 1996; Wertz & Sayette, 2001). In lower socioeconomic (SES) neighborhoods with visible drug activity there are more opportunities to use drugs and drug sub-cultures likely reduce inhibitions about drug use, thereby increasing the likelihood of use (Wagner & Anthony, 2002; Linton, Jennings, Latkin, Gomez, & Mehta, 2014; Wertz & Sayette, 2001; Cochran, Grella & Mays, 2012; Rhodes et al., 2005).
Further, stress produced by living in lower SES neighborhoods primes an individual for substance use disorders (Sinha, 2001). Chronic stress is associated with PFC dysfunction (Qin, Hermans, van Marle, Luo, & Fernandez, 2009; Bondi, Rodriguez, Gould, Frazer, & Morilak, 2008; Brown, Henning, & Wellman, 2005; Cerqueira, Mailliet, Almeida, Jay, & Sousa, 2007; Mika, et al., 2012), which perpetuates impairments in emotional regulation (Li & Sinha, 2008). These and related deficits have been shown to increase vulnerability to substance use disorders (Medina et al., 2008; Verdejo-Garcia, Lopez-Torrecillas, Gimenez, & Perez-Garcia, 2004; Verdejo-Garcia, Rivas-Perez, Lopez-Torrecillas, & Perez-Garcia, 2006).
Given the important role of the PFC in yielding strategically-guided behavior (rather than behavior that is reactive to immediate environmental demands), coupled with evidence suggesting poor living conditions adversely affects PFC functioning, it is important to examine the relationship between PFC functioning and substance use among individuals residing in communities with high rates of drug activity. However, assessing neurocognitive factors often is not feasible given the time, effort and financial cost associated with administering assessments. As a result, few studies have examined the relationship between neurocognitive factors and substance use within community samples of young adults.
The purpose of this study was to address current gaps in the literature by focusing on the association of exposure to neighborhood drug activity, neurobehavioral traits and marijuana use among a sample of young adult females. Our focus on African Americans is critical given this group is exposed to multiple and unique risk factors (Wu, Temple, Shokar, Nguyen-Oghalai, & Grady, 2010; Finlay, White, Mun, Cronley, & Lee, 2012; Chen & Jacobson, 2012; Saxe et al., 2001), are among those least likely to receive treatment for substance use disorders (Alegria, Carson, Goncalves, & Keefe, 2011; Wells, Klap, Koike & Sherbourne, 2001), and suffers the highest rates of morbidities associated with drug use (Gil, Wagner, Tubman, 2004; Zapolski, Pedersen, McCarthy, & Smith, 2014; Green et al., 2010). Moreover, while comparing disadvantaged females to females from higher SES and African Americans to Whites is useful, these approaches provide limited information for designing tailored interventions. As a result, researchers are increasingly focusing on within group differences (see Wu et al., 2010). Therefore, using a sample of African American females from high risk communities we hypothesized: (1) performance on neurobehavioral measures will be associated with marijuana use and (2) exposure to neighborhood drug activity will be associated with marijuana use. Our goal is to identify contextual factors related to marijuana use and better understand who and what should be targeted for interventions within high-risk communities in an on-going effort to develop tailored interventions.
MATERIAL AND METHODS
Procedures
Data for this paper were drawn from a larger cross-sectional study that aimed to explain racial disparities in sexually transmitted diseases among young adult females by considering the influence of social and cultural neighborhood factors on sexual partnerships, sexual norms and behaviors of females residing in lower SES neighborhoods. The sample included 240 African American and White females aged 18–30 years recruited using snowball sampling techniques. Participants were recruited via street recruitment. Target areas included neighborhoods identified as low SES using census-based neighborhood social and economic indicators (e.g., mean household income and percent of female headed households). In addition, flyers were distributed at local community colleges and health clinics and we placed advertisements in local newspapers. To be eligible for participation in the study, females had to meet the following criteria:(a) identify as African American or White; (b) be between 18 and 30 years of age; (c) reside in lower SES neighborhoods in Baltimore City; and (d) have no history of regular drug use, excluding alcohol and marijuana.
Those who met the study’s eligibility criteria were asked to complete a face-to-face semi-structured interview with trained research assistants. After providing informed consent, participants answered detailed questions about drug use and sexual behaviors, social networks, psychosocial factors and socio-demographics. Participants also completed a neurobehavioral battery. Each participant provided a urine sample that was tested for the presence of psychoactive drugs. All assessments were conducted in a private interview room at the research site. All participants received remuneration for their time and effort. The Johns Hopkins Bloomberg School of Public Health Institutional Review Board approved the study.
For this paper, our focus is on a sub-sample of 120 African American females. The majority (88%) resided in neighborhoods where juvenile drug arrest rates ranged from 47 to 128 per 1,000. These rates were substantially higher than Baltimore City’s rate of 32 per 1,000 (Baltimore Neighborhood Indicators Alliance, 2008).
Measures
Demographic factors.
Participants provided information about age and education. Age was treated as a continuous variable. Education data were converted to a dichotomous variable (i.e., less than 12 years and Diploma/GED).
The Frontal Systems Behavior Scale (FrSBe):
The FrSBe consists of 46 items designed to measure: (1) apathy (i.e., low levels of initiation and persistence, score range 14–70), (2) disinhibition (i.e., low inhibitory control, score range 15–75) and (3) executive dysfunction (i.e., problems with attention, working memory, and planning, score range 17–85). Each subscale is intended to measure behavioral problems associated with specific frontally mediated cortical circuits: (1) the medial PFC (apathy subscale), (2) the OFC (disinhibition subscale) and (3) the dorsolateral PFC (executive dysfunction subscale). The FrSBe has demonstrated good reliability and validity in both normal and clinical populations (Carvalho, Ready, Malloy, & Grace, 2013; Grace & Malloy, 2001; Velligan, Ritch, Sui, DiCocco, & Huntzinger, 2002; Basso, et al., 2008) and has been used in substance use research (Lyvers, Jamieson, & Thorberg, 2013; Spinella, 2003; Verdejo-Garcia, Bechara et al., 2006; Verdejo-Garcia, Rivas-Perez et al., 2006). For the purposes of data analyses two groups were created for each subscale (i.e., persons scoring below the mean and persons scoring above the mean).
Neighborhood drug activity.
Two items drawn from a modified version of neighborhood environment scale were used to assess perceived neighborhood drug activity: (1) In my neighborhood I see people using or selling drug; and (2) In my neighborhood drug dealers earn the most money (see Crum, et al., 1996). Response options included true or false. Participants endorsing one or both of the items were placed in the exposure category.
Marijuana use:
On-site urinalysis for drug metabolites was performed using the Multi-Drug 12 Panel Test for the rapid detection of THC/marijuana; cocaine and its metabolite, benzoylecgonine; PCP (phencyclidine); morphine and its related metabolites derived from opium (opiates); methamphetamines (including ecstasy); methadone; amphetamines; barbiturates; benzodiazepines and tricyclic antidepressants. In addition, participants responded to the following three item: (1) in the past seven days did you smoke marijuana; (2) in the past seven days on how many days did you smoke marijuana; and (3) how old were you the first time you used marijuana.
Data Analysis
Using SPSS 20 we employed descriptive statistics to obtain frequencies and mean scores. We used Pearson’s chi square tests and t-tests to examine differences among individuals who tested positive for marijuana and those who tested negative for marijuana on neurobehavioral traits and exposure to drug activity. Logistic regression analyses were executed to examine the association of neighborhood drug activity, neurobehavioral traits, and marijuana use. First unadjusted odds ratios (ORs) and 95% confidence intervals (CIs) were obtained for each covariate and the outcome variable, marijuana use measured by urinalysis. Next, a model that included all covariates (i.e., apathy, behavioral disinhibition, executive dysfunction, perceived neighborhood drug activity, age and education) was tested. Adjusted ORs and 95% CIs were obtained.
RESULTS
Of the 120 participants seven had missing data, therefore the final analytic sample included 113 females. The mean age was 23.6 (sd=3.5) years and 73% completed high school. Forty four percent of females tested positive for marijuana. The average age at first use was 14.6 years (sd=2.8). Sixty two percent reported exposure to neighborhood drug activity. Table 1 summarizes the sample characteristics.
Table 1.
Sample Characteristics (N=113)
Variable | N (%)/M(sd) |
---|---|
Age | 23.6 (3.5) |
Education | |
< 12 years | 31 (27.4) |
Diploma/GED | 82 (72.6) |
Neighborhood drug activity | 70 (61.9) |
Marijuana use (urinalysis) | 50 (44.2) |
Apathy | 25.8 (6.8) |
Behavioral Disinhibition | 28.4 (8.4) |
Executive Dysfunction | 33.7 (10.0) |
Among those testing positive for marijuana (n=50), 55% reported smoking marijuana in the 24 hours prior to the assessment. Three out of four reported using marijuana in the week prior to the assessment. The mean number of days of marijuana use during the past week was 4.1 (sd=2.8). Compared to non-marijuana users, marijuana users had significantly high mean scores on behavioral disinhibition (32.2 (sd=7.9) vs. 25.3 (sd=7.6) (t=4.6, p< .001)) and executive dysfunction (36.9 (sd=10.1) vs 31.1(sd=9.2) (t=3.1, p<.01). The mean score for apathy among users of marijuana was 27.8 (sd=6.0) compared to 24.8 (sd=6.4) among females who did not test positive for marijuana (t=1.8; p<.10). Sixty percent of marijuana users compared to 64% of non-users reported exposure to neighborhood drug activity (X2=0.14, p=.70).
Results from the unadjusted logistic regression analysis yielded significant results for the association of behavioral disinhibition and marijuana use (OR = 3.2, 95%CI = 1.47, 6.96) and executive dysfunction and marijuana use (OR =2.6, 95%CI =1.20, 5.52). Apathy was not associated with marijuana use. No relationship emerged between neighborhood drug activity and marijuana use (see Table 2).
Table 2.
Results of logistic regression analyses examining the association of neighborhood drug activity, neurobehavioral traits and marijuana use (N=113)
Variable | % Testing positive for marijuana | Unadjusted OR (95% CI) | Adjusted OR (95%CI) |
---|---|---|---|
Age | -- | 1.1 (0.97, 1.20) | 1.1 (0.99, 1.27) |
Education | |||
< 12 years | 66.7 | 1.0 | 1.0 |
Diploma/GED | 39.3 | 3.1 (1.36, 7.02) | 2.3 (0.88, 6.13) |
Apathy | |||
Below mean | 36.9 | 1.0 | 1.0 |
Above mean | 54.2 | 2.1 (0.94, 4.31) | 0.99 (0.38, 2.52) |
Behavioral Disinhibition | |||
Below mean | 32.3 | 1.0 | 1.0 |
Above mean | 60.4 | 3.2 (1.47, 6.96)** | 2.6 (1.02, 6.57)* |
Executive Dysfunction | |||
Below mean | 33.9 | 1.0 | 1.0 |
Above mean | 56.9 | 2.6 (1.20, 5.52)** | 1.4 (0.52, 4.07) |
Neighborhood drug activity | |||
No | 47.7 | 1.0 | 1.0 |
Yes | 45.2 | 0.9 (0.43, 1.91) | 1.0 (0.43, 2.30) |
p<.05
p<.01
When all covariates were entered into the equation, simultaneously, only behavioral disinhibition emerged as a correlate of marijuana use (AOR = 2.6, 95%CI = 1.02, 6.57). The relationship between executive dysfunction and marijuana use was no longer significant (AOR = 1.4, 95%CI = 0.52, 4.07). No relationship emerged between exposure to neighborhood drug activity and marijuana or apathy and marijuana.
DISCUSSION
We examined the association of exposure to neighborhood drug activity, neurobehavioral traits, and current marijuana use among a sample of young adult African American females from disadvantaged communities. Consistent with extant literature, behavioral disinhibition was related to recent marijuana use (Bolla, Eldreth, Matochik, & Cadet, 2005; Lyvers et al., 2013; Piechatzek et al., 2009; Spinella, 2003). Previous longitudinal research has identified disinhibition as a plausible risk factor for cannabis use disorder (Tarter et al, 2003; Ridenour, Tarter, Reynolds, Mezzich, Kirisci, &Vanyukov, 2009). Unique to this study is the finding that behavioral disinhibition, as measured by the FrSBe, was positively associated with marijuana use, while controlling for the effects of exposure to neighborhood drug activity.
In the adjusted model, executive dysfunction was not associated with marijuana use. This finding is somewhat contradictory to results from previous neurocognitive work that demonstrated an association between marijuana use and deficits in information processing, decision making, attention, and working memory (Boggio et al., 2010; Bolla et al., 2005; Crane, Schuster, Fusar-Poli, & Gonzalez, 2013; Crane, Schuster, & Gonzalez, 2013; Fontes et al., 2011a, 2011b; Lyvers et al., 2013; Thames, Arbid, & Sayegh, 2014; Verdejo-Garcia et al., 2007; Verdejo-Garcia, Rivas-Perez et al., 2006). Discrepancies in findings may be due to methodological differences. Specifically, differences in duration and severity of drug use must be taken into consideration. In the current study, we used a brief questionnaire to measure neurobehavioral traits in a community sample of young adults. The majority of previous studies reporting an association of executive dysfunction and marijuana use have used clinical samples or older populations (Verdejo-Garcia et al., 2007; Verdejo-Garcia, Rivas-Perez et al., 2006) and employed comprehensive batteries of neuropsychological tests or neuroimaging (Bolla et al., 2005; Crane, Schuster, Fusar-Poli et al., 2013; Crane, Schuster, & Gonzalez 2013; Fontes et al., 2011a, 2011b; Martin-Santos et al., 2010; Thames et al., 2014).
Similarly, we did not find a relationship between apathy and marijuana use. However, a small base of research identifies apathy as a correlate of marijuana use (Verdejo-Garcia, Rivas-Perez et al. (2006; Cherek, Lane, & Dougherty, 2002; Lane, Cherek, Pietras, & Steinberg, 2005) and the apathy subscale was designed to assess everyday behavioral deficits associated with the ACC, an area of the brain known to be strongly affected by THC intoxication (Martin-Santos et al., 2010). More longitudinal research focused on apathy and marijuana use is needed.
Exposure to neighborhood drug activity and marijuana use were not related. Increased exposure to contextual disadvantages is presumed to place African Americans at heighten risk for poor health behaviors, such as drug use (Wilson, 1987; Rhodes 2002). Moreover, it is well documented that African Americans living in disadvantaged urban neighborhoods are exposed to drugs in their community more than their white counterparts or persons residing in more affluent neighborhoods (Crum et al., 1996). However, neighborhood drug activity has not been linked, consistently, to increased drug use among African American young persons (Ridenour et al., 2009; Crum et al., 1996; Furr-Holden et al., 2014; Lambert, Brown, Phillips, & Ialongo, 2004). Thus, while drugs may be more readily available in neighborhoods with drug activity, the simple assumption that exposure to drug activity increases drug use may not be correct (Crum, et al., 1996; Wagner & Anthony, 2002; Wertz & Sayette, 2001; Cochran, et al, 2012). This relationship is likely complex and requires consideration of the synergistic effects of exposure, intra-person factors (e.g., neurobehavioral traits), and other social and cultural factors (Mennis & Mason, 2012; Ridenour et al., 2009; Ridenour et al., 2013). Furthermore, the relationship may vary by type of drug, gender and race/ethnicity (Karriker-Jaffe, 2011).
Our findings must be considered in light of the study’s limitations. First, we cannot infer causality due to the study’s cross-sectional design. Second, our small sample size likely resulted in reduced power to detect relationships and limited our ability to test more comprehensive models (e.g., neurobehavioral traits as moderators of the association of exposure to drugs and marijuana use). In addition, our sampling strategy limited the generalizability of the findings. A longitudinal study design would allow us to better understand the relationship between neurobehavioral traits and marijuana use. Increasing the sample size would increase the power to detect relationships, allow for the testing moderation models and increase the validity of the findings. Next, using random sampling techniques would yield a more representative sample and, thereby, improve external validity. Measurement issues are also a concern, particularly as they relate the validity and reliability of our two item self-report measure of neighborhood drug activity. However, it should be noted that at present there is no gold standard for measuring neighborhood drug activity. Previous research has used objective measures (e.g., geocoded drug arrest data) (see Jennings, Taylor, Salhi, Furr-Holden, & Ellen, 2012; Linton et al., 2014) as well as self-report measures, which typically consists of one or two items, to assess exposure to neighborhood drug activity (see Crum et al., 1996 and Jennings et al., 2012).
CONCLUSIONS
In conclusion, the results suggest different neurobehavioral domains may be uniquely related to marijuana use. For African American females exposed to risk environments the extent to which that they are able to control impulses may provide some protection against engaging in marijuana use. Given a small base of research indicating intact neurocognitive functioning might serve as protective function against adverse outcomes among high risk populations (Mitchell Severtson, & Latimer, 2007), more research focused on the moderating effects of behavioral disinhibition on the association of exposure to neighborhood drug activity and marijuana use may prove beneficial. In addition, our findings support the utility of the FrSBe as a brief valid assessment for measuring frontally-mediated neurobehavioral traits relevant to substance use disorders (Winhusen et al., 2013; Lyvers et al., 2013). However, future studies aimed at examining the influence of neighborhood drug activity might benefit from more precise measures of neighborhood drug activity. More research to replicate and expand on the present findings is warranted.
Research Highlights.
Marijuana use was prevalent among this sample of young adult females.
Behavioral disinhibition was positively associated with recent marijuana use.
Exposure to neighborhood drug activity was not associated with marijuana use.
Acknowledgements.
The authors would like to thank Ms. April Lawson who assisted in the data collection and management of the study.
Role of Funding Sources.
Funding for this study was provided by National Institute on Drug Abuse (NIDA) (R21DA025543). NIDA had no role in the study design, collection, analysis or interpretation of the data, writing the manuscript, or the decision to submit the paper for publication.
This work was supported by grants from the National Institute on Drug Abuse (R21DA025543).
List of Abbreviations:
- FrSBe
Frontal System Behavior Scale
- ACC
anterior cingulate cortex
- OFC
orbitofrontal cortex
- PFC
prefrontal cortex
Footnotes
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Conflict of Interest. There are no conflicts of interest
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