Response perseveration and adaptation in heavy marijuana-smoking adolescents
Introduction
There is now strong evidence to suggest that marijuana smoking produces both acute and lasting detrimental effects on human behavioral and brain functions (Bolla et al., 2002, Chait and Pierri, 1992, Gruber and Yurgelun-Todd, 2005, Kalant, 2004, Lane and Cherek, 2002, Pope et al., 2001, Pope et al., 2003, Solowij et al., 2002, Volkow et al., 1996, Wilson et al., 2000). The extent and duration of these effects have been difficult to characterize, owing in part to limitations in control over experimental conditions (e.g., duration and amount of use) and proper matching control groups (see Kalant, 2004, Pope, 2002, Solowij et al., 2002).
Despite a considerable amount of recent work focused on characterizing neural and behavioral consequences of persistent, heavy marijuana use, relatively little attention has been devoted to the consequences of marijuana use during adolescence (Crowley et al., 1998, Fergusson et al., 2002, Kamon et al., 2005, Lane et al., 2005, Schwartz et al., 1989, Vandrey et al., 2005, Young et al., 2002). The limited effort devoted to adolescent populations represents a shortcoming in research efforts. Approximately 30% of all marijuana users in the US are adolescents, and use rates among adolescents have increased over the past 12 years (Johnston et al., 2005, National Institute on Drug Abuse, 2004). Equally compelling is epidemiological evidence showing that peak risk for marijuana dependence occurs at age 17 (Wagner & Anthony, 2002). These data suggest that adolescence may be a period of heightened exposure to marijuana, increased risk for heavy marijuana use, and perhaps a period of peak vulnerability to deleterious drug effects (Fergusson et al., 2003, Kelley et al., 2004, Spear, 2000). The present study focused on a group of adolescents between the age of 14 and 18, who were currently smoking marijuana on a regular basis (4 to 7 days per week), often multiple times per day. Thus, this represented a group of individuals who may show deficits in cognitive and behavioral performances related, in part, to heavy marijuana use.
Studies to date have commonly employed neuropsychological test batteries and/or brain imaging techniques to measure marijuana effects related to heavy use. These studies suggest that chronic marijuana users show impairments relative to controls on tests that measure behavioral and cognitive processes such as response perseveration, adaptation, and flexibility decision making, using laboratory tests such as the Wisconsin Card Sort Task (WCST), the Stroop Test, and the Iowa Gambling Task (Bolla et al., 2002, Pope et al., 2003, Solowij et al., 2002, Whitlow et al., 2004). These deficits appear to be related to atypical patterns of brain activation in mesolimbic and prefrontal regions.
There is also evidence that marijuana smoking may disrupt behavioral processes involving learning and motivation (Lane et al., 2004, Lane et al., 2005, Paule et al., 1992, Stiglick and Kalant, 1983). Studies with human participants have demonstrated that reinforced behavior patterns can be altered by acute Δ9 THC administration (Foltin et al., 1989, Kamien et al., 1994, Lane and Cherek, 2002, Lane et al., 2004). Previously, we demonstrated that acute administration of marijuana altered response adaptation, using a choice-based laboratory task designed to measure sensitivity to continually changing reinforcement contingencies (Lane & Cherek, 2002). At high doses (3.89% Δ9 THC), subjects tended to perseverate on a preferred response option, despite the fact that the reinforcement density (rate of monetary reward) on that option systematically decreased throughout the session, and thus produced reduced earnings.
In the present study, we employed both the WCST and a variation of the response adaptation procedure used in Lane and Cherek (2002) to study a group of adolescents who were current, regular marijuana smokers and a group of control adolescents with little drug use history. We previously demonstrated diminished performance on a laboratory task of motivation in a similar group of adolescent heavy marijuana smokers (Lane et al., 2005). Based on previous results of both acute and chronic marijuana smoking, we expected to find impaired performance on the WCST and diminished sensitivity to changes in reinforcement contingencies in marijuana-smoking adolescents, particularly with regard to response flexibility and adaptation.
Section snippets
Participants
Male and female adolescent participants (14–18 years old) responded to local newspaper advertisements. All participants were recruited via ads seeking individuals for behavioral research. No specific details were provided regarding desired participant characteristics or the nature of the study. Based on information obtained during initial telephone interviews, potential participants were brought to the laboratory for more extensive interviews covering physical and mental health status, and drug
Results
Table 1 provides demographic and psychometric data for the MJ+ and control groups. The groups were statistically different in age (MJ+ subjects were about 10.5 months older), history of nicotine use (more smokers in the MJ+ group), number meeting DSM criteria for conduct disorder (more CD in the MJ+ group), cognitive aptitude as measured by the Shipley (controls scored higher, but both were close to the age-adjusted mean of 50), and the Youth Self Report (YSR) withdrawn and delinquency
Discussion
Adolescents who smoked marijuana on a regular basis (four to seven days per week) and met abuse or dependence criteria were compared to a control group of adolescents with little drug use history on two experimental tasks measuring problem solving, response preseveration, and response adaptation — the WSCT and a task with concurrently available response options that changed over the course of a 50-min session. When controlling statistically for differences in nicotine use, history of other drug
Acknowledgements
This research was supported by National Institutes of Health/NIDA grant R01 DA 12968. This research was approved by the University of Texas Health Science Center, Houston Committee for the Protection of Human Subjects. We wish to thank Sheila White and Ehren Bradbury for valuable technical assistance. Correspondence concerning this article should be addressed to Scott D. Lane, Department of Psychiatry and Behavioral Sciences, University of Texas Health Science Center - Houston, 1300 Moursund
References (56)
- et al.
Protective and risk effects of peer relations and social support on antisocial behaviour in adolescents from multi-problem milieus
Journal of Adolescence
(1997) - et al.
Cannabis dependence, withdrawal, and reinforcing effects among adolescents with conduct symptoms and substance use disorders
Drug and Alcohol Dependence
(1998) - et al.
Validity of structured clinical evaluations in adolescents with conduct and substance problems
Journal or the American Academy of Child and Adolescent Psychiatry
(2001) - et al.
Motivational effects of smoked marijuana: Behavioral contingencies and high-probability recreational activities
Pharmacology Biochemistry and Behavior
(1989) - et al.
Neuroimaging of marijuana smokers during inhibitory processing: A pilot investigation
Cognitive Brain Research
(2005) - et al.
Do hallucinogens cause residual neuropsychological toxicity?
Drug and Alcohol Dependence
(1999) Long-term effects of exposure to cannabis
Current Opinion in Pharmacology
(2005)Adverse effects of cannabis on health: An update of the literature since 1996
Progress in Neuropsychopharmacology and Biological Psychiatry
(2004)- et al.
A contingency management intervention for adolescent marijuana abuse and conduct problems
Journal or the American Academy of Child and Adolescent Psychiatry
(2005) - et al.
Marijuana effects on sensitivity to reinforcement in humans
Neuropsychopharmacology
(2002)