|Year : 2019 | Volume
| Issue : 2 | Page : 113-119
Cognitive functions in alcohol use and cannabis use disorder: A cross-sectional study
Ottilingam Somasundaram Ravindran1, G Nandini2, Natarajan Shanmugasundaram1, V Vivian Kapil1
1 Department of Psychiatry, Sri Ramachandra Institute of Higher Education and Research, Chennai, Tamil Nadu, India
2 Department of Clinical Psychology, Sri Ramachandra Institute of Higher Education and Research, Chennai, Tamil Nadu, India
|Date of Web Publication||22-Jul-2020|
Ottilingam Somasundaram Ravindran
No. 30 (New No. 17), 23rd Cross Street, Besant Nagar, Chennai - 600 090, Tamil Nadu
Source of Support: None, Conflict of Interest: None
Background and Aim: Alcohol and cannabis misuse have an impact on neurocognition. This cross-sectional study evaluated the neuropsychological performance of individuals with alcohol dependence and cannabis dependence with concomitant alcohol use. Materials and Methods: We recruited individuals with alcohol dependence (n = 21) and cannabis dependence with concomitant alcohol use (n = 17) and age being 18–60 years as per the International Classification of Diseases-10th revision criteria. Convenience sampling was done. All the participants were evaluated by a comprehensive neuropsychological battery. Comparisons involving neuropsychological measures were performed using Mann–Whitney U-test. Results: Participants with cannabis dependence with co-occurring alcohol use showed significantly poorer performance than the participants with alcohol dependence on tasks assessing processing speed, working memory, verbal learning and memory, visuospatial ability, and language skills Conclusions: Participants with cannabis dependence with co-occurring alcohol use exhibited poorer cognitive performance on several neuropsychological measures than the participants with alcohol dependence. Age, duration, and early age of cannabis use initiation have no links with cognitive performance in the cannabis + alcohol group.
Keywords: Alcohol, cannabis, cognition, neuropsychological testing
|How to cite this article:|
Ravindran OS, Nandini G, Shanmugasundaram N, Kapil V V. Cognitive functions in alcohol use and cannabis use disorder: A cross-sectional study. J Mental Health Hum Behav 2019;24:113-9
|How to cite this URL:|
Ravindran OS, Nandini G, Shanmugasundaram N, Kapil V V. Cognitive functions in alcohol use and cannabis use disorder: A cross-sectional study. J Mental Health Hum Behav [serial online] 2019 [cited 2022 May 25];24:113-9. Available from: https://www.jmhhb.org/text.asp?2019/24/2/113/290524
| Introduction|| |
Substance misuse is a matter of public health concern in India. Substances such as alcohol and cannabis (also known as marijuana) are psychoactive drugs that may change brain function and structure after chronic use and result in cognitive and behavioral deficits that remain even after detoxification. Neuropsychological studies indicate progressive disturbances of cognitive functions, mainly regarding memory and the so-called frontal functions in the majority of patients with alcohol dependence syndrome.,, These disturbances are responsible for disorders in the working memory and affect executive functions, planning, and solution of complex problems or undertaken decisions. These disorders constrain the possibilities of flexible changes of action strategies and reduce behavior control and suppress psychosocial adaption abilities. Other researchers also demonstrated deficits in verbal and visual memory, working memory, visuospatial functioning, reasoning, inhibition, and processing speed among individuals with alcohol dependence.,
The high rates of marijuana and alcohol use among adolescents are of great concern because ongoing neurodevelopment occurs throughout adolescence and emerging adulthood, and exposure to neurotoxic compounds during this period may alter healthy brain development. Heavy marijuana using adolescents and young adults has demonstrated deficits in attention, verbal learning and memory, psychomotor speed, and sequencing functioning within several hours to days of last use., Evidence further suggests that adolescent onset (initiation before age 16, approximately) is an important risk factor and predicts poorer neural health and neurocognitive outcome over time.
Marijuana is often used in combination with alcohol. Many alcohol-using populations have moderate-to-high levels of marijuana use; similarly, many marijuana-using teens have significant exposure to heavy drinking. More recently, Jacobus et al. have found that heavy cannabis use in adolescence was linked to a number of neurocognitive deficits when studied individuals with cannabis dependence who also had co-occurring alcohol use. While most existing studies examine the impact of alcohol or marijuana use separately, understanding the impact of concomitant use is also highly relevant. The interactive effects of concomitant alcohol and marijuana use are less clear. Therefore, consideration of comorbid alcohol may be an important area of examination in studies of the effects of cannabis on neurocognition. Much of the existing literature cannot report confidently if cognitive decrements are primarily related to alcohol to marijuana or to use of both substances. We hypothesized that individuals with co-occurring dependence of marijuana and alcohol would show poorer neuropsychological performance relative to individuals with alcohol dependence. With this background, we did the current study to distinguish the impact of alcohol and the concomitant use of marijuana and alcohol on various neurocognitive domains.
| Materials and Methods|| |
A cross-sectional study was done using a convenience sampling. We recruited individuals with alcohol dependence (n = 21) and individuals with cannabis dependence with co-occurring alcohol use (n = 17) who were seeking treatment from the De-addiction Inpatient Services of the Department of Psychiatry of Sri Ramachandra Institute of Higher Education and Research in Chennai. We did the study from January 2019 to June 2019. The following inclusion criteria were used for individuals with alcohol dependence: diagnosis of alcohol dependence (F 10.20) as per the International Classification of Diseases-10th revision (ICD-10), age being 18–60 years, and minimum educational qualification of 6th standard. Exclusion criteria included those with acute unstable medical illnesses or neurological disorders or those with comorbid severe mental illnesses or polysubstance use (except nicotine dependence). Inclusion criteria for individuals with cannabis dependence include diagnosis of cannabis dependence (F 12.2) as per the ICD-10, age being 18–60 years, and minimum educational qualification of 6th standard. Exclusion criteria included those with cannabis use in the past 1 week, those with acute unstable medical illnesses or neurological disorders, or those with comorbid severe mental illnesses or polysubstance use (except limited exposure with alcohol and nicotine dependence). We took written informed consent from the patients and their relatives. The study was approved by the Institutional Ethics Committee of our institution.
Eligible participants were invited to participate in the study that incorporated a battery of neurocognitive assessments. Participants completed the battery of neuropsychological assessment lasting approximately 1 h in a single session. The battery included nine neuropsychological tests which measure eight neuropsychological domains. Visuospatial function was assessed using the Block Design subtest from the Wechsler Adult Intelligence Scale, 4th edition, India (WAIS-IVINDIA). We assessed the processing speed using the Coding and Symbol Search subtests from the WAIS-IVINDIA. Executive function was assessed using the trail making test (TMT)-B. We assessed the attention using the Digit Span subtest from the WAIS-IVINDIA. Visual memory was assessed using the Visual Reproduction subtest from the Wechsler Memory Scale, 3rd edition, India (WMS-IIIINDIA). The Spatial Span subtest from the WMS-IIIINDIA was used to assess the working memory. We assessed the verbal learning and memory using the Verbal Paired Associates subtest from the WMS-IIIINDIA. The Information subtest from the Postgraduate Institute Battery of Brain Dysfunction was administered to assess the language skills. We administered the battery within one session, keeping in accordance with the prescribed standard method in the manual. The second author (GN), with experience in neuropsychological testing, administered the assessment in a quiet room. The domains of cognition assessed, the neuropsychological assessments administered, and short explanations of the assessment tools are shown in [Table 1].
|Table 1: Domains of cognition, neuropsychological tests, and test description|
Click here to view
The data were analyzed using the Statistical Package for the Social Sciences for Windows, version 16 (SPSS Inc., Chicago, IL, USA). Comparisons were made using the Mann–Whitney U-test. Correlation was used to measure the association between two measured quantities. Statistical significance was fixed at P < 0.05.
| Results|| |
As evident from [Table 2], the age range of the participants was 18–60 years. The mean age (standard deviation) of the participants in both Group 1 and Group 2 was 37.71 (6.37) and 21.47 (2.00) years, respectively. All the participants in Group 2 (100%) fall under the age range of 18–35 years. More married (90.5%) and employed (52.3%) individuals were present in the participants with alcohol dependence. The mean age of onset of drinking was 20.00 (standard deviation [SD] – 2.51) years of age in the participants with alcohol dependence, and the mean age of initiation of co-occurring cannabis + alcohol use was 17.76 (SD – 1.90) years in the MJ + ALC group. The mean duration of drinking was 14.95 (SD – 6.97) years in Group 1, whereas the mean duration of dependence of co-occurring cannabis + alcohol use was 4.41 (SD – 1.97) years in Group 2. With regard to family history of substance dependence, more number of participants (58.8%) in the MJ + ALC group have family history of alcoholism. Participants with alcohol dependence have more number of relapses (57%) and 5.8% of participants belonging to the MJ + ALC group relapsed to marijuana.
[Table 3] displays the means and standard deviations for the 9 neurocognitive tests. As [Table 3] shows, compared with participants with alcohol dependence, participants in the MJ + ALC group have shown neuropsychological decrements in various cognitive domains, including visuospatial ability, processing speed (Symbol Search; P = 0.005), working memory (Spatial Span; P = 0.001), verbal learning and memory (Verbal Paired Associates; P = 0.003), and language skills (Information; P = 0.004). There were no significant differences between the two groups in terms of executive functions (as assessed with TMT-B), attention (as assessed with Digit Span test), and visual memory as assessed with Visual Reproduction test.
The relationship between age, duration, and age of initiation of cannabis use and cognitive performance of the participants in the cannabis + alcohol group was examined [Table 4]. There was no significant correlation between age, duration, and age of onset of cannabis use and cognitive functions.
|Table 4: Correlation between age, duration, and age of onset with cognitive performance in the MJ+ALC group|
Click here to view
| Discussion|| |
Alcohol and cannabis misuse are related to impaired cognition. This study evaluated the neuropsychological performance of participants with alcohol dependence and marijuana dependence with co-occurring alcohol use (MJ + ALC). Significant group differences were detected between the two groups in which the participants with marijuana dependence with co-occurring alcohol use have shown cognitive decrements in the domains of visuospatial ability, processing speed, working memory, verbal learning and memory, and language skills.
Participants in the MJ + ALC group have obtained low scores on the Block Design test than the other group which measures the visuospatial ability. The above results are comparable to the findings of previous researchers who reported the association of poor visuospatial ability with protracted substance use. This could suggest that adolescent substance use-related visuospatial problems may be particularly enduring or vulnerable to the impact of chronic use of cannabis. The results of the current findings suggest that heavy use of cannabis use during late adolescence and early adulthood may produce long-term cognitive disadvantages, primarily in visuospatial abilities. The above findings are in line with findings in previous studies.
Regarding processing speed, participants in the MJ + ALC group scored lesser than the other group on the measures of Symbol Search (processing speed) and Coding (visual-motor speed) subtests from the WAIS-IVINDIA suggest that they have slower information processing abilities and our findings are similar to the findings of previous researchers. Information processing is a fundamental aspect of attention and concentration and a basic building block of higher-order cognitive processing. Cortical regions, such as the prefrontal cortex, are important for cognitive processing, an integral component of most psychomotor tasks including symbol search and coding. Previous reports indicated that recently abstinent smokers had reduced activation in motor cortical areas and such deactivation could still be observed after 28 days of cannabis discontinuation. Other factors that may have contributed to poor performance in participants with cannabis dependence were co-occurring alcohol use. Similar findings have been reported by other researchers.
On the domain of working memory, participants in the MJ + ALC group have obtained low scores on the Spatial Span subtest from the WMS-IIIINDIA, which shows evidence of poorer working memory than the participants with alcohol dependence, and our finding is consistent with other researchers. Previous studies reported the detrimental effects of cannabis use on measures of verbal updating of working memory which consists of continuous refreshing/updating of working memory contents in order to set task demands and optimize performance. These results are consistent with other human studies showing dose-related negative effects of severity of cannabis use on updating measures in participants with polydrug dependence. There is also evidence showing that participants with cannabis dependence have abnormally increased hippocampal activation in response to executive task demands. Therefore, hippocampal dysfunction may also play a prominent role on cannabis-induced updating deficits.
On the domain of verbal learning and memory, participants in the MJ + ALC group have shown impairments on the Verbal Paired Associates subtest from the WMS-IIIINDIA than the participants of alcohol dependence, suggesting that participants with marijuana dependence with co-occurring alcohol use have impaired verbal learning and memory deficits. Prior studies have also suggested that the use of alcohol alone may be more detrimental than combined use of alcohol plus marijuana While the excitotoxic effects of alcohol on the brain have been demonstrated, further evidence suggests that the antioxidant properties of marijuana may have a paradoxical “protective effect” from alcohol's neurotoxic consequences. Contrary to this findings, participants with MJ + ALC dependence in the current study have shown worse verbal memory performance than the participants with alcohol dependence. Participants with cannabis dependence of this study tended to drink less alcohol the more entrenched they were in the cannabis use, and cannabis was used separately to when alcohol was used. Simons et al. reported that experienced participants of cannabis dependence had different motives for using cannabis versus alcohol and similarly found that participants in their sample did not consistently use the two substances concurrently. We had intended to examine the potential effects of cause of both substances but found that they were rarely ever used together on the same day. There has been a scant literature suggesting neuroprotective effects of cannabis when co-used with alcohol. These results suggest that the effects of alcohol alone may differ from the concomitant use of alcohol and other drugs on the brain and cognition.
On language skills, we found out that participants in the MJ + ALC group scored lower than the participants with alcohol dependence on the Information subtest from the Postgraduate Institute Battery of Brain Dysfunction. The results of the current study demonstrated that participants in the MJ + ALC group have shown decreased verbal performance and concur with many other studies among participants with cannabis dependence. The Information subtest is considered as a measure of crystallized intelligence measuring knowledge acquired through experience or learning. Our findings also concur with those of Meier et al. who reported that marijuana use is related to a vulnerability in measures of crystallized intelligence.
The domains in which (namely, executive function, attention, and visual memory) the two groups do not differ significantly though mean differences were observed. On executive function, participants in the MJ + ALC group committed more perseverative errors in the TMT-B, indicating that they have impaired cognitive flexibility and set shifting than the participants of alcohol dependence. Previous research suggests that exposure to cannabis in early adolescence may lead to lower mental flexibility. Although our study shows that the participants are early-onset users (mean age being 17.76 years), there was no significant correlation between age of onset of cannabis use and executive functioning. Our finding is consistent with previous research which reported that marijuana use during adolescence is associated with a poorer executive functioning (e.g., sequencing ability). This neuropsychological profile is consistent with the hypothesis, based on adult studies, that marijuana is primarily associated with frontal, hippocampal, and cerebellar dysfunction.
There is no significant difference between the two groups on the domain of attention, though mean differences were observed. Our current findings show that the MJ + ALC group has shown relatively subtle dysfunctions in attentional processing than the participants with alcohol dependence indicating problems in the efficient selection of relevant stimulus information and in filtering out irrelevant material. Similar findings have been reported by other researchers. Early-onset cannabis was shown to impair attentional process, but in the current study, there is no significant correlation between early-onset cannabis use and attention.
With regard to visual memory, as measured by the Visual Reproduction subtest from the WMS-IIIINDIA, there is no significant difference between the two groups, though mean differences were observed. Participants in the MJ + ALC group scored lesser than the participants with alcohol dependence, showing that they have poorer visual memory and our findings are consistent with the findings of a previous research. A previous study of hippocampal-dependent pictorial-associative memory task in participants abstinent from cannabis dependence found that task performance did not differ between moderately using young adults and nonuser controls, but recall accuracy decreased as a function of exposure to cannabis and decreased activation was observed in dependents in bilateral parahippocampal regions and in the right dorsolateral prefrontal cortex during learning. These results indicate that cannabis may have long-term effects on short-term memory in cannabis-abusing adolescents and youths. Participants with cannabis dependence with an abstinence of 7 days were only included in this study because previous studies have reported that cognitive dysfunction maybe due to recent use or withdrawal, rather than persistent changes associated with chronic use which might add significance to the findings. Taken together, these results support greater vulnerability to neurocognitive dysfunction associated with cannabis use in emerging adults.
The results of the current study should be interpreted in light of several limitations. First, the data sample consisting of 21 and 17 participants per study group may limit the overall generalizability of the study findings. Second, both the participants with alcohol dependence and cannabis dependence groups were largely composed of male participants. Gender differences in the relationships between cannabis use and neural functioning are becoming a growing area of research, and our future research will focus on with larger sample size to identify whether substance use and neurocognitive associations exist similarly for both genders. Third, there are a significant number of known confounding variables, which are not taken into account such as frequency and/or amount of cannabis use during the time of assessment. Fourth, our study excluded adolescent participants with cannabis dependence because they are particularly vulnerable to the effects of addictive drugs as it is a developing brain. Future studies might examine the neurocognitive outcomes of various substance use trajectories, particularly during critical periods of brain maturation as well as factors that either contribute to cognitive decline or are neuroprotective during the transition to young adulthood.
| Conclusions|| |
The current study examined the neuropsychological profile of participants with alcohol dependence and cannabis dependence with co-occurring alcohol use. Participants with cannabis dependence with co-occurring alcohol use demonstrated numerous cognitive deficits, most notably in verbal learning and memory, visuospatial ability, working memory, processing speed, and verbal abilities. Given the currently high rates of alcohol, cannabis, and concurrent use, it is important that participants with potential dependence and their families better understand the unique influence of each drug and the additive impact of concomitant use to a developing brain.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Bechara A, Dolan S, Denburg N, Hindes A, Anderson SW, Nathan PE. Decision-making deficits linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers. Neuropsychologia 2001;39:376-89.
Cunha PJ, Novaes MA. Neurocognitive assessment in alcohol abuse and dependence: Implications for treatment. Braz J Psychiatry 2004;26 Suppl 1:S23-7.
Rosenbloom MJ, O'Reilly A, Sassoon SA, Sullivan EV, Pfefferbaum A. Persistent cognitive deficits in community-treated alcoholic men and women volunteering for research: Limited contribution from psychiatric comorbidity. J Stud Alcohol 2005;66:254-65.
Blume AW, Schmaling KB, Marlett GA. Memory, executive cognitive function, and readiness to change drinking behavior. Addict Behav 2005;30:301-14.
Duka T, Townshend JM, Collier K, Stephens DN. Impairment in cognitive functions after multiple detoxifications in alcoholic inpatients. Alcohol Clin Exp Res 2003;27:1563-72.
Townshend JM, Duka T. Binge drinking, cognitive performance and mood in a population of young social drinkers. Alcohol Clin Exp Res 2005;29:317-25.
Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, et al
. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 2004;101:8174-9.
Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB. Brain maturation in adolescence and young adulthood: Regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 2010;20:534-48.
Squeglia LM, Jacobus J, Tapert SF. The influence of substance use on adolescent brain development. Clin EEG Neurosci 2009;40:31-8.
Hanson KL, Winward JL, Schweinsburg AD, Medina KL, Brown SA, Tapert SF. Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addict Behav 2010;35:970-6.
Solowij N, Jones KA, Rozman ME, Davis SM, Ciarrochi J, Heaven PC, et al
. Verbal learning and memory in adolescent cannabis users, alcohol users and non-users. Psychopharmacology (Berl) 2011;216:131-44.
Gruber SA, Dahlgren MK, Sagar KA, Gönenç A, Lukas SE. Worth the wait: Effects of age of onset of marijuana use on white matter and impulsivity. Psychopharmacology (Berl) 2014;231:1455-65.
Agosti V, Nunes E, Levin F. Rates of psychiatric comorbidity among U.S. residents with lifetime cannabis dependence. Am J Drug Alcohol Abuse 2002;28:643-52.
Jacobus J, Squeglia LM, Infante MA, Castro N, Brumback T, Meruelo AD, et al
. Neuropsychological performance in adolescent marijuana users with co-occurring alcohol use: A three-year longitudinal study. Neuropsychology 2015;29:829-43.
Wechsler D. Wechsler adult intelligence scale. In: Administration and Scoring Manual. 4th
ed. India: NCS Pearson; 2013.
Reitan RM. Trail Making Test. Tucson. AZ:Reitan Neuropsychological Laboratory;1992.
Wechsler D. Wechsler memory scale. In: Administration and Scoring Manual. 3rd
ed. India: NCS Pearson; 2009.
Pershad D, Verma SK. Handbook of Postgraduate Institute of Battery of Brain Dysfunction. India: National Psychological Corporation; 1980.
Sullivan EV, Rosenbloom MJ, Pfefferbaum A. Pattern of motor and cognitive deficits in detoxified alcoholic men. Alcohol Clin Exp Res 2000;24:611-21.
Hanson KL, Medina KL, Padula CB, Tapert SF, Brown SA. Impact of adolescent alcohol and drug use on neuropsychological functioning in young adulthood: 10-year outcomes. J Child Adolesc Subst Abuse 2011;20:135-54.
Kelleher LM, Stough C, Sergejew AA, Rolfe T. The effects of cannabis on information-processing speed. Addict Behav 2004;29:1213-9.
Bosker WM, Karschner EL, Lee D, Goodwin RS, Hirvonen J, Innis RB, et al
. Psychomotor function in chronic daily cannabis smokers during sustained abstinence. PLoS One 2013;8:e53127.
Pillay SS, Rogowska J, Kanayama G, Gruber S, Simpson N, Pope HG Jr., et al
. Cannabis and motor function: fMRI changes following 28 days of discontinuation. Exp Clin Psychopharmacol 2008;16:22-32..
Bolla KI, Brown K, Eldreth D, Tate K, Cadet JL. Dose-related neurocognitive effects of marijuana use. Neurology 2002;59:1337-43.
Miyake A, Friedman NP, Emerson MJ, Witzky AH, Howerther A. The unity and diversity of executive function and their contribution to complex frontal lobe tasks: A latent variable analysis. Cogn Psychol 2000;41:49-100.
Verdejo-Garcia A, Benbrook A, Funderburk F, David P, Cadet JL, Bolla KI. The differential relationship between cocaine use and marijuana use on decision-making performance over repeat testing with the Iowa Gambling Task. Drug Alcohol Depend 2007;90:2-11.
Jacobus J, McQueeny T, Bava S, Schweinsburg BC, Frank LR, Yang TT, et al
. White matter integrity in adolescents with histories of marijuana use and binge drinking. Neurotoxicol Teratol 2009;31:349-55.
Crews FT, Waage HG, Wilkie MB, Lauder JM. Ethanol pretreatment enhances NMDA excitotoxicity in biogenic amine neurons: Protection by brain derived neurotrophic factor. Alcohol Clin Exp Res 1999;23:1834-42.
Hamelink C, Hampson A, Wink DA, Eiden LE, Eskay RL. Comparison of cannabidiol, antioxidants, and diuretics in reversing binge ethanol-induced neurotoxicity. J Pharmacol Exp Ther 2005;314:780-8.
Simons J, Correia CJ, Carey KB. A comparison of motives for marijuana and alcohol use among experienced users. Addict Behav 2000;25:153-60.
Parrott A, Gouzoulis-Meyfrank E, Rodgers J, Solowij N. Ecstasy/MDMA and cannabis: The complexities of their interactive neuropsychological effects. J Psychopharmacol 2004;18:579-82.
Messinis L, Kyprianidou A, Malefaki S, Papathanasopoulos P. Neuropsychological deficits in long-term frequent cannabis users. Neurology 2006;66:737-9.
Kaufman A, Lichtenberger E. Assessing Adolescent and Adult Intelligence. 3rd
ed. Hoboken, NJ: Wiley; 2006.
Meier MH, Caspi A, Ambler A, Harrington H, Houts R, Keefe RS, et al
. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc Natl Acad Sci U S A 2012;109:E2657-64.
Fontes MA, Bolla KI, Cunha PJ, Almeida PP, Jungerman F, Laranjeira RR, et al
. Cannabis use before age 15 and subsequent executive functioning. Br J Psychiatry 2011;198:442-7.
Ehrenreich H, Rinn T, Kunert HJ, Moeller MR, Poser W, Schilling L, et al
. Specific attentional dysfunction in adults following early start of cannabis use. Psychopharmacology (Berl) 1999;142:295-301.
Block RI, O'Leary DS, Hichwa RD, Augustinack JC, Boles Ponto LL, Ghoneim MM, et al
. Effects of frequent marijuana use on memory-related regional cerebral blood flow. Pharmacol Biochem Behav 2002;72:237-50.
Solowij N, Michie PT, Fox AM. Differential impairments of selective attention due to frequency and duration of cannabis use. Biol Psychiatry 1995;37:731-9.
Schwartz RH, Gruenewald PJ, Klitzner M, Fedio P. Short-term memory impairment in cannabis-dependent adolescents. Am J Dis Child 1989;143:1214-9.
Jager G, Van Hell HH, De Win MM, Kahn RS, Van Den Brink W, Van Ree JM, et al
. Effects of frequent cannabis use on hippocampal activity during an associative memory task. Eur Neuropsychopharmacol 2007;17:289-97.
Pope HG Jr., Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D. Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 2001;58:909-15.
[Table 1], [Table 2], [Table 3], [Table 4]