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Official websites use. Share sensitive information only on official, secure websites. MDMA use is commonly accompanied by use of other substances, most notably cannabis. Both MDMA and cannabis have probable effects on cognition. This paper reviews research into long-term effects on cognition which are likely to represent neurotoxicity. Research is hampered by numerous confounds and methodological difficulties. With recent cannabis use there is both an acute and a residual effect on cognition, making it important to have a significant abstinence period from cannabis when studying effects of MDMA in recreational users of both substances. It would appear that MDMA does indeed have subtle long-term effects on complex memory and executive functions that are independent of cannabis and may remain with abstention. This is consistent with evidence of disruption of the serotonin system in animal and human studies. Chronic effects on cognition due to cannabis are less consistently demonstrated, but more sensitive tests including electrophysiological measures have revealed long-term deficits in attention. Keywords: 3,; 4-methylenedioxymethamphetamine; 'ecstasy'; cannabis; cognitive performance; neurotoxicity. The controversy surrounding the risks posed to society and to the mental health of individuals by the use of illicit psychoactive drugs continues unabated. Despite much research, many of the long-term risks related to the use of these drugs have not been clearly defined or quantified, but remain central to the debate over their legal status. There has been stronger evidence of chronic effects of MDMA on cognitive functions and in this review we will focus on these, as well as on the less well documented confounding role played by cannabis, the illicit drug most widely used by MDMA users, and on the effects on cognition of cannabis per se. Taking MDMA leads to an acute massive neuronal release of serotonin 5-HT , followed by a period of depletion before levels return to normal. More chronic toxic effects appear also to involve primarily the 5-HT system, with the demonstration of serotonergic degeneration in several animal species, including non-human primates 3. This suggests that MDMA may have long-term effects on cognition. Important difficulties are faced by researchers investigating the effects of MDMA on humans. First and foremost, there are ethical and legal proscriptions to repeatedly administering an illicit and potentially toxic drug in controlled laboratory conditions. This means that studies are mostly restricted to recreational users, with the possible consequence of inaccurate self-report of the amounts of MDMA used. Furthermore, 'ecstasy' tablets bought on the black market contain a variable amount of MDMA 5 , and may contain a variety of other substances, including the closely related 3,4-methylenedioxyamphetamine MDA and 3,4-methylenedioxyethylamphetamine MDEA , caffeine, ephedrine, selegiline, amphetamine, ketamine, and LSD 6 , 7. Thus, amounts of MDMA consumed by experimental subjects are estimates and extraneous substances may affect findings. Premorbid differences between users and controls in intellectual, cognitive or psychological functions also need to be addressed. Furthermore, most MDMA users take other psychoactive drugs, including alcohol and illicit drugs, and these may have their own effects on cognition. Importantly, acute and chronic effects are often masked by too short an abstinence period for both MDMA and cannabis, especially the latter when the focus is on MDMA. One of the first indications of chronic cognitive deficits resulting from MDMA came in 8. Impairment of initial and delayed paragraph recall was described in 9 subjects compared to age-matched normative values. Subjects had taken an average of approximately 'ecstasy' tablets. They reported abstinence from MDMA for an average of about 66 days prior to testing and from all psychoactive drugs for 3 weeks. Performance on other cognitive tests was unimpaired. Results were, however, limited by the small number of subjects, the past use of other psychoactive substances, the fact that they were given a tryptophan infusion prior to testing and the lack of a control group. Furthermore, some of the subjects had psychiatric histories. The period of abstinence was undefined, so that possible lingering effects following recent MDMA or other drug taking were not excluded. The MDMA groups were significantly impaired on immediate and delayed word recall, but not on other cognitive tests information processing speed, sustained attention. An important flaw was that details of other illicit drugs were not recorded. This study was noteworthy for finding deficits in light users. No significant differences in memory function were found between the two groups. However, impairment in immediate verbal and delayed visual memory was found in the heavier MDMA users when estimated monthly dose of MDMA was included in regression models. Both subjects and control groups had taken other illicit substances, thus achieving some control for this potential confounder. However, levels of use were much greater in the MDMA group. Shortly after the above studies, in , we instigated a study of MDMA recruiting participants via advertisements in the popular press The sample size of 36 was relatively large for the field and MDMA use was greater than in most preceding studies estimated mean tablets. Subjects were identified for whom MDMA was the primary drug and who reported using other drugs only irregularly. They had not consumed any illicit drug for a mean of 78 days prior to the testing. Thus, impairments were unlikely to represent either acute MDMA effects, which last approximately hours after a dose 12 , or lingering effects which may last several days and may reflect the time course of regeneration of 5-HT. Both sides of the brain were implicated and the patterned deficit profile excluded explanations based on non-specific factors such as subjects' motivation. Mood, as assessed by the Beck Depression Inventory, also did not affect results. Cannabis was clearly identified as the next most commonly used illicit substance; however, none of the deficits showed any correlation with frequency or amount of cannabis used. Nevertheless, the difficulty in identifying a pattern to the MDMA deficits prompted a second study looking more closely at the role played by cannabis. Both user groups performed more poorly than controls on tests of verbal and visual memory, verbal fluency, speed of processing and manual dexterity. However, there was little difference between user groups on any of the tests. Thus, deficits appeared more closely related to cannabis than MDMA. Recent cannabis use may have affected findings, as the requested abstinence period from cannabis was 48 hours and a number of subjects reported even less than this. Notwithstanding these findings, MDMA has continued to be implicated in contemporaneous research, and further work in our department with electrophysiological measures highlighted residual effects that were independent of cannabis. Croft et al 14 focussed on the suspected neurophysiological correlate of MDMA-related cognitive impairment, namely depressed 5-HT function. This follows the argument that, if the relationship were reversed, such that impaired 5-HT predisposed an individual to 'risky behaviour' including MDMA use, then frequency of MDMA use and not total tablets consumed would be more closely related to the 5-HT deficit. The total number of tablets consumed would be determined by the stage of the subject's MDMA 'career' when recruited to the study. This study also found that cannabis was not related to the 5-HT deficit. Now in the new millennium there have been a plethora of studies on the cognitive effects of chronic MDMA use. Before reviewing these, the cognitive effects of cannabis will be considered. Cannabis is a popular drug of choice in the rave subculture and is also taken by MDMA users to ameliorate the low mood and irritability of the 'coming down' period after MDMA use. The neuropsychological effects of cannabis can be divided into acute and residual Acute effects are those associated with intoxication. Considering first acute influences, cross-sectional studies experimentally administering cannabis to subjects have indeed supported the existence of a syndrome of acute intoxication, with mood change, perceptual changes and characteristic cognitive impairments in memory and attention, motor skills, reaction time and skilled activities After the period of acute intoxication, it takes some time for performance to return to pre-dose levels, suggesting a drug residue effect. For example, performance on a flight simulator was impaired for up to 24 hours in aircraft pilots after smoking cannabis In light users there has been evidence of a drug residue effect for hours following a dose, but no clear evidence of a deficit persisting for more than 48 hours. Users have been tested after a period of abstinence to exclude acute or drug residue effects, although the length of this period has varied from study to study. In the s and s studies were roughly equally divided with respect to positive and negative results. Most had serious methodological flaws. In general abstinence periods were less than 24 hours or unrecorded, thus drug residue effects may easily have explained findings. Two early reports of chronic deficits resulting from cannabis were subject to limitations. In groups that were small and not well matched for gender and use of other drugs, Schwartz et al 18 compared 10 cannabis dependent users after 6 weeks of supervised abstinence with control groups of polydrug users and non-users. Visual retention and verbal memory for prose passages were found to be impaired. A larger scale study importantly matched users and 72 non-using controls in intellectual ability prior to onset of cannabis use Light and intermediate use was not associated with deficits. The user group had, however, experienced other drugs far more extensively and there was only a 24 hour unsupervised abstinence period. In more rigorous studies, a consistent theme has been attention impairment as a result of heavy or long-term use, as well as memory impairment. A study comparing groups of heavy and light cannabis users with a supervised abstinence period of 19 hours before testing found impairments in mental flexibility attentional set shifting in heavy users Learning of word lists was also impaired. The group differences remained after some statistical control of potential confounding variables, such as estimated levels of premorbid cognitive functioning and use of alcohol and other substances. In a Costa Rican sample having an abstinence period of 72 hours verified by urinalysis, subtle deficits in selective and divided attention associated with working memory and in verbal memory were disclosed that were specific to long-term users The most recent report 22 found that long-term cannabis takers mean of 24 years use performed significantly less well on verbal memory than shorter-term mean 10 years and non-user controls. Impairments were not severe, but learning, retention and retrieval were all affected following a median self-reported abstinence period of 17 hours. There was some suggestion of attention impairment, although executive tasks were generally unimpaired. Problems with this study include the fact that the cannabis users recruited were seeking treatment for dependence due to concerns including that of subjective cognitive impairment and may thus not be representative of cannabis users in general. The abstinence period was short and groups differed in use of other drugs; however, attempts were made to control these factors statistically. Performance measures on several tests correlated significantly with the duration of cannabis use, suggesting a chronic neurotoxic effect. Interestingly, apart from a time estimation task, no deficits were shown in shorter-term users with a mean use of 10 years and who were using cannabis daily. Although the studies described so far used abstinence periods of hours, it is still not clear if the deficits found were neurotoxic effects or whether they were due to a residue of cannabinoids in the brain. The principal active component of cannabis, deltatetrahydrocannabinol, accumulates in fatty tissue, and has a tissue elimination half-life of about 7 days In heavy users cannabinoids may remain in the body for more than two months after cessation This prompted a study by Pope et al 25 in long-term heavy users of cannabis throughout 28 days of monitored abstinence confirmed by urinalysis. Deficits were found on memory of word lists detectable at least 7 days after discontinuation of the drug and which were related to initial urinary cannabinoid concentration. These appeared to be reversible phenomena associated with recent drug exposure - attributable either to cannabinoids lingering in the CNS or to withdrawal from abruptly stopping use. An association between cumulative lifetime use of cannabis and cognitive deterioration was not found. After 28 days of abstinence, users showed virtually no differences from control subjects on a battery of 10 neuropsychological tests. Thus, impairments were related to recent cannabis exposure and were reversible with abstention. These findings are compatible with studies that found no significant long-term effects on IQ measures and the Mini Mental State Examination 26 , A metaanalysis of 13 of the more methodologically sound studies also found no significant evidence for chronic deficits in 7 out of 8 neuropsychological ability zones, with a possible small effect in only one domain, namely learning Finally, looking at electrophysiological evidence of attention impairment, Solowij et al 29 , 30 examined cortical event related potentials for anomalies of processing negativity in an auditory detection task. The ability to focus attention and filter out irrelevant information was impaired progressively with the number of years of cannabis use and only partial recovery was evident in former heavy users after a mean of approximately 2 years abstinence. In summary, there is clear evidence that cannabis has a residual effect on cognition that lasts hours after even a single episode of smoking. This needs to be considered when investigating effects of MDMA. Frequent smoking may lead to an accumulation of CNS cannabinoids and a drug residue effect may persist for much longer and may be continuously present. It is likely to include impaired focussed attention and working memory as well as impaired visual and verbal memory. There is less evidence for chronic neurotoxic effects following cannabis; however, there may be more subtle deficits influencing attention, such as those demonstrated electrophysiologically which appear to be related to duration of cannabis use. Studies into MDMA should aim for periods of abstinence from cannabis of some weeks rather than days, to avoid or minimize residual effects, particularly if cannabis is taken frequently. It also has to be borne in mind that withdrawal effects - characterised by insomnia, restlessness and irritability - in heavy cannabis users may affect cognitive performance. However, a more complex effect with MDMA and cannabis potentiating or diminishing the impact of the other on cognition cannot be ruled out. Participants were only required to abstain from taking other psychoactive drugs on the day of the study, so that effects from their recent use were not excluded. The MDMA group had impaired immediate and delayed prose recall compared to both control groups. Performance on other cognitive tests, including executive function and working memory, was unimpaired. Abstinence from MDMA was reported to be more than 21 days; however, subjects were asked to refrain from cannabis only on the day of the study. No significant deficits were associated with the cannabis groups, but of note was that in the MDMA group heavier use of cannabis was associated with stronger cognitive deficits. A similar design was used by Rodgers 34 to investigate lighter MDMA users average of 20 times after 2 months abstinence from MDMA and 1 month abstinence from cannabis, although this was not confirmed by drug screening. Deficits associated with MDMA were found on delayed recall of visual and verbal paired associates. Abstinence from all psychoactive agents for one week was checked by urine drug screening. MDMA groups were impaired on memory span and word and figure recognition. The MDMA groups had consumed more cannabis, cocaine and amphetamines; however, deficits remained after some statistical control for this had been introduced. Thus, while there is a growing consensus that memory deficits remain when past use of other drugs and psychosocial factors are considered, none of the recent studies are free from methodological confounds. MDMA has inevitably been taken with other drugs, and while our review suggests that cannabis may not produce memory deficits as a long-term residual effect, synergistic effects cannot be ruled out, but even more pertinently abstinence periods have been poorly controlled. For example, with an abstinence period from all drugs of only 24 hours, Bhattachary and Powell 36 found impaired immediate and delayed prose recall and executive function verbal fluency. Similarly, Fox et al 37 , although requesting participants to be free of MDMA and other illicit drugs for at least 2 weeks, only requested them to be free of cannabis for 1 day prior to testing. Then with an abstinence period from all drugs of 2 weeks confirmed by drug screening, but with no control group and with polydrug use in the MDMA group, a longitudinal study found that continued use of MDMA over one year was associated with decline in immediate and delayed prose recall Consensus is also emerging for deficits in working memory and central executive functions in heavier MDMA users, though with less consistency across reports compared with deficits of long-term memory. Furthermore, these studies remain fraught with the same methodological confounds. With no defined abstinence period for other drugs and limited statistical control for their past use and with no definition of an MDMA-free period in current heavy MDMA takers about tablets , Wareing et al 39 found impairment in aspects of central executive functioning random letter generation along with impaired accuracy of information processing. A study designed to avoid effects of recent psychoactive drug taking included abstinence periods from all recreational drugs of at least three weeks with confirmation of drugfree status by drug screening However, MDMA subjects had used more recreational drugs than controls and this may have contributed to cognitive impairments. Requiring participants not to have smoked cannabis for three days and not to have consumed other drugs for 24 hours, both relatively short abstinence periods, Heffernan et al 41 investigated the central executive functions involved in prospective memory i. Impairments remained significant when a measure of statistical control was used for consumption of cannabis and other drugs; nevertheless use of other drugs was much greater in MDMA groups. In the first study, subjects with subjective problems attributed to MDMA mean of about tablets were compared with MDMA users without these problems mean of about tablets and controls Deficits were disclosed on executive planning and spatial working memory which related to total MDMA consumption and were not related to subjective problems, suggesting that damage may occur without conscious appraisal. However, the second study 43 provided somewhat conflicting results whereby participants were unimpaired on most measures of prefrontal functioning. Here less heavy MDMA polydrug users mean of about tablets were compared with controls. The MDMA group showed deficits in memory tasks sensitive to involvement of temporal structures or in a manner similar to patients with temporal pathology. Results remained significant when measures of drug use which differed between subjects and controls were used as covariates. In both these studies, subjects were requested to be free of psychoactive drugs for 2 weeks, but this was not tested. The discrepancy regarding executive functions was attributed to lower total doses and shorter duration of MDMA taking in the second study. Executive function was subtly impaired in a recent study of heavy users that looked more closely at duration of toxic effect with abstinence Subjects had consumed averages of tablets across the different groups and included a group of ex-MDMA users who had been abstinent for at least 6 months. Participants were required to abstain from cannabis for 24 hours and other illicit drugs for 1 week. Subtle executive impairment was again described in what was predominantly an EEG study In subjects abstinent from all drugs for at least a week, a test of executive function rule shift card test correlated negatively with MDMA use in the past year. Interestingly, MDMA use also correlated with EEG coherence, a measure of synchronisation of firing, in posterior brain sites overlying visual association pathways, possibly indicating dysfunctional local connectivity. Correlations between reported total MDMA exposure and measures of cognitive impairment suggest that deficits are primarily associated with MDMA and support evidence of chronic toxicity in heavier users. Estimated lifetime consumption of MDMA has been found to correlate with verbal memory functions 33 , 36 , 37 , 44 , and with working memory and executive function 33 , However, the fact that MDMA exposure calculations are based on self report and that the amount of MDMA in a tablet may vary considerably make such calculations problematic. Furthermore, the fact that individuals with higher lifetime MDMA consumption tend also to have higher levels of consumption of other drugs needs consideration when assessing regression or correlation analyses. It also has to be considered that MDMA induced neurotoxicity may not simply relate to cumulative dose, but that patterns of use may be important and single high doses of MDMA may represent a particular risk, although this has not been widely studied in humans. Morgan et al 44 suggested that cognitive impairment resulting from MDMA might be a long-lasting phenomenon. Deficits in verbal recall and working memory persisted for at least 6 months and for an average of 2 years after cessation of use. Wareing et al 39 also found that working memory impairment persisted for at least 6 months and Reneman et al 46 reported that verbal recall remained affected at 1 year after stopping use. There has been, however, tentative evidence of some recovery of memory in a small group of 3 MDMA users who had abstained for more than 6 months Some of the studies mentioned have provided evidence of an association between cognition and indirect biological evidence of 5-HT disruption. Memory span has been found correlated with cortisol response to a serotonergic challenge Reneman et al 48 found impairment in verbal delayed recall to be associated with prefrontal cortex neuronal loss or dysfunction as indicated by altered N-acetylaspartate to creatinine ratio on magnetic resonance spectroscopy. Subjects were 8 heavy MDMA users who had been abstinent for a week. These studies were supportive of relationships between 5-HT disruption and cognitive dysfunction, but were small and not controlled for use of other substances. A larger SPECT study by Reneman et al 46 did not, however, find brain pre-synaptic 5-HT transporter densities in the cortex to be associated with cognitive measures. Receptor density was significantly lower in MDMA users compared to controls, but not in ex-MDMA users who had stopped at least one year before the study, suggesting that the effect was reversible. By contrast, verbal recall remained impaired in ex-MDMA users. They did not report a correlation between receptor binding and neuropsychological measures. Transporter reduction in many regions was inversely correlated with time since last dose, suggesting again that this may represent a reversible effect. MDMA is almost never taken without other drugs, most notably cannabis. Studies of cannabis without MDMA have provided clear evidence of acute and shortterm effects on attention and memory with possibly the only long-term effects being on frontal attentional networks. In contrast, there is evidence that MDMA does chronically impair complex memory tasks hippocampus and, in heavier users, higher executive information processing frontal cortex as well. Much of the evidence is compromised by the fact that short-term residual effects of cannabis and sometimes even acute effects cannot be ruled out. Furthermore, synergistic effects of cannabis and MDMA may explain effects on cognition. Circumstantial evidence correlating total lifetime dose of MDMA with cognitive measures does imply that MDMA is more likely to be the culprit than interaction with cannabis, but in the absence of evidence from pure groups this cannot be known for certain. The cognitive impairment associated with MDMA and cannabis is not large relative to normal cognitive variability among individuals. Nevertheless, it may be sufficient to affect scholastic performance or those embarking on intellectually challenging careers and may become more manifest as neuronal reserve diminishes with age. Conversely, impairments may resolve with prolonged abstinence. If deficits in MDMA users are indeed a clinical manifestation of serotonergic dysfunction, as some biological studies would suggest, this is cause for concern that users may have increased risk of other psychiatric conditions with strong serotonergic aspects, including depression, schizophrenia, anxiety, impulsivity, aggression, and obsessivecompulsive disorder. As a library, NLM provides access to scientific literature. World Psychiatry. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel.

Chronic cognitive impairment in users of 'ecstasy' and cannabis

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