MDMA, serotonergic neurotoxicity, and the diverse functional deficits of recreational ‘Ecstasy’ users

doi:10.1016/j.neubiorev.2013.04.016

Neuroscience & Biobehavioral Reviews

Volume 37, Issue 8, September 2013, Pages 1466-1484

https://doi.org/10.1016/j.neubiorev.2013.04.016 Get rights and content

Highlights

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Serotonin is a modulator for many different psychobiological functions.
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Abstinent Ecstasy/MDMA users show serotonergic reductions.
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Abstinent users show deficits in those functions modulated by serotonin.
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They occur in memory, cognition, sleep, vision, pain, mood, psychiatric status.
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These structural and functional changes are related to lifetime dosage.

Abstract

Serotonergic neurotoxicity following MDMA is well-established in laboratory animals, and neuroimaging studies have found lower serotonin transporter (SERT) binding in abstinent Ecstasy/MDMA users. Serotonin is a modulator for many different psychobiological functions, and this review will summarize the evidence for equivalent functional deficits in recreational users. Declarative memory, prospective memory, and higher cognitive skills are often impaired. Neurocognitive deficits are associated with reduced SERT in the hippocampus, parietal cortex, and prefrontal cortex. EEG and ERP studies have shown localised reductions in brain activity during neurocognitive performance. Deficits in sleep, mood, vision, pain, psychomotor skill, tremor, neurohormonal activity, and psychiatric status, have also been demonstrated. The children of mothers who take Ecstasy/MDMA during pregnancy have developmental problems. These psychobiological deficits are wide-ranging, and occur in functions known to be modulated by serotonin. They are often related to lifetime dosage, with light users showing slight changes, and heavy users displaying more pronounced problems. In summary, abstinent Ecstasy/MDMA users can show deficits in a wide range of biobehavioral functions with a serotonergic component.

Section snippets

MDMA and serotonergic neurotoxicity: general introduction

The methamphetamine derivative MDMA (3,4-methylenedioxymethamphetamine), has a particular affinity for the serotonin transporter, and by reversing its normal reuptake actions, causes a massive efflux of serotonin into the synaptic cleft (Berger et al., 1992). Hence an acute dose of MDMA can release around 80% of available serotonin (5-hydroxytryptamine, 5-HT) into the synaptic cleft (Green et al., 1995). In laboratory animals, repeated dosing with MDMA can damage the serotonergic

Serotonergic neurotoxicity in laboratory animals: pre-clinical findings

Serotonergic neurotoxicity following MDMA is a robust empirical phenomenon in many laboratory species. Single high doses of MDMA, or repeated administrations of lower doses, can lead to a pronounced reduction in markers for serotonin across higher brain regions, along with other indices of serotonergic change. The first studies to reveal this were undertaken in the mid-1980s (Ricaurte et al., 1985, Schmidt, 1987, Stone et al., 1987). Subsequent research has confirmed those early findings, and

Psychobiological functions with a serotonergic input: brief overview

As noted earlier, Jacobs and Fornal (1995) stated that serotonin was ‘implicated in virtually everything’ but ‘responsible for nothing’. Their review concluded that serotonin had a regulatory role (my italics) for many different psychobiological functions, including sleep, aggression, sex, pain, mood state, cardiovascular activity, respiratory control, nutrient intake, and psychomotor output. All these areas therefore need to be empirically studied in abstinent Ecstasy/MDMA users. One important

Neuroimaging studies with neurocognitive assessments

This section will review studies of brain activity (EEG, ERP, or neuroimaging) which involved parallel psychological assessments. As noted earlier, McCann et al. (2008) and Kish et al. (2010) found significant SERT reductions in their fMRI studies of abstinent Ecstasy/MDMA users. In relation to neurocognition, McCann et al. (2008) showed that memory task performance was inversely associated with SERT binding levels, in the dorso-lateral prefrontal cortex, orbitofrontal cortex, and parietal

Seeking help for Ecstasy/MDMA related problems

Comparatively few Ecstasy/MDMA users seek professional help for drug-related problems. Gunnarsson et al. (2004) surveyed 104 18 year-old high school students in Sweden, where 25% reported taking illicit recreational drugs, mostly amphetamine or Ecstasy. Amongst these stimulant users, 38% reported psychiatric symptoms which they attributed to drug usage, including low spiritedness and depression, anxiety/worry, and feelings of unreality. Yet none of them had sought medical help for their mental

MDMA and serotonergic neurotoxicity: early theoretical proposals

The notion that the functional problems of Ecstasy/MDMA users reflect serotonergic neurotoxicity, was proposed in the first human study. Peroutka (1989) surveyed 100 recreational users, and reported that with repeated usage, there was a tendency for the good effects of MDMA to diminish, and the negative drug effects to increase. It was reported that: ‘freshman love it, sophomores like it, juniors are ambivalent, and seniors are afraid of it’. Peroutka (1989) commented that these initial

Acknowledgements

This article was written during a sabbatical period at the Centre for Human Psychopharmacology, Swinburne University, in Melbourne, Australia.

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ReviewMDMA, serotonergic neurotoxicity, and the diverse functional deficits of recreational ‘Ecstasy’ users

Highlights

Abstract

Section snippets

MDMA and serotonergic neurotoxicity: general introduction

Serotonergic neurotoxicity in laboratory animals: pre-clinical findings

Psychobiological functions with a serotonergic input: brief overview

Neuroimaging studies with neurocognitive assessments

Seeking help for Ecstasy/MDMA related problems

MDMA and serotonergic neurotoxicity: early theoretical proposals

Acknowledgements

Drug Alc. Depend.

Int. Rev. Neurobiol.

Eur. J. Pharmacol.

Eur. J. Pharmacol.

Pharmacol. Biochem. Behav.

Accid. Anal. Prevent.

Biol. Psychiatry

J. Subst. Abuse

Psychiatry Res.

Trends Cogn. Sci.

Drug Alc. Depend.

Drug Alcohol Depend.

Drug Alcohol Depend.

Neuroimage

Pharmacol. Biochem. Behav.

Drug Alc. Depend

Lancet

Lancet

Biol. Psychol.

Evidence of neurotoxicity of ecstasy: sustained effects on electroencephalographic activity in polydrug users

PLoS One

Persistent effects of (+/−) 3,4-methylenedioxymethamphetamine (MDMA, “ecstasy”) on human sleep

Sleep

Ecstasy (MDMA)-addicted subjects show increased serum levels of brain-derived neurotrophic factor, independently from a rise in drug-induced psychotic symptoms

Addict. Biol.

Neuropsychological effects of 3,4-methylenedioxymethamphetamine (MDMA or ecstasy) in recreational users

Clin. Neuropsychol.

Effects of ambient temperature on the relative reinforcing strength of MDMA using a choice procedure in monkeys

Psychopharmacology (Berl.)

Human Ecstasy use is associated with increased cortical excitability: an fMRI study

Neuropsychopharmacology

Recreational ecstasy use: acute effects potentiated by ambient conditions?

Neuropsychobiology

Brain serotonin function in MDMA (Ecstasy) users: evidence for persistent neurotoxicity

Neuropsychopharmacol. Rev.

The nature of 3, 4-methylenedioxymethamphetamine (MDMA)-induced serotonergic dysfunction: evidence for and against the neurodegeneration hypothesis

Curr. Neuropharmacol.

Procedural and declarative memory task performance, and the memory consolidation function of sleep, in recent and abstinent ecstasy/MDMA users

J. Psychopharmacol.

Memory impairment in abstinent MDMA (Ecstasy”) users

Neurology

Verbal memory deficits are correlated with prefrontal hypometabolism in 18FDG PET of recreational MDMA users

PLoS One

Preliminary evidence of motor impairment among polysubstance 3,4-methylenedioxymethamphetamine users with intact neuropsychological functioning

J. Int. Neuropsychol. Soc.

Methylenedioxymethamphetamine (‘Ecstasy’)-induced immunosuppression: a cause for concern?

Br. J. Pharmacol.

Prospective associations between meth/amphetamine (speed) and MDMA (ecstasy) use and depressive symptoms in secondary school students

J. Epidemiol. Commun. Health

Ecstasy induced reduction of the availability of the brain serotonin transporter as revealed by [11C] (+) McN5652-PET and the multi-linear reference tissue model: loss of transporter or artifact of tracer kinetic modelling?

J. Psychopharmacol.

Long-term effects of ecstasy” use on serotonin transporters of the brain investigated by PET

J. Nucl. Med.

Event related potential (ERP) evidence for selective impairment of verbal recollection in abstinent recreational methylenedioxymethamphetamine (Ecstasy”)/polydrug users

Psychopharmacology (Berl)

Long-term effects of MDMA (Ecstasy) on the human central nervous system revealed by visual evoked potentials

Add. Biol.

Ecstasy abuse and dependence: applicability and reliability of DSM-IV criteria among adolescents and young adults

Hum. Psychopharmacol.

Methylenedioxymethamphetamine (MDMA, ‘Ecstasy’): a stressor on the immune system

Immunology

Serotonin revisited

Psychopharmacology (Berl)

Visual cortex activation using the fMRI BOLD method in human MDMA (ecstasy) users

Neuroimaging research in human MDMA users: a review

Psychopharmacology (Berl)

Electrophysiological evidence of serotonergic impairment in long-term MDMA (Ecstasy) users

Am. J. Psychiatry

Eating attitudes, weight concerns, and beliefs about drug effects in women who use ecstasy

Review
MDMA, serotonergic neurotoxicity, and the diverse functional deficits of recreational ‘Ecstasy’ users