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Human ecstasy (MDMA) polydrug users have altered brain activation during semantic processing

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Abstract

Rationale

Ecstasy (3,4-methylenedioxymethamphetamine [MDMA]) polydrug users have verbal memory performance that is statistically significantly lower than that of control subjects. Studies have correlated long-term MDMA use with altered brain activation in regions that play a role in verbal memory.

Objectives

The aim of our study was to examine the association of lifetime ecstasy use with semantic memory performance and brain activation in ecstasy polydrug users.

Methods

A total of 23 abstinent ecstasy polydrug users (age = 24.57 years) and 11 controls (age = 22.36 years) performed a two-part functional magnetic resonance imaging (fMRI) semantic encoding and recognition task. To isolate brain regions activated during each semantic task, we created statistical activation maps in which brain activation was greater for word stimuli than for non-word stimuli (corrected p < 0.05).

Results

During the encoding phase, ecstasy polydrug users had greater activation during semantic encoding bilaterally in language processing regions, including Brodmann areas 7, 39, and 40. Of this bilateral activation, signal intensity with a peak T in the right superior parietal lobe was correlated with lifetime ecstasy use (r s = 0.43, p = 0.042). Behavioral performance did not differ between groups.

Conclusions

These findings demonstrate that ecstasy polydrug users have increased brain activation during semantic processing. This increase in brain activation in the absence of behavioral deficits suggests that ecstasy polydrug users have reduced cortical efficiency during semantic encoding, possibly secondary to MDMA-induced 5-HT neurotoxicity. Although pre-existing differences cannot be ruled out, this suggests the possibility of a compensatory mechanism allowing ecstasy polydrug users to perform equivalently to controls, providing additional support for an association of altered cerebral neurophysiology with MDMA exposure.

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Acknowledgments

This work was supported by the National Institutes of Health with grants R01 DA015137 and R21 DA020149 to Dr. Cowan and grant K12 DA00357 to Dr. Benningfield (National Institute on Drug Abuse); grant K01 MH083052 to Dr Blackford and grant R21 MH087803-02 to Dr Salomon (National Institute of Mental Health); and Vanderbilt Clinical and Translational Science Award UL1 TR000445 (National Center for Research Resources).

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Authors and Affiliations

  1. Vanderbilt Addiction Center, Vanderbilt University School of Medicine, Nashville, TN, 37212, USA

    Tristan J. Watkins, Vidya Raj, Mary S. Dietrich, Jennifer U. Blackford, Ronald M. Salomon, Margaret M. Benningfield, Christina R. Di Iorio & Ronald L. Cowan

  2. Psychiatric Neuroimaging Program, Vanderbilt University School of Medicine, Nashville, TN, 37212, USA

    Tristan J. Watkins, Vidya Raj, Mary S. Dietrich, Jennifer U. Blackford, Ronald M. Salomon, Margaret M. Benningfield, Christina R. Di Iorio & Ronald L. Cowan

  3. Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA, 90024-1759, USA

    Junghee Lee

  4. Department of Biostatistics, Vanderbilt University Schools of Medicine and Nursing, Nashville, TN, 37212, USA

    Mary S. Dietrich

  5. Vanderbilt University Institute of Imaging Science, Nashville, TN, 37232, USA

    Aize Cao

  6. Department of Psychology, Vanderbilt University, Nashville, TN, 37240, USA

    Jennifer U. Blackford, Sohee Park & Ronald L. Cowan

  7. Department of Psychiatry, Vanderbilt University School of Medicine, 1601 23rd Avenue South, Suite 3057, Nashville, TN, 37212, USA

    Tristan J. Watkins

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  1. Tristan J. Watkins
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  2. Vidya Raj
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Correspondence to Tristan J. Watkins.

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Watkins, T.J., Raj, V., Lee, J. et al. Human ecstasy (MDMA) polydrug users have altered brain activation during semantic processing. Psychopharmacology 227, 41–54 (2013). https://doi.org/10.1007/s00213-012-2936-1

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