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Neurochemical and behavioral comparisons of contingent and non-contingent methamphetamine exposure following binge or yoked long-access self-administration paradigms

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Abstract

Rationale

Abuse of the psychostimulant methamphetamine (METH) can cause long-lasting damage to brain monoaminergic systems and is associated with profound mental health problems for users, including lasting cognitive impairments. Animal models of METH exposure have been useful in dissecting the molecular effects of the drug on cognition, but many studies use acute, non-contingent “binge” administrations of METH which do not adequately approximate human METH use. Long-term METH exposure via long-access (LgA) self-administration paradigms has been proposed to more closely reflect human use and induce cognitive impairments.

Objective

To better understand the role of contingency and patterns of exposure in METH-induced cognitive impairments, we analyzed behavioral and neurochemical outcomes in adult male rats, comparing non-contingent “binge” METH administration with contingent (LgA) METH self-administration and non-contingent yoked partners.

Results

Binge METH (40 mg/kg, i.p., over 1 day) dramatically altered striatal and hippocampal dopamine, DOPAC, 5-HT, 5-HIAA, BDNF, and TrkB 75 days after drug exposure. In contrast, 6-h LgA METH self-administration (cumulative 24.8–48.9 mg METH, i.v., over 16 days) altered hippocampal BDNF in both contingent and yoked animals but reduced striatal 5-HIAA in only contingent animals. Neurochemical alterations following binge METH administration were not accompanied by cognitive deficits in Morris water maze, novel object recognition, or Y-maze tests. However, contingent LgA METH self-administration resulted in impaired spatial memory in the water maze.

Conclusions

Overall, substantial differences in neurochemical markers between METH exposure and self-administration paradigms did not consistently translate to deficits in cognitive tasks, highlighting the complexity of correlating METH-induced neurochemical changes with cognitive outcomes.

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Funding

The authors received support from the NIDA-IRP and the NIA-IRP for this research. TMK was supported by an IRTA postdoctoral fellowship. CAS and CB were supported by IRTA post-baccalaureate fellowships. AHN is supported by Z1A DA000424.

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Author notes

  1. Catherine A. Schweppe

    Present address: Department of Neurology, University of California Los Angeles, 635 Charles E Young Drive South, Los Angeles, CA, 90095, USA

Authors and Affiliations

  1. Molecular Targets and Medications Discovery Branch, National Institute on Drug Abuse – Intramural Research Program, National Institutes of Health, Baltimore, 333 Cassell Drive, Baltimore, MD, 21224, USA

    Catherine A. Schweppe, Caitlin Burzynski, Eliot L. Gardner, Zheng-Xiong Xi, Amy Hauck Newman & Thomas M. Keck

  2. Molecular Neuropsychiatry Research Branch, National Institute on Drug Abuse – Intramural Research Program, National Institutes of Health, Baltimore, 333 Cassell Drive, Baltimore, MD, 21224, USA

    Subramaniam Jayanthi, Bruce Ladenheim & Jean Lud Cadet

  3. Neuroplasticity and Behavior Unit, Laboratory of Neurosciences, National Institute on Aging – Intramural Research Program, National Institutes of Health, Baltimore, MD, 21224, USA

    Henriette van Praag

  4. Department of Biomedical Science, Charles E. Schmidt College of Medicine, and Brain Institute, Florida Atlantic University, Jupiter, FL, 33458, USA

    Henriette van Praag

  5. Department of Chemistry & Biochemistry, Department of Molecular & Cellular Biosciences, College of Science and Mathematics, Rowan University, 201 Mullica Hill Road, Glassboro, NJ, 08028, USA

    Thomas M. Keck

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  1. Catherine A. Schweppe
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Correspondence to Thomas M. Keck.

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All experiments were conducted in accordance with the Guide for the Care and Use of Laboratory Animals (US National Academy of Sciences) and were approved by the Animal Care and Use Committee of the National Institute on Drug Abuse under protocols 09-CNRB-25 and 13-BNRB-48.

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Schweppe, C.A., Burzynski, C., Jayanthi, S. et al. Neurochemical and behavioral comparisons of contingent and non-contingent methamphetamine exposure following binge or yoked long-access self-administration paradigms. Psychopharmacology 237, 1989–2005 (2020). https://doi.org/10.1007/s00213-020-05513-z

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