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Cited by 49Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchParkinson's Disease Mechanisms and Treatments

Amphetamine Elicits Opposing Actions on Readily Releasable and Reserve Pools for Dopamine

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Covey, Dan P., Juliano, Steven A., Garris, Paul A.·2013·PLoS ONE
DOI 10.1371/journal.pone.0060763PMC PMC3643976
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Abstract

Amphetamine, a highly addictive drug with therapeutic efficacy, exerts paradoxical effects on the fundamental communication modes employed by dopamine neurons in modulating behavior. While amphetamine elevates tonic dopamine signaling by depleting vesicular stores and driving non-exocytotic release through reverse transport, this psychostimulant also activates phasic dopamine signaling by up-regulating vesicular dopamine release. We hypothesized that these seemingly incongruent effects arise from amphetamine depleting the reserve pool and enhancing the readily releasable pool. This novel hypothesis was tested using in vivo voltammetry and stimulus trains of varying duration to access different vesicular stores. We show that amphetamine actions are stimulus dependent in the dorsal striatum. Specifically, amphetamine up-regulated vesicular dopamine release elicited by a short-duration train, which interrogates the readily releasable pool, but depleted release elicited by a long-duration train, which interrogates the reserve pool. These opposing actions of vesicular dopamine release were associated with concurrent increases in tonic and phasic dopamine responses. A link between vesicular depletion and tonic signaling was supported by results obtained for amphetamine in the ventral striatum and cocaine in both striatal sub-regions, which demonstrated augmented vesicular release and phasic signals only. We submit that amphetamine differentially targeting dopamine stores reconciles the paradoxical activation of tonic and phasic dopamine signaling. Overall, these results further highlight the unique and region-distinct cellular mechanisms of amphetamine and may have important implications for its addictive and therapeutic properties.

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  • Amphetamine increases synaptic extracellular dopamine and norepinephrine levels.

    “The main mechanism of action of AMP is to increase synaptic extracellular DA and NE levels (44, 52, 59, 60, 67, 68, 71, 78, 80, 85, 87, 94, 105, 107, 128).”

    From The pharmacology of amphetamine and methylphenidate: Relevance to the neurobiology of attention-deficit/hyperactivity disorder and other psychiatric comorbidities (2018) · cites this paper as [52]

    The Introduction (page unavailable) says amphetamine enhances dopamine signaling through transporter reversal, reduced uptake, and increased vesicular release. The Discussion also describes increases in extracellular dopamine transients. Our copy does not establish an increase in norepinephrine, so it supports only the dopamine part of the claim. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • The primary pharmacologic effect of both amphetamine and methylphenidate is to increase central dopamine and norepinephrine activity.

    “The primary pharmacologic effect of both amphetamine and methylphenidate is to increase central dopamine and norepinephrine activity, which impacts executive and attentional function.”

    From The pharmacology of amphetamine and methylphenidate: Relevance to the neurobiology of attention-deficit/hyperactivity disorder and other psychiatric comorbidities (2018) · cites this paper as [52]

    The Introduction and Results section on phasic dopamine signaling report that amphetamine increases dopamine signaling. The paper does not establish the corresponding claim for methylphenidate or increased norepinephrine activity; methylphenidate appears in the supplied evidence only in a reference. Page numbers are unavailable in our copy. (LLM, conf=0.88)

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  • Amphetamine's effect on synaptic dopamine and norepinephrine is mediated by inhibition of dopamine and norepinephrine transporters, reducing reuptake.

    “This effect is mediated by inhibition of DA transporters (DAT) and NE transporters (NET) (44, 52, 58), which reduces the reuptake of these molecules from the synapse.”

    From The pharmacology of amphetamine and methylphenidate: Relevance to the neurobiology of attention-deficit/hyperactivity disorder and other psychiatric comorbidities (2018) · cites this paper as [52]

    The Results section ('Psychostimulant effects on vesicular dopamine release and dopamine uptake'; page not provided) reports that amphetamine significantly decreased dopamine uptake in both striatal regions, and the Introduction links amphetamine to inhibited dopamine uptake. The cited paper does not establish the claim about norepinephrine transporters (NET) or reduced norepinephrine reuptake. (LLM, conf=0.88)

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Authors
Covey, D. P., Juliano, S. A., & Garris, P. A.
Affiliations
Illinois State University (US)
Corresponding author
Garris, Paul A.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-05-03
Volume
8
Issue
5
Pages
e60763
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0060763
PMC
PMC3643976
OpenAlex
W2030500089
Cited by
49
References
81
Citations by year
2025: 2 · 2024: 4 · 2023: 3 · 2022: 1 · 2021: 7 · 2020: 3 · 2019: 4 · 2018: 2 · 2017: 5 · 2016: 8 · 2015: 5 · 2014: 3 · 2013: 2
FWCI
2.94
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ISU Red - Research and eData (Illinois State University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (0754615)
  • Illinois State University
  • National Institutes of Health
  • National Institute on Drug Abuse (R03DA021770, DA021770)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Keywords
amphetamine, dopamine release, readily releasable pool, reserve pool, dorsal striatum, ventral striatum, cocaine, psychostimulants, dopaminergic neurons, in vivo voltammetry
MeSH terms
Action Potentials, Central Nervous System Stimulants, Animals, Cocaine, Corpus Striatum, Dextroamphetamine, Dopamine, Electric Stimulation, Male, Synaptic Transmission, Rats, Sprague-Dawley, Dopamine Uptake Inhibitors, Secretory Vesicles, Rats, Dopaminergic Neurons

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