Biphasic mechanisms of amphetamine action at the dopamine terminal

J Neurosci. 2014 Apr 16;34(16):5575-82. doi: 10.1523/JNEUROSCI.4050-13.2014.

Abstract

In light of recent studies suggesting that amphetamine (AMPH) increases electrically evoked dopamine release ([DA]o), we examined discrepancies between these findings and literature that has demonstrated AMPH-induced decreases in [DA]o. The current study has expanded the inventory of AMPH actions by defining two separate mechanisms of AMPH effects on [DA]o at high and low doses, one dopamine transporter (DAT) independent and one DAT dependent, respectively. AMPH concentrations were measured via microdialysis in rat nucleus accumbens after intraperitoneal injections of 1 and 10 mg/kg and yielded values of ∼10 and 200 nM, respectively. Subsequently, voltammetry in brain slices was used to examine the effects of low (10 nM), moderate (100 nM), and high (10 μM) concentrations of AMPH across a range of frequency stimulations (one pulse; five pulses, 20 Hz; 24 pulses, 60 Hz). We discovered biphasic, concentration-dependent effects in WT mice, in which AMPH increased [DA]o at low concentrations and decreased [DA]o at high concentrations across all stimulation types. However, in slices from DAT-KO mice, [DA]o was decreased by all concentrations of AMPH, demonstrating that AMPH-induced increases in [DA]o are DAT dependent, whereas the decreases at high concentrations are DAT independent. We propose that low AMPH concentrations are insufficient to disrupt vesicular sequestration, and therefore AMPH acts solely as a DAT inhibitor to increase [DA]o. When AMPH concentrations are high, the added mechanism of vesicular depletion leads to reduced [DA]o. The biphasic mechanisms observed here confirm and extend the traditional actions of AMPH, but do not support mechanisms involving increased exocytotic release.

Keywords: dopamine transporter; knock-out; nucleus accumbens; phasic; tonic; voltammetry.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amphetamine / metabolism
  • Amphetamine / pharmacology*
  • Animals
  • Biophysical Phenomena / drug effects*
  • Dopamine / metabolism*
  • Dopamine Plasma Membrane Transport Proteins / deficiency
  • Dopamine Uptake Inhibitors / pharmacology*
  • Dose-Response Relationship, Drug
  • Fenfluramine / pharmacology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • In Vitro Techniques
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nucleus Accumbens / drug effects*
  • Nucleus Accumbens / metabolism*
  • Rats
  • Serotonin Agents / pharmacology
  • Time Factors

Substances

  • Dopamine Plasma Membrane Transport Proteins
  • Dopamine Uptake Inhibitors
  • Serotonin Agents
  • Fenfluramine
  • Amphetamine
  • Dopamine