Hydrogen peroxide modulates neuronal excitability and membrane properties in ventral horn neurons of the rat spinal cord

Neuroscience. 2016 Sep 7:331:206-20. doi: 10.1016/j.neuroscience.2016.06.033. Epub 2016 Jun 23.

Abstract

Hydrogen peroxide (H2O2), a reactive oxygen species, is an important signaling molecule for synaptic and neuronal activity in the central nervous system; it is produced excessively in brain ischemia and spinal cord injury. Although H2O2-mediated modulations of synaptic transmission have been reported in ventral horn (VH) neurons of the rat spinal cord, the effects of H2O2 on neuronal excitability and membrane properties remain poorly understood. Accordingly, the present study investigated such effects using a whole-cell patch-clamp technique. The bath-application of H2O2 decreased neuronal excitability accompanied by decreased input resistance, firing frequency, and action potential amplitude and by increased rheobase. These H2O2-mediated changes were induced by activation of extrasynaptic, but not synaptic, GABAA receptors. Indeed, GABAergic tonic currents were enhanced by H2O2. On the other hand, the amplitude of medium and slow afterhyperpolarization (mAHP and sAHP), which plays important roles in controlling neuronal excitability and is mediated by small-conductance calcium-activated potassium (SK) channels, was significantly decreased by H2O2. When extrasynaptic GABAA receptors were completely blocked, these decreases of mAHP and sAHP persisted, and H2O2 increased excitability, suggesting that H2O2 per se might have the potential to increase neuronal excitability via decreased SK channel conductance. These findings indicate that activating extrasynaptic GABAA receptors or SK channels may attenuate acute neuronal damage caused by H2O2-induced hyperexcitability and therefore represent a novel therapeutic target for the prevention and treatment of H2O2-induced motor neuron disorders.

Keywords: afterhyperpolarization; extrasynaptic GABA(A) receptor; patch clamp; small-conductance calcium-activated potassium channel; tonic current.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anterior Horn Cells / drug effects
  • Anterior Horn Cells / physiology*
  • Bicuculline / pharmacology
  • Dose-Response Relationship, Drug
  • Hydrogen Peroxide / metabolism*
  • Hydrogen Peroxide / pharmacology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology*
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology
  • Neurotransmitter Agents / pharmacology
  • Patch-Clamp Techniques
  • Rats, Wistar
  • Receptors, GABA-A / metabolism
  • Receptors, Glycine / metabolism
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism
  • Strychnine / pharmacology
  • Synapses / drug effects
  • Synapses / metabolism
  • Tissue Culture Techniques
  • gamma-Aminobutyric Acid / metabolism
  • gamma-Aminobutyric Acid / pharmacology

Substances

  • Neurotransmitter Agents
  • Receptors, GABA-A
  • Receptors, Glycine
  • Small-Conductance Calcium-Activated Potassium Channels
  • gamma-Aminobutyric Acid
  • Hydrogen Peroxide
  • Strychnine
  • Bicuculline