Early adenosine release contributes to hypoxia-induced disruption of stimulus-induced sharp wave-ripple complexes in rat hippocampal area CA3

Eur J Neurosci. 2015 Jul;42(2):1808-17. doi: 10.1111/ejn.12941. Epub 2015 Jun 12.

Abstract

We investigated the effects of hypoxia on sharp wave-ripple complex (SPW-R) activity and recurrent epileptiform discharges in rat hippocampal slices, and the mechanisms underlying block of this activity. Oxygen levels were measured using Clark-style oxygen sensor microelectrodes. In contrast to recurrent epileptiform discharges, oxygen consumption was negligible during SPW-R activity. These network activities were reversibly blocked when oxygen levels were reduced to 20% or less for 3 min. The prolongation of hypoxic periods to 6 min caused reversible block of SPW-Rs during 20% oxygen and irreversible block when 0% oxygen (anoxia) was applied. In contrast, recurrent epileptiform discharges were more resistant to prolonged anoxia and almost fully recovered after 6 min of anoxia. SPW-Rs were unaffected by the application of 1-butyl-3-(4-methylphenylsulfonyl) urea, a blocker of KATP channels, but they were blocked by activation of adenosine A1 receptors. In support of a modulatory function of adenosine, the amplitude and incidence of SPW-Rs were increased during application of the A1 receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine (DPCPX). Interestingly, hypoxia decreased the frequency of miniature excitatory post-synaptic currents in CA3 pyramidal cells, an effect that was converted into increased frequency by the adenosine A1 agonist DPCPX. In addition, DPCPX also delayed the onset of hypoxia-mediated block of SPW-Rs. Our data suggest that early adenosine release during hypoxia induces a decrease in pre-synaptic glutamate release and that both might contribute to transient block of SPW-Rs during hypoxia/anoxia in area CA3.

Keywords: adenosine A1 receptor; brain slice; oxygen consumption; recurrent epileptiform discharges.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / metabolism
  • Adenosine A1 Receptor Antagonists / pharmacology
  • Animals
  • Bicuculline / pharmacology
  • CA3 Region, Hippocampal / physiology*
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology*
  • Female
  • GABA-A Receptor Antagonists / pharmacology
  • Hypoxia / physiopathology*
  • In Vitro Techniques
  • Nerve Net / drug effects
  • Nerve Net / physiology*
  • Oxygen / metabolism
  • Patch-Clamp Techniques
  • Pyramidal Cells / physiology*
  • Quinoxalines / pharmacology
  • Rats
  • Rats, Wistar
  • Valine / analogs & derivatives
  • Valine / pharmacology
  • Xanthines / pharmacology

Substances

  • Adenosine A1 Receptor Antagonists
  • Excitatory Amino Acid Antagonists
  • GABA-A Receptor Antagonists
  • Quinoxalines
  • Xanthines
  • FG 9041
  • 2-amino-5-phosphopentanoic acid
  • 1,3-dipropyl-8-cyclopentylxanthine
  • Valine
  • Adenosine
  • Oxygen
  • Bicuculline