Spontaneous epileptiform activity mediated by GABA(A) receptors and gap junctions in the rat hippocampal slice following long-term exposure to GABA(B) antagonists

Neuropharmacology. 2002 Sep;43(4):563-72. doi: 10.1016/s0028-3908(02)00156-9.

Abstract

Recent evidence suggests that excessive GABA(A) receptor-mediated transmission can lead to neuronal hyperexcitability and hypersynchrony. We show now that exposure of a rat hippocampal slice to GABA(B) receptor antagonists (CGP 55845A and CGP 35348) in the absence of ionotropic glutamatergic transmission leads to a progressive synchronization of spontaneous interneuronal activity. In about 30% of over 200 slices examined, the GABA(A)-mediated spontaneous activity produced field responses in the CA1 soma region with a positive-going phase of up to 5 mV, followed by a long-lasting negative deflection with a simultaneous extracellular K(+) transient. These bicarbonate-dependent GABAergic ictal-like events (GIEs) were associated with biphasic (hyperpolarizing/depolarizing) intracellular responses and with synchronous bursting of the pyramidal neurons. The GIEs could not be reversed by wash-out of the GABA(B) receptor antagonists or by baclofen, but they were inhibited by agonists acting on presynaptic mu-opioid and cannabinoid (CB1) receptors pointing to a down-regulation of presynaptic GABA(B) receptors. GIEs were dependent on intracellular carbonic anhydrase, and potentiated by maneuvers that increase intracellular pH. They were blocked by the Cx36-specific gap-junction (gj) blocker, quinine/quinidine, as well as by the broad-spectrum gj blocker, octanol. These data suggest that enhanced GABAergic activity with functional interneuronal connectivity via gjs is sufficient to trigger epileptiform activity in the absence of ionotropic glutamatergic transmission.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • Animals
  • Carbonic Anhydrase Inhibitors / pharmacology
  • Electric Stimulation
  • Electrophysiology
  • Epilepsy / chemically induced
  • Epilepsy / physiopathology*
  • Female
  • GABA Antagonists / pharmacology*
  • Gap Junctions / drug effects
  • Gap Junctions / physiology*
  • Hippocampus / drug effects
  • Hippocampus / physiology*
  • Hydrogen-Ion Concentration
  • In Vitro Techniques
  • Interneurons / drug effects
  • Interneurons / physiology
  • Male
  • Membrane Potentials / physiology
  • Organophosphorus Compounds / pharmacology
  • Patch-Clamp Techniques
  • Phosphinic Acids / pharmacology
  • Propanolamines / pharmacology
  • Quinoxalines / pharmacology
  • Rats
  • Rats, Wistar
  • Receptors, GABA-A / drug effects
  • Receptors, GABA-A / physiology*
  • Receptors, GABA-B / drug effects
  • Receptors, GABA-B / physiology*

Substances

  • Carbonic Anhydrase Inhibitors
  • GABA Antagonists
  • Organophosphorus Compounds
  • Phosphinic Acids
  • Propanolamines
  • Quinoxalines
  • Receptors, GABA-A
  • Receptors, GABA-B
  • 2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline
  • CGP 55845A
  • 2-Amino-5-phosphonovalerate
  • CGP 35348