Kainate receptor-mediated inhibition of presynaptic Ca2+ influx and EPSP in area CA1 of the rat hippocampus

J Physiol. 1998 Jun 15;509 ( Pt 3)(Pt 3):833-45. doi: 10.1111/j.1469-7793.1998.833bm.x.

Abstract

1. The effect of a low concentration (1 microM) of kainate (kainic acid; KA) on presynaptic calcium (Ca2+) influx at the Schaffer collateral-commissural (SCC) synapse was examined in rat hippocampal slices. 2. Following selective loading of the presynaptic terminals with the fluorescent Ca2+ indicator rhod-2 AM, transient increases in the presynaptic Ca2+ concentration (pre[Ca2+]t) and field excitatory postsynaptic potentials (EPSPs) evoked by electrical stimulation of the SCC pathway were recorded simultaneously. 3. Bath application of 1 microM KA reversibly suppressed field EPSPs and pre[Ca2+]t to 37.7 +/- 4.0 % and 72.9 +/- 2.4 % of control, respectively. Excitatory postsynaptic currents (EPSCs) recorded with the use of the whole-cell patch-clamp technique were also suppressed by 1 microM KA to 42.6 +/- 6.3 % of control. A quantitative analysis of the decreases in pre[Ca2+]t and the amplitude of field EPSP during KA application suggests that KA inhibits transmission primarily by reducing the pre[Ca2+]t. 4. Consistent with a presynaptic site for these effects, paired-pulse facilitation (PPF) was enhanced by 1 microM KA. 5. A substantial KA-induced suppression of NMDA receptor-mediated EPSPs was detected when AMPA receptors were blocked by the AMPA receptor-selective antagonist GYKI 52466 (100 microM). 6. The suppressive effect of KA on field EPSPs and pre[Ca2+]t was antagonized by the KA antagonist NS-102 (10 microM). 7. These results suggest that the presynaptic inhibitory action of KA at the hippocampal CA1 synapse is primarily due to the inhibition of Ca2+ influx into the presynaptic terminals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Animals
  • Anti-Anxiety Agents*
  • Benzodiazepines / pharmacology
  • Calcium / metabolism*
  • Calcium / pharmacokinetics
  • Excitatory Amino Acid Agonists / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Hippocampus / chemistry
  • Hippocampus / cytology
  • Hippocampus / physiology*
  • Indoles / pharmacology
  • Kainic Acid / analogs & derivatives
  • Kainic Acid / pharmacology
  • Neuromuscular Depolarizing Agents / pharmacology
  • Oximes / pharmacology
  • Patch-Clamp Techniques
  • Presynaptic Terminals / chemistry*
  • Presynaptic Terminals / physiology
  • Rats
  • Rats, Wistar
  • Receptors, Kainic Acid / physiology*
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Rhodamines
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology

Substances

  • Anti-Anxiety Agents
  • Excitatory Amino Acid Agonists
  • Excitatory Amino Acid Antagonists
  • Indoles
  • Neuromuscular Depolarizing Agents
  • Oximes
  • Receptors, Kainic Acid
  • Receptors, N-Methyl-D-Aspartate
  • Rhodamines
  • GYKI 52466
  • Benzodiazepines
  • 5-nitro-6,7,8,9-tetrahydrobenzo(G)indole-2,3-dione-3-oxime
  • domoic acid
  • Kainic Acid
  • Calcium