Role of Ionotropic Glutamate Receptors in Long-Term Potentiation in Rat Hippocampal CA1 Oriens-Lacunosum Moleculare Interneurons

J Neurosci. 2009 Jan 28;29(4):939-50. doi: 10.1523/JNEUROSCI.3251-08.2009.

Abstract

Some interneurons of the hippocampus exhibit NMDA receptor-independent long-term potentiation (LTP) that is induced by presynaptic glutamate release when the postsynaptic membrane potential is hyperpolarized. This "anti-Hebbian" form of LTP is prevented by postsynaptic depolarization or by blocking AMPA and kainate receptors. Although both AMPA and kainate receptors are expressed in hippocampal interneurons, their relative roles in anti-Hebbian LTP are not known. Because interneuron diversity potentially conceals simple rules underlying different forms of plasticity, we focus on glutamatergic synapses onto a subset of interneurons with dendrites in stratum oriens and a main ascending axon that projects to stratum lacunosum moleculare, the oriens-lacunosum moleculare (O-LM) cells. We show that anti-Hebbian LTP in O-LM interneurons has consistent induction and expression properties, and is prevented by selective inhibition of AMPA receptors. The majority of the ionotropic glutamatergic synaptic current in these cells is mediated by inwardly rectifying Ca(2+)-permeable AMPA receptors. Although GluR5-containing kainate receptors contribute to synaptic currents at high stimulus frequency, they are not required for LTP induction. Glutamatergic synapses on O-LM cells thus behave in a homogeneous manner and exhibit LTP dependent on Ca(2+)-permeable AMPA receptors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anesthetics, Local / pharmacology
  • Animals
  • Biophysics
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • GABA Antagonists / pharmacology
  • Hippocampus / cytology*
  • In Vitro Techniques
  • Interneurons / drug effects
  • Interneurons / physiology*
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology*
  • Lysine / analogs & derivatives
  • Lysine / metabolism
  • Male
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology
  • Patch-Clamp Techniques / methods
  • Phosphinic Acids / pharmacology
  • Picrotoxin / pharmacology
  • Propanolamines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, AMPA / physiology*
  • Receptors, Kainic Acid / physiology*
  • Tetrodotoxin / pharmacology

Substances

  • Anesthetics, Local
  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Phosphinic Acids
  • Propanolamines
  • Receptors, AMPA
  • Receptors, Kainic Acid
  • Picrotoxin
  • CGP 55845A
  • Tetrodotoxin
  • biocytin
  • Lysine