Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala

Nature. 1998 Aug 13;394(6694):683-7. doi: 10.1038/29312.

Abstract

Fear conditioning is a paradigm that has been used as a model for emotional learning in animals. The cellular correlate of fear conditioning is thought to be associative N-methyl-D-aspartate (NMDA) receptor-dependent synaptic plasticity within the amygdala. Here we show that glutamatergic synaptic transmission to inhibitory interneurons in the basolateral amygdala is mediated solely by alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors. In contrast to AMPA receptors at inputs to pyramidal neurons, these receptors have an inwardly rectifying current-voltage relationship, indicative of a high permeability to calcium. Tetanic stimulation of inputs to interneurons caused an immediate and sustained increase in the efficacy of these synapses. This potentiation required a rise in postsynaptic calcium, but was independent of NMDA receptor activation. The potentiation of excitatory inputs to interneurons was reflected as an increase in the amplitude of the GABA(A)-mediated inhibitory synaptic current in pyramidal neurons. These results demonstrate that excitatory synapses onto interneurons within a fear conditioning circuit show NMDA-receptor independent long-term potentiation. This plasticity might underlie the increased synchronization of activity between neurons in the basolateral amygdala after fear conditioning.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala / cytology
  • Amygdala / physiology*
  • Animals
  • Calcium / metabolism*
  • Cell Membrane Permeability
  • Conditioning, Classical / physiology
  • Electrophysiology
  • Evoked Potentials
  • Fear / physiology
  • In Vitro Techniques
  • Interneurons / physiology*
  • Long-Term Potentiation / physiology*
  • Neural Inhibition
  • Neurons / physiology
  • Patch-Clamp Techniques
  • Potassium / metabolism
  • Rats
  • Rats, Wistar
  • Receptors, AMPA / chemistry
  • Receptors, AMPA / physiology*
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Synaptic Transmission / physiology
  • gamma-Aminobutyric Acid / physiology

Substances

  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • gamma-Aminobutyric Acid
  • glutamate receptor ionotropic, AMPA 2
  • Potassium
  • Calcium