Extinction of cued fear memory involves a distinct form of depotentiation at cortical input synapses onto the lateral amygdala

Ingie Hong, Beomjong Song, Sukwon Lee, Jihye Kim, Jeongyeon Kim, Sukwoo Choi

Research output: Contribution to journalArticlepeer-review

Abstract

The amygdala is known to be a critical storage site of conditioned fear memory. Among the two major pathways to the lateral amygdala (LA), the cortical pathway is known to display a presynaptic long-term potentiation which is occluded with fear conditioning. Here we show that fear extinction results in a net depression of conditioning-induced potentiation at cortical input synapses onto the LA (C-LA synapses). Fear conditioning induced a significant potentiation of excitatory postsynaptic currents at C-LA synapses compared with naïve and unpaired controls, whereas extinction apparently reversed this potentiation. Paired-pulse low-frequency stimulation (pp-LFS) induced synaptic depression in the C-LA pathway of fear-conditioned rats, but not in naïve or unpaired controls, indicating that the pp-LFS-induced depression is specific to associative learning-induced changes (pp-LFS-induced depotentiation ex vivo). Importantly, extinction occluded pp-LFS-induced depotentiationex vivo, suggesting that extinction shares some mechanisms with the depotentiation. pp-LFS-induced depotentiation ex vivo required NMDA receptor (NMDAR) activity, consistent with a previous finding that blockade of amygdala NMDARs impaired fear extinction. In addition, pp-LFS-induced depotentiationex vivo required activity of group II metabotropic glutamate receptors (mGluRs), known to be present at presynaptic terminals, but not AMPAR internalization, consistent with a presynaptic mechanism for pp-LFS-induced depotentiationex vivo. This result is in contrast with another form of ex vivo depotentiation in the thalamic pathway that requires both group I mGluR activity and AMPAR internalization. We thus suggest that extinction of conditioned fear involves a distinct form of depotentiation at C-LA synapses, which depends upon both NMDARs and group II mGluRs.

Original languageEnglish (US)
Pages (from-to)2089-2099
Number of pages11
JournalEuropean Journal of Neuroscience
Volume30
Issue number11
DOIs
StatePublished - Dec 2009
Externally publishedYes

Keywords

  • Amygdala
  • Cortico-amygdala pathway
  • Depotentiation
  • Fear extinction
  • NMDA receptor
  • Rat

ASJC Scopus subject areas

  • Neuroscience(all)

Fingerprint

Dive into the research topics of 'Extinction of cued fear memory involves a distinct form of depotentiation at cortical input synapses onto the lateral amygdala'. Together they form a unique fingerprint.

Cite this