Reversible plasticity of fear memory-encoding amygdala synaptic circuits even after fear memory consolidation

PLoS One. 2011;6(9):e24260. doi: 10.1371/journal.pone.0024260. Epub 2011 Sep 19.

Abstract

It is generally believed that after memory consolidation, memory-encoding synaptic circuits are persistently modified and become less plastic. This, however, may hinder the remaining capacity of information storage in a given neural circuit. Here we consider the hypothesis that memory-encoding synaptic circuits still retain reversible plasticity even after memory consolidation. To test this, we employed a protocol of auditory fear conditioning which recruited the vast majority of the thalamic input synaptic circuit to the lateral amygdala (T-LA synaptic circuit; a storage site for fear memory) with fear conditioning-induced synaptic plasticity. Subsequently the fear memory-encoding synaptic circuits were challenged with fear extinction and re-conditioning to determine whether these circuits exhibit reversible plasticity. We found that fear memory-encoding T-LA synaptic circuit exhibited dynamic efficacy changes in tight correlation with fear memory strength even after fear memory consolidation. Initial conditioning or re-conditioning brought T-LA synaptic circuit near the ceiling of their modification range (occluding LTP and enhancing depotentiation in brain slices prepared from conditioned or re-conditioned rats), while extinction reversed this change (reinstating LTP and occluding depotentiation in brain slices prepared from extinguished rats). Consistently, fear conditioning-induced synaptic potentiation at T-LA synapses was functionally reversed by extinction and reinstated by subsequent re-conditioning. These results suggest reversible plasticity of fear memory-encoding circuits even after fear memory consolidation. This reversible plasticity of memory-encoding synapses may be involved in updating the contents of original memory even after memory consolidation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala / cytology
  • Amygdala / drug effects
  • Amygdala / physiology*
  • Animals
  • Conditioning, Classical / physiology
  • Excitatory Amino Acid Agents / pharmacology
  • Excitatory Postsynaptic Potentials / physiology
  • Extinction, Psychological / physiology
  • Fear / physiology
  • Glycine / analogs & derivatives
  • Glycine / pharmacology
  • Long-Term Potentiation / physiology
  • Male
  • Memory / physiology*
  • Neural Pathways / physiology
  • Neuronal Plasticity / physiology*
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Resorcinols / pharmacology
  • Synaptic Potentials / physiology
  • Synaptic Transmission / physiology*
  • Thalamus / cytology
  • Thalamus / drug effects
  • Thalamus / physiology

Substances

  • Excitatory Amino Acid Agents
  • Resorcinols
  • 3,5-dihydroxyphenylglycine
  • Glycine