Arc expression identifies the lateral amygdala fear memory trace

Mol Psychiatry. 2016 Mar;21(3):364-75. doi: 10.1038/mp.2015.18. Epub 2015 Mar 24.

Abstract

Memories are encoded within sparsely distributed neuronal ensembles. However, the defining cellular properties of neurons within a memory trace remain incompletely understood. Using a fluorescence-based Arc reporter, we were able to visually identify the distinct subset of lateral amygdala (LA) neurons activated during auditory fear conditioning. We found that Arc-expressing neurons have enhanced intrinsic excitability and are preferentially recruited into newly encoded memory traces. Furthermore, synaptic potentiation of thalamic inputs to the LA during fear conditioning is learning-specific, postsynaptically mediated and highly localized to Arc-expressing neurons. Taken together, our findings validate the immediate-early gene Arc as a molecular marker for the LA neuronal ensemble recruited during fear learning. Moreover, these results establish a model of fear memory formation in which intrinsic excitability determines neuronal selection, whereas learning-related encoding is governed by synaptic plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation / adverse effects
  • Action Potentials / drug effects
  • Action Potentials / genetics
  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Basolateral Nuclear Complex / cytology
  • Basolateral Nuclear Complex / metabolism*
  • Central Nervous System Stimulants / pharmacology
  • Choline O-Acetyltransferase / metabolism
  • Conditioning, Classical / physiology*
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Fear / physiology*
  • Glutamate Decarboxylase / metabolism
  • In Vitro Techniques
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Memory / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons / physiology
  • Patch-Clamp Techniques
  • Phosphopyruvate Hydratase / metabolism
  • Picrotoxin / pharmacology
  • Proto-Oncogene Proteins c-fos / metabolism

Substances

  • Bacterial Proteins
  • Central Nervous System Stimulants
  • Cytoskeletal Proteins
  • Luminescent Proteins
  • Nerve Tissue Proteins
  • Proto-Oncogene Proteins c-fos
  • activity regulated cytoskeletal-associated protein
  • yellow fluorescent protein, Bacteria
  • Picrotoxin
  • Choline O-Acetyltransferase
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1
  • Phosphopyruvate Hydratase