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Extinction of Learned Fear Induces Hippocampal Place Cell Remapping
Journal article   Open access   Peer reviewed

Extinction of Learned Fear Induces Hippocampal Place Cell Remapping

Melissa E Wang, Robin K Yuan, Alexander T Keinath, Manuel M Ramos Álvarez and Isabel A Muzzio
The Journal of neuroscience, Vol.35(24), pp.9122-9136
06/17/2015
DOI: 10.1523/JNEUROSCI.4477-14.2015
PMCID: PMC4469738
PMID: 26085635
url
https://doi.org/10.1523/JNEUROSCI.4477-14.2015View
Published (Version of record) Open Access

Abstract

The extinction of learned fear is a hippocampus-dependent process thought to embody new learning rather than erasure of the original fear memory, although it is unknown how these competing contextual memories are represented in the hippocampus. We previously demonstrated that contextual fear conditioning results in hippocampal place cell remapping and long-term stabilization of novel representations. Here we report that extinction learning also induces place cell remapping in C57BL/6 mice. Specifically, we observed cells that preferentially remapped during different stages of learning. While some cells remapped in both fear conditioning and extinction, others responded predominantly during extinction, which may serve to modify previous representations as well as encode new safe associations. Additionally, we found cells that remapped primarily during fear conditioning, which could facilitate reacquisition of the original fear association. Moreover, we also observed cells that were stable throughout learning, which may serve to encode the static aspects of the environment. The short-term remapping observed during extinction was not found in animals that did not undergo fear conditioning, or when extinction was conducted outside of the conditioning context. Finally, conditioning and extinction produced an increase in spike phase locking to the theta and gamma frequencies. However, the degree of remapping seen during conditioning and extinction only correlated with gamma synchronization. Our results suggest that the extinction learning is a complex process that involves both modification of pre-existing memories and formation of new ones, and these traces coexist within the same hippocampal representation.
Action Potentials - physiology Animals Avoidance Learning - physiology Extinction, Psychological - physiology Fear - physiology Fear - psychology Hippocampus - cytology Hippocampus - physiology Male Mice Mice, Inbred C57BL

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