Cited by 117Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchMemory Processes and Influences

Hippocampal-amygdala memory circuits govern experience-dependent observational fear

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Terranova, Joseph I., Yokose, Jun, Osanai, Hisayuki, Marks, William D., Yamamoto, Jun, Ogawa, Sachie K., Kitamura, Takashi·2022·Neuron

Abstract

The empathic ability to vicariously experience the other's fearful situation, a process called observational fear (OF), is critical to survive in nature and function in society. OF can be facilitated by both prior similar fear experience in the observer and social familiarity with the demonstrator. However, the neural circuit mechanisms of experience-dependent OF (Exp OF) remain unknown. Here, we demonstrate that hippocampal-basolateral amygdala (HPC-BLA) circuits in mice without involving the anterior cingulate cortex, considered a center of OF, mediate Exp OF. Dorsal HPC neurons generate fear memory engram cells in BLA encoding prior similar fear experiences, which are essential for Exp OF. On the other hand, ventral HPC neurons respond to the familiar demonstrator's aversive situation during Exp OF, which reactivates the fear memory engram cells in BLA to elicit Exp OF. Our study provides new insights into the memory engram-dependent perception-action coupling that underlies empathic behaviors like Exp OF.

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Crossref · 10.1016/j.neuron.2022.01.019

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  • Hippocampal-to-basolateral amygdala circuits are necessary for enhanced social fear learning in mice that previously experienced a footshock.

    “Recently hippocampal-to-BLA circuits were found to be necessary for enhanced social fear learning in mice that previously experienced a footshock [108].”

    From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [108]

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  1. Roy DS, Park Y-G, Ogawa SK, Cho JH, Choi H, Kamensky L, Martin J, Chung K, and Tonegawa S (2019). Brain-wide mapping of contextual fear memory engram ensembles supports the dispersed engram complex hypothesis. bioRxiv, 668483.

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Authors
Terranova, J. I., Yokose, J., Osanai, H., Marks, W. D., Yamamoto, J., Ogawa, S. K., & Kitamura, T.
Affiliations
The University of Texas Southwestern Medical Center (US)
Venue
Neuron
Publisher
Elsevier BV
Published
2022-04
Volume
110
Issue
8
Pages
1416-1431.e13
ISSN
0896-6273 (ISSN-L)
OpenAlex
W4210843030
Cited by
117
References
115
Citations by year
2026: 27 · 2025: 35 · 2024: 21 · 2023: 23 · 2022: 11
FWCI
11.60
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Uehara Memorial Foundation
  • National Institute of Mental Health (F32MH119721, F32MH122082, R01MH120134, R01MH125916, T32MH076690)
  • Japan Society for the Promotion of Science (201860198)
  • National Institute on Drug Abuse (T32DA007290)
  • Daiichi Sankyo Foundation of Life Science
  • Brain and Behavior Research Foundation (26391, 28801)
  • Brain Research Foundation (BRFSG-2018-04)
  • Whitehall Foundation (2019-05-38)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
hippocampus, basolateral amygdala, empathy, social familiarity, perception-action coupling, anterior cingulate cortex
MeSH terms
Amygdala, Animals, Fear, Gyrus Cinguli, Hippocampus, Mice, Basolateral Nuclear Complex

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