Hippocampal-amygdala memory circuits govern experience-dependent observational fear

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

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Pages (from-to)1416-1431.e13
JournalNeuron
Volume110
Issue number8
DOIs
StatePublished - Apr 20 2022

Keywords

  • amygdala
  • anterior cingulate cortex
  • contextual fear conditioning
  • emotional empathy
  • hippocampus
  • memory engram cells
  • observational fear
  • perception-action coupling
  • social memory

ASJC Scopus subject areas

  • Neuroscience(all)

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