Intrinsic excitability changes in amygdala neurons following observational fear conditioning in mice

Abstract

Observational fear conditioning (OFC) is used to study the social transmission of aversive information within a social context. In a typical experiment, observers exhibit defensive responses after witnessing a demonstrator’s reaction to repeated footshocks. Despite its relevance to socially acquired fear, the underlying cellular plasticity remain poorly understood. In this study, we investigated changes in the intrinsic excitability of amygdala neurons following OFC. In Experiment 1, we classified amygdala neurons into burst, regular and late-firing types, and found that burst-firing neurons in the basolateral amygdala (BLA) and late-firing neurons in the central amygdala (CeA) of the observer mice showed increased intrinsic neuronal excitability. In Experiment 2, we found that intrinsic excitability changes in both BLA and CeA neurons were selectively enhanced when observers witnessed the demonstrator’s high-frequency jumping behavior, but not freezing. In Experiment 3, an opaque wall and a distractor were used to investigate the role of visual transmission during OFC. Although both the opaque wall and the distractor blocked observer’s fear response, burst-firing BLA neurons in the distractor group nonetheless exhibited enhanced excitability, whereas late-firing CeA neurons did not. These findings suggest that amygdala subpopulations play dissociable roles in OFC: burst-firing BLA neurons appear to be involved in processing emotionally salient sensory cues, while late-firing CeA neurons appear to mediate the expression of socially acquired fear.