Extinction recall of fear memories formed before stress is not affected despite amygdalar hyperactivity

Abstract

Stress is known to exert its detrimental effects not only by enhancing fear, but also by impairing its extinction. However, in earlier studies stress exposure invariably preceded both processes. Thus, compared to unstressed animals, stressed animals had to extinguish fear memories from higher levels of freezing caused by prior exposure to stress. Here we decouple the two processes to examine if stress specifically impairs fear extinction. Strikingly, when fear memories were formed before stress exposure, thereby allowing animals to initiate extinction from comparable levels of fear, recall of fear extinction was unaffected. Despite this we observed a persistent increase in theta activity in the BLA. Theta activity in the mPFC, by contrast, was normal. Stress also disrupted mPFC-BLA theta-frequency synchrony and directional coupling. Thus, in the absence of the fear-enhancing effects of stress, the expression of fear reflects normal regulation of mPFC activity, not stress-induced hyperactivity in the amygdala.