Systems consolidation induces flexible egocentric-allocentric recall for observational fear memory

Abstract Observers can learn to fear the context where they witnessed a demonstrator’s aversive events, a socially-transmitted learning called observational contextual fear conditioning (CFC), which is essential for survival. While observers should recall memory of observational CFC from their (egocentric) perspective or a demonstrator’s (allocentric) perspective depending on ecological contexts, the neural mechanisms remain unclear. Here, we show that remote observational CFC memory is both egocentrically and allocentrically recalled, whereas recent observational CFC memory is only egocentrically recalled. Egocentric recall of recent observational CFC memory requires dorsal hippocampus activity, while, surprisingly, both egocentric and allocentric recall of remote observational CFC memory requires the medial prefrontal cortex (mPFC)-basolateral amygdala pathway. Finally, mPFC activity during observational CFC is necessary for remote, but not recent, egocentric and allocentric recall of observational CFC memory. Our data provide new insights into flexible recall strategies of observational CFC memory and functional reorganization of circuits underlying memory consolidation.