Highlights

•Hippocampal activity during remote recall is essential for systems reconsolidation

•New hippocampal engram cells are recruited for systems reconsolidation

•Adult neurogenesis is necessary for the recruitment of new hippocampal engrams

•Systems reconsolidation enables memory updating with new information

Recalling systems-consolidated neocortex-dependent remote memories re-engages the hippocampus in a process called systems reconsolidation. However, underlying mechanisms, particularly for the origin of the reinstated hippocampal memory engram, remain elusive. By developing a triple-event labeling tool and employing two-photon imaging, we trace hippocampal engram ensembles from memory acquisition to systems reconsolidation and find that remote recall recruits a new engram ensemble in the hippocampus for subsequent memory retrieval. Consistently, recruiting new engrams is supported by adult hippocampal neurogenesis-mediated silencing of original engrams. This new engram ensemble receives currently experienced contextual information, incorporates new information into the remote memory, and supports remote memory updating. Such a reconstructed hippocampal memory is then integrated with the valence of remote memory via medial prefrontal cortex projection-mediated activity coordination between the hippocampus and amygdala. Thus, the reconstruction of new memory engrams underlies systems reconsolidation, which explains how remote memories are updated with new information.