Emerging many-to-one weighted mapping in hippocampus-amygdala network underlies memory formation

Abstract

Abstract Memories are crucial for daily life, yet the network-level organizing principles governing neural representations of experiences remain unknown. Employing dual-site in vivo recording in freely behaving male mice, here we show that hippocampal dorsal CA1 (dCA1) and basolateral amygdala (BLA) utilize distinct coding strategies for novel experiences. A small assembly of BLA neurons emerged active during memory acquisition and persisted through consolidation, whereas most dCA1 neurons were engaged in both processes. Machine learning decoding revealed that dCA1 population spikes predicted BLA assembly firing rate, suggesting that most dCA1 neurons concurrently index an episodic event by rapidly establishing weighted communication with a specific BLA assembly – a process we term “many-to-one weighted mapping.” We also found that dCA1 reactivations preceded BLA assembly activity preferably during elongated and enlarged dCA1 ripples. Using a closed-loop strategy, we demonstrated that suppressing BLA activity after large dCA1 ripples impaired memory. These findings highlight a many-to-one weighted mapping mechanism underlying both the acquisition and consolidation of new memories.