De novo inter-regional coactivations of preconfigured local ensembles support memory

Neuronal ensembles in the amygdala, ventral hippocampus, and prefrontal cortex are involved in fear memory; however, how inter-regional ensemble interactions support memory remains elusive. Using multi-regional large-scale electrophysiology in the aforementioned structures of fear-conditioned rats, we found that the local ensembles activated during fear memory acquisition are inter-regionally coactivated during the subsequent sleep period, which relied on brief bouts of fast network oscillations. During memory retrieval, the coactivations reappeared, together with fast oscillations. Coactivation-participating-ensembles were configured prior to memory acquisition in the amygdala and prefrontal cortex but developed through experience in the hippocampus. Our findings suggest that elements of a given memory are instantly encoded within various brain regions in a preconfigured manner, whereas hippocampal ensembles and the network for inter-regional integration of the distributed information develop in an experience-dependent manner to form a new memory, which is consistent with the hippocampal memory index hypothesis. The authors show that fear-memory-related cell-ensembles in the amygdala, hippocampus, and prefrontal cortex are inter-regionally co-activated in post-learning sleep. The co-activations are hosted by fast network oscillations and re-appear during recall.

Automated summary

This study reveals that neuronal ensembles activated during fear memory acquisition in the amygdala, ventral hippocampus, and prefrontal cortex are inter-regionally coactivated during sleep, with the help of fast network oscillations. These coactivations reappear during memory retrieval. The ensembles in the amygdala and prefrontal cortex are configured prior to memory acquisition, while those in the hippocampus develop through experience.