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Memory supporting inter-regional networks among preconfigured local ensembles developed through experience.
Hiroyuki Miyawaki (Hiroyuki Miyawaki, Kenji Mizuseki)

Animals acquire memory through experience and change their behavior by retrieving the memory. Memory is represented as a combination of simultaneously activated neurons within a brain region, as known as a neuronal ensemble. Memory-related ensembles have been reported in various brain regions, which indicates elements of a given memory are parallelly processed in multiple brain regions. However, it is still elusive how the brain integrates the information distributed across multiple regions. To investigate this point, we performed large-scale electrophysiological recordings in the amygdala, ventral hippocampus, and prefrontal cortex of fear-conditioned rats.
We found that the local ensembles activated during fear conditioning are inter-regionally coactivated during the subsequent sleep periods. However, such coactivations are not detected during the sleep periods preceding the conditioning sessions. During memory retrieval, the coactivations reappeared, together with the fast oscillations. Both during sleep periods and memory retrieval sessions, the coactivations cooccurred with brief bouts of fast network oscillations in the involved regions. We also revealed that local ensembles participating in the inter-regional coactivation were configured prior to memory acquisition in the amygdala and prefrontal cortex.
Our findings suggest that preconfigured local ensembles in various brain regions instantly encode elements of a given memory, whereas inter-regional networks for information integration develop in an experience-dependent manner. The newly developed inter-regional network might change the meaning tied to a given ensemble, which supports memory.

Miyawaki, H., Mizuseki, K. De novo inter-regional coactivations of preconfigured local ensembles support memory. Nature Communications 13: 1272, 2022.

Schematic diagram showing dynamics of local and inter-regional networks. Coactivations of the amygdala–prefrontal ensemble pairs developed during conditioning, while those of the hippocampus–prefrontal cortex emerged during the subsequent sleep periods. These inter-regional coactivations were hosted by fast network oscillations such as hippocampal sharp-wave ripples (SWRs), amygdala high-frequency oscillations (HFOs), and prefrontal cortical ripples (cRipples). In the amygdala and prefrontal cortex, ensembles participating in the coactivation were configured prior to conditioning.

Department of Physiology, Graduate School of Medicine, Osaka City University, Japan