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Offline hippocampal reactivation during dentate spikes supports flexible memory
Neuron ( IF 14.7 ) Pub Date : 2024-09-24 , DOI: 10.1016/j.neuron.2024.08.022
Stephen B. McHugh, Vítor Lopes-dos-Santos, Manfredi Castelli, Giuseppe P. Gava, Sophie E. Thompson, Shu K.E. Tam, Katja Hartwich, Brook Perry, Robert Toth, Timothy Denison, Andrew Sharott, David Dupret

Stabilizing new memories requires coordinated neuronal spiking activity during sleep. Hippocampal sharp-wave ripples (SWRs) in the cornu ammonis (CA) region and dentate spikes (DSs) in the dentate gyrus (DG) are prime candidate network events for supporting this offline process. SWRs have been studied extensively, but the contribution of DSs remains unclear. By combining triple-ensemble (DG-CA3-CA1) recordings and closed-loop optogenetics in mice, we show that, like SWRs, DSs synchronize spiking across DG and CA principal cells to reactivate population-level patterns of neuronal coactivity expressed during prior waking experience. Notably, the population coactivity structure in DSs is more diverse and higher dimensional than that seen during SWRs. Importantly, suppressing DG granule cell spiking selectively during DSs impairs subsequent flexible memory performance during multi-object recognition tasks and associated hippocampal patterns of neuronal coactivity. We conclude that DSs constitute a second offline network event central to hippocampal population dynamics serving memory-guided behavior.

中文翻译:


齿状尖峰期间的离线海马再激活支持灵活的记忆



稳定新记忆需要在睡眠期间协调神经元尖峰活动。山毛尖波波纹 (SWR) 和齿状回 (DG) 中的齿状尖峰 (DS) 是支持此离线过程的主要候选网络事件。SWRs 已被广泛研究,但 DS 的贡献仍不清楚。通过在小鼠中结合三集成 (DG-CA3-CA1) 记录和闭环光遗传学,我们表明,与 SWR 一样,DS 在 DG 和 CA 主细胞之间同步加标,以重新激活在先前清醒经历期间表达的神经元共性细胞群水平模式。值得注意的是,DSs 中的群体共活性结构比 SWR 期间看到的更多样化和更高维。重要的是,在 DS 期间选择性地抑制 DG 颗粒细胞尖峰会损害多对象识别任务期间随后的灵活记忆性能和相关的神经元共性海马模式。我们得出结论,DSs 构成了第二个离线网络事件,它是海马群体动力学的核心,服务于记忆引导的行为。
更新日期:2024-09-24
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