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Dentate Gyrus Sharp Waves, a Local Field Potential Correlate of Learning in the Dentate Gyrus of Mice.
Journal of Neuroscience ( IF 4.4 ) Pub Date : 2020-09-09 , DOI: 10.1523/jneurosci.2275-19.2020
Kolja Meier 1, 2 , Andrea Merseburg 2, 3 , Dirk Isbrandt 3, 4 , Stephan Lawrence Marguet 2, 3 , Fabio Morellini 1
Affiliation  

The hippocampus plays an essential role in learning. Each of the three major hippocampal subfields, dentate gyrus (DG), CA3, and CA1, has a unique function in memory formation and consolidation, and also exhibit distinct local field potential (LFP) signatures during memory consolidation processes in non-rapid eye movement (NREM) sleep. The classic LFP events of the CA1 region, sharp-wave ripples (SWRs), are induced by CA3 activity and considered to be an electrophysiological biomarker for episodic memory. In LFP recordings along the dorsal CA1-DG axis from sleeping male mice, we detected and classified two types of LFP events in the DG: high-amplitude dentate spikes (DSs), and a novel event type whose current source density (CSD) signature resembled that seen during CA1 SWR, but which, most often, occurred independently of them. Because we hypothesize that this event type is similarly induced by CA3 activity, we refer to it as dentate sharp wave (DSW). We show that both DSWs and DSs differentially modulate the electrophysiological properties of SWR and multiunit activity (MUA). Following two hippocampus-dependent memory tasks, DSW occurrence rates, ripple frequencies, and ripple and sharp wave (SW) amplitudes were increased in both, while SWR occurrence rates in dorsal CA1 increased only after the spatial task. Our results suggest that DSWs, like SWRs, are induced by CA3 activity and that DSWs complement SWRs as a hippocampal LFP biomarker of memory consolidation.

SIGNIFICANCE STATEMENT Awake experience is consolidated into long-term memories during sleep. Memory consolidation crucially depends on sharp-wave ripples (SWRs), which are local field potential (LFP) patterns in hippocampal CA1 that increase after learning. The dentate gyrus (DG) plays a central role in the process of memory formation, prompting us to cluster sharp waves (SWs) in the DG [dentate SWs (DSWs)] during sleep. We show that both DSW coupling to CA1 SWRs, and their occurrence rates, robustly increase after learning trials. Our results suggest that the DG is directly affected by memory consolidation processes. DSWs may thus complement SWRs as a sensitive electrophysiological biomarker of memory consolidation in mice.



中文翻译:

Dentate Gyrus Sharp Waves(Dentate Gyrus尖锐波),是小鼠Dentate Gyrus中与学习相关的局部场电位。

海马在学习中起着至关重要的作用。海马的三个主要子域齿状回(DG),CA3和CA1在记忆形成和巩固中具有独特的功能,并且在非快速眼动的记忆巩固过程中还表现出独特的局部场电位(LFP)信号(NREM)睡觉。CA1区域诱发了CA1区域的经典LFP事件,即尖波波纹(SWR),被认为是情节记忆的电生理生物标记。在睡眠中的雄性小鼠的沿背CA1-DG轴的LFP记录中,我们在DG中检测并分类了两种类型的LFP事件:高振幅齿状尖峰(DSs)和一种新型事件类型,其电流源密度(CSD)签名与在CA1 SWR期间看到的情况相似,但最常见的情况是与它们无关。因为我们假设该事件类型是由CA3活性类似地诱导的,所以我们将其称为齿状尖波(DSW)。我们表明,DSWs和DSs差异地调节SWR和多单元活动(MUA)的电生理特性。继两项海马依赖性记忆任务后,DSW发生率,脉动频率以及脉动和锐波(SW)幅度均增加,而背侧CA1的SWR发生率仅在执行空间任务后才增加。我们的结果表明,DSW与SWR一样,是由CA3活性诱导的,并且DSW是SWR的补充,是记忆整合的海马LFP生物标志物。我们表明,DSWs和DSs差异地调节SWR和多单元活动(MUA)的电生理特性。继两项海马依赖性记忆任务后,DSW发生率,脉动频率以及脉动和锐波(SW)幅度均增加,而背侧CA1的SWR发生率仅在执行空间任务后才增加。我们的结果表明,DSW与SWR一样,是由CA3活性诱导的,并且DSW是SWR的补充,是记忆整合的海马LFP生物标记。我们表明,DSWs和DSs差异地调节SWR和多单元活动(MUA)的电生理特性。继两项海马依赖性记忆任务后,DSW发生率,脉动频率以及脉动和锐波(SW)幅度均增加,而背侧CA1的SWR发生率仅在执行空间任务后才增加。我们的结果表明,DSW与SWR一样,是由CA3活性诱导的,并且DSW是SWR的补充,是记忆整合的海马LFP生物标记。

重要声明睡眠中的清醒经历被整合为长期记忆。内存整合至关重要地取决于尖波波纹(SWR),它们是海马CA1中的局部场电势(LFP)模式,在学习后会增加。齿状回(DG)在记忆形成过程中起着核心作用,促使我们在睡眠过程中在DG [齿状SW(DSW)]中聚集尖锐的波(SW)。我们显示,在学习试验后,DSW与CA1 SWR的耦合及其发生率均稳步提高。我们的结果表明DG直接受内存合并过程的影响。因此,DSW可以补充SWR,作为小鼠记忆整合的敏感电生理生物标志物。

更新日期:2020-09-10
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