CA1 hippocampal network activity changes during sleep-dependent memory consolidation.

CA1 hippocampal network activity changes during sleep-dependent memory consolidation.
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DOI:
10.3389/fnsys.2014.00061
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发表时间:
2014
影响因子:
3
通讯作者:
Aton SJ
Aton SJ
中科院分区:
医学3区
文献类型:
--
作者:
Ognjanovski N;Maruyama D;Lashner N;Zochowski M;Aton SJ

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在单次情境恐惧条件反射(CFC)后的最初几个小时内的睡眠对于脑内介导的记忆巩固是必不可少的。最近的研究揭示了记忆形成所需的细胞内机制,这些机制受到后调节睡眠和睡眠剥夺的影响。然而,几乎没有什么是已知的回路水平的活动变化,在睡眠期间,这些细胞内通路的激活的基础。在这里,我们连续记录了自由行为小鼠的CA 1区域,以表征主动记忆巩固过程中发生的神经元和网络活动变化。C57 BL/6 J小鼠植入定制的立体电极记录阵列,以监测单个CA 1神经元的活动、局部场电位(LFP)和肌电图活动。在24小时的基线记录期间,以及单次试验CFC或Sham调节后24小时,对睡眠结构和状态特异性CA 1活动模式进行评估。我们发现CFC的巩固与显著的睡眠结构变化无关,但伴随着CA 1神经元放电的长期增加,以及δ,θ和γ频率CA 1 LFP活动的增加。这些变化发生在睡眠和清醒状态,并可能在记忆形成过程中驱动海马体内的突触可塑性。我们还发现,功能连接内的CA 1网络,通过功能聚类算法(FCA)分析记录的神经元之间的尖峰定时关系进行评估,在巩固CFC变得更加稳定。这种网络稳定性的增加在假条件反射后不存在,在CFC后慢波睡眠(SWS)期间最明显,并且在CFC后觉醒期间可以忽略不计。因此,在编码和回忆之间的间隔,SWS可能通过促进CA 1网络的稳定性来稳定海马情境恐惧记忆(CFM)痕迹。
A period of sleep over the first few hours following single-trial contextual fear conditioning (CFC) is essential for hippocampally-mediated memory consolidation. Recent studies have uncovered intracellular mechanisms required for memory formation which are affected by post-conditioning sleep and sleep deprivation. However, almost nothing is known about the circuit-level activity changes during sleep that underlie activation of these intracellular pathways. Here we continuously recorded from the CA1 region of freely-behaving mice to characterize neuronal and network activity changes occurring during active memory consolidation. C57BL/6J mice were implanted with custom stereotrode recording arrays to monitor activity of individual CA1 neurons, local field potentials (LFPs), and electromyographic activity. Sleep architecture and state-specific CA1 activity patterns were assessed during a 24 h baseline recording period, and for 24 h following either single-trial CFC or Sham conditioning. We find that consolidation of CFC is not associated with significant sleep architecture changes, but is accompanied by long-lasting increases in CA1 neuronal firing, as well as increases in delta, theta, and gamma-frequency CA1 LFP activity. These changes occurred in both sleep and wakefulness, and may drive synaptic plasticity within the hippocampus during memory formation. We also find that functional connectivity within the CA1 network, assessed through functional clustering algorithm (FCA) analysis of spike timing relationships among recorded neurons, becomes more stable during consolidation of CFC. This increase in network stability was not present following Sham conditioning, was most evident during post-CFC slow wave sleep (SWS), and was negligible during post-CFC wakefulness. Thus in the interval between encoding and recall, SWS may stabilize the hippocampal contextual fear memory (CFM) trace by promoting CA1 network stability.