Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France, and.
Division of Vascular Neurology and Rehabilitation, Department of Neurology, University Hospital Zürich, Zürich, 8057, Switzerland.
J Neurosci. 2018 Mar 21;38(12):3026-3038. doi: 10.1523/JNEUROSCI.3058-17.2018. Epub 2018 Feb 19.
Gamma oscillations are involved in long-range coupling of distant regions that support various cognitive operations. Here we show in adult male rats that synchronized bursts of gamma oscillations bind the hippocampus (HPC) and prefrontal cortex (mPFC) during slow oscillations and slow-wave sleep, a brain state that is central for consolidation of memory traces. These gamma bursts entrained the firing of the local HPC and mPFC neuronal populations. Neurons of the nucleus reuniens (NR), which is a structural and functional hub between HPC and mPFC, demonstrated a specific increase in their firing before gamma burst onset, suggesting their involvement in HPC-mPFC binding. Chemical inactivation of NR disrupted the temporal pattern of gamma bursts and their synchronization, as well as mPFC neuronal firing. We propose that the NR drives long-range hippocampo-prefrontal coupling via gamma bursts providing temporal windows for information exchange between the HPC and mPFC during slow-wave sleep. Long-range coupling between hippocampus (HPC) and prefrontal cortex (mPFC) is believed to support numerous cognitive functions, including memory consolidation occurring during sleep. Gamma-band synchronization is a fundamental process in many neuronal operations and is instrumental in long-range coupling. Recent evidence highlights the role of nucleus reuniens (NR) in consolidation; however, how it influences hippocampo-prefrontal coupling is unknown. In this study, we show that HPC and mPFC are synchronized by gamma bursts during slow oscillations in anesthesia and natural sleep. By manipulating and recording the NR-HPC-mPFC network, we provide evidence that the NR actively promotes this long-range gamma coupling. This coupling provides the hippocampo-prefrontal circuit with a novel mechanism to exchange information during slow-wave sleep.
γ 振荡参与远距离耦合，支持各种认知操作。在这里，我们在成年雄性大鼠中表明，在慢波振荡和慢波睡眠期间，γ 振荡同步爆发将海马体（HPC）和前额叶皮层（mPFC）绑定在一起，慢波睡眠是记忆痕迹巩固的核心脑状态。这些γ 爆发使局部 HPC 和 mPFC 神经元群体的放电同步。核间回（NR）是 HPC 和 mPFC 之间的结构和功能枢纽，其神经元在 γ 爆发开始前表现出特定的放电增加，这表明它们参与了 HPC-mPFC 绑定。NR 的化学失活破坏了 γ 爆发及其同步性，以及 mPFC 神经元的放电。我们提出，NR 通过 γ 爆发驱动长程海马体-前额叶耦合，为 HPC 和 mPFC 之间在慢波睡眠期间的信息交换提供时间窗口。海马体（HPC）和前额叶皮层（mPFC）之间的长程耦合被认为支持许多认知功能，包括睡眠期间发生的记忆巩固。γ 波段同步是许多神经元操作的基本过程，对长程耦合至关重要。最近的证据强调了核间回（NR）在巩固中的作用；然而，它如何影响海马体-前额叶耦合尚不清楚。在这项研究中，我们表明在麻醉和自然睡眠期间，HPC 和 mPFC 通过 γ 爆发在慢波振荡中同步。通过操纵和记录 NR-HPC-mPFC 网络，我们提供了证据表明 NR 积极促进这种长程 γ 耦合。这种耦合为海马体-前额叶回路提供了一种在慢波睡眠期间交换信息的新机制。
