Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies.
Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies.
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DOI：
10.1126/science.abf3119
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发表时间：
2021-04-02
期刊：
影响因子：
--
通讯作者：
Buzsáki G
中科院分区：
文献类型：
--
作者：
Fernández-Ruiz A;Oliva A;Soula M;Rocha-Almeida F;Nagy GA;Martin-Vazquez G;Buzsáki G
学习诱导大脑回路的动态重组，但这一过程背后的神经元机制还不清楚。区域间伽马频率振荡（~30至130 Hz）已被假定为精确协调上游和下游神经元集合的机制，例如，在海马系统中。外侧（LEC）和内侧（MEC）内嗅皮层接收来自两个不同的皮层层次流（“什么”和“哪里”路径）的输入，并将这些神经元信息传递给海马。然而，这些信息被海马回路包装、整合或分离的机制还有待探索。在上游区域的伽马时间帧内发射的神经元组件可以最有效地释放它们的下游伙伴。这种伽马时间尺度的组织对于生理功能来说似乎是必不可少的，因为损害海马体中尖峰的精确定时的操作通常会影响行为。然而，在适当的行为情况下，不同的伽马频率通信的直接支持是缺失的。为了使生理操作更接近于行为，我们设计了“空间”和“对象”学习任务，并研究了MEC和LEC输入与海马齿状回中的目标神经元组件之间的γ频率通信的选择性参与。我们将这些相关的观察结果与LEC和MEC中γ振荡的光遗传学扰动相结合，分别测试它们在通路特异性神经元通信和学习中的作用。在空间学习，快速伽马（100至150赫兹）振荡同步MEC和齿状回和夹带主要颗粒细胞。在对象的学习，缓慢的伽马（30至50赫兹）振荡同步LEC和齿状回，并优先招募苔藓细胞和CA 3锥体神经元，建议任务特定的路由MEC和LEC消息的形式，选定的细胞类型的伽马周期尖峰包。低频和高频伽马子带分别在齿状分子层的外三分之一和中三分之一中占主导地位，并且它们的振幅最大值被锁定到θ振荡的不同阶段。MEC和LEC的γ频率光遗传学扰动分别导致空间和物体学习任务中的学习障碍。在相同的动物中，齿状层特定的低和高频率的伽马子带和尖峰-伽马LFP耦合被选择性地减少，再加上齿状神经元的空间和对象相关参数的恶化。这些研究结果表明，MEC和LEC和海马细胞组件之间的独特的γ频率特异性通信是路由任务相关信息的关键，我们的选择性γ波段扰动实验表明，它们支持学习的特定方面。我们假设，发送神经元的信息隔离伽马频率载波允许一个目标“读者”区，以消除歧义收敛输入。总的来说，这些结果表明，特定的投射伽马模式以特定于任务的方式动态地参与大脑区域中功能相关的细胞组装。不同神经元群体的任务特异性参与和伽马频率耦合。第一行：MEC（左）和LEC（右）的伽马频率扰动期间的空间（左）和对象（右）学习受损。第二行：MEC和LEC项目的高频（gammaF）和低频（gammaS）的伽马振荡DG，分别和夹带颗粒细胞，苔藓细胞，和CA 3锥体神经元的任务特异性的方式。伽马振荡被认为是协调跨大脑区域的功能专门化神经元集合的尖峰时间。为了验证这一假设，我们光遗传学扰动伽马尖峰定时在大鼠内侧（MEC）和外侧（LEC）内嗅皮层和空间和对象学习任务，分别发现损伤。MEC和LEC同步与海马齿状回通过高和低γ频率的节奏，分别从事颗粒细胞或苔藓细胞和CA 3锥体细胞的任务依赖性的方式。γ扰动破坏了学习诱导的目标神经元组装组织。我们的研究结果表明，特定的路径γ振荡路由任务相关的信息之间的不同的神经元亚群内鼻-海马电路。我们假设区域间伽玛时间尺度的尖峰协调是神经元通信的一种机制。
Learning induces a dynamic reorganization of brain circuits but the neuronal mechanisms underlying this process are not well understood. Interregional gamma-frequency oscillations (~30 to 130 Hz) have been postulated as a mechanism to precisely coordinate upstream and downstream neuronal ensembles, for example, in the hippocampal system. The lateral (LEC) and medial (MEC) entorhinal cortex receive inputs from two distinct streams of cortical hierarchy (the “what” and the “where” paths) and convey these neuronal messages to the hippocampus. However, the mechanisms by which such messages are packaged and integrated or segregated by hippocampal circuits had yet to be explored. Neuronal assemblies firing within gamma time frames in an upstream region can most effectively discharge their downstream partners. This gamma-time-scale organization appears essential for physiological functions because manipulations that impair precision timing of spikes in the hippocampus often affect behavior. However, direct support for distinct gamma-frequency communication in appropriate behavioral situations is missing. To bring physiological operations closer to behavior, we designed “spatial” and “object” learning tasks and examined the selective engagement of gamma-frequency communication between the MEC and LEC inputs and their target neuronal assemblies in the hippocampal dentate gyrus. We combined these correlational observations with optogenetic perturbation of gamma oscillations in LEC and MEC, respectively, to test their roles in pathway-specific neuronal communication and learning. During spatial learning, fast gamma (100 to 150 Hz) oscillations synchronized MEC and dentate gyrus and entrained predominantly granule cells. During object learning, slow gamma (30 to 50 Hz) oscillations synchronized LEC and dentate gyrus and preferentially recruited mossy cells and CA3 pyramidal neurons, suggesting task-specific routing of MEC and LEC messages in the form of gamma-cycle-spike packets of selected cell types. The low- and high-frequency gamma sub-bands were dominant in the outer and middle third of the dentate molecular layer, respectively, and their amplitude maxima were locked to different phases of theta oscillation. Gamma frequency optogenenetic perturbation of MEC and LEC led to learning impairments in a spatial and object learning task, respectively. In the same animals, the dentate layer–specific low- and high-frequency gamma sub-bands and spike-gamma LFP coupling were selectively reduced, coupled with deterioration of spatial and object-related parameters of dentate neurons. These findings demonstrate that distinct gamma-frequency-specific communication between MEC and LEC and the hippocampal cell assemblies are critical for routing task-relevant information, and our selective gamma-band perturbation experiments suggest that they support specific aspects of learning. We hypothesize that sending neuronal messages by segregated gamma-frequency carriers allows a target “reader” area to disambiguate convergent inputs. In general, these results demonstrate that specific projected gamma patterns dynamically engage functionally related cell assemblies across brain regions in a task-specific manner. Task-specific engagement and gamma-frequency coupling of distinct neuronal populations. First row: Impairment of spatial (left) and object (right) learning during gamma-frequency perturbation of MEC (left) and LEC (right). Second row: MEC and LEC project high-frequency (gammaF) and low-frequency (gammaS) gamma oscillations to DG, respectively, and entrain granule cells, mossy cells, and CA3 pyramidal neurons in a task-specific manner. Gamma oscillations are thought to coordinate the spike timing of functionally specialized neuronal ensembles across brain regions. To test this hypothesis, we optogenetically perturbed gamma spike timing in the rat medial (MEC) and lateral (LEC) entorhinal cortices and found impairments in spatial and object learning tasks, respectively. MEC and LEC were synchronized with the hippocampal dentate gyrus through high- and low-gamma-frequency rhythms, respectively, and engaged either granule cells or mossy cells and CA3 pyramidal cells in a task-dependent manner. Gamma perturbation disrupted the learning-induced assembly organization of target neurons. Our findings imply that pathway-specific gamma oscillations route task-relevant information between distinct neuronal subpopulations in the entorhinal-hippocampal circuit. We hypothesize that interregional gamma-time-scale spike coordination is a mechanism of neuronal communication.
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影响因子：
16.2
作者：
Bosman CA;Schoffelen JM;Brunet N;Oostenveld R;Bastos AM;Womelsdorf T;Rubehn B;Stieglitz T;De Weerd P;Fries P
通讯作者：
Fries P
影响因子：
25
作者：
Dupret, David;O'Neill, Joseph;Pleydell-Bouverie, Barty;Csicsvari, Jozsef
通讯作者：
Csicsvari, Jozsef
影响因子：
16.2
作者：
Danielson NB;Turi GF;Ladow M;Chavlis S;Petrantonakis PC;Poirazi P;Losonczy A
通讯作者：
Losonczy A
影响因子：
25
作者：
Connor CE;Knierim JJ
通讯作者：
Knierim JJ
影响因子：
13.9
作者：
Buzsáki G;Wang XJ
通讯作者：
Wang XJ