Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning.
Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning.
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DOI：
10.1371/journal.pbio.1001267
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发表时间：
2012
期刊：
影响因子：
9.8
通讯作者：
Burgess N
中科院分区：
文献类型：
--
作者：
Kaplan R;Doeller CF;Barnes GR;Litvak V;Düzel E;Bandettini PA;Burgess N
一项虚拟空间导航的多模态神经成像研究将海马theta节律的作用扩展到人类记忆和自我导向学习。海马体对情景性或陈述性记忆至关重要，而θ波节律与记忆处理有关，但θ波对记忆的功能贡献仍然是激烈猜测的主题。最近的证据表明，海马体可能是意志学习的网络中枢。与人类实验相反，行为啮齿类动物海马区的电生理记录主要是反映意志运动的θ波振荡，这与空间探索和编码有关。这篇文献提出了一个令人惊讶的跨物种预测，即人类海马体的θ节律通过协调探索性运动来支持记忆，为自主学习服务。我们通过设计一个与多模态神经成像相结合的交互式人类空间导航范式，研究了θ波、空间探索和记忆编码之间的联系。我们使用非侵入性全头部脑磁图（MEG）来观察θ波振荡，使用功能性磁共振成像（fMRI）来观察与意志运动和学习相关的大脑区域。我们发现，在虚拟运动的自我启动过程中，θ波能量增加，并且与随后的记忆表现和环境熟悉度相关。在静态的导航前检索阶段观察到与表现相关的海马体θ波增加，在此阶段进行后续导航计划。此外，在显示运动相关θ波增加的任务期间，显示副海马体的fMRI活动减少，而海马体和其他大脑区域的活动增加，这些区域与先前观察到的意志学习网络显著重叠（在平稳时期，可以看到相反的模式）。这些功能磁共振成像的变化也与参与者的表现有关。我们的研究结果表明，人类海马体的θ节律通过协调探索性运动来支持记忆，为自主学习服务。这些发现直接将海马体在啮齿动物空间探索中的作用扩展到人类记忆和自主学习。大脑区域内和区域间的神经活动可以在不同的频率范围内振荡（如α、γ和θ频率），这些不同的频率范围与不同的功能相关。例如，在行为端正的啮齿动物中，海马体中的θ波节律（4-12赫兹）在运动开始时非常突出，并且与空间探索有关。然而，最近在人类身上的证据表明，人类的海马体参与指导自主学习。这表明，人类海马体的θ节律通过协调探索性运动来支持记忆，为自主学习服务。在这项研究中，我们通过使用虚拟导航范式，结合非侵入性记录和功能成像技术，测试了在啮齿动物海马中发现的与运动启动相关的θ波节律是否存在人类类似物。我们的记录显示，确实，θ波能量的增加与运动启动有关。我们还研究了与记忆编码的关系，我们发现与检索前计划相关的海马体θ振荡预测了记忆表现。成像结果显示，在完成任务的过程中，与运动相关的θ波也显示出海马体以及其他与自主学习相关的大脑区域的活动增加。这些发现直接将海马θ节律在啮齿动物空间探索中的作用扩展到人类记忆和自主学习。
A multimodal neuroimaging study of virtual spatial navigation extends the role of the hippocampal theta rhythm to human memory and self-directed learning. The hippocampus is crucial for episodic or declarative memory and the theta rhythm has been implicated in mnemonic processing, but the functional contribution of theta to memory remains the subject of intense speculation. Recent evidence suggests that the hippocampus might function as a network hub for volitional learning. In contrast to human experiments, electrophysiological recordings in the hippocampus of behaving rodents are dominated by theta oscillations reflecting volitional movement, which has been linked to spatial exploration and encoding. This literature makes the surprising cross-species prediction that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. We examined the links between theta, spatial exploration, and memory encoding by designing an interactive human spatial navigation paradigm combined with multimodal neuroimaging. We used both non-invasive whole-head Magnetoencephalography (MEG) to look at theta oscillations and Functional Magnetic Resonance Imaging (fMRI) to look at brain regions associated with volitional movement and learning. We found that theta power increases during the self-initiation of virtual movement, additionally correlating with subsequent memory performance and environmental familiarity. Performance-related hippocampal theta increases were observed during a static pre-navigation retrieval phase, where planning for subsequent navigation occurred. Furthermore, periods of the task showing movement-related theta increases showed decreased fMRI activity in the parahippocampus and increased activity in the hippocampus and other brain regions that strikingly overlap with the previously observed volitional learning network (the reverse pattern was seen for stationary periods). These fMRI changes also correlated with participant's performance. Our findings suggest that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. These findings directly extend the role of the hippocampus in spatial exploration in rodents to human memory and self-directed learning. Neural activity both within and across brain regions can oscillate in different frequency ranges (such as alpha, gamma, and theta frequencies), and these different ranges are associated with distinct functions. In behaving rodents, for example, theta rhythms (4–12 Hz) in the hippocampus are prominent during the initiation of movement and have been linked to spatial exploration. Recent evidence in humans, however, suggests that the human hippocampus is involved in guiding self-directed learning. This suggests that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. In this study, we tested whether there is a human analogue for the movement-initiation-related theta rhythm found in the rodent hippocampus by using a virtual navigation paradigm, combined with non-invasive recordings and functional imaging techniques. Our recordings showed that, indeed, theta power increases are linked to movement initiation. We also examined the relationship to memory encoding, and we found that hippocampal theta oscillations related to pre-retrieval planning predicted memory performance. Imaging results revealed that periods of the task showing movement-related theta also showed increased activity in the hippocampus, as well as other brain regions associated with self-directed learning. These findings directly extend the role of the hippocampal theta rhythm in rodent spatial exploration to human memory and self-directed learning.
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DOI：
10.1523/jneurosci.6021-09.2010
发表时间：
2010-05-26
期刊：
The Journal of neuroscience : the official journal of the Society for Neuroscience
影响因子：
--
作者：
Brown TI;Ross RS;Keller JB;Hasselmo ME;Stern CE
通讯作者：
Stern CE
影响因子：
5.3
作者：
Cornwell, Brian R.;Johnson, Linda L.;Grillon, Christian
通讯作者：
Grillon, Christian
DOI：
10.1073/pnas.1014528108
发表时间：
2011-06-28
影响因子：
11.1
作者：
Addante, Richard J.;Watrous, Andrew J.;Ranganath, Charan
通讯作者：
Ranganath, Charan
影响因子：
2.6
作者：
Abrahams, S;Pickering, A;Morris, RG
通讯作者：
Morris, RG
影响因子：
16.2
作者：
Adhikari, Avishek;Topiwala, Mihir A.;Gordon, Joshua A.
通讯作者：
Gordon, Joshua A.