Dynamic synchronization between hippocampal representations and stepping.

Dynamic synchronization between hippocampal representations and stepping.
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DOI:
10.1038/s41586-023-05928-6
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发表时间:
2023-05
期刊:
影响因子:
64.8
通讯作者:
Frank, Loren M.
Frank, Loren M.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Joshi, Abhilasha;Denovellis, Eric L.;Mankili, Abhijith;Meneksedag, Yagiz;Davidson, Thomas J.;Gillespie, Anna K.;Guidera, Jennifer A.;Roumis, Demetris;Frank, Loren M.

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海马体是哺乳动物大脑中表达空间表征的结构,对导航至关重要。导航,反过来,错综复杂地依赖于运动,然而,目前的帐户表明海马空间表征和运动过程的细节之间的分离。具体来说,海马体被认为主要代表高阶认知和运动变量,如位置,速度和运动方向,而推动动物的肢体运动可以主要在皮层下回路中计算和表示,包括脊髓,脑干和小脑。海马的表征是否真的与运动过程的详细结构脱钩仍然未知。为了解决这个问题,在这里,我们同时监测海马的空间表示和正在进行的肢体运动基础运动在快速的时间尺度。我们发现,在自由行为的大鼠前肢步进周期是有节奏的,在运动过程中在8 Hz左右达到峰值,匹配运动过程中海马活动和空间表征的约8 Hz调制。我们还发现,前肢触地的时间(踏步周期的“植物”时间)与海马体对空间的表征之间存在精确的时间协调。值得注意的是,植物时间与最接近大鼠鼻子实际位置的海马表示一致,而在这些植物时间之间,海马表示朝向可能的未来位置发展。当大鼠接近空间决策时,这种同步是特别可检测的。总之,我们的研究结果揭示了一个深刻的和动态的协调在几十毫秒的时间尺度之间的中央认知表征和外围运动过程。这种协调与认知需求迅速联系和分离,非常适合支持认知和感觉运动回路之间的快速信息交换。大鼠实验表明,海马体中的空间表征与前肢步进周期密切协调,特别是当空间决策接近时,并提供了对这种同步如何支持信息处理的见解。
The hippocampus is a mammalian brain structure that expresses spatial representations and is crucial for navigation. Navigation, in turn, intricately depends on locomotion; however, current accounts suggest a dissociation between hippocampal spatial representations and the details of locomotor processes. Specifically, the hippocampus is thought to represent mainly higher-order cognitive and locomotor variables such as position, speed and direction of movement, whereas the limb movements that propel the animal can be computed and represented primarily in subcortical circuits, including the spinal cord, brainstem and cerebellum. Whether hippocampal representations are actually decoupled from the detailed structure of locomotor processes remains unknown. To address this question, here we simultaneously monitored hippocampal spatial representations and ongoing limb movements underlying locomotion at fast timescales. We found that the forelimb stepping cycle in freely behaving rats is rhythmic and peaks at around 8 Hz during movement, matching the approximately 8 Hz modulation of hippocampal activity and spatial representations during locomotion. We also discovered precisely timed coordination between the time at which the forelimbs touch the ground (‘plant’ times of the stepping cycle) and the hippocampal representation of space. Notably, plant times coincide with hippocampal representations that are closest to the actual position of the nose of the rat, whereas between these plant times, the hippocampal representation progresses towards possible future locations. This synchronization was specifically detectable when rats approached spatial decisions. Together, our results reveal a profound and dynamic coordination on a timescale of tens of milliseconds between central cognitive representations and peripheral motor processes. This coordination engages and disengages rapidly in association with cognitive demands and is well suited to support rapid information exchange between cognitive and sensory–motor circuits. Experiments in rats show that spatial representations in the hippocampus are closely coordinated with the forelimb stepping cycle, particularly when spatial decisions are approaching, and provide insight into how this synchronization supports information processing.
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