Commutative Properties of Head Direction Cells during Locomotion in 3D: Are All Routes Equal?
Commutative Properties of Head Direction Cells during Locomotion in 3D: Are All Routes Equal?
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DOI：
10.1523/jneurosci.2789-19.2020
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发表时间：
2020-02
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影响因子：
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通讯作者：
Patrick Lachance;Julie R. Dumont;Pelin Ozel;Jennifer L Marcroft;J. Taube
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作者：
Patrick Lachance;Julie R. Dumont;Pelin Ozel;Jennifer L Marcroft;J. Taube
导航通常需要在三维(3D)空间中移动。最近的研究假设了头部方向(HD)细胞如何编码3D空间的两种不同的模型：旋转平面假设和双轴模型。为了区分这些模型，我们记录了雌性大鼠的HD细胞，当它们沿着水平和垂直表面从高架平台到立方体装置顶部的不同路线时。导航通常需要在三维(3D)空间中移动。最近的研究假设了头部方向(HD)细胞如何编码3D空间的两种不同的模型：旋转平面假设和双轴模型。为了区分这些模型，我们记录了雌性大鼠的HD细胞，当它们沿着水平和垂直表面从高架平台到立方体装置顶部的不同路线时。我们比较了HD细胞在不同平面上的首选放电方向(PFD)，并解决了HD细胞放电是否具有交换性的问题--动物路线的顺序是否会影响细胞PFD的最终结果？大鼠通过一个、两个或三个垂直墙从地板移动到立方体顶部的直接或间接路线。虽然旋转平面假说解释了动物穿越水平拐角时的PFD移动，但当动物穿越垂直拐角时，细胞的PFD可以用双轴模型更好地解释。反应也遵循双轴模型(1)在黑暗条件下，(2)大鼠被动运动，(3)在器官旋转后，(4)绕内垂直角运动，(5)跨越45°外垂直角。动物穿过不同平面的顺序并没有影响细胞的PFD结果，这表明反应是互换的。HD细胞的峰值放电率在每个表面上基本相等。这些发现表明，动物相对于重力的方向在决定细胞的PFD方面起着重要作用，前庭和本体感觉线索推动了这些计算。意义陈述在三维(3D)世界中导航是一项复杂的任务，需要保持相对于局部和全局线索的适当方向感。啮齿动物头部方向(HD)细胞被认为是这种定向感的辅助细胞，但大多数HD细胞的研究集中在2D环境中的导航。我们研究了当大鼠在多个垂直和水平方向的平面之间移动时，HD细胞的反应，证明HD细胞的方向表征在几个实验条件下都与局部(当前运动平面)和全局(重力)线索对齐，包括黑暗和被动运动。这些发现为哺乳动物大脑中3D空间的处理提供了关键的见解。
Navigation often requires movement in three-dimensional (3D) space. Recent studies have postulated two different models for how head direction (HD) cells encode 3D space: the rotational plane hypothesis and the dual-axis model. To distinguish these models, we recorded HD cells in female rats while they traveled different routes along both horizontal and vertical surfaces from an elevated platform to the top of a cuboidal apparatus. Navigation often requires movement in three-dimensional (3D) space. Recent studies have postulated two different models for how head direction (HD) cells encode 3D space: the rotational plane hypothesis and the dual-axis model. To distinguish these models, we recorded HD cells in female rats while they traveled different routes along both horizontal and vertical surfaces from an elevated platform to the top of a cuboidal apparatus. We compared HD cell preferred firing directions (PFDs) in different planes and addressed the issue of whether HD cell firing is commutative—does the order of the animal's route affect the final outcome of the cell's PFD? Rats locomoted a direct or indirect route from the floor to the cube top via one, two, or three vertical walls. Whereas the rotational plane hypothesis accounted for PFD shifts when the animal traversed horizontal corners, the cell's PFD was better explained by the dual-axis model when the animal traversed vertical corners. Responses also followed the dual-axis model (1) under dark conditions, (2) for passive movement of the rat, (3) following apparatus rotation, (4) for movement around inside vertical corners, and (5) across a 45° outside vertical corner. The order in which the animal traversed the different planes did not affect the outcome of the cell's PFD, indicating that responses were commutative. HD cell peak firing rates were generally equivalent along each surface. These findings indicate that the animal's orientation with respect to gravity plays an important role in determining a cell's PFD, and that vestibular and proprioceptive cues drive these computations. SIGNIFICANCE STATEMENT Navigating in a three-dimensional (3D) world is a complex task that requires one to maintain a proper sense of orientation relative to both local and global cues. Rodent head direction (HD) cells have been suggested to subserve this sense of orientation, but most HD cell studies have focused on navigation in 2D environments. We investigated the responses of HD cells as rats moved between multiple vertically and horizontally oriented planar surfaces, demonstrating that HD cells align their directional representations to both local (current plane of locomotion) and global (gravity) cues across several experimental conditions, including darkness and passive movement. These findings offer critical insights into the processing of 3D space in the mammalian brain.