Page Hector J I, Wilson Jonathan J, Jeffery Kate J
Institute of Behavioural Neuroscience, Department of Experimental Psychology, Division of Psychology and Language Sciences, University College London , London , United Kingdom.
J Neurophysiol. 2018 Jan 1;119(1):192-208. doi: 10.1152/jn.00501.2017. Epub 2017 Oct 11.
In the mammalian brain, allocentric (Earth-referenced) head direction, called azimuth, is encoded by head direction (HD) cells, which fire according to the facing direction of the animal's head. On a horizontal surface, rotations of the head around the dorsoventral (D-V) axis, called yaw, correspond to changes in azimuth and elicit appropriate updating of the HD "compass" signal to enable large-scale navigation. However, if the animal moves through three-dimensional (3D) space then there is no longer a simple relationship between yaw rotations and azimuth changes, and so processing of 3D rotations is needed. Construction of a global 3D compass would require complex integration of 3D rotations, and also a large neuronal population, most neurons of which would be silent most of the time since animals rarely sample all available 3D orientations. We propose that, instead, the HD system treats the 3D space as a set of interrelated 2D surfaces. It could do this by updating activity according to both yaw rotations around the D-V axis and rotations of the D-V axis around the gravity-defined vertical axis. We present preliminary data to suggest that this rule operates when rats move between walls of opposing orientations. This dual-axis rule, which we show is straightforward to implement using the classic one-dimensional "attractor" architecture, allows consistent representation of azimuth even in volumetric space and thus may be a general feature of mammalian directional computations even for animals that swim or fly. NEW & NOTEWORTHY Maintaining a sense of direction is complicated when moving in three-dimensional (3D) space. Head direction cells, which update the direction sense based on head rotations, may accommodate 3D movement by processing both rotations of the head around the axis of the animal's body and rotations of the head/body around gravity. With modeling we show that this dual-axis rule works in principle, and we present preliminary data to support its operation in rats.
在哺乳动物大脑中,以自我为中心(以地球为参照)的头部方向,即方位角,由头部方向(HD)细胞编码,这些细胞根据动物头部的朝向方向放电。在水平面上,头部围绕背腹(D-V)轴的旋转,即偏航,对应于方位角的变化,并引发HD“罗盘”信号的适当更新,以实现大规模导航。然而,如果动物在三维(3D)空间中移动,那么偏航旋转与方位角变化之间就不再存在简单的关系,因此需要对3D旋转进行处理。构建一个全局3D罗盘需要对3D旋转进行复杂的整合,并且还需要大量的神经元群体,其中大多数神经元在大多数时间都是沉默的,因为动物很少对所有可用的3D方向进行采样。我们提出,相反,HD系统将3D空间视为一组相互关联的2D表面。它可以通过根据围绕D-V轴的偏航旋转以及D-V轴围绕重力定义的垂直轴的旋转来更新活动来做到这一点。我们提供的初步数据表明,当大鼠在相反方向的墙壁之间移动时,该规则会起作用。我们表明,使用经典的一维“吸引子”架构可以直接实现这种双轴规则,即使在体积空间中也能一致地表示方位角,因此即使对于游泳或飞行的动物,这也可能是哺乳动物方向计算的一个普遍特征。新内容与值得注意之处 在三维(3D)空间中移动时,保持方向感很复杂。基于头部旋转更新方向感的头部方向细胞可以通过处理头部围绕动物身体轴的旋转以及头部/身体围绕重力的旋转来适应3D运动。通过建模我们表明,这种双轴规则原则上是有效的,并且我们提供了初步数据来支持其在大鼠中的运作。