scholarly journals A proposed rule for updating of the head direction cell reference frame following rotations in three dimensions

2016 ◽  
Author(s):  
Jonathan Wilson ◽  
Hector Page ◽  
Kate Jeffery

In the mammalian brain, allocentric (Earth-referenced) heading direction, called azimuth, is encoded by head direction (HD) cells, which fire according to the facing direction of the rat's head. If the animal is on a horizontal surface then egocentric (self-referenced) rotations of the head around the dorso-ventral axis, called yaw, correspond to changes in azimuth, and elicit appropriate updating of the HD signal. However, if the surface is sloping steeply then yaw rotations no longer map linearly to changes in azimuth. The brain could solve this problem simply by always firing according to direction on the local (sloping) surface instead; however, if the animal moves between surfaces having different compass orientations then errors would accumulate in the subsequent azimuth signal. These errors could be avoided if the HD system instead combines two updating rules: yaw rotations around the D-V axis and rotations of the D-V axis around the gravity-defined vertical axis. We show here that when rats move between vertical walls of different orientations then HD cells indeed rotate their activity by an amount corresponding to the amount of vertical-axis rotation. With modelling, we then show how this reference-frame rotation, which may be driven by inputs from the vestibular nuclei or vestibulocerebellum, allows animals to maintain a simple yaw-based updating rule while on a given plane, but also to avoid accumulation of heading errors when moving between planes.

2018 ◽  
Vol 119 (1) ◽  
pp. 192-208 ◽  
Author(s):  
Hector J. I. Page ◽  
Jonathan J. Wilson ◽  
Kate J. Jeffery

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.


1992 ◽  
Vol 2 (1) ◽  
pp. 1-14
Author(s):  
Charles Schnabolk ◽  
Theodore Raphan

Off-vertical-axis rotation (OVAR) in darkness generates continuous compensatory eye velocity. No model has yet been presented that defines the signal processing necessary to estimate head velocity in three dimensions for arbitrary rotations during OVAR. The present study develops a model capable of estimating all 3 components of head velocity in space accurately. It shows that processing of two patterns of otolith activation, one delayed with respect to the other, for each plane of eye movement is not sufficient. (A pattern in this context is an array of signals emanating from the otoliths. Each component of the array is a signal corresponding to a class of otolith hair cells with a given polarization vector as described by Tou and Gonzalez in 1974.) The key result is that estimation of head velocity in space can be achieved by processing three temporally displaced patterns, each representing a sampling of gravity as the head rotates. A vector cross product of differences between pairs of the sampled gravity vectors implements the estimation. An interesting property of this model is that the component of velocity about the axis of rotation reduces to that derived previously using the pattern estimator model described by Raphan and Schnabolk in 1988 and Fanelli et al in 1990. This study suggests that the central nervous system (CNS) maintains a current as well as 2 delayed representations of gravity at every head orientation during rotation. It also suggests that computing vector cross products and implementing delays may be fundamental operations in the CNS for generating orientation information associated with motion.


2019 ◽  
Vol 121 (1) ◽  
pp. 4-37 ◽  
Author(s):  
Michael E. Shinder ◽  
Jeffrey S. Taube

Head direction (HD) cells fire when the animal faces that cell’s preferred firing direction (PFD) in the horizontal plane. The PFD response when the animal is oriented outside the earth-horizontal plane could result from cells representing direction in the plane of locomotion or as a three-dimensional (3D), global-referenced direction anchored to gravity. To investigate these possibilities, anterodorsal thalamic HD cells were recorded from restrained rats while they were passively positioned in various 3D orientations. Cell responses were unaffected by pitch or roll up to ~90° from the horizontal plane. Firing was disrupted once the animal was oriented >90° away from the horizontal plane and during inversion. When rolling the animal around the earth-vertical axis, cells were active when the animal’s ventral surface faced the cell’s PFD. However, with the rat rolled 90° in an ear-down orientation, pitching the rat and rotating it around the vertical axis did not produce directionally tuned responses. Complex movements involving combinations of yaw-roll, but usually not yaw-pitch, resulted in reduced directional tuning even at the final upright orientation when the rat had full visual view of its environment and was pointing in the cell’s PFD. Directional firing was restored when the rat’s head was moved back-and-forth. There was limited evidence indicating that cells contained conjunctive firing with pitch or roll positions. These findings suggest that the brain’s representation of directional heading is derived primarily from horizontal canal information and that the HD signal is a 3D gravity-referenced signal anchored to a direction in the horizontal plane. NEW & NOTEWORTHY This study monitored head direction cell responses from rats in three dimensions using a series of manipulations that involved yaw, pitch, roll, or a combination of these rotations. Results showed that head direction responses are consistent with the use of two reference frames simultaneously: one defined by the surrounding environment using primarily visual landmarks and a second defined by the earth’s gravity vector.


2013 ◽  
Vol 109 (3) ◽  
pp. 873-888 ◽  
Author(s):  
Jeffrey S. Taube ◽  
Sarah S. Wang ◽  
Stanley Y. Kim ◽  
Russell J. Frohardt

Many species navigate in three dimensions and are required to maintain accurate orientation while moving in an Earth vertical plane. Here we explored how head direction (HD) cells in the rat anterodorsal thalamus responded when rats locomoted along a 360° spiral track that was positioned vertically within the room at the N, S, E, or W location. Animals were introduced into the vertical plane either through passive placement ( experiment 1) or by allowing them to run up a 45° ramp from the floor to the vertically positioned platform ( experiment 2). In both experiments HD cells maintained direction-specific firing in the vertical plane with firing properties that were indistinguishable from those recorded in the horizontal plane. Interestingly, however, the cells' preferred directions were linked to different aspects of the animal's environment and depended on how the animal transitioned into the vertical plane. When animals were passively placed onto the vertical surface, the cells switched from using the room (global cues) as a reference frame to using the vertically positioned platform (local cues) as a reference frame, independent of where the platform was located. In contrast, when animals self-locomoted into the vertical plane, the cells' preferred directions remained anchored to the three-dimensional room coordinates and their activity could be accounted for by a simple 90° rotation of the floor's horizontal coordinate system to the vertical plane. These findings highlight the important role that active movement signals play for maintaining and updating spatial orientation when moving in three dimensions.


2014 ◽  
Vol 111 (9) ◽  
pp. 1903-1919 ◽  
Author(s):  
Ian Moreau-Debord ◽  
Christophe Z. Martin ◽  
Marianne Landry ◽  
Andrea M. Green

To contribute appropriately to voluntary reaching during body motion, vestibular signals must be transformed from a head-centered to a body-centered reference frame. We quantitatively investigated the evidence for this transformation during online reach execution by using galvanic vestibular stimulation (GVS) to simulate rotation about a head-fixed, roughly naso-occipital axis as human subjects made planar reaching movements to a remembered location with their head in different orientations. If vestibular signals that contribute to reach execution have been transformed from a head-centered to a body-centered reference frame, the same stimulation should be interpreted as body tilt with the head upright but as vertical-axis rotation with the head inclined forward. Consequently, GVS should perturb reach trajectories in a head-orientation-dependent way. Consistent with this prediction, GVS applied during reach execution induced trajectory deviations that were significantly larger with the head forward compared with upright. Only with the head forward were trajectories consistently deviated in opposite directions for rightward versus leftward simulated rotation, as appropriate to compensate for body vertical-axis rotation. These results demonstrate that vestibular signals contributing to online reach execution have indeed been transformed from a head-centered to a body-centered reference frame. Reach deviation amplitudes were comparable to those predicted for ideal compensation for body rotation using a biomechanical limb model. Finally, by comparing the effects of application of GVS during reach execution versus prior to reach onset we also provide evidence that spatially transformed vestibular signals contribute to at least partially distinct compensation mechanisms for body motion during reach planning versus execution.


2020 ◽  
Vol 57 (1) ◽  
pp. 21-40
Author(s):  
Alexandra Wallenberg ◽  
Michelle Dafov ◽  
David Malone ◽  
John Craddock

A harzburgite intrusion, which is part of the trailside mafic complex) intrudes ~2900-2950 Ma gneisses in the hanging wall of the Laramide Bighorn uplift west of Buffalo, Wyoming. The harzburgite is composed of pristine orthopyroxene (bronzite), clinopyroxene, serpentine after olivine and accessory magnetite-serpentinite seams, and strike-slip striated shear zones. The harzburgite is crosscut by a hydrothermally altered wehrlite dike (N20°E, 90°, 1 meter wide) with no zircons recovered. Zircons from the harzburgite reveal two ages: 1) a younger set that has a concordia upper intercept age of 2908±6 Ma and a weighted mean age of 2909.5±6.1 Ma; and 2) an older set that has a concordia upper intercept age of 2934.1±8.9 Ma and a weighted mean age 2940.5±5.8 Ma. Anisotropy of magnetic susceptibility (AMS) was used as a proxy for magmatic intrusion and the harzburgite preserves a sub-horizontal Kmax fabric (n=18) suggesting lateral intrusion. Alternating Field (AF) demagnetization for the harzburgite yielded a paleopole of 177.7 longitude, -14.4 latitude. The AF paleopole for the wehrlite dike has a vertical (90°) inclination suggesting intrusion at high latitude. The wehrlite dike preserves a Kmax fabric (n=19) that plots along the great circle of the dike and is difficult to interpret. The harzburgite has a two-component magnetization preserved that indicates a younger Cretaceous chemical overprint that may indicate a 90° clockwise vertical axis rotation of the Clear Creek thrust hanging wall, a range-bounding east-directed thrust fault that accommodated uplift of Bighorn Mountains during the Eocene Laramide Orogeny.


2006 ◽  
Vol 65 (6) ◽  
pp. 429-439 ◽  
Author(s):  
Keisuke Kushiro ◽  
Jun Maruta

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