A dual-axis rotation rule for updating the head direction cell reference frame during movement in three dimensions

Abstract

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.

The place-cell representation of volumetric space in rats

“…This could look to combine recordings with behavioral training, to increase sampling of the more difficult vertical dimension. Our results, combined with those from recent experiments on the head direction system 27, 28 suggest that the rodent spatial navigation network may be far better at mapping three-dimensional space than previously thought. This confirms the relevance of rodents such as rats in studying these representations and raises questions regarding three dimensional encoding of other spatial cells such as grid and boundary cells.…”

Multiplexed code of navigation variables in anterior limbic areas

“…Our recordings in the ATN consisted predominantly of antero-dorsal nuclei neurons. The presence of a large population of HDC in the ATN of rats (Taube et al 1995; Blair and Sharp 1996; Zugaro et al 2001; Peyrache et al 2015, 2017; Page et al 2017) and mice (Yoder and Taube 2009) is well documented.…”

“…One of the most striking properties of the rodent navigation system is the existence of characteristic cell populations that represent well-defined navigation variables. For instance, place cells are pyramidal neurons in the hippocampus (O’Keefe 1971, 1796) that encode the animal’s allocentric position, and head direction (HD) cells in the antero-dorsal thalamic nuclei form a neuronal compass (Taube et al 1995; Blair and Sharp 1996; Zugaro et al 2001; Peyrache et al 2015, 2017; Page et al 2017). Place cells and HD cells are thought the prominent neuron types in these regions, where no other navigational variables have been reported.…”

A gravity-based three-dimensional compass in the mouse brain

“…Head direction (HD) cells, which encode allocentric head orientation analogous to a "neural compass" are a primordial component of the mammalian (Taube 2007; Finkelstein et al 2015) and fly (Seelig and Jayaraman, 2015; Green et al, 2017; Turner-Evans et al, 2017; Kim et al, 2017) spatial navigation system. Originally identified in the rat dorsal presubiculum (Taube et al 1990a,b; Preston-Ferrer et al 2016; Simonnet et al 2018), HD cells have been subsequently found in multiple brain regions, including the anterior thalamus (Taube et al 1995; Peyrache et al 2015, 2017; Page et al 2017; Shinder and Taube 2011, 2014, 2018), parasubiculum (Kornienko et al 2018), retrosplenial cortex (Chen et al 1994a,b; Cho et al 2001; Jacob et al 2017; Lozano et al 2017), and entorhinal cortex (Sargolini et al 2006; Kornienko et al 2018; Park et al 2018).…”