Three-dimensional tuning of head direction cells in rats

Abstract

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.

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

“…firing rate for all tilt position at a given azimuth) of the tuning curve is shown at the azimuth PD. When exclusively tested during pitch in this plane (green line; as Shinder and Taube, 2018, did), the cell’s tilt modulation is much broader and the cell’s firing at ND is barely above its firing when the animal is upright (red). (b) Average azimuth tuning curve when upright, peaking at 5°.…”

“…Lower panel: Firing rate measured along a pitch trajectory; Solid green curves: actual data; Dashed green curves: simulated data (see below). (d) Experiment by Shinder and Taube (2018): Tilt tuning was tested when animals faced the azimuth PD. Note that firing is elevated in the vicinity of upright.…”

“…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).…”

“…Thus, the two observations (gravity-anchored tilt tuning in macaques and 3D HD tuning in bats) have remained segregated. Furthermore, tuning to tilt has never been shown in rodents, and some researchers proposed that it may be restricted to aerial and tree-dwelling species but absent in ground-dwelling species like rodents (Calton and Taube 2005; Shinder and Taube 2018).…”

“…Head azimuth is updated when the head rotates within one surface (yaw, cyan arrows) or when it rotates in the earth-horizontal plane (green arrow when transitioning from surface 2 to 3). If azimuth is updated by yaw rotations only (yaw-only frame, YO; Shinder and Taube, 2018), the compass will not maintain allocentric consistency since it will register only 270° when the head returns to its initial position. (c) Tilted azimuth (TA) reference frame (Laurens and Angelaki, 2018), where head direction is measured in a compass co-planar with the head-horizontal plane but aligned with the EH compass along the line intersecting the two planes (here, the 0-180° line).…”