Degradation of Head Direction Cell Activity during Inverted Locomotion

Abstract

Head direction (HD) cells in the rat limbic system carry information about the direction the head is pointing in the horizontal plane. Most previous studies of HD functioning have used animals locomoting in an upright position or ascending/descending a vertical wall. In the present study, we recorded HD cell activity from the anterodorsal thalamic nucleus while the animal was locomoting in an upside-down orientation. Rats performed a shuttle-box task requiring them to climb a vertical wall and locomote across the ceiling of the apparatus while inverted to reach an adjoining wall before ascending into the reward compartment. The apparatus was oriented toward the preferred direction of the recorded cell, or the 180°opposite direction. When the animal was traversing the vertical walls of the apparatus, the HD cells remained directionally tuned as if the walls were an extension of the floor. When the animal was locomoting inverted on the ceiling, however, cells showed a dramatic change in activity. Nearly one-half (47%) of the recorded cells exhibited no directional specificity during inverted locomotion, despite showing robust directional tuning on the walls before and after inversion. The remaining cells showed significantly degraded measures of directional tuning and random shifts of the preferred direction relative to the floor condition while the animal was inverted. It has previously been suggested that the HD system uses head angular velocity signals from the vestibular system to maintain a consistent representation of allocentric direction. These findings suggest that being in an inverted position causes a distortion of the vestibular signal controlling the HD system.

Updating of the spatial reference frame of head direction cells in response to locomotion in the vertical plane

“…This result therefore contrasts with those in the HorizontalPlatform and Horizontal-Rotation sessions where the room, and not the platform, was used as the reference frame. More importantly, this result also indicates that the reference frame in the vertical plane was not always a simple 90°transforma-tion of the horizontal plane into the vertical plane and is not consistent with the predictions of the earlier studies (Calton and Taube 2005;Stackman et al 2000). Note that in these earlier studies the animals were able to locomote freely between the horizontal and vertical planes, whereas in the present study the animals were passively moved by hand from their home cage to the start location on the spiral track.…”

“…6A) and 2) the orientation of the rectangular platform during the prior Horizontal-Rotation session. In sum, these results indicate that, in general, the HD cells continued to use the room as a reference frame when the animals were placed on the vertically positioned platform, and are consistent with previous hypotheses (Calton and Taube 2005;Stackman et al 2000) suggesting that when locomoting in the vertical plane animals extend the floor's horizontal coordinate system to the vertical wall surface through a 90°r otation of the horizontal coordinate system (Fig. 1).…”

“…Previous studies have reported that HD cell responses on vertical surfaces are related to how the cells fire when the animal locomotes on a nearby horizontal surface (Calton and Taube 2005;Stackman et al 2000). Specifically, these studies postulated that the reference frame on the vertical surface can be viewed within the three-dimensional (3D) coordinate frame of the room and the vertical plane coordinate system is simply a 90°rotation of the floor's x-y coordinate system into the vertical plane that the rat is situated in (Fig.…”

“…1). Another study monitored HD cell activity as the rat traveled a circular pattern that included two trips through the vertical plane (floor ¡ wall ¡ ceiling ¡ wall ¡ floor) and similarly found that HD cells responded on the walls as if they were an extension of the floor's coordinate system (Calton and Taube 2005). For both of these studies, when the rat was on the vertical surface the monitoring of HD cell activity was limited to a narrow range of directions that was aligned with the rat's longitudinal body axis, because the behavioral tasks did not require the animal to look around while it was traversing the walls up or down.…”

The neural correlates of navigation beyond the hippocampus

“…To perform the task successfully when starting from one of four locations required a more flexible representation of space -a cognitive map-like strategy. Because HD cell firing is disrupted when rats are inverted (Calton and Taube, 2005), taken together, these results suggest that an intact HD signal is required to perform the task accurately when a cognitive map-like strategy is needed. Gibson et al (2013) recently confirmed that HD cell firing in the ADN was absent on this task when rats were inverted, and despite the absence of normal HD cell activity they were still able to perform the task when started from one or two locations.…”