Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes

TLDR

Navigation depends on a constantly updated head direction (HD) signal, mainly driven by visual landmarks but also by self‑motion cues when landmarks are absent, yet previous studies confounded visual cues by using arenas within the same room. To test the relationship between HD cell activity and path integration, the authors recorded HD cells while rats navigated a 14‑unit T‑maze and a multi‑room maze with unique arenas in different rooms connected by a passageway. HD cells were recorded as rats traversed the two maze configurations, allowing comparison of firing direction stability across environments with varying visual and self‑motion cue availability. HD firing directions remained relatively stable within the 14‑unit T‑maze (shifts <45°), were more variable across rooms in the multi‑room maze, increased variability in darkness, and overall self‑motion cues could maintain the HD signal in the absence of familiar visual cues, though visual information—even unfamiliar—enhanced directional precision.

Abstract

Successful navigation requires a constantly updated neural representation of directional heading, which is conveyed by head direction (HD) cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD cell activity and path integration by recording HD cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD cell preferred firing directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of directional perception.