The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Highlights

• Inhibition of prepositus→dorsal tegmental pathway impairs head direction (HD) cell stability

• This instability is consistent with a disruption of angular head velocity inputs

• Influencing HD cell stability during navigation impairs homing behavior

Summary

The rat limbic system contains head direction (HD) cells that fire according to heading in the horizontal plane, and these cells are thought to provide animals with an internal compass. Previous work has found that HD cell tuning correlates with behavior on navigational tasks, but a direct, causal link between HD cells and navigation has not been demonstrated. Here, we show that pathway-specific optogenetic inhibition of the nucleus prepositus caused HD cells to become directionally unstable under dark conditions without affecting the animals’ locomotion. Then, using the same technique, we found that this decoupling of the HD signal in the absence of visual cues caused the animals to make directional homing errors and that the magnitude and direction of these errors were in a range that corresponded to the degree of instability observed in the HD signal. These results provide evidence that the HD signal plays a causal role as a neural compass in navigation.