Cellular Basis of Head Direction and Contextual Cues in the Insect Brain

Animals rely upon integrated sensory information for spatial navigation. A question of wide importance in navigation is how sensory cues get transformed into neural codes that represent the animal's orientation within its proximal environment. Here, we investigated the possibility of head-direction coding in the central complex of the cockroach, Blaberus discoidalis. We used extracellular recordings in restrained animals that were rotated on a platform relative to a fixed landmark. The passive rotations allowed us to test for head-direction coding in the absence of self-generated motion cues. Our results indicate that individual cells in the central complex encode the animal's heading relative to a landmark's position in several ways. In some cells, directional tuning was established even in the absence of visual cues, suggesting that the directional code can be maintained solely based on the internal motion cues derived from the passive rotations. Additionally, some cells in the central complex encoded rotation-direction history, a navigational context cue, by increasing or decreasing the firing rate during the stationary periods following clockwise or counterclockwise rotations. Together, these results unveil head-direction cell-like activity in the insect central complex, which highly resemble similarly functioning cells in the mammalian brain that encode head direction. We predict that the observed head-orientation coding and directionally sensitive cells are essential components of the brain circuitry mediating insect navigation.