Maintaining a stable head direction representation in naturalistic visual environments

Abstract

Many animals rely on a representation of head direction for flexible, goal-directed navigation. In insects, a compass-like head direction representation is maintained in a conserved brain region called the central complex. This head direction representation is updated by self-motion information and by tethering to sensory cues in the surroundings through a plasticity mechanism. However, under natural settings, some of these sensory cues may temporarily disappear--for example, when clouds hide the sun--and prominent landmarks at different distances from the insect may move across the animals field of view during translation, creating potential conflicts for a neural compass. We used two-photon calcium imaging in head-fixed Drosophila behaving in virtual reality to monitor the flys compass during navigation in immersive naturalistic environments with approachable local landmarks. We found that the flys compass remains stable even in these settings by tethering to available global cues, likely preserving the animals ability to perform compass-driven behaviors such as maintaining a constant heading.