Flight-induced Compass Representation in the Monarch Butterfly Heading Network

For navigation, animals use a robust internal compass. Compass navigation is crucial for long-distance migrating animals like monarch butterflies, which use the sun to navigate over 4,000 km to their overwintering sites every fall. Sun-compass neurons of the central complex have only been recorded in immobile butterflies, and experimental evidence for encoding the animal's heading in these neurons is still missing. Although the activity of central-complex neurons exhibits a locomotor-dependent modulation in many insects, the function of such modulations remains unexplored. Here, we developed tetrode recordings from tethered flying monarch butterflies to reveal how flight modulates heading representation. We found that, during flight, heading-direction neurons change their tuning, transforming the central-complex network to function as a global compass. This compass is characterized by the dominance of processing steering feedback and allows for robust heading representation even under unreliable visual scenarios, an ideal strategy for maintaining a migratory heading over enormous distances.