Stable Neural Coding of Heading Across Locomotory Modes in the Insect Compass

To establish a robust representation of heading, animals rely on a multimodal compass with input from visual cues and self-motion information produced during locomotion1-5. How animals capable of multiple modes of locomotion, such as walking and flying, maintain a stable heading representation across these different modes remains unexplored. Here, we demonstrate that the neural coding of heading in Monarch butterflies (Danaus plexippus) is remarkably stable across locomotor modes, allowing heading information acquired during walking to also be used in flight.Tetrode recordings from the central complex, the brain region encoding heading in insects2,6-8, allowed us to monitor the neural activity of individual butterflies while transitioning from quiescence to walking and from walking to flight. Comparing azimuthal tuning across these behavioral modes, we found dramatic state-dependent shifts that transformed a frontally biased heading coding in quiescence into a continuous, full 360° heading representation during walking and flight. This 360° heading representation was established even in an ambiguous visual setting and when the animals’ eyes were occluded, showing that proprioceptive inputs during self-controlled movement generate a heading signal that is independent of locomotor mode. Remarkably, despite the fundamentally different proprioceptive feedback from wings versus legs, individual neurons preserved an invariant heading representation across walking and flight. This demonstrates that the central complex in Monarch butterflies integrates locomotor-specific inputs into a unified heading signal, maintaining a coherent heading representation across diverse locomotor modes, establishing an efficient navigation system capable of transferring relevant heading information from one mode of locomotion to another.