State-dependent egocentric and allocentric heading representation in the monarch butterfly brain

Abstract Head direction can be represented in a self-centered egocentric or a viewpoint-invariant allocentric reference frame. Using the most efficient representation is especially crucial for migrating animals, like monarch butterflies (Danaus plexippus) that use the sun for orientation. With tetrode recordings from the brain of tethered flying monarch butterflies, we examined the reference frame in which insects encode heading. We show that compass neurons switch their reference frame in a state-dependent manner. In quiescence, they encode sun-bearing angles, allowing the butterfly to map the environment within an egocentric frame. However, during flight, the same neurons encode heading within an allocentric frame. This switch converts the sun from a local to a global cue, an ideal strategy for maintaining a migratory heading over large distance. One-Sentence Summary Heading information is encoded in different state-dependent reference frames in the monarch butterfly central complex