Neurons sensitive to sky compass signals in the brain of the Madeira cockroach Rhyparobia maderae

Many insects are formidable navigators illustrated by homing behavior in bees and ants or regular seasonal migrations in butterflies, moths, and others. For spatial orientation, many insects rely on celestial cues, in particular the position of the sun or the polarization pattern of the blue sky generated by the sun. In all species studied celestial polarization is perceived by photoreceptors in a highly specialized dorsal rim area of the eye. Studies in various insects showed that the central complex utilizes these and other sensory inputs to create an internal compass-like representation of external space for vector navigation. Cockroaches, likewise, rely on visual and antennal input for navigational decisions mediated by the central complex. To explore the possible contribution of sky compass signals, we have characterized the responsiveness of neurons of the optic lobe and central complex of the Madeira cockroach Rhyparobia maderae to the angle of polarized light and the azimuth of unpolarized light spots representing the sun or the chromatic gradient of the sky. Strong responses to polarization angle and to changing polarization angle were found in several cell types connecting both optic lobes. Responses to sky compass signals in neurons of the central complex were less pronounced, but were significant in several cell types corresponding to neurons encoding sun compass signals in other species. Although the Madeira cockroach is a nocturnal scavenger and the existence of a specialized dorsal eye region has not been established, sky compass signals likely play a substantial role in behavioral decisions.