Integration of celestial compass cues in the central complex of the locust brain.

Abstract

Many insects rely on celestial compass cues such as the polarization pattern of the sky for spatial orientation. In the desert locust, the central complex (CX) houses multiple sets of neurons, sensitive to the oscillation plane of polarized light and thus probably acts as an internal polarization compass. We investigated whether other sky compass cues like direct sunlight or the chromatic gradient of the sky might contribute to this compass. We recorded from polarization-sensitive CX neurons while an unpolarized green or ultraviolet light spot was moved around the head of the animal. All types of neuron that were sensitive to the plane of polarization (E-vector) above the animal also responded to the unpolarized light spots in an azimuth-dependent way. The tuning to the unpolarized light spots was independent of wavelength, suggesting that the neurons encode solar azimuth based on direct sunlight and not on the sky chromatic gradient. Two cell types represented the natural 90 deg relationship between solar azimuth and zenithal E-vector orientation, providing evidence to suggest that solar azimuth information supports the internal polarization compass. Most neurons showed advances in their tuning to the E-vector and the unpolarized light spots dependent on rotation direction, consistent with anticipatory signaling. The amplitude of responses and its variability were dependent on the level of background firing, possibly indicating different internal states. The integration of polarization and solar azimuth information strongly suggests that besides the polarization pattern of the sky, direct sunlight might be an important cue for sky compass navigation in the locust.