Matched-filter coding of sky polarization results in an internal sun compass in the brain of the desert locust

Abstract

Many animals use celestial cues for spatial orientation. These include the sun and, in insects, the polarization pattern of the sky, which depends on the position of the sun. The central complex in the insect brain plays a key role in spatial orientation. In desert locusts, the angle of polarized light in the zenith above the animal and the direction of a simulated sun are represented in a compass-like fashion in the central complex, but how both compasses fit together for a unified representation of external space remained unclear. To address this question, we analyzed the sensitivity of intracellularly recorded central-complex neurons to the angle of polarized light presented from up to 33 positions in the animal's dorsal visual field and injected Neurobiotin tracer for cell identification. Neurons were polarization sensitive in large parts of the virtual sky that in some cells extended to the horizon in all directions. Neurons, moreover, were tuned to spatial patterns of polarization angles that matched the sky polarization pattern of particular sun positions. The horizontal components of these calculated solar positions were topographically encoded in the protocerebral bridge of the central complex covering 360° of space. This whole-sky polarization compass does not support the earlier reported polarization compass based on stimulation from a small spot above the animal but coincides well with the previously demonstrated direct sun compass based on unpolarized light stimulation. Therefore, direct sunlight and whole-sky polarization complement each other for robust head direction coding in the locust central complex.