Neural coding underlying the cue preference for celestial orientation

Diurnal and nocturnal African dung beetles use celestial cues, such
as the sun, the moon, and the polarization pattern, to roll dung
balls along straight paths across the savanna. Although nocturnal
beetles move in the same manner through the same environment
as their diurnal relatives, they do so when light conditions are at
least 1 million-fold dimmer. Here, we show, for the first time to
our knowledge, that the celestial cue preference differs between
nocturnal and diurnal beetles in a manner that reflects their
contrasting visual ecologies. We also demonstrate how these cue
preferences are reflected in the activity of compass neurons in the
brain. At night, polarized skylight is the dominant orientation cue
for nocturnal beetles. However, if we coerce them to roll during
the day, they instead use a celestial body (the sun) as their primary
orientation cue. Diurnal beetles, however, persist in using a
celestial body for their compass, day or night. Compass neurons
in the central complex of diurnal beetles are tuned only to the
sun, whereas the same neurons in the nocturnal species switch
exclusively to polarized light at lunar light intensities. Thus, these
neurons encode the preferences for particular celestial cues and alter
their weighting according to ambient light conditions. This flexible
encoding of celestial cue preferences relative to the prevailing visual
scenery provides a simple, yet effective, mechanism for enabling
visual orientation at any light intensity.