History-dependent spiking facilitates efficient encoding of polarization angles in neurons of the central complex

Many insects use the polarization pattern of the sky for spatial orientation. Since flying insects perform rapid maneuvers, including saccadic yaw turns which alternate with translational flight, they perceive highly dynamic polarization input to their navigation system. The tuning of compass-neurons in the central complex of insects, however, has been mostly investigated with polarized-light stimuli that rotated at slow and constant velocities, and thus were lacking these natural dynamics. Here we investigated the dynamic response properties of compass-neurons, using intracellular recordings in the central complex of bumblebees. We generated naturalistic stimuli by rotating a polarizer either according to a sequence of head orientations that have been reported from freely flying bumblebees, or at constant velocities between 30°/s and 1920°/s, spanning almost the entire range of naturally occurring rotation velocities. We found that compass neurons responded reliably across the entire range of the presented stimuli. In their responses, we observed a dependency on spiking history. We further investigated this dependency using a rate code model taking spiking history into account. Extending the model to a neuronal population with different polarization tuning, which mirrored the neuronal architecture of the central complex, suggests that spiking history has a directly impact on the overall population activity, which has two effects: First, it facilitates faster responses to stimulus changes during highly dynamic flight maneuvers, and increases sensitivity for course deviations during straight flight. Second, population activity during phases of constant polarization input is reduced, which might conserve energy during straight flight.