Linking the Input to the Output: New Sets of Neurons Complement the Polarization Vision Network in the Locust Central Complex

Polarized light is a key feature of the blue sky, used by many animals as a sensory cue for compass navigation. Like other insects, locusts perceive the E-vector orientation of polarized light with a specialized region of their compound eye, the dorsal rim area. Neurons in the brain relay this information through several processing stages to the central complex. The central complex has a modular neuroarchitecture, composed of vertical columns and horizontal layers. Several types of central-complex neurons respond to dorsally presented, rotating E-vectors with tonic modulation of their firing frequency. These neurons were found at the input stage of the central complex, as well as near the proposed output stage, where neurons are tuned to form a compass-like representation of E-vector orientations underlying the columnar organization of the central complex. To identify neurons suited to link input and output elements, we recorded intracellularly from 45 neurons of the central complex. We report several novel types of polarization-sensitive neurons. One of these is suited to fill the gap between input and output stages of the central-complex polarization vision network. Three types of neurons were sensitive to polarized light in only 50% of experiments suggesting that they are recruited to the network depending on behavioral context. Finally, we identified two types of neurons suited to transfer information toward thoracic motor circuits. The data underscore the key role of two subunits of the central complex, the lower division of the central body and the protocerebral bridge, in sky compass orientation.