Two compasses in the central complex of the locust brain

Abstract

Manymigratory insects rely on a celestial compass for spatial orientation. Several features of the daytime sky, all generated by the sun, can be exploited for navigation. Two of these are the position of the sun and the pattern of polarized skylight. Neurons of the central complex (CX), a group of neuropils in the central brain of insects, have been shown to encode sky compass cues. In desert locusts, the CX holds a topographic, compass-like representation of the plane of polarized light (E-vector) presented from dorsal direction. In addition, these neurons also encode the azimuth of an unpolarized light spot, likely representing the sun. Here, we investigate whether, in addition to E-vector orientation, the solar azimuth is represented topographically in the CX. We recorded intracellularly from eight types of CX neuron while stimulating animals of either sex with polarized blue light from zenithal direction and an unpolarized green light spot rotating around the animal’s head at different elevations. CX neurons did not code for elevation of the unpolarized light spot. However, two types of columnar neuron showed a linear correlation between innervated slice in theCXand azimuth tuning to the unpolarized green light spot, consistent with an internal compass representation of solar azimuth. Columnar outputs of the CX also showed a topographic representation of zenithal E-vector orientation, but the two compasses were not linked to each other. Combined stimulation with unpolarized green and polarized blue light suggested that the two compasses interact in a nonlinear way.