Receptive field structures for two celestial compass cues at the input stage of the central complex in the locust brain

Abstract

ABSTRACT Successful navigation depends on an animal's ability to perceive its spatial orientation relative to visual surroundings. Heading direction in insects is represented in the central complex (CX), a navigation center in the brain, to generate steering commands. In insects that navigate relative to sky compass signals, CX neurons are tuned to celestial cues indicating the location of the sun. The desert locust CX contains a compass-like representation of two related celestial cues: the direction of unpolarized direct sunlight and the pattern of polarized light, which depends on the sun position. Whether congruent tuning to these two compass cues emerges within the CX network or is inherited from CX input neurons is unclear. To address this question, we intracellularly recorded from GABA-immunoreactive TL neurons, which are input elements to the locust CX (corresponding to R neurons in Drosophila), while applying visual stimuli simulating unpolarized sunlight and polarized light across the hemisphere above the animal. We show that TL neurons have large receptive fields for both types of stimuli. However, faithful integration of polarization angles across the dorsal hemisphere, or matched-filter ability to encode particular sun positions, was found in only two out of 22 recordings. Those two neurons also showed a good match in sun position coding through polarized and unpolarized light signaling, whereas 20 neurons showed substantial mismatch in signaling of the two compass cues. The data, therefore, suggest that considerable refinement of azimuth coding based on sky compass signals occurs at the synapses from TL neurons to postsynaptic CX compass neurons.