Neural correlates of diverse navigational strategies

Insects have evolved diverse and remarkable strategies for navigating in various ecologies all over the world. In particular, central place foragers, such as bees and ants, have become renowned for their fascinating navigational capabilities. At the heart of insect navigation lies a brain area known as the central complex (CX). Functionally, the CX integrates world-centric sensory information with self-motion cues to generate an internal map of angular position. It plays a role in driving motor commands and has been suggested as the neural substrate for encoding travel direction, as well as navigational vectors theorized to be involved in path integration. Interestingly, the CX appears to have been highly anatomically conserved, even across insect species that diverged hundreds of millions of years ago. The conserved nature of the CX stands in juxtaposition to the extraordinary diversity of insect behavior. How does a highly conserved brain area give rise to such diverse navigational behavior? Using block-face electron microscopy combined with neuron tracing and synapse annotation, we analyzed CX circuits in six species of bees and ants: the honeybee, the bumblebee (Paper 1), the sweat bee, the army ant, the desert ant, and the bull ant. Our data suggests that there are core circuits that have been exceptionally well preserved across evolutionary time. Namely, the head direction circuit (Paper 2) which contains neurons that share total numbers, projectivity, and connectivity motifs from flies to bees and ants. In contrast, inputs from sensory areas vary to a much larger degree. Our data suggests that the relative contribution of parallel input pathways depends strongly on the information available in the habitat of a species. Also variable are the circuits that encode self-motion, something which is fundamental for building navigationally relevant internal representations (Paper 3). Altogether, these neuroanatomical maps provide the framework for future functional and modeling studies that seek to understand how sensory information is transformed into behavioral decisions within the context of navigation.