The neuronal building blocks of the navigational toolkit in the central complex of insects

The central complex in the brain of insects is a group of midline-spanning neuropils at the interface between sensory and premotor tasks of the brain. It is involved in sleep control, decision-making and most prominently in goal-directed locomotion behaviors. The recently published connectome of the central complex of Drosophila melanogaster is a milestone in understanding the intricacies of the central-complex circuits and will provide inspiration for testable hypotheses for the coming years. Here, I provide a basic neuroanatomical description of the central complex of Drosophila and other species and discuss some recent advancements, some of which, such as the discovery of coordinate transformation through vector math, have been predicted from connectomics data.

Introduction

Spatial orientation is perhaps the most fundamental and vital task of the nervous system of all nonsessile animals. Any goal-directed behavior, such as food search, mate-finding, escaping, or homing, requires prior knowledge of the orientation of the animal’s body in space with respect to a defined external system of cues. Therefore, the nervous system has to hold internal representations of the axes of the body that is attached to it (Figure 1a). It also has to encode the heading direction: the spatial relationship between the sensory organs, which are often located on the head, and external stimuli that can be tracked. This heading direction does not always coincide with the traveling direction (Figure 1b). Therefore, it is important, especially for more sophisticated orientation behaviors, such as vector navigation, that the neuronal system also tracks the actual travel direction of the body. It is further useful (and for vector navigation indispensable) to be able to estimate travel velocity and integrate it over time to gauge distances. Many of the representations and mechanisms outlined above have specific neuronal correlates in the central complex (CX).

Volumetric movement (i.e. movement in 3D space) entails translation along or rotation around the three cardinal axes of the body (i.e. it has six degrees of freedom, Figure 1a). While the ability to perform a stable flight generally requires control over all six degrees of freedom, traveling between two points requires mainly control over movements in the horizontal plane. Although there is some evidence that neurons in the CX are not only tuned to azimuth (i.e. orientation in the horizontal plane), but also to elevation of visual stimuli 1, 2, 3, so far, most neuronal correlates of directional coding that have been identified in the CX, were limited to the horizontal plane 4, 5, 6, 7, 8••, 9••. One possible reason for this is that insects stabilize their gaze in the rollandpitch axes through compensatory head movements using visual and mechanosensory feedback, thereby reducing the input to the head-centered sensory systems to the horizontal plane 10, 11. A second possibility is that the restraining of insects to this plane in physiological setups has so far precluded the discovery of a three-dimensional system as described in mammals [12].

Electrophysiological work in crickets, monarch butterflies, dung beetles, bees, and particularly in locusts has elucidated many sensory and physiological properties of central-complex neurons in the past 20 years 13, 14, 15, 16, 17, 18, 19, 1, 3. In the past decade, the genetic toolkit available in Drosophila has advanced our understanding of the inner workings of the central- complex circuits at a breathtaking pace. In this review, I aim to provide a guided tour through the central complex, following the flow and processing of spatial information rather than providing a comprehensive overview of recent publications, which has been nicely done elsewhere 20, 21, 22.