A framework for constructing insect steering circuits

Insects perform a variety of goal-directed navigation behaviours, in which steering is controlled by a comparison between their current and desired heading direction. Recent work has uncovered the details of such a steering circuit in the fruit fly Drosophila melanogaster. Here we analyse the principles behind the neuroanatomy and physiology of this circuit to derive five general rules which can be used to construct a class of steering circuits which operate in the same way. These rules are surprisingly permissive, suggesting that across insect species, steering circuits may have differing wiring while remaining functionally identical. We simulate several examples, including an irregular circuit that conforms to the rules, and circuits that break the rules, and examine their ability to control steering towards a varying goal direction. We argue that the principled approach we apply here could be applied more generally in performing comparative analyses in neuroscience.Author summary: Steering towards a goal is a fundamental animal behaviour. In fruit flies, the brain circuits underlying this behaviour appear to operate by comparing the animal’s current heading with a desired goal direction, where both angles are encoded in activity across a neural array. Here, we consider the geometric principles needed to obtain reliable steering output for any goal direction from such an encoding. This leads to a set of rules governing steering circuit construction. This framework can be used to construct steering circuits which vary significantly in structure, yet perform the task in the same way. We demonstrate this by simulating example circuits which are shown to be functionally equivalent, while being structurally unique. We also explore cases where the rules are broken, which impairs a circuit’s ability to steer. We argue that this principled or ‘rule-based’ approach to analysing neuroanatomy can help to highlight the features of a neural circuit which make it functionally distinct, and is hence valuable when examining the similarities and differences between the neuroanatomy of different species.