Many animals keep track of their angular heading over time while navigating through their environment. However, a neural-circuit architecture for computing heading has not been experimentally defined in any species. Here we describe a set of clockwise- and anticlockwise-shifting neurons in the Drosophila central complex whose wiring and physiology provide a means to rotate an angular heading estimate based on the fly’s angular velocity. We show that each class of shifting neurons exists in two subtypes, with spatiotemporal activity profiles that suggest different roles for each subtype at the start and end of tethered-walking turns. Shifting neurons are required for the heading system to properly track the fly’s heading in the dark, and stimulation of these neurons induces predictable shifts in the heading signal. The central features of this biological circuit are analogous to those of computational models proposed for head-direction cells in rodents and may shed light on how neural systems, in general, perform integration. A neural circuit in Drosophila reveals how the fly’s internal sense of heading rotates when it turns. Spatial navigation has been shown to rely in part on 'head-direction neurons', which act like an internal compass in several animal species, but the neuronal circuits that generate and update the persistent activity of these cells are unknown. Now Gaby Maimon and colleagues identify two types of upstream neurons that tell the Drosophila head-direction signal when to rotate, and by how much, as the animal's head turns. The P-EN1 neurons act like a gas pedal at the start of the rotation, whereas P-EN2 neurons act like a brake at the end of it, while the magnitude of an asymmetry between left- and right-hand side P-EN neurons marks the velocity of head rotation. These findings will not only inform computational models proposed for spatial integration in other species, such as ants, bees and rodents, but could also help neuroscientists to understand how brains in general integrate transient inputs into persistent activity.

A neural circuit architecture for angular integration in Drosophila