A multi-ring shifter network computes head direction in zebrafish

From insects to fish to mammals, many species have an internal compass: a set of recurrently connected neurons that combines motor feedback, vestibular signals, and external cues to compute the animal's heading direction. Whether the underlying mechanism is universal across different species is unresolved. In Drosophila melanogaster, for instance, the central complex contains three anatomically separate neuron rings. Two rings receive countervailing velocity signals that shift neuronal activity bumps around all three rings. By contrast, a single-ring compass has been discovered in the anterior hindbrain of zebrafish, consistent with a single-ring attractor network that invokes velocity-modulated synaptic connections instead of separate shifter circuits. However, as we now show, the zebrafish's anatomical scaffold harbors three intermingled rings, including two "hidden" shifter rings. We prove that the activity bump in all three functional rings can overlap perfectly, making the rings hard to distinguish except through the shifter neurons' skewed tuning to rotation velocity. In addition, we find that head-direction cells in Drosophila and zebrafish exhibit V-shaped velocity tuning, a feature not predicted by classical models. Taken together, our results suggest that at least two evolutionarily distant species have converged onto the same basic three-ring compass mechanism.