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 combine motor feedback, vestibular signals, and external cues to compute the animals heading direction. Whether the underlying mechanism is universal across different species is unresolved. In Drosophila, for instance, the central complex contains three connected, yet anatomically separate, functional neuron rings. Two rings receive countervailing velocity signals that shift neuronal activity bumps around all three rings. An alternative, classical continuous-attractor model invokes only one ring but requires velocity-modulated synaptic connections. A single-ring compass has been discovered in the anterior hindbrain of zebrafish. Using theory and experiments, we find, however, that three rings, including two shifter rings, are intermingled on the same anatomical scaffold. Zebrafish and Drosophila, therefore, use the same basic compass mechanism, suggestive of convergent evolution.