The neuroanatomical ultrastructure and function of a biological ring attractor

ABSTRACT Neural representations of head direction have been discovered in many species. A large body of theoretical work has proposed that the dynamics associated with these representations is generated, maintained, and updated by recurrent network structures called ring attractors. We performed electron microscopy-based circuit reconstruction and RNA profiling of identified cell types in the heading direction system of Drosophila melanogaster to directly determine the underlying neural network. We identified network motifs that have been hypothesized to maintain the heading representation in darkness, update it when the animal turns, and tether it to visual cues. Functional studies provided additional support for the proposed roles of individual circuit elements. We also discovered recurrent connections between neuronal arbors with mixed pre- and post-synaptic specializations. Overall, our results confirm that the Drosophila heading direction network contains the core components of a ring attractor while also revealing unpredicted structural features that might enhance the network’s computational power.