Theoretical principles explain the structure of the insect head direction circuit

To navigate their environment, insects need to keep track of their orientation. Previous work has shown that insects encode their head direction as a sinusoidal activity pattern around a ring of neurons arranged in an eight-column structure. However, it is unclear whether this sinusoidal encoding of head direction is just an evolutionary coincidence or if it offers a particular functional advantage. To address this question, we establish the basic mathematical requirements for direction encoding and show that it can be performed by many circuits, all with different activity patterns. Among these activity patterns, we prove that the sinusoidal one is the most noise-resilient, but only when coupled with a sinusoidal connectivity pattern between the encoding neurons. We compare this predicted optimal connectivity pattern with anatomical data from the head direction circuits of the locust and the fruit fly, finding that our theory agrees with experimental evidence. Furthermore, we demonstrate that our predicted circuit can emerge using Hebbian plasticity, implying that the neural connectivity does not need to be explicitly encoded in the genetic program of the insect but rather can emerge during development. Finally, we illustrate that in our theory, the consistent presence of the eight-column organisation of head direction circuits across multiple insect species is not a chance artefact but instead can be explained by basic evolutionary principles.