Predictive coding and oscillations underlie the optomotor response in distant insect lineages

Abstract The optomotor response (OMR) refers to animals’ distinctive turning response to rotating visual stimuli. It is assumed to be a predictable Stimulus-Response (S-R) behavior. Here we show in two phylogenetically and ecologically distant insects (ants and earwigs) that it is not the case. Insects’ turning responses were not determined by the detected visual-motion, but by the computation of optic flow prediction errors, which we could infer by manipulating the visual-feedback expected from their own movements. Moreover, both insects displayed regular oscillations of angular velocity, which were modulated by the prediction errors. This produces a closed-loop system yielding complex dynamics and a stochastic moment-to-moment behavior, which can be captured with a simple predictive computational model. We conclude that internal oscillators and predictive coding, as well as their closed-loop interaction, are ancestral features of insect brains conserved across more than 350 million years. The OMR is a by-product of this control system and appears deterministic only when averaging animals’ responses.