A cerebellum-like circuit in the lateral line system of fish cancels mechanosensory input associated with its own movements

Abstract

An animal's own movement exerts a profound impact on sensory input to its nervous system. Peripheral sensory receptors do not distinguish externally generated stimuli from stimuli generated by an animal's own behavior (reafference) – although the animal often must. One way that nervous systems can solve this problem is to provide movement-related signals (copies of motor commands and sensory feedback) to sensory systems, which can then be used to generate predictions that oppose or cancel out sensory responses to reafference. Here, we studied the use of movement-related signals to generate sensory predictions in the lateral line medial octavolateralis nucleus (MON) of the little skate. In the MON, mechanoreceptive afferents synapse on output neurons that also receive movement-related signals from central sources, via a granule cell parallel fiber system. This parallel fiber system organization is characteristic of a set of so-called cerebellum-like structures. Cerebellum-like structures have been shown to support predictive cancellation of reafference in the electrosensory systems of fish and the auditory system of mice. Here, we provide evidence that the parallel fiber system in the MON can generate predictions that are negative images of (and therefore cancel) sensory input associated with respiratory and fin movements. The MON, found in most aquatic vertebrates, is probably one of the most primitive cerebellum-like structures and a starting point for cerebellar evolution. The results of this study contribute to a growing body of work that uses an evolutionary perspective on the vertebrate cerebellum to understand its functional diversity in animal behavior.