Structural and functional organization of visual responses in the inferior olive of larval zebrafish.

The olivo-cerebellar system plays an important role in vertebrate sensorimotor control. Here we investigate sensory representations in the IO of larval zebrafish and their spatial organization. Using single-cell labeling of genetically identified IO neurons we find that they can be divided into at least two distinct groups based on their spatial location, dendritic morphology, and axonal projection patterns. In the same genetically targeted population, we recorded calcium activity in response to a set of visual stimuli using two-photon imaging. We found that most IO neurons showed direction-selective and binocular responses to visual stimuli and that functional properties were spatially organized within the IO. Light-sheet functional imaging that allowed for simultaneous activity recordings at the soma and axonal level revealed tight coupling between functional properties, soma location and axonal projection patterns of IO neurons. Taken together, our results suggest that anatomically-defined classes of IO neurons correspond to distinct functional types, and that topographic connections between IO and cerebellum contribute to organization of the cerebellum into distinct functional zones. Significance Statement Using the transparent larval zebrafish, we systematically recorded the responses of Inferior Olive (IO) neurons to visual motion stimuli that drive optomotor and optokinetic behaviors. We find that most IO neurons respond selectively to one or more such stimuli. Individual neurons are tuned to specific directions of motion and different functional types are distributed non-uniformly in the IO. Furthermore, we were able to link the functional type of the IO neurons with their location, morphology and projection patterns. This shows how topographically organized projections from the IO play an important role in channeling behaviorally-relevant information to the cerebellum in zebrafish larvae.