Abstract
Terrestrial animals compute shortcuts through their environment by integrating self-motion vectors containing distance and direction information. The sensory and neural mechanisms underlying this navigational feat have been extensively documented, but their evolutionary origins remain unexplored. Among extant vertebrates, the teleost fish make up one of the most diverse and earliest-branching phylogenetic groups, and provide a powerful system to study the origins of vertebrate spatial processing. However, how freely-swimming teleost fish collect and compute metric spatial information underwater are unknown. Using the Picasso triggerfish, Rhinecanthus aculeatus, we investigate the functional and mechanistic basis of distance estimation in teleost fish for the first time. We show that a fish can learn and remember distance travelled with remarkable accuracy. By analysing swimming trajectories, we form hypotheses about how distance is represented in the teleost brain, and propose that distance may be encoded by dedicated neural structures in a similar way to terrestrial vertebrates. Finally, we begin exploring the sensory mechanisms underlying distance estimation in fish. Many walking animals use a step counter for odometry. By quantifying finbeat use during our distance task, we show that a functionally equivalent finbeat counter is unlikely to provide reliable and precise distance information in an aquatic environment.
