Three-dimensional spatial cognition: freely swimming fish accurately learn and remember metric information in a volume

•Freely swimming fish can move with six degrees of freedom.•We investigate how these animals navigate in three dimensions.•Fish accurately encoded the rewarded three-dimensional direction.•Deviations from original trajectory were similar in horizontal and vertical axes.•Consistent with hypothesis that how animals move affects how space is learned.

All animals live and move through three-dimensional environments, yet we do not understand how three-dimensional space is learned, remembered and used. Pelagic fish are ideal model organisms for studying three-dimensional spatial cognition as they move freely through volumes with six degrees of freedom. This is in contrast to surface-bound animals, such as rats, which are constrained to three degrees of freedom of movement. The type of movement that vertebrates display, whether freely moving through volumes (flying or swimming) or surface-bound, might shape their representation of space. We investigated true three-dimensional spatial cognition in an animal that moves freely within volumetric space. We interrogated the three-dimensional trajectories of freely swimming fish (banded tetras, Astyanax fasciatus) that were previously trained to navigate towards a reward inside a maze with horizontal and vertical components. The fish accurately encoded the rewarded three-dimensional direction. As predicted, free-swimming deviations from their original constrained trajectory were similar in both the horizontal and vertical axes, unlike in surface-bound rats. This equality between dimensions is the first direct evidence consistent with the hypothesis that the way animals move through their environment shapes how they learn and use spatial information, indicating a previously unknown adaptation in cognitive representations of space.