Abstract: To navigate around their local environment, animals must recognise their own position with respect to their goal. This task can be completed successfully if they have a representation of space in their brain, built upon learning and remembering environmental features. This representation can be thought of as a neural map. Previous research has focused on how animals navigate horizontally, however most must also move vertically. This is exemplified by flying or swimming animals, which move with six degrees of freedom (unlike surface constrained animals that move with three). By using behavioural experimental and theoretical approaches, we study both the sensory basis of 3D navigation in fish and also how the information gained from the environment is learned and remembered. We show that the vertical and horizontal components of space are stored separately in the fishes’ representation of space, which simplifies the problem of encoding complex information in the brain, and that the vertical axis contains particularly salient spatial cues, including hydrostatic pressure. We also demonstrate that fish that swim freely through a volume of water are able to accurately learn and remember 3D metric information – that is, distance and direction. Our work suggests that the spatial information obtained by a fish’s sensory systems is pulled together into a supramodal representation of space that is similar to the place cells in the hippocampus of mammals. We also suggest the putative neurones that encode space in fish fire with a spherical distribution, allowing the animals to navigate effectively in three-dimensions.