The Representation of Three-Dimensional Space in Fish

In mammals, the so-called "seat of the cognitive map" is located in place cells within the hippocampus. Recent work suggests that the shape of place cell fields might be defined by the animals' natural movement; in rats the fields appear to be laterally compressed (meaning that the spatial map of the animal is more highly resolved in the horizontal dimensions than in the vertical), whereas the place cell fields of bats are statistically spherical (which should result in a spatial map that is equally resolved in all three dimensions). It follows that navigational error should be equal in the horizontal and vertical dimensions in animals that travel freely through volumes, whereas in surface-bound animals would demonstrate greater vertical error. Here, we describe behavioral experiments on pelagic fish in which we investigated the way that fish encode three-dimensional space and we make inferences about the underlying processing. Our work suggests that fish, like mammals, have a higher order representation of space that assembles incoming sensory information into a neural unit that can be used to determine position and heading in three-dimensions. Further, our results are consistent with this representation being encoded isotropically, as would be expected for animals that move freely through volumes. Definitive evidence for spherical place fields in fish will not only reveal the neural correlates of space to be a deep seated vertebrate trait, but will also help address the questions of the degree to which environment spatial ecology has shaped cognitive processes and their underlying neural mechanisms.