The Representation of Three-Dimensional Space in Fish

Abstract

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.

Volumetric spatial behaviour in rats reveals the anisotropic organisation of navigation

“…Given the anisotropic neural coding observed in these spaces, the increased energetic cost of moving vertically and the increased computational demands of planning trajectories, the aim of the current experiment was to investigate how rats navigate three-dimensional volumetric environments. Because of the evolutionary and kinaesthetic differences between ecologically volumetric animals such as fish (Burt de Perera et al 2016 ) and bats (Yartsev and Ulanovsky 2013 ) when compared to humans, we used rats as a closer biological and electrophysiological model. Despite their essentially surface-bound nature, rats exhibit many three-dimensional behaviours similar to those of humans.…”

Hippocampus, Retrosplenial and Parahippocampal Cortices Encode Multicompartment 3D Space in a Hierarchical Manner

“…Indeed, place cells and head direction cells found in flying bats were observed to be sensitive to all 3 axes ( Yartsev and Ulanovsky 2013 ; Finkelstein et al 2014 ). Behavioral experiments with fish also indicated a volumetric 3D representation of space ( Burt de Perera et al 2016 ). However, as suggested by Jeffery et al (2015) , extending spatial encoding from 2D to 3D space comes with complications such as the noncommutative property of 3D rotation, and a fully volumetric representation of 3D space might be costly and unnecessary for certain environments and species.…”

Body-relative horizontal–vertical anisotropy in human representations of traveled distances

“…In fact, this seems not to be the case: Yartsev and Ulanovsky ( 2013 ) showed that place cells in flying bats seem to encode space similar along the horizontal and vertical dimensions. A study on pelagic fish reported that these fish possess isotropic representations of the environment (Burt de Perera et al 2016 ). These findings suggest that isotropy versus anisotropy of 3D spatial representations depends on the investigated species.…”