A population code for spatial representation in the larval zebrafish telencephalon

The vertebrate telencephalon is the site of complex cognitive processes such as spatial cognition. The larval zebrafish telencephalon is a compact circuit of ~10,000 neurons that nevertheless contains homologous structures to the mammalian basal ganglia and limbic system (e.g. hippocampus and amygdala). However, despite long-standing evidence that spatial navigation and learning in adult fish requires an intact telencephalon, cells believed to underlie spatial cognition in mammals (e.g. place and grid cells) have yet to be established in any fish species. Using a tracking microscope to image brain-wide activity at cellular resolution in freely swimming larval zebrafish, we can compute the spatial specificity of every cell in the zebrafish brain. Strikingly, in every animal, cells with the highest spatial specificity are enriched in the zebrafish telencephalon. These cells form a population code of space, from which we can decode the animal’s spatial location across time. In a novel environment, the activity of these place-encoding cells undergoes remapping. In a constant environment, the activity manifold of place-encoding cells gradually untangles across time. Given the compact nature of the zebrafish telencephalon, this reduced model system is uniquely positioned for building a complete mechanistic model of spatial cognition.