A telencephalon cell type atlas for goldfish reveals diversity in the evolution of spatial structure and cell types.

Teleost fish form the largest group of vertebrates and show a tremendous variety of adaptive behaviors, making them critically important for the study of brain evolution and cognition. The neural basis mediating these behaviors remains elusive. We performed a systematic comparative survey of the goldfish telencephalon. We mapped cell types using single-cell RNA sequencing and spatial transcriptomics, resulting in de novo molecular neuroanatomy parcellation. Glial cells were highly conserved across 450 million years of evolution separating mouse and goldfish, while neurons showed diversity and modularity in gene expression. Specifically, somatostatin interneurons, famously interspersed in the mammalian isocortex for local inhibitory input, were curiously aggregated in a single goldfish telencephalon nucleus but molecularly conserved. Cerebral nuclei including the striatum, a hub for motivated behavior in amniotes, had molecularly conserved goldfish homologs. We suggest elements of a hippocampal formation across the goldfish pallium. Last, aiding study of the teleostan everted telencephalon, we describe substantial molecular similarities between goldfish and zebrafish neuronal taxonomies.

Toward Naturalistic Neuroscience of Navigation: Opportunities in Coral Reef Fish.

The ability to navigate in the world is crucial to many species. One of the most fundamental unresolved issues in understanding animal navigation is how the brain represents spatial information. Although navigation has been studied extensively in many taxa, the key efforts to determine the neural basis of navigation have focused on mammals, usually in lab experiments, where the allocated space is typically very small; e.g., up to one order of magnitude the size of the animal, is limited by artificial walls, and contains only a few objects. This type of setting is vastly different from the habitat of animals in the wild, which is open in many cases and is virtually limitless in size compared to its inhabitants. Thus, a fundamental open question in animal navigation is whether small-scale, spatially confined, and artificially crafted lab experiments indeed reveal how navigation is enacted in the real world. This question is difficult to study given the technical problems associated with in vivo electrophysiology in natural settings. Here, we argue that these difficulties can be overcome by implementing state of the art technology when studying the rivulated rabbitfish, Siganus rivulatus as the model animal. As a first step toward this goal, using acoustic tracking of the reef, we demonstrate that individual S. rivulatus have a defined home range of about 200 m in length, from which they seldom venture. They repeatedly visit the same areas and return to the same sleeping grounds, thus providing evidence for their ability to navigate in the reef environment. Using a clustering algorithm to analyze segments of daily trajectories, we found evidence of specific repeating patterns in behavior within the home range of individual fish. Thus, S. rivulatus appears to have the ability to carry out its daily routines and revisit places of interest by employing sophisticated means of navigation while exploring its surroundings. In the future, using novel technologies for wireless recording from single cells of fish brains, S. rivulatus can emerge as an ideal system to study the neural basis of navigation in natural settings and lead to "electrophysiology in the wild."

From fish out of water to new insights on navigation mechanisms in animals.

Navigation is a critical ability for animal survival and is important for food foraging, finding shelter, seeking mates and a variety of other behaviors. Given their fundamental role and universal function in the animal kingdom, it makes sense to explore whether space representation and navigation mechanisms are dependent on the species, ecological system, brain structures, or whether they share general and universal properties. One way to explore this issue behaviorally is by domain transfer methodology, where one species is embedded in another species' environment and must cope with an otherwise familiar (in our case, navigation) task. Here we push this idea to the limit by studying the navigation ability of a fish in a terrestrial environment. For this purpose, we trained goldfish to use a Fish Operated Vehicle (FOV), a wheeled terrestrial platform that reacts to the fish's movement characteristics, location and orientation in its water tank to change the vehicle's; i.e., the water tank's, position in the arena. The fish were tasked to "drive" the FOV towards a visual target in the terrestrial environment, which was observable through the walls of the tank, and indeed were able to operate the vehicle, explore the new environment, and reach the target regardless of the starting point, all while avoiding dead-ends and correcting location inaccuracies. These results demonstrate how a fish was able to transfer its space representation and navigation skills to a wholly different terrestrial environment, thus supporting the hypothesis that the former possess a universal quality that is species-independent.