Like most animals, the survival of fish depends on navigation in space. This capacity has been documented in behavioral studies that have revealed navigation strategies. However, little is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. We found that cells in the lateral pallium of the goldfish encode the edges of the environment, the fish head direction, the fish swimming speed, and the fish swimming velocity-vector. This study sheds light on how information related to navigation is represented in the brain of fish and addresses the fundamental question of the neural basis of navigation in this group of vertebrates.

Navigation by mammals is believed to rely on a network of neurons in the hippocampal formation, which includes the hippocampus, the medial entorhinal cortex (MEC), and additional nearby regions. Neurons in these regions represent spatial information by tuning to the position, orientation, and speed of the animal in the form of head direction cells, speed cells, grid cells, border cells, and unclassified spatially modulated cells. While the properties of single cells are well studied, little is known about the functional structure of the network in the MEC. Here, we use a generalized linear model to study the network of spatially modulated cells in the MEC. We found connectivity patterns between all spatially encoding cells and not only grid cells. In addition, the neurons' past activity contributed to the overall activity patterns. Finally, position-modulated cells and head direction cells differed in the dependence of the activity on the history. Our results indicate that MEC neurons form a local interacting network to support spatial information representations and suggest an explanation for their complex temporal properties.

Like most animals, the survival of fish depends crucially on navigation in space.This capacity has been documented in numerous behavioral studies that have revealed navigation strategies and the sensory modalities used for navigation. All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/291013 doi: bioRxiv preprint first posted online Mar. 28, 2018; Navigation is a fundamental behavioral capacity facilitating survival in many animal species (4-7). It involves the continuous estimation and representation of the agent's position and direction in the environment which are implemented in the planning and execution of movements and trajectories towards target locations (8,9). Navigation has been investigated extensively on numerous taxa across the animal kingdom but attempts to probe its neural substrate have mainly been focused on mammals (10) and insects (11). In mammals, neurons in the hippocampal formation encode information about the position and orientation of the animal in space (8-10, 12, 13 (18,19). In insects, a ring-shaped neural network in the central complex of fruit fly was shown to represent its heading direction (11).To better understand space representation in other taxa, we explored the neural substrate of navigation in the goldfish (Carassius auratus). These fish are known to be able to navigate either by exploiting an allocentric or an egocentric frame of reference.This may imply that the goldfish has the ability to build an internal representation of space in the form of a cognitive map (3). This would include cognitive map-like navigation strategies to find a goal when starting from an unfamiliar initial position, or taking shorter alternative routes (shortcuts) when possible (2,3,20,21). Furthermore, goldfish use many environmental cues, such that any single cue would not be crucial in itself to navigating in the environment (21).In addition to these behavioral studies, lesion studies on goldfish have shown that the telencephalon is crucial for spatial navigation. Damage to the lateral pallium in the telencephalon leads to dramatic impairment in allocentric spatial memory and learning, but not when the lesion affects other parts of the telencephalon (21). These finding are similar to results from lesions studies of the hippocampus in mammals and further confirm that the lateral pallium in goldfish is a possible homologue of the mammalian All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/291013 doi: bioRxiv preprint first posted online Mar. 28, 2018; hippocampus (3, 22) (but see also (23)). While these works have contributed to suggesting where the possible navigation mechanism is located in the...