Remote activation of place codes by gaze in a highly visual animal

Abstract

Vision enables many animals to perform spatial reasoning from remote locations. By viewing distant landmarks, animals recall spatial memories and plan future trajectories. Although these spatial functions depend on hippocampal place cells, the relationship between place cells and active visual behavior is unknown. Here, we studied a highly visual animal, the chickadee, in a behavior that required alternating between remote visual search and spatial navigation. We leveraged the unique head-directed nature of avian vision to track gaze in freely moving animals. We discovered a profound link between place coding and gaze. Place cells activated not only when the chickadee was in a specific location, but also when it simply gazed at that location from a distance. Gaze coding was precisely timed by fast, ballistic head movements called "head saccades". On each saccadic cycle, the hippocampus switched between encoding a prediction of what the bird was about to see and a reaction to what it actually saw. The temporal structure of these responses was coordinated by subclasses of interneurons that fired at different phases of the saccade. We suggest that place and gaze coding are components of a unified process by which the hippocampus represents the location that an animal is currently attending to. This process allows the hippocampus to implement both local and remote spatial functions.