Dynamic cognitive representations in the dorsal pallium of adult zebrafish

Brains rely on internal models of the world to interpret sensory input and to simulate the future. In the mammalian hippocampal-entorhinal network, environments are represented by cognitive maps that contain spatially selective neurons such as place, grid, head direction and object-vector cells. Neurons with allocentric spatial tuning have recently been discovered also in non-mammalian organisms including larval zebrafish but it remains unclear to what extent these neurons establish internal cognitive representations. We measured neuronal activity in telencephalic area Dc of head-fixed adult zebrafish exploring a novel, richly structured virtual reality. Neurons were sharply tuned to one or multiple locations and collectively represented environmental space. Activity fields exhibited neuron-specific associations to visual landmarks, indicating a prominent vectorial component in spatial representations. Population activity evolved and became increasingly informative as fish explored the environment. When landmarks were removed after familiarization, landmark-associated activity partially persisted and subsets of neurons reported prediction errors, implying that activity was in part driven by an internal representation. Strong functional coupling among neuronal ensembles and winner-take-all dynamics suggest that representations evolve by refinements of pre-structured networks. The teleost brain therefore generates internal models of structured environments that are optimized by experience and enable cognitive inference and prediction.