Retrosplenial Cortical Representations of Space and Future Goal Locations Develop with Learning

Recent findings suggest that long-term spatial and contextual memories depend on the retrosplenial cortex (RSC) [1–5]. RSC damage impairs navigation in humans and rodents [6–8], and the RSC is closely interconnected with brain regions known to play a role in navigation, including the hippocampus and anterior thalamus [9, 10]. Navigation-related neural activity is seen in humans [11] and rodents, including spatially localized firing [12, 13], directional firing [12, 14, 15], and responses to navigational cues [16]. RSC neuronal activity is modulated by allocentric, egocentric, and route-centered spatial reference frames [17, 18], consistent with an RSC role in integrating different kinds of navigational information [19]. However, the relationship between RSC firing patterns and spatial memory remains largely unexplored, as previous physiology studies have not employed behavioral tasks with a clear memory demand. To address this, we trained rats on a continuous T-maze alternation task and examined RSC firing patterns throughout learning. We found that the RSC developed a distributed population-level representation of the rat's spatial location and current trajectory to the goal as the rats learned. After the rats reached peak performance, RSC firing patterns began to represent the upcoming goal location as the rats approached the choice point. These neural simulations of the goal emerged at the same time that lesions impaired alternation performance, suggesting that the RSC gradually acquired task representations that contribute to navigational decision-making. Miller et al. find that spatial representations develop in the retrosplenial cortex (RSC) as rats learn a memory guided spatial navigation task. Spatial information is encoded in the form of population firing patterns, and, after learning, these firing patterns simulate future goal locations, suggesting an RSC role in navigational planning.