Adaptation of hippocampal spatial and contextual representations to task structure

The hippocampus is fundamental for spatial and contextual memory. CA1 pyramidal neurons (CA1PNs) exhibit spatially tuned activity during navigation, but how their context-dependent tuning evolves during learning and upon context change is incompletely understood. We monitored Ca²⁺ activity of dorsal CA1PNs in mice in a virtual go/no-go task series that required both spatial navigation and rule learning based on nonspatial environmental features. Spatial and context-dependent activity of CA1PNs developed sequentially during learning, parallel with behavioral performance. Upon switching to a new task condition involving familiar and novel environments, neuronal activity disorganized rapidly and extensively even in the unchanged environment. In contrast, reward reversal in unchanged environments induced more gradual activity changes, associated with behavioral adaptation. Our results indicate that, during learning a spatial-contextual task, CA1PNs initially generalize between environments coding primarily spatial position, but, with experience, their activity gradually reorganizes to form partially distinct representations within a shared contextual framework.