Masala, N.; Donahue, M. M.; Boublil, B. L.; Martinez, G. I.; Abouelatta, H.; Miller, K. B.; Sabariego, M.; Ewell, L. A.

Learning to navigate a changing environment requires the ability to detect when a reward no longer matches a previous expectation. While the hippocampus is essential for adapting behavior strategies when reward expectations are violated and is known to integrate goal-related information into spatial maps, the precise dynamics by which these maps update during an unexpected reduction in reward magnitude is not well understood. Using longitudinal calcium imaging of neuronal activity in behaving mice, we found that hippocampal CA1 population activity encodes reward magnitude through elevated event rates at high value locations. Within this population, we discovered a specialized group of reward tethered place cells that bind spatial context to reward magnitude. These reward tethered place cells exhibit spatial fields across the environment while simultaneously exhibiting activity anchored to high-value reward locations. Upon reward reduction, CA1 population activity equalizes and these neurons undergo a selective and rapid remapping that precedes behavioral adjustment to the reward downshift. The broader spatial map remains intact, indicating that this change allows the animal to update the value of a goal while preserving a stable representation of its surroundings. This selective reorganization of hippocampal firing patterns could support adaptive decision making by updating internal models of the world when expectations are violated.