Changing reward expectation transforms spatial encoding and retrieval in the hippocampus

Abstract

Internal states of reward expectation play a central role in influencing the strength of spatial memories. At the cellular level, spatial memories are represented through the firing dynamics of hippocampal place cells. However, it remains unclear how internal states of reward expectation influence place cell dynamics and exert their effects on spatial memories. Here we show that when reward expectation is altered, the same environment becomes encoded by a distinct ensemble of place cells at all locations. Further, when reward expectation is high versus low, place cells demonstrate enhanced reliability during navigation and greater stability across days at all locations within the environment. These findings reveal that when rewards are expected, neuromodulatory circuits that represent internal reward expectation support and strengthen the encoding and retrieval of spatial information by place cells at all locations that lead to reward. This enhanced spatial memory can be used to guide future decisions about which locations are most likely to lead to rewards that are crucial for survival.