Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats

Although extensive behavioral studies have demonstrated that hippocampal lesions impair navigation toward specific places, the role of hippocampal neuronal activity in the development of efficient navigation during place learning remains unknown. The aim of the present study was to investigate how hippocampal neuronal activity changes as rats learn to navigate efficiently to acquire rewards in an open field. Rats were pre-trained in a random reward task where intracranial self-stimulation rewards were provided at random locations. Then, the rats were trained in a novel place task where they were rewarded at two specific locations as they repeatedly shuttled between them. Hippocampal neuronal activity was recorded during the course of learning of the place task. The rats learned reward sites within several sessions, and gradually developed efficient navigation strategies throughout the learning sessions. Some hippocampal neurons gradually changed spatial firing as the learning proceeded, and discharged robustly near the reward sites when efficient navigation was established. Over the learning sessions, the neuronal activity was highly correlated to formation of efficient shuttling trajectories between the reward sites. At the end of the experiment, spatial firing patterns of the hippocampal neurons were re-examined in the random reward task. The specific spatial firing patterns of the neurons were preserved if the rats navigated, as if they expected to find rewards at the previously valid locations. However, those specific spatial firing patterns were not observed in rats pursuing random trajectories. These results suggest that hippocampal neurons have a crucial role in formation of an efficient navigation.