Reward value invariant place responses and reward site associated activity in hippocampal neurons of behaving rats

To investigate the involvement of the hippocampal‐accumbens system in goal‐oriented displacement behaviors, hippocampal neuronal activity was recorded in rats learning and recalling new distributions of different volumes of liquid reward among the arms of a plus maze. Each arm had a reward box containing a water trough and identical visual cues that could be illuminated independently. As the water‐restricted rat successively visited the respective boxes, it received 7, 5, and 3 drops of water, and then 1 drop, provided at 1‐s intervals. (Reward distributions were reassigned daily and mid‐session.) In the training phase, reward boxes were lit individually. In the recall phase, the lamps on all arms were lit and then turned off as the rat visited the boxes in order of descending value. Neuronal firing rates were analyzed for changes related to reward value or to shifts between learning and recall phases. The principal finding is that place responses remained unchanged after these manipulations and that these neurons showed no evidence of explicit coding of reward value. In addition, two other types of responses appeared while the rat was stationary at the reward boxes awaiting multiple rewards. These were observed primarily in neurons within the dentate gyrus, but also in CA1. Position‐selective reward site responses were regular at 20–60 impulses per second, while position‐independent discharges bursted irregularly at about 5 impulses per second. Such responses could explain controversial reports of reward dependence in hippocampal neurons. The higher incidence of the latter responses in the temporal (“ventral”) hippocampus is consistent with the distinctive anatomical and functional properties of this subregion. Hippocampus 2003;13:117–132. © 2003 Wiley‐Liss, Inc.