A test of the time estimation hypothesis of place cell goal-related activity

Place cells are hippocampal pyramidal neurons that discharge strongly in relation to the rat's location in the environment. We recently reported that many place cells recorded from rats performing place or cue navigation tasks also discharged when they were at the goal location rather than in the primary firing field. Furthermore, subtle differences in discharge timing were found in the two navigation tasks, with activity occurring later in the place task compared to the cue task. Here we tested the possibility that such delayed firing in the place task may reflect the differential involvement of time estimation, which would allow the rat to predict forthcoming reward delivery. More specifically, we reasoned that failure to obtain a reward after a fixed 2s delay in the place task reliably reflected the rat's misplacement relative to the correct location, thus making time a valuable cue to help the rat perform the task. To test this hypothesis, well-trained rats were run on a partial extinction procedure in place and cue navigation tasks so that no feed-back signal was provided about their actual accuracy during extinction periods. Although the time estimation hypothesis predicts that only in the place task will the rat make correction movements at the end of goal periods during extinction, we found that such movements occurred in all rats, indicating correct time estimation in both place and cue tasks. We briefly discuss the results in the light of current computational theories of hippocampal function.