Tracking the Course of Hippocampal Representations during Learning: When Is the Map Required?

Distinct ensembles of hippocampal cells can be active in numerous contexts, but specific cognitive maps tend to be retrieved on repeat visits to the same place. During aging, the reliability of map retrieval in CA1 networks is reduced; this provides a unique opportunity to investigate correlations between inconsistent activity patterns in circuits hypothesized to enable context encoding and hippocampus-dependent learning ability. Here, CA1 pyramidal cells were recorded in six young and six old rats, while memory for specific locations was probed using a place-dependent eyeblink conditioning task. Rats were conditioned twice daily for 31 days, during which a total of 8259 and 7042 cells were recorded from young and old rats, respectively. Spontaneous remapping, a change in location of the majority of place fields between two consecutive sessions in the same environment, was observed in two young rats and four old rats during this task, but only after at least 13 days of training. Under these conditions the altered network representation did not result in loss of spatial accuracy of the blink, and in fact those rats with the best place conditioning remapped the most, whereas those with the best memory in a spatial water maze task remapped the least. These results suggest that when the hippocampal representation for a particular context is weak or unstable, such as can occur in senescence, extra-hippocampal systems that mediate alternate learning strategies are more likely to dominate behavior.