Hippocampal dynamics predict interindividual cognitive differences in rats.

ABSTRACT

There are important and sustained interindividual differences in cognition during aging. Here, we investigated hippocampal spatial representations in a rat model of cognitive aging characterized by individual differences in a mnemonic task. Individual cognitive capabilities in old rats were assessed in a delayed non-matching-to-position task. We recorded hippocampal CA1 place cells as the rats explored a familiar environment. Unlike the usual place cells commonly described in the literature, we found that a significant fraction of pyramidal neurons recorded in our study showed a substantial delayed onset of their place field activity. We established that this firing onset delay naturally occurs under basal conditions in old rats and is positively correlated with the remapping status of the animals. The lack of firing during the first few hundred seconds after the animals were introduced into a familiar environment was also associated with an increased locomotion in the remapping rats. This delayed activity is central to understanding the individual basis of age-related cognitive impairment and to resolving numerous discrepancies in the literature on the place cell contribution to the etiology of aged-related decline. Finally, we also found a positive correlation between the degree of firing variability of place cells ("overdispersion") and performance during the long delays in the delayed non-matching-to-position task. Place cell overdispersion might provide the functional basis for interindividual differences in behavior and cognition.