Remapping to discriminate contexts with hippocampal population codes

Abstract

Changes in the environment and in the internal state of an organism result in differences in hippocampal population activity, which is referred to as remapping. Studies of remapping have not only revealed the existence of a combinatorial code for space, objects, and time in hippocampus, but have also provided substantial insight into intrahippocampal computations that facilitate the acquisition, storage, and retrieval of memory. Hippocampal representations of remembered events consist of neuronal activity in place fields, which represent the location of the event, and of particular firing rates within each place field, which can reflect the current configuration of sensory inputs encountered at the current location. Perhaps not surprisingly, there is no fixed transfer function between sensory stimuli and hippocampal representations, but the firing patterns of place cells are flexibly configured and can be flexibly reconfigured. For example, the earlier processing stages in the hippocampal circuit, dentate gyrus, and CA3 generate neuronal activity patterns that distinguish new experiences from those that are already stored in memory. The new hippocampal representations can be more distinct than expected from the similarity of the current sensory input pattern compared to similar remembered patterns (pattern separation). Pattern separation may be particularly important for episodic memories because many novel experiences consist of new components that are added to otherwise familiar situations. Conversely, if parts of an event are recognized as familiar, the activation of hippocampal representations can be refined to retrieve full memories and to precisely resemble patterns that were stored earlier (pattern completion). In addition, a gradual drift of activity in hippocampal cell populations over time can be used for estimating the recency of a memory. Each hippocampal map can thus simultaneously represent the where, what, and when aspects of distinct experiences and code for the similarity between experiences.