Study of the hippocampal place cell system has greatly enhanced our understanding of memory encoding for distinct places, but how episodic memories for distinct experiences occurring within familiar environments are encoded is less clear. We developed a spatial decision-making task in which male rats learned to navigate a multi-arm maze to a goal location for food reward while avoiding maze arms in which aversive stimuli were delivered. Task learning induced partial remapping in CA1 place cells, allowing us to identify both remapping and stable cell populations. Remapping cells were recruited into sharp wave ripples (SWRs) and associated replay events to a greater extent than stable cells, despite having similar firing rates during navigation of the maze. Our results suggest that recruitment into replay events may be a mechanism to incorporate new contextual information into a previously formed and stabilized spatial representation.SIGNIFICANCE STATEMENT:Hippocampal place cells provide a map of space which animals use to navigate. This map can change to reflect changes in the physical properties of the environment in which the animal finds itself, and also in response to non-physical contextual changes, such as changes in valence of specific locations within that environment. We show here that cells which change their spatial tuning after a change in context are preferentially recruited into SWR-associated replay events compared to stable non-remapping cells. Thus, our data lend strong support to the hypothesis that replay is a mechanism for the storage of new spatial maps.
Study of the hippocampal place cell system has greatly enhanced our understanding of memory encoding for distinct places, but how episodic memories for distinct experiences occurring within familiar environments are encoded is not clear. One possibility is that different place cell populations encode details of the novel experience or maintain the representation of the unchanged environment. We developed an aversive spatial decision making task which induced partial remapping in CA1, allowing us to identify both remapping and stable cell populations.We found that remapping cells exhibited distinct features not present in stable cells. During memory encoding, their theta phase preferences shifted to earlier phases, when CA3 inputs are strongest. Further, their recruitment into replay events increased during learning, unlike that of stable cells. Our demonstration of a sub-population of place cells identified on the basis of their degree of remapping and exhibiting unique changes in their spike firing properties with learning lend support to a model in which novel and familiar spatial/contextual information is encoded and maintained, respectively, by separate place cell populations.
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