HIPPOCAMPAL REPLAY IN A NOVEL ENVIRONMENT: INFORMATION CONTENT AND INTERACTION WITH PREFRONTAL NEURONAL ACTIVITIES
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Date
2014-03-10
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Johns Hopkins University
Abstract
Hippocampal place-cell replay has been proposed as a fundamental mechanism of learning and memory, which might support navigational learning and planning. An important hypothesis of relevance to these proposed functions is that the information encoded in replay should reflect the topological structure of experienced environments, that is, which places in the environment are connected with which others. Here we report several attributes of replay observed in rats exploring a novel forked environment that support the hypothesis. First, we observed that spatially overlapping replays depicting divergent trajectories through the fork recruited the same population of cells with the same firing rates to represent the common portion of the trajectories. Second, replay tended to be directional and to flip the represented direction at the fork. Third, replay-associated sharp-wave-ripple events in the local field potential exhibited substructure that mapped onto the maze topology. Thus the spatial complexity of our recording environment was accurately captured by replay: the underlying neuronal activities reflected the bifurcating shape, and both directionality and associated ripple structure reflected the segmentation of the maze. Moreover, we observed that replays occurred rapidly after small numbers of experiences. To further investigate the potential role of sequence replay in cross-structural network functions, we addressed the question of whether and how hippocampal replay interacts with prefrontal processes. We found strong modulations of simultaneously recorded medial prefrontal neuronal activities by running direction on track arms as well as reward conditions at arm ends, indicating their active involvement in task performance. Importantly, prefrontal neurons exhibited substantial firing-rate changes consistently at the occurrences of hippocampal replay, with a subset of neurons showing significantly different response patterns to replays representing different arms of the maze. Our results suggest that hippocampal replay rapidly captures learned information about environmental topology to support a role in navigation, possibly through informing prefrontal activities in spatial decision making processes.
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Keywords
Hippocampus, Place cells, Replay, Prefrontal cortex, Spatial Navigation