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      Awake replay of remote experiences in the hippocampus

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      Nature neuroscience

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          Abstract

          Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal–neocortical networks. Replay is present during both sleep and waking behavior, but while sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was most robust when the animal had recently been in motion as compared to during extended periods of quiescence. These results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.

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          Most cited references35

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          Loss of recent memory after bilateral hippocampal lesions.

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            Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point.

            Neural ensembles were recorded from the CA3 region of rats running on T-based decision tasks. Examination of neural representations of space at fast time scales revealed a transient but repeatable phenomenon as rats made a decision: the location reconstructed from the neural ensemble swept forward, first down one path and then the other. Estimated representations were coherent and preferentially swept ahead of the animal rather than behind the animal, implying it represented future possibilities rather than recently traveled paths. Similar phenomena occurred at other important decisions (such as in recovery from an error). Local field potentials from these sites contained pronounced theta and gamma frequencies, but no sharp wave frequencies. Forward-shifted spatial representations were influenced by task demands and experience. These data suggest that the hippocampus does not represent space as a passive computation, but rather that hippocampal spatial processing is an active process likely regulated by cognitive mechanisms.
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              Reactivation of hippocampal ensemble memories during sleep.

              Simultaneous recordings were made from large ensembles of hippocampal "place cells" in three rats during spatial behavioral tasks and in slow-wave sleep preceding and following these behaviors. Cells that fired together when the animal occupied particular locations in the environment exhibited an increased tendency to fire together during subsequent sleep, in comparison to sleep episodes preceding the behavioral tasks. Cells that were inactive during behavior, or that were active but had non-overlapping spatial firing, did not show this increase. This effect, which declined gradually during each post-behavior sleep session, may result from synaptic modification during waking experience. Information acquired during active behavior is thus re-expressed in hippocampal circuits during sleep, as postulated by some theories of memory consolidation.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                29 April 2009
                14 June 2009
                July 2009
                1 January 2010
                : 12
                : 7
                : 913-918
                Affiliations
                W.M. Keck Center for Integrative Neuroscience and Department of Physiology, University of California, San Francisco, CA 94143-0444
                Author notes

                Author Contributions

                M.K and L.F. designed the experimental paradigm; M.K. carried out all of the data collection and the majority of the analyses; L.F. carried out the remaining analyses; M.K. and L.F. wrote the manuscript.

                Article
                nihpa113938
                10.1038/nn.2344
                2750914
                19525943
                6a78d014-b9ff-42a4-aaa6-3f16a5dcd35a
                History
                Funding
                Funded by: National Institute of Mental Health : NIMH
                Award ID: R01 MH080283-01 ||MH
                Funded by: National Institute of Mental Health : NIMH
                Award ID: P50 MH077970-01 ||MH
                Categories
                Article

                Neurosciences
                Neurosciences

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