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Short-Range Temporal Interactions in Sleep; Hippocampal Spike Avalanches Support a Large Milieu of Sequential Activity Including Replay

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      Abstract

      Hippocampal neural systems consolidate multiple complex behaviors into memory. However, the temporal structure of neural firing supporting complex memory consolidation is unknown. Replay of hippocampal place cells during sleep supports the view that a simple repetitive behavior modifies sleep firing dynamics, but does not explain how multiple episodes could be integrated into associative networks for recollection during future cognition. Here we decode sequential firing structure within spike avalanches of all pyramidal cells recorded in sleeping rats after running in a circular track. We find that short sequences that combine into multiple long sequences capture the majority of the sequential structure during sleep, including replay of hippocampal place cells. The ensemble, however, is not optimized for maximally producing the behavior-enriched episode. Thus behavioral programming of sequential correlations occurs at the level of short-range interactions, not whole behavioral sequences and these short sequences are assembled into a large and complex milieu that could support complex memory consolidation.

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      Most cited references 26

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      Modularity and community structure in networks

       M. Newman (2006)
      Many networks of interest in the sciences, including a variety of social and biological networks, are found to divide naturally into communities or modules. The problem of detecting and characterizing this community structure has attracted considerable recent attention. One of the most sensitive detection methods is optimization of the quality function known as "modularity" over the possible divisions of a network, but direct application of this method using, for instance, simulated annealing is computationally costly. Here we show that the modularity can be reformulated in terms of the eigenvectors of a new characteristic matrix for the network, which we call the modularity matrix, and that this reformulation leads to a spectral algorithm for community detection that returns results of better quality than competing methods in noticeably shorter running times. We demonstrate the algorithm with applications to several network data sets.
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        Reverse replay of behavioural sequences in hippocampal place cells during the awake state.

        The hippocampus has long been known to be involved in spatial navigational learning in rodents, and in memory for events in rodents, primates and humans. A unifying property of both navigation and event memory is a requirement for dealing with temporally sequenced information. Reactivation of temporally sequenced memories for previous behavioural experiences has been reported in sleep in rats. Here we report that sequential replay occurs in the rat hippocampus during awake periods immediately after spatial experience. This replay has a unique form, in which recent episodes of spatial experience are replayed in a temporally reversed order. This replay is suggestive of a role in the evaluation of event sequences in the manner of reinforcement learning models. We propose that such replay might constitute a general mechanism of learning and memory.
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          The organization of recent and remote memories.

          A fundamental question in memory research is how our brains can form enduring memories. In humans, memories of everyday life depend initially on the medial temporal lobe system, including the hippocampus. As these memories mature, they are thought to become increasingly dependent on other brain regions such as the cortex. Little is understood about how new memories in the hippocampus are transformed into remote memories in cortical networks. However, recent studies have begun to shed light on how remote memories are organized in the cortex, and the molecular and cellular events that underlie their consolidation.
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            Author and article information

            Affiliations
            [1 ]Department of Neurological Sciences, University of Vermont College of Medicine, Burlington, Vermont, 05405, United States of America
            [2 ]Department of Neurosurgery, University of California Los Angeles, Los Angeles, California, 90095, United States of America
            [3 ]Neurosciences Unit, University College London Institute of Child Health, London, United Kingdom
            University of Lethbridge, CANADA
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            Conceived and designed the experiments: JMM AST RCS. Performed the experiments: AST. Analyzed the data: JMM AST AEH. Wrote the paper: JMM AST AEH RCS.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, CA USA )
            1932-6203
            11 February 2016
            2016
            : 11
            : 2
            26866597
            4750866
            10.1371/journal.pone.0147708
            PONE-D-15-37131
            (Editor)
            © 2016 Mahoney et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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            Figures: 6, Tables: 4, Pages: 25
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            Funding
            The work was supported by the following: National Institutes of Health grants (RCS): NS074450, NS073083, and R01-NS075249; and Great Ormond Street Hospital Children’s Charity (RCS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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            Biology and Life Sciences
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            Physiological Processes
            Sleep
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