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      Memory trace replay: the shaping of memory consolidation by neuromodulation

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          Highlights

          • Memory trace replay results from lingering excitability and synaptic plasticity.

          • The balance of replay mechanisms may be determined by neuromodulation.

          • Acetylcholine release can shape the direction of replay in sharp wave ripples.

          • Dopamine release can dictate which cell assemblies are replayed.

          Abstract

          The consolidation of memories for places and events is thought to rely, at the network level, on the replay of spatially tuned neuronal firing patterns representing discrete places and spatial trajectories. This occurs in the hippocampal-entorhinal circuit during sharp wave ripple events (SWRs) that occur during sleep or rest. Here, we review theoretical models of lingering place cell excitability and behaviorally induced synaptic plasticity within cell assemblies to explain which sequences or places are replayed. We further provide new insights into how fluctuations in cholinergic tone during different behavioral states might shape the direction of replay and how dopaminergic release in response to novelty or reward can modulate which cell assemblies are replayed.

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          Most cited references94

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          Memory--a century of consolidation.

          J McGaugh (2000)
          The memory consolidation hypothesis proposed 100 years ago by Müller and Pilzecker continues to guide memory research. The hypothesis that new memories consolidate slowly over time has stimulated studies revealing the hormonal and neural influences regulating memory consolidation, as well as molecular and cellular mechanisms. This review examines the progress made over the century in understanding the time-dependent processes that create our lasting memories.
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            The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat.

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              Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval.

              The hippocampus is required for the encoding, consolidation and retrieval of event memories. Although the neural mechanisms that underlie these processes are only partially understood, a series of recent papers point to awake memory replay as a potential contributor to both consolidation and retrieval. Replay is the sequential reactivation of hippocampal place cells that represent previously experienced behavioral trajectories and occurs frequently in the awake state, particularly during periods of relative immobility. Awake replay may reflect trajectories through either the current environment or previously visited environments that are spatially remote. The repetition of learned sequences on a compressed time scale is well suited to promote memory consolidation in distributed circuits beyond the hippocampus, suggesting that consolidation occurs in both the awake and sleeping animal. Moreover, sensory information can influence the content of awake replay, suggesting a role for awake replay in memory retrieval.
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                Author and article information

                Contributors
                Journal
                Trends Neurosci
                Trends Neurosci
                Trends in Neurosciences
                Elsevier Applied Science Publishing
                0166-2236
                1878-108X
                1 September 2015
                September 2015
                : 38
                : 9
                : 560-570
                Affiliations
                [1 ]School of Physiology and Pharmacology, University of Bristol, Bristol, BS8 1TD, UK
                [2 ]Medical Research Council Brain Network Dynamics Unit at the University of Oxford, Department of Pharmacology, Oxford, OX1 3TH, UK
                Article
                S0166-2236(15)00155-1
                10.1016/j.tins.2015.07.004
                4712256
                26275935
                5bafa476-f7aa-4b9c-97d8-64b5f69a07a2
                © 2015 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                Categories
                Review

                Neurosciences
                hippocampus,sharp-wave ripples,replay,synaptic plasticity,dopamine,acetylcholine
                Neurosciences
                hippocampus, sharp-wave ripples, replay, synaptic plasticity, dopamine, acetylcholine

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