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      Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas

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          Abstract

          The discovery of experience-dependent brain reactivation during both slow-wave (SW) and rapid eye-movement (REM) sleep led to the notion that the consolidation of recently acquired memory traces requires neural replay during sleep. To date, however, several observations continue to undermine this hypothesis. To address some of these objections, we investigated the effects of a transient novel experience on the long-term evolution of ongoing neuronal activity in the rat forebrain. We observed that spatiotemporal patterns of neuronal ensemble activity originally produced by the tactile exploration of novel objects recurred for up to 48 h in the cerebral cortex, hippocampus, putamen, and thalamus. This novelty-induced recurrence was characterized by low but significant correlations values. Nearly identical results were found for neuronal activity sampled when animals were moving between objects without touching them. In contrast, negligible recurrence was observed for neuronal patterns obtained when animals explored a familiar environment. While the reverberation of past patterns of neuronal activity was strongest during SW sleep, waking was correlated with a decrease of neuronal reverberation. REM sleep showed more variable results across animals. In contrast with data from hippocampal place cells, we found no evidence of time compression or expansion of neuronal reverberation in any of the sampled forebrain areas. Our results indicate that persistent experience-dependent neuronal reverberation is a general property of multiple forebrain structures. It does not consist of an exact replay of previous activity, but instead it defines a mild and consistent bias towards salient neural ensemble firing patterns. These results are compatible with a slow and progressive process of memory consolidation, reflecting novelty-related neuronal ensemble relationships that seem to be context- rather than stimulus-specific. Based on our current and previous results, we propose that the two major phases of sleep play distinct and complementary roles in memory consolidation: pretranscriptional recall during SW sleep and transcriptional storage during REM sleep.

          Abstract

          Rats exposed to novel objects during periods of wakefulness generate neural activity that is correlated with patterns observed in subsequent sleep episodes

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          Most cited references53

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          Loss of recent memory after bilateral hippocampal lesions.

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            Place units in the hippocampus of the freely moving rat.

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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
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                January 2004
                20 January 2004
                : 2
                : 1
                : e24
                Affiliations
                [1] 1Department of Neurobiology, Duke University Medical Center Durham, North CarolinaUnited States of America
                [2] 2Institute of Statistics and Decision Sciences, Duke University Durham, North CarolinaUnited States of America
                [3] 3Department of Biomedical Engineering, Duke University Durham, North CarolinaUnited States of America
                [4] 4Department of Psychological Brain Sciences, Duke University Durham, North CarolinaUnited States of America
                [5] 5Duke University Center for Neuro-Engineering, Duke University Durham, North CarolinaUnited States of America
                Article
                10.1371/journal.pbio.0020024
                314474
                14737198
                b1164ae0-8931-4b13-8118-6b41f2217312
                Copyright: © 2004 Ribeiro 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 work is properly cited
                History
                : 1 September 2003
                : 21 November 2003
                Categories
                Research Article
                Neuroscience
                Rattus (Rat)

                Life sciences
                Life sciences

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