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- Title
Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas.
- Authors
Ribeiro, Sidarta; Gervasoni, Damien; Soares, Ernesto S.; Yi Zhou; Shih-Chieh Lin; Pantoja, Janaina; Lavine, Michael; Nicolelis, Miguel A. L.; Schultz, Wolfram
- 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 experiencedependent 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...
- Subjects
RAPID eye movement sleep; MEMORY; PROSENCEPHALON; SLEEP stages; EYE movements; NEURONS; HIPPOCAMPUS (Brain); LIMBIC system; CEREBRAL cortex
- Publication
PLoS Biology, 2004, Vol 2, Issue 1, p0126
- ISSN
1544-9173
- Publication type
Article
- DOI
10.1371/journal.pbio.0020024