Original Research ARTICLE

Front. Neurosci., 15 October 2007 | doi: 10.3389/neuro.

Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus

  • 1 Edmond and Lily Safra International Institute of Neuroscience of Natal (ELS-IINN), Natal, Brazi
  • 2 Department of Physiology, Universidade Federal do Rio Grande do Norte (UFRN), Natal, Brazil
  • 3 Department of Neurobiology, Duke University Medical Center, 101 Research Drive, Durham, USA
  • 4 CNRS UMR5167 – Université Claude Bernard Lyon 1, Faculté de Médecine Läennec, Lyon, France
  • 5 Laboratory of Neural Ensemble Technology, École Polytechnique Fédéale de Lausanne, Lausanne, Switzerland

Episodic and spatial memories engage the hippocampus during acquisition but migrate to the cerebral cortex over time. We have recently proposed that the interplay between slow-wave (SWS) and rapid eye movement (REM) sleep propagates recent synaptic changes from the hippocampus to the cortex. To test this theory, we jointly assessed extracellular neuronal activity, local field potentials (LFP), and expression levels of plasticity-related immediate-early genes (IEG) arc and zif-268 in rats exposed to novel spatio-tactile experience. Post-experience firing rate increases were strongest in SWS and lasted much longer in the cortex (hours) than in the hippocampus (minutes). During REM sleep, firing rates showed strong temporal dependence across brain areas: cortical activation during experience predicted hippocampal activity in the first post-experience hour, while hippocampal activation during experience predicted cortical activity in the third post-experience hour. Four hours after experience, IEG expression was specifically upregulated during REM sleep in the cortex, but not in the hippocampus. Arc gene expression in the cortex was proportional to LFP amplitude in the spindle-range (10–14 Hz) but not to firing rates, as expected from signals more related to dendritic input than to somatic output. The results indicate that hippocampo-cortical activation during waking is followed by multiple waves of cortical plasticity as full sleep cycles recur. The absence of equivalent changes in the hippocampus may explain its mnemonic disengagement over time.

Citation: Sidarta Ribeiro, Xinwu Shi, Matthew Engelhard, Yi Zhou, Hao Zhang, Damien Gervasoni, Shi-Chieh Lin, Kazuhiro Wada, Nelson A. M. Lemos and Miguel A. L. Nicolelis (2007). Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus. Front. Neurosci. 1: 1. 43-55. doi: 10.3389.neuro.01/

Received: 15 August 2007; Paper pending published: 01 September 2007;
Accepted: 01 September 2007; Published online: 15 October 2007.

Edited by:

Idan Segev, Hebrew University, Israel

Reviewed by:

Robert Stickgold, Center for Sleep and Cognition, Harvard Medical School, USA; Sumimal Datta, Sleep and Cognitive Neuroscience Laboratory, Boston University, School of Medicine

Copyright: © 2007 Ribeiro, Shi, Engelhard, Zhou, Zhang, Gervasoni, Lin, Wada, Lemos and Nicolelis. This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

*Correspondence: Sidarta Ribeiro, Edmond and Lily Safra International Institute of Neuroscience of Natal(ELS-IINN), Rua Professor Francisco Luciano de Oliveira 2460, Bairro Candelaria, Natal, RN, 59066-060, Brazil. e-mail: ribeiro@natalneuro.org.br

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