Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning

  1. Oxana Eschenko1,3,
  2. Wiâm Ramadan1,
  3. Matthias Mölle2,
  4. Jan Born2, and
  5. Susan J. Sara1,4,5
  1. 1 Neuromodulation, Neuroplasticity and Cognition, Centre National de la Recherche Scientifique (CNRS), UMR 7102, 75005 Paris, France;
  2. 2 Department of Neuroendocrinology, University of Lübeck, 23538 Lübeck, Germany

Abstract

High-frequency oscillations, known as sharp-wave/ripple (SPW-R) complexes occurring in hippocampus during slow-wave sleep (SWS), have been proposed to promote synaptic plasticity necessary for memory consolidation. We recorded sleep for 3 h after rats were trained on an odor-reward association task. Learning resulted in an increased number SPW-Rs during the first hour of post-learning SWS. The magnitude of ripple events and their duration were also elevated for up to 2 h after the newly formed memory. Rats that did not learn the discrimination during the training session did not show any change in SPW-Rs. Successful retrieval from remote memory was likewise accompanied by an increase in SPW-R density and magnitude, relative to the previously recorded baseline, but the effects were much shorter lasting and did not include increases in ripple duration and amplitude. A short-lasting increase of ripple activity was also observed when rats were rewarded for performing a motor component of the task only. There were no increases in ripple activity after habituation to the experimental environment. These experiments show that the characteristics of hippocampal high-frequency oscillations during SWS are affected by prior behavioral experience. Associative learning induces robust and sustained (up to 2 h) changes in several SPW-R characteristics, while after retrieval from remote memory or performance of a well-trained procedural aspect of the task, only transient changes in ripple density were induced.

Footnotes

  • 3 Max Planck Institute for Biological Cybernetics, Department of Physiology of Cognitive Processes, D-72076 Tübingen, Germany;

  • 4 Collège de France, Centre National de la Recherche Scientifique, F-75005, Paris, France.

  • 5 Corresponding author.

    5 E-mail sjsara{at}ccr.jussieu.fr; fax 33-1-44273252.

  • Article is online at http://www.learnmem.org/cgi/doi/10.1101/lm.726008.

    • Received August 3, 2007.
    • Accepted January 24, 2008.
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