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Induction of sharp wave–ripple complexes in vitro and reorganization of hippocampal networks

Nature Neuroscience volume 8, pages 1560–1567 (2005)Cite this article

Abstract

Hippocampal sharp wave–ripple complexes (SPW-Rs) occur during slow-wave sleep and behavioral immobility and are thought to represent stored information that is transferred to the neocortex during memory consolidation. Here we show that stimuli that induce long-term potentiation (LTP), a neurophysiological correlate of learning and memory, can lead to the generation of SPW-Rs in rat hippocampal slices. The induced SPW-Rs have properties that are identical to spontaneously generated SPW-Rs: they originate in CA3, propagate to CA1 and subiculum and require AMPA/kainate receptors. Their induction is dependent on NMDA receptors and involves changes in interactions between clusters of neurons in the CA3 network. Their expression is blocked by low-frequency stimulation but not by NMDA receptor antagonists. These data indicate that induction of LTP in the recurrent CA3 network may facilitate the generation of SPW-Rs.

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Figure 1: Recurrent stimulation induces SPW-Rs in area CA3.
Figure 2: Sample recording of HFS-induced SPW-Rs.
Figure 3: Origin of HFS-induced SPW-Rs.
Figure 4: Stimulation dependence and pharmacological properties of SPW-Rs.
Figure 5: Facilitated SPW-R induction in the presence of a physiological concentration of extracellular Mg2+.
Figure 6: Different types of changes in neuronal behavior during evolvement of SPW-Rs.
Figure 7: Stimulus-specific cell response in area CA3 during HFS-induced SPW-R activity.

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Acknowledgements

This research was supported by the Sonderforschungsbereich 515. We are grateful for discussions with M.J. Gutnick and D. Schmitz, and for technical assistance and the development of data analysis tools by H. Siegmund and H.J. Gabriel. We acknowledge participation of N. Maggio in some of the recordings in dorsal hippocampal slices.

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Authors and Affiliations

  1. Institute for Neurophysiology, Charité-Universitätsmedizin Berlin, Tucholskystrasse 2, Berlin, 10117, Germany

    Christoph J Behrens, Leander P van den Boom, Livia de Hoz, Alon Friedman & Uwe Heinemann

  2. Department of Neurosurgery, Zlotowski Centre for Neuroscience, Ben-Gurion University of the Negev and Soroka Medical Center, Beer-Sheva, 84105, Israel

    Alon Friedman

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Correspondence to Uwe Heinemann.

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Supplementary information

Supplementary Fig. 1

Spontaneous SPW-R activity recorded in the CA3 region. (PDF 354 kb)

Supplementary Fig. 2

SPW-R induction parallels induction of LTP in area CA3. (PDF 99 kb)

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Behrens, C., van den Boom, L., de Hoz, L. et al. Induction of sharp wave–ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8, 1560–1567 (2005). https://doi.org/10.1038/nn1571

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