Abstract

Gamma rhythms are known to contribute to the process of memory encoding. However, little is known about the underlying mechanisms at the molecular, cellular and network levels. Using local field potential recording in awake behaving mice and concomitant field-potential and whole-cell recordings in slice preparations we found that gamma rhythms lead to activity-dependent modification of hippocampal networks, including alterations in sharp wave-ripple complexes. Network plasticity, expressed as long-lasting increases in sharp wave-associated synaptic currents, exhibits enhanced excitatory synaptic strength in pyramidal cells that is induced postsynaptically and depends on metabotropic glutamate receptor-5 activation. In sharp contrast, alteration of inhibitory synaptic strength is independent of postsynaptic activation and less pronounced. Further, we found a cell type-specific, directionally biased synaptic plasticity of two major types of GABAergic cells, parvalbumin- and cholecystokinin-expressing interneurons. Thus, we propose that gamma frequency oscillations represent a network state that introduces long-lasting synaptic plasticity in a cell-specific manner.

Article and author information

Author details

  1. Shota Zarnadze

    Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Peter Bäuerle

    Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Julio Santos-Torres

    Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Claudia Böhm

    Neuroscience Research Center, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Dietmar Schmitz

    Neuroscience Research Center, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Jörg RP Geiger

    Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Tamar Dugladze

    Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Tengis Gloveli

    Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany
    For correspondence
    tengis.gloveli@charite.de
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Marlene Bartos, Albert-Ludwigs-Universität Freiburg, Germany

Ethics

Animal experimentation: All animal procedures were approved by the Regional Berlin Animal Ethics Committee (Permits: G0151/12 and T 0124/05) and were in full compliance with national regulations. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Version history

  1. Received: February 2, 2016
  2. Accepted: May 23, 2016
  3. Accepted Manuscript published: May 24, 2016 (version 1)
  4. Accepted Manuscript updated: May 26, 2016 (version 2)
  5. Version of Record published: June 30, 2016 (version 3)

Copyright

© 2016, Zarnadze et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Shota Zarnadze
  2. Peter Bäuerle
  3. Julio Santos-Torres
  4. Claudia Böhm
  5. Dietmar Schmitz
  6. Jörg RP Geiger
  7. Tamar Dugladze
  8. Tengis Gloveli
(2016)
Cell-specific synaptic plasticity induced by network oscillations
eLife 5:e14912.
https://doi.org/10.7554/eLife.14912

Share this article

https://doi.org/10.7554/eLife.14912

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