Cell-specific synaptic plasticity induced by network oscillations

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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.

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Shota Zarnadze

Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany

Competing interests
The authors declare that no competing interests exist.
Peter Bäuerle

Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany

Competing interests
The authors declare that no competing interests exist.
Julio Santos-Torres

Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany

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The authors declare that no competing interests exist.
Claudia Böhm

Neuroscience Research Center, Charité -Universitätsmedizin Berlin, Berlin, Germany

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The authors declare that no competing interests exist.
Dietmar Schmitz

Neuroscience Research Center, Charité -Universitätsmedizin Berlin, Berlin, Germany

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The authors declare that no competing interests exist.
Jörg RP Geiger

Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany

Competing interests
The authors declare that no competing interests exist.
Tamar Dugladze

Institute of Neurophysiology, Charité -Universitätsmedizin Berlin, Berlin, Germany

Competing interests
The authors declare that no competing interests exist.
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.

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.

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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.