Coherent Phasic Excitation during Hippocampal Ripples

Nikolaus Maier; Álvaro Tejero-Cantero; Anja L. Dorrn; Jochen Winterer; Prateep S. Beed; Genela Morris; Richard Kempter; James F.A. Poulet; Christian Leibold; Dietmar Schmitz

doi:10.1016/j.neuron.2011.08.016

Coherent Phasic Excitation during Hippocampal Ripples

Nikolaus Maier, Álvaro Tejero-Cantero, Anja L. Dorrn, Jochen Winterer, Prateep S. Beed, Genela Morris, Richard Kempter, James F.A. Poulet, Christian Leibold, Dietmar Schmitz

Department of Neurobiology

Research output: Contribution to journal › Article › peer-review

Abstract

High-frequency hippocampal network oscillations, or "ripples," are thought to be involved in episodic memory. According to current theories, memory traces are represented by assemblies of principal neurons that are activated during ripple-associated network states. Here we performed in vivo and in vitro experiments to investigate the synaptic mechanisms during ripples. We discovered postsynaptic currents that are phase-locked to ripples and coherent among even distant CA1 pyramidal neurons. These fast currents are consistent with excitatory postsynaptic currents (EPSCs) as they are observed at the equilibrium potential of Cl ^-, and they display kinetics characteristic of EPSCs. Furthermore, they survived after intracellular blockade of GABAergic transmission and are effective to regulate the timing of action potentials. In addition, our data show a progressive synchronization of phasic excitation and inhibition during the course of ripples. Together, our results demonstrate the presence of phasic excitation during ripples reflecting an exquisite temporal coordination of assemblies of active pyramidal cells.

Original language	English
Pages (from-to)	137-152
Number of pages	16
Journal	Neuron
Volume	72
Issue number	1
DOIs	https://doi.org/10.1016/j.neuron.2011.08.016
State	Published - 6 Oct 2011

Bibliographical note

Funding Information:
We wish to thank Sarah Shoichet, Anja Gundlfinger, Alexey Ponomarenko, Christian Wozny, José R. Donoso, Nikolai Axmacher, and Robert Schmidt for constructive comments on earlier versions of the manuscript; Peter Barry (UNSW) for advice on estimation of LJPs; Roger D. Traub for valuable discussions; as well as Serena Dudek and Robert J. Bridges for help on establishing recordings with DNDS. We highly appreciate the technical assistance of Susanne Rieckmann and Anke Schönherr. This study has been supported by grants from the DFG (Exc 257, SFB 618, and Le-2250/2-1) and the BMBF (BCCN, grant numbers 01GQ0440 and 01GQ0410) and the ERC starting grant (260590).

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2011.08.016

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title = "Coherent Phasic Excitation during Hippocampal Ripples",

abstract = "High-frequency hippocampal network oscillations, or {"}ripples,{"} are thought to be involved in episodic memory. According to current theories, memory traces are represented by assemblies of principal neurons that are activated during ripple-associated network states. Here we performed in vivo and in vitro experiments to investigate the synaptic mechanisms during ripples. We discovered postsynaptic currents that are phase-locked to ripples and coherent among even distant CA1 pyramidal neurons. These fast currents are consistent with excitatory postsynaptic currents (EPSCs) as they are observed at the equilibrium potential of Cl -, and they display kinetics characteristic of EPSCs. Furthermore, they survived after intracellular blockade of GABAergic transmission and are effective to regulate the timing of action potentials. In addition, our data show a progressive synchronization of phasic excitation and inhibition during the course of ripples. Together, our results demonstrate the presence of phasic excitation during ripples reflecting an exquisite temporal coordination of assemblies of active pyramidal cells.",

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note = "Funding Information: We wish to thank Sarah Shoichet, Anja Gundlfinger, Alexey Ponomarenko, Christian Wozny, Jos{\'e} R. Donoso, Nikolai Axmacher, and Robert Schmidt for constructive comments on earlier versions of the manuscript; Peter Barry (UNSW) for advice on estimation of LJPs; Roger D. Traub for valuable discussions; as well as Serena Dudek and Robert J. Bridges for help on establishing recordings with DNDS. We highly appreciate the technical assistance of Susanne Rieckmann and Anke Sch{\"o}nherr. This study has been supported by grants from the DFG (Exc 257, SFB 618, and Le-2250/2-1) and the BMBF (BCCN, grant numbers 01GQ0440 and 01GQ0410) and the ERC starting grant (260590). ",

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AU - Tejero-Cantero, Álvaro

AU - Dorrn, Anja L.

AU - Winterer, Jochen

AU - Beed, Prateep S.

AU - Morris, Genela

AU - Kempter, Richard

AU - Poulet, James F.A.

AU - Leibold, Christian

AU - Schmitz, Dietmar

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Coherent Phasic Excitation during Hippocampal Ripples

Abstract

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