Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations

Eran Stark; Lisa Roux; Ronny Eichler; Yuta Senzai; Sebastien Royer; György Buzsáki

doi:10.1016/j.neuron.2014.06.023

Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations

Eran Stark^*, Lisa Roux, Ronny Eichler, Yuta Senzai, Sebastien Royer, György Buzsáki

^*Corresponding author for this work

Neuroscience

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

316 Scopus citations

Abstract

High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation, frequency control, and spatial coherence of the rhythm are poorly understood. Using multisite optogenetic manipulations in freely behaving rodents, we found that depolarization of a small group of nearby pyramidal cells was sufficient toinduce high-frequency oscillations, whereas closed-loop silencing of pyramidal cells or activation of parvalbumin- (PV) or somatostatin-immunoreactive interneurons aborted spontaneously occurring ripples. Focal pharmacological blockade of GABA_A receptors abolished ripples. Localized PV interneuron activation paced ensemble spiking, and simultaneous induction of high-frequency oscillations at multiple locations resulted in a temporally coherent pattern mediated by phase-locked interneuron spiking. These results constrain competing models of ripple generation and indicate that temporally precise local interactions between excitatory and inhibitory neurons support ripple generation in the intact hippocampus.

Original language	English (US)
Pages (from-to)	467-480
Number of pages	14
Journal	Neuron
Volume	83
Issue number	2
DOIs	https://doi.org/10.1016/j.neuron.2014.06.023
State	Published - Jul 16 2014

Funding

We thank Kamran Diba, Daniel English, Kenji Mizuseki, Adrien Peyrache, Erik Schomburg, Anton Sirota, and Lucas Sjulson for insightful comments; Shigeyoshi Fujisawa for help maintaining transgenic animals; and Ed Boyden, Karl Deisseroth, and Karel Svoboda for providing AAV viruses. This work was supported by the Rothschild Foundation (to E.S.), Human Frontiers in Science Project LT-000346/2009-L (to E.S.), Machiah Foundation (to E.S.), NIH NS034994, NIH MH54671, NIH NS074015, and the Mathers Foundation.

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2014.06.023

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abstract = "High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation, frequency control, and spatial coherence of the rhythm are poorly understood. Using multisite optogenetic manipulations in freely behaving rodents, we found that depolarization of a small group of nearby pyramidal cells was sufficient toinduce high-frequency oscillations, whereas closed-loop silencing of pyramidal cells or activation of parvalbumin- (PV) or somatostatin-immunoreactive interneurons aborted spontaneously occurring ripples. Focal pharmacological blockade of GABAA receptors abolished ripples. Localized PV interneuron activation paced ensemble spiking, and simultaneous induction of high-frequency oscillations at multiple locations resulted in a temporally coherent pattern mediated by phase-locked interneuron spiking. These results constrain competing models of ripple generation and indicate that temporally precise local interactions between excitatory and inhibitory neurons support ripple generation in the intact hippocampus.",

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AU - Roux, Lisa

AU - Eichler, Ronny

AU - Senzai, Yuta

AU - Royer, Sebastien

AU - Buzsáki, György

PY - 2014/7/16

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N2 - High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation, frequency control, and spatial coherence of the rhythm are poorly understood. Using multisite optogenetic manipulations in freely behaving rodents, we found that depolarization of a small group of nearby pyramidal cells was sufficient toinduce high-frequency oscillations, whereas closed-loop silencing of pyramidal cells or activation of parvalbumin- (PV) or somatostatin-immunoreactive interneurons aborted spontaneously occurring ripples. Focal pharmacological blockade of GABAA receptors abolished ripples. Localized PV interneuron activation paced ensemble spiking, and simultaneous induction of high-frequency oscillations at multiple locations resulted in a temporally coherent pattern mediated by phase-locked interneuron spiking. These results constrain competing models of ripple generation and indicate that temporally precise local interactions between excitatory and inhibitory neurons support ripple generation in the intact hippocampus.

AB - High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation, frequency control, and spatial coherence of the rhythm are poorly understood. Using multisite optogenetic manipulations in freely behaving rodents, we found that depolarization of a small group of nearby pyramidal cells was sufficient toinduce high-frequency oscillations, whereas closed-loop silencing of pyramidal cells or activation of parvalbumin- (PV) or somatostatin-immunoreactive interneurons aborted spontaneously occurring ripples. Focal pharmacological blockade of GABAA receptors abolished ripples. Localized PV interneuron activation paced ensemble spiking, and simultaneous induction of high-frequency oscillations at multiple locations resulted in a temporally coherent pattern mediated by phase-locked interneuron spiking. These results constrain competing models of ripple generation and indicate that temporally precise local interactions between excitatory and inhibitory neurons support ripple generation in the intact hippocampus.

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Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations

Abstract

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ASJC Scopus subject areas

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