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Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition

Nature Neuroscience volume 15, pages 769–775 (2012)Cite this article

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A Corrigendum to this article was published on 22 November 2013

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Abstract

A consortium of inhibitory neurons control the firing patterns of pyramidal cells, but their specific roles in the behaving animal are largely unknown. We performed simultaneous physiological recordings and optogenetic silencing of either perisomatic (parvalbumin (PV) expressing) or dendrite-targeting (somatostatin (SOM) expressing) interneurons in hippocampal area CA1 of head-fixed mice actively moving a treadmill belt rich with visual-tactile stimuli. Silencing of either PV or SOM interneurons increased the firing rates of pyramidal cells selectively in their place fields, with PV and SOM interneurons having their largest effect during the rising and decaying parts of the place field, respectively. SOM interneuron silencing powerfully increased burst firing without altering the theta phase of spikes. In contrast, PV interneuron silencing had no effect on burst firing, but instead shifted the spikes' theta phase toward the trough of theta. These findings indicate that perisomatic and dendritic inhibition have distinct roles in controlling the rate, burst and timing of hippocampal pyramidal cells.

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Figure 1: Self movement–controlled local stimuli generate hippocampal cell sequences.
Figure 2: Light-assisted silencing of PV and SOM neurons.
Figure 3: Firing activity of different cell types during SWRs and theta oscillations.
Figure 4: Light-induced changes in firing patterns.
Figure 5: SOM interneurons control spike bursts in pyramidal cells.
Figure 6: Theta oscillations are not affected by focal disinhibition.
Figure 7: Within-theta timing of spikes is regulated by PV interneurons.

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Change history

  • 05 June 2012

    In the version of this article initially published, the Figure 3a legend described the ripple-activated neurons as representing oriens-lacunosum moleculare interneurons and the ripple-suppressed as representing bistratified interneurons. The reverse is true. The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We thank G.F. Turi, T. Adelman and T. Tabachnik for technical contributions, and D. Huber for useful advice. This work was supported by the Howard Hughes Medical Institute, the US National Institutes of Health (NS34994, MH54671), the James S. McDonnell Foundation and the World Class Institute (WCI) Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology of Korea (NRF grant number: WCI 2009-003). A.L. was supported by the Kavli and Searle Foundations.

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Author notes

  1. Boris V Zemelman

    Present address: Present address: Center for Learning and Memory, University of Texas at Austin, Austin, Texas, USA.,

Authors and Affiliations

  1. Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, Virginia, USA

    Sébastien Royer, Boris V Zemelman, Attila Losonczy, Jinhyun Kim, Frances Chance, Jeffrey C Magee & György Buzsáki

  2. Center for Functional Connectomics, Korea Institute of Science and Technology, Seoul, Republic of Korea

    Sébastien Royer & Jinhyun Kim

  3. Department of Neuroscience, Columbia University, New York, New York, USA

    Attila Losonczy

  4. Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey, USA

    György Buzsáki

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Contributions

The experiments were designed by S.R., J.C.M. and G.B. S.R. developed the treadmill and optical probe and performed the in vivo experiments and analysis. B.V.Z. and J.K. generated the Cre-dependent viruses. B.V.Z. generated the SOM-Cre mice. A.L. and F.C. performed the in vitro physiological experiments. A.L. performed the histological experiments. S.R., J.C.M. and G.B. wrote the manuscript.

Corresponding authors

Correspondence to Jeffrey C Magee or György Buzsáki.

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The authors declare no competing financial interests.

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Supplementary Text and Figures

Supplementary Figures 1–10 (PDF 13022 kb)

Supplementary Movie 1

Head-restrained mouse running on the treadmill belt. After a complete turn of the belt, water (10% sucrose) is delivered through a lick tube. Electrophysiological recording setup is not shown. (MOV 22689 kb)

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Royer, S., Zemelman, B., Losonczy, A. et al. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15, 769–775 (2012). https://doi.org/10.1038/nn.3077

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