Somatostatin-positive interneurons in the dentate gyrus of mice provide local- and long-range septal synaptic inhibition

Abstract

Somatostatin-expressing-interneurons (SOMIs) in the dentate gyrus (DG) control formation of granule cell (GC) assemblies during memory acquisition. Hilar-perforant-path-associated interneurons (HIPP cells) have been considered to be synonymous for DG-SOMIs. Deviating from this assumption, we show two functionally contrasting DG-SOMI-types. The classical feedback-inhibitory HIPPs distribute axon fibers in the molecular layer. They are engaged by converging GC-inputs and provide dendritic inhibition to the DG circuitry. In contrast, SOMIs with axon in the hilus, termed hilar interneurons (HILs), provide perisomatic inhibition onto GABAergic cells in the DG and project to the medial septum. Repetitive activation of glutamatergic inputs onto HIPP cells induces long-lasting-depression (LTD) of synaptic transmission but long-term-potentiation (LTP) of synaptic signals in HIL cells. Thus, LTD in HIPPs may assist flow of spatial information from the entorhinal cortex to the DG, whereas LTP in HILs may facilitate the temporal coordination of GCs with activity patterns governed by the medial septum.

Article and author information

Author details

  1. Mei Yuan

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  2. Thomas Meyer

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  3. Christoph Benkowitz

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  4. Shakuntala Savanthrapadian

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  5. Laura Ansel-Bollepalli

    Institute for Physiology, University of Kiel, Kiel, Germany
    Competing interests
    No competing interests declared.
  6. Angelica Foggetti

    Institute for Physiology, University of Kiel, Kiel, Germany
    Competing interests
    No competing interests declared.
  7. Peer Wulff

    Institute for Physiology, University of Kiel, Kiel, Germany
    Competing interests
    No competing interests declared.
  8. Pepe Alcami

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  9. Claudio Elgueta

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  10. Marlene Bartos

    Institute for Physiology I, University of Freiburg, Freiburg, Germany
    For correspondence
    marlene.bartos@physiologie.uni-freiburg.de
    Competing interests
    Marlene Bartos, Reviewing editor, elife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9741-1946

Funding

Deutsche Forschungsgemeinschaft (FOR2143)

  • Marlene Bartos

Volkswagen Foundation (Lichtenberg Award)

  • Marlene Bartos

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Gary L Westbrook, Vollum Institute, United States

Ethics

Animal experimentation: All animal procedures were performed in accordance to national and european legislations (license no.: G-11/53; X-12/20D).

Version history

  1. Received: August 31, 2016
  2. Accepted: April 1, 2017
  3. Accepted Manuscript published: April 3, 2017 (version 1)
  4. Version of Record published: April 18, 2017 (version 2)

Copyright

© 2017, Yuan 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. Mei Yuan
  2. Thomas Meyer
  3. Christoph Benkowitz
  4. Shakuntala Savanthrapadian
  5. Laura Ansel-Bollepalli
  6. Angelica Foggetti
  7. Peer Wulff
  8. Pepe Alcami
  9. Claudio Elgueta
  10. Marlene Bartos
(2017)
Somatostatin-positive interneurons in the dentate gyrus of mice provide local- and long-range septal synaptic inhibition
eLife 6:e21105.
https://doi.org/10.7554/eLife.21105

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https://doi.org/10.7554/eLife.21105