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

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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.

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Mei Yuan

Institute for Physiology I, University of Freiburg, Freiburg, Germany

Competing interests
No competing interests declared.
Thomas Meyer

Institute for Physiology I, University of Freiburg, Freiburg, Germany

Competing interests
No competing interests declared.
Christoph Benkowitz

Institute for Physiology I, University of Freiburg, Freiburg, Germany

Competing interests
No competing interests declared.
Shakuntala Savanthrapadian

Institute for Physiology I, University of Freiburg, Freiburg, Germany

Competing interests
No competing interests declared.
Laura Ansel-Bollepalli

Institute for Physiology, University of Kiel, Kiel, Germany

Competing interests
No competing interests declared.
Angelica Foggetti

Institute for Physiology, University of Kiel, Kiel, Germany

Competing interests
No competing interests declared.
Peer Wulff

Institute for Physiology, University of Kiel, Kiel, Germany

Competing interests
No competing interests declared.
Pepe Alcami

Institute for Physiology I, University of Freiburg, Freiburg, Germany

Competing interests
No competing interests declared.
Claudio Elgueta

Institute for Physiology I, University of Freiburg, Freiburg, Germany

Competing interests
No competing interests declared.
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.

"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.

Ethics

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

Copyright

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.