1. Neuroscience

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

  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  Is a corresponding author
  1. University of Freiburg, Germany
  2. University of Kiel, Germany
https://doi.org/10.7554/eLife.21105
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

Metrics

  • 4,715
    views
  • 970
    downloads
  • 68
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    A new ‘CFS tracking’ paradigm reveals uniform suppression depth regardless of target complexity or salience

    David Alais, Jacob Coorey ... Matthew J Davidson
    Research Article

    When the eyes view separate and incompatible images, the brain suppresses one image and promotes the other into visual awareness. Periods of interocular suppression can be prolonged during continuous flash suppression (CFS) – when one eye views a static ‘target’ while the other views a complex dynamic stimulus. Measuring the time needed for a suppressed image to break CFS (bCFS) has been widely used to investigate unconscious processing, and the results have generated controversy regarding the scope of visual processing without awareness. Here, we address this controversy with a new ‘CFS tracking’ paradigm (tCFS) in which the suppressed monocular target steadily increases in contrast until breaking into awareness (as in bCFS) after which it decreases until it again disappears (reCFS), with this cycle continuing for many reversals. Unlike bCFS, tCFS provides a measure of suppression depth by quantifying the difference between breakthrough and suppression thresholds. tCFS confirms that (i) breakthrough thresholds indeed differ across target types (e.g. faces vs gratings, as bCFS has shown) – but (ii) suppression depth does not vary across target types. Once the breakthrough contrast is reached for a given stimulus, all stimuli require a strikingly uniform reduction in contrast to reach the corresponding suppression threshold. This uniform suppression depth points to a single mechanism of CFS suppression, one that likely occurs early in visual processing because suppression depth was not modulated by target salience or complexity. More fundamentally, it shows that variations in bCFS thresholds alone are insufficient for inferring whether the barrier to achieving awareness exerted by interocular suppression is weaker for some categories of visual stimuli compared to others.

    1. Cell Biology
    2. Neuroscience

    KIS counteracts PTBP2 and regulates alternative exon usage in neurons

    Marcos Moreno-Aguilera, Alba M Neher ... Carme Gallego
    Research Article Updated

    Alternative RNA splicing is an essential and dynamic process in neuronal differentiation and synapse maturation, and dysregulation of this process has been associated with neurodegenerative diseases. Recent studies have revealed the importance of RNA-binding proteins in the regulation of neuronal splicing programs. However, the molecular mechanisms involved in the control of these splicing regulators are still unclear. Here, we show that KIS, a kinase upregulated in the developmental brain, imposes a genome-wide alteration in exon usage during neuronal differentiation in mice. KIS contains a protein-recognition domain common to spliceosomal components and phosphorylates PTBP2, counteracting the role of this splicing factor in exon exclusion. At the molecular level, phosphorylation of unstructured domains within PTBP2 causes its dissociation from two co-regulators, Matrin3 and hnRNPM, and hinders the RNA-binding capability of the complex. Furthermore, KIS and PTBP2 display strong and opposing functional interactions in synaptic spine emergence and maturation. Taken together, our data uncover a post-translational control of splicing regulators that link transcriptional and alternative exon usage programs in neuronal development.

    1. Genetics and Genomics
    2. Neuroscience

    Genetic Chimerism: Marmosets contain multitudes

    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.