Silent synapses generate sparse and orthogonal action potential firing in adult-born hippocampal granule cells

  1. Liyi Li
  2. Sebastien Sultan
  3. Stefanie Heigele
  4. Charlotte Schmidt-Salzmann
  5. Nicolas Toni
  6. Josef Bischofberger  Is a corresponding author
  1. University of Basel, Switzerland
  2. University of Lausanne, Switzerland
  3. University Hospital Freiburg, Germany

Abstract

In adult neurogenesis young neurons connect to the existing network via formation of thousands of new synapses. At early developmental stages, glutamatergic synapses are sparse, immature and functionally ‘silent’, expressing mainly NMDA receptors. Here we show in 2- to 3-week-old young neurons of adult mice, that brief-burst activity in glutamatergic fibers is sufficient to induce postsynaptic AP firing in the absence of AMPA receptors. The enhanced excitability of the young neurons lead to efficient temporal summation of small NMDA currents, dynamic unblocking of silent synapses and NMDA-receptor-dependent AP firing. Therefore, early synaptic inputs are powerfully converted into reliable spiking output. Furthermore, due to high synaptic gain, small dendritic trees and sparse connectivity, neighboring young neurons are activated by different distinct subsets of afferent fibers with minimal overlap. Taken together, synaptic recruitment of young neurons generates sparse and orthogonal AP firing, which may support sparse coding during hippocampal information processing.

Article and author information

Author details

  1. Liyi Li

    Department of Biomedicine, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Sebastien Sultan

    Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Stefanie Heigele

    Department of Biomedicine, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Charlotte Schmidt-Salzmann

    Klinik für Innere Medizin I, University Hospital Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Nicolas Toni

    Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Josef Bischofberger

    Department of Biomedicine, University of Basel, Basel, Switzerland
    For correspondence
    josef.bischofberger@unibas.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4006-1663

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Project 31003A_13301)

  • Josef Bischofberger

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the FELASA Guide for the Care and Use of Laboratory Animals. The protocol for use and care of experimental animals (mice) in this project was approved by the Animal Ethics Advisory committee of the Kanton Basel (2385_26940, 2438_26489, Kantonales Verterinaeramt BS, Switzerland).

Reviewing Editor

  1. Yukiko Goda, RIKEN, Japan

Publication history

  1. Received: November 24, 2016
  2. Accepted: August 7, 2017
  3. Accepted Manuscript published: August 8, 2017 (version 1)
  4. Version of Record published: September 1, 2017 (version 2)

Copyright

© 2017, Li 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. Liyi Li
  2. Sebastien Sultan
  3. Stefanie Heigele
  4. Charlotte Schmidt-Salzmann
  5. Nicolas Toni
  6. Josef Bischofberger
(2017)
Silent synapses generate sparse and orthogonal action potential firing in adult-born hippocampal granule cells
eLife 6:e23612.
https://doi.org/10.7554/eLife.23612