Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus

  1. Thomas P Jensen  Is a corresponding author
  2. Olga Kopach
  3. Leonid P Savchenko
  4. James Peter Reynolds
  5. Dmitri A Rusakov  Is a corresponding author
  1. University College London, United Kingdom

Abstract

Dendritic integration of synaptic inputs involves their increased electrotonic attenuation at distal dendrites, which can be counterbalanced by the increased synaptic receptor density. However, during network activity the influence of individual synapses depends on their release fidelity, the dendritic distribution of which remains poorly understood. Here, we employed classical optical quantal analyses and a genetically encoded optical glutamate sensor in acute hippocampal slices of rats and mice to monitor release at CA3-CA1 synapses. We find that their release probability increases with greater distances from the soma. Similar-fidelity synapses tend to group together whereas release probability shows no trends regarding the branch ends. Simulations with a realistic CA1 pyramidal cell hosting stochastic synapses suggest that the observed trends boost signal transfer fidelity, particularly at higher input frequencies. Because high-frequency bursting has been associated with learning, the release probability pattern we have found may play a key role in memory trace formation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1 - 4.

Article and author information

Author details

  1. Thomas P Jensen

    UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
    For correspondence
    t.jensen@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  2. Olga Kopach

    UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3921-3674
  3. Leonid P Savchenko

    UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. James Peter Reynolds

    UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Dmitri A Rusakov

    UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
    For correspondence
    d.rusakov@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9539-9947

Funding

Wellcome Trust (212251_Z_18_Z)

  • Dmitri A Rusakov

European Research Council (323113)

  • Dmitri A Rusakov

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

Ethics

Animal experimentation: Animal procedures were subject to local ethical approval and adhered to the European Commission Directive (86/609/ EEC) and the United Kingdom Home Office (Scientific Procedures) Act of 1986. Experiments were carried out under the UK HO Project licence PPL707524.

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Publication history

  1. Received: August 29, 2020
  2. Accepted: January 12, 2021
  3. Accepted Manuscript published: January 13, 2021 (version 1)
  4. Version of Record published: January 25, 2021 (version 2)
  5. Version of Record updated: January 27, 2021 (version 3)

Copyright

© 2021, Jensen 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. Thomas P Jensen
  2. Olga Kopach
  3. Leonid P Savchenko
  4. James Peter Reynolds
  5. Dmitri A Rusakov
(2021)
Release probability increases towards distal dendrites boosting high-frequency signal transfer in the rodent hippocampus
eLife 10:e62588.
https://doi.org/10.7554/eLife.62588