Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning

  1. Rui Ponte Costa  Is a corresponding author
  2. Robert C Froemke
  3. Per Jesper Sjöström
  4. Mark C W van Rossum
  1. University of Edinburgh, United Kingdom
  2. New York University School of Medicine, United States
  3. McGill University, Canada

Abstract

Although it is well known that long-term synaptic plasticity can be expressed both pre- and postsynaptically, the functional consequences of this arrangement have remained elusive. We show that spike-timing-dependent plasticity with both pre- and postsynaptic expression develops receptive fields with reduced variability and improved discriminability compared to postsynaptic plasticity alone. These long-term modifications in receptive field statistics match recent sensory perception experiments. Moreover, learning with this form of plasticity leaves a hidden postsynaptic memory trace that enables fast relearning of previously stored information, providing a cellular substrate for memory savings. Our results reveal essential roles for presynaptic plasticity that are missed when only postsynaptic expression of long-term plasticity is considered, and suggest an experience-dependent distribution of pre- and postsynaptic strength changes.

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Author details

  1. Rui Ponte Costa

    Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    rui.costa@cncb.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  2. Robert C Froemke

    Skirball Institute for Biomolecular Medicine, Departments of Otolaryngology, Neuroscience and Physiology, New York University School of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Per Jesper Sjöström

    The Research Institute of the McGill University Health Centre, Department of Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Mark C W van Rossum

    Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Version history

  1. Received: June 15, 2015
  2. Accepted: August 25, 2015
  3. Accepted Manuscript published: August 26, 2015 (version 1)
  4. Version of Record published: September 29, 2015 (version 2)
  5. Version of Record updated: November 30, 2016 (version 3)
  6. Version of Record updated: June 20, 2017 (version 4)

Copyright

© 2015, Ponte Costa 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. Rui Ponte Costa
  2. Robert C Froemke
  3. Per Jesper Sjöström
  4. Mark C W van Rossum
(2015)
Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
eLife 4:e09457.
https://doi.org/10.7554/eLife.09457

Share this article

https://doi.org/10.7554/eLife.09457

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