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

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Cite this article as: eLife 2015;4:e09457 doi: 10.7554/eLife.09457

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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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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.
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.
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.
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

Sacha B Nelson, Brandeis University, United States

Publication history

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

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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.