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

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 wit...

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Main Authors: Rui Ponte Costa, Robert C Froemke, P Jesper Sjöström, Mark CW van Rossum
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/09457
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author Rui Ponte Costa
Robert C Froemke
P Jesper Sjöström
Mark CW van Rossum
author_facet Rui Ponte Costa
Robert C Froemke
P Jesper Sjöström
Mark CW van Rossum
author_sort Rui Ponte Costa
collection DOAJ
description 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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spelling doaj.art-20cac632329d4c14987808719b6fcba32022-12-22T04:32:17ZengeLife Sciences Publications LtdeLife2050-084X2015-08-01410.7554/eLife.09457Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learningRui Ponte Costa0https://orcid.org/0000-0003-2595-2027Robert C Froemke1P Jesper Sjöström2https://orcid.org/0000-0001-7085-2223Mark CW van Rossum3https://orcid.org/0000-0001-6525-6814Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom; Neuroinformatics Doctoral Training Centre, School of Informatics, University of Edinburgh, Edinburgh, United Kingdom; The Research Institute of the McGill University Health Centre, Department of Neurology and Neurosurgery, McGill University, Montreal, Canada; Centre for Neural Circuits and Behaviour, University of Oxford, Oxford, United KingdomSkirball Institute for Biomolecular Medicine, Departments of Otolaryngology, Neuroscience and Physiology, New York University School of Medicine, New York, United States; Center for Neural Science, New York University, New York, United StatesThe Research Institute of the McGill University Health Centre, Department of Neurology and Neurosurgery, McGill University, Montreal, CanadaInstitute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh, United KingdomAlthough 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.https://elifesciences.org/articles/09457memory savingssynaptic transmissionpre- and postsynaptic long-term plasticitylearning rulesreceptive fieldsspike-timing-dependent plasticity
spellingShingle Rui Ponte Costa
Robert C Froemke
P Jesper Sjöström
Mark CW van Rossum
Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
eLife
memory savings
synaptic transmission
pre- and postsynaptic long-term plasticity
learning rules
receptive fields
spike-timing-dependent plasticity
title Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
title_full Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
title_fullStr Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
title_full_unstemmed Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
title_short Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning
title_sort unified pre and postsynaptic long term plasticity enables reliable and flexible learning
topic memory savings
synaptic transmission
pre- and postsynaptic long-term plasticity
learning rules
receptive fields
spike-timing-dependent plasticity
url https://elifesciences.org/articles/09457
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AT robertcfroemke unifiedpreandpostsynapticlongtermplasticityenablesreliableandflexiblelearning
AT pjespersjostrom unifiedpreandpostsynapticlongtermplasticityenablesreliableandflexiblelearning
AT markcwvanrossum unifiedpreandpostsynapticlongtermplasticityenablesreliableandflexiblelearning