Bidirectional synaptic plasticity rapidly modifies hippocampal representations
- Rutgers, The State University of New Jersey, United States
- Howard Hughes Medical Institute, Baylor College of Medicine, United States
- Howard Hughes Medical Institute, United States
- Stanford University, United States
Abstract
Learning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neurons. Here we found that this behavioral timescale synaptic plasticity (BTSP) can also reshape existing place fields via bidirectional synaptic weight changes that depend on the temporal proximity of plateau potentials to pre-existing place fields. When evoked near an existing place field, plateau potentials induced less synaptic potentiation and more depression, suggesting BTSP might depend inversely on postsynaptic activation. However, manipulations of place cell membrane potential and computational modeling indicated that this anti-correlation actually results from a dependence on current synaptic weight such that weak inputs potentiate and strong inputs depress. A network model implementing this bidirectional synaptic learning rule suggested that BTSP enables population activity, rather than pairwise neuronal correlations, to drive neural adaptations to experience.
Data availability
The complete dataset, Python code for data analysis and model simulation, and additional MATLAB and Igor analysis scripts are available at https://github.com/neurosutras/BTSP.
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Bidirectional synaptic plasticity rapidly modifies hippocampal representationsPublicly available at Github (https://github.com).
Article and author information
Author details
Funding
National Institutes of Health (U19NS104590)
- Aaron D Milstein
- Ivan Soltesz
National Institute of Mental Health (R01MH121979)
- Aaron D Milstein
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Katalin Toth, University of Ottawa, Canada
Ethics
Animal experimentation: All experimental methods were approved by the Janelia or Baylor College of Medicine Institutional Animal Care and Use Committees (Protocol 12-84 & 15-126).
Version history
- Preprint posted: February 5, 2020 (view preprint)
- Received: August 13, 2021
- Accepted: December 8, 2021
- Accepted Manuscript published: December 9, 2021 (version 1)
- Accepted Manuscript updated: December 10, 2021 (version 2)
- Version of Record published: January 20, 2022 (version 3)
Copyright
© 2021, Milstein 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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Bidirectional synaptic plasticity rapidly modifies hippocampal representations
eLife 10:e73046.
https://doi.org/10.7554/eLife.73046
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