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Bidirectional synaptic plasticity rapidly modifies hippocampal representations independent of correlated activity

View ORCID ProfileAaron D. Milstein, Yiding Li, View ORCID ProfileKatie C. Bittner, Christine Grienberger, View ORCID ProfileIvan Soltesz, Jeffrey C. Magee, View ORCID ProfileSandro Romani
doi: https://doi.org/10.1101/2020.02.04.934182
Aaron D. Milstein
1Dept. of Neurosurgery and Stanford Neurosciences Institute, Stanford University School of Medicine, Stanford, CA
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Yiding Li
2Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX
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Katie C. Bittner
3Howard Hughes Medical Institute, Janelia Research Campus, Ashburn, VA
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Christine Grienberger
2Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX
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Ivan Soltesz
1Dept. of Neurosurgery and Stanford Neurosciences Institute, Stanford University School of Medicine, Stanford, CA
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Jeffrey C. Magee
2Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX
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  • For correspondence: Jeffrey.Magee@bcm.edu romanis@janelia.hhmi.org
Sandro Romani
3Howard Hughes Medical Institute, Janelia Research Campus, Ashburn, VA
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  • For correspondence: Jeffrey.Magee@bcm.edu romanis@janelia.hhmi.org
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Abstract

According to standard models of synaptic plasticity, correlated activity between connected neurons drives changes in synaptic strengths to store associative memories. Here we tested this hypothesis in vivo by manipulating the activity of hippocampal place cells and measuring the resulting changes in spatial selectivity. We found that the spatial tuning of place cells was rapidly reshaped via bidirectional synaptic plasticity. To account for the magnitude and direction of plasticity, we evaluated two models – a standard model that depended on synchronous pre- and post-synaptic activity, and an alternative model that depended instead on whether active synaptic inputs had previously been potentiated. While both models accounted equally well for the data, they predicted opposite outcomes of a perturbation experiment, which ruled out the standard correlation-dependent model. Finally, network modeling suggested that this form of bidirectional synaptic plasticity enables population activity, rather than pairwise neuronal correlations, to drive plasticity in response to changes in the environment.

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Posted February 05, 2020.
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Bidirectional synaptic plasticity rapidly modifies hippocampal representations independent of correlated activity
Aaron D. Milstein, Yiding Li, Katie C. Bittner, Christine Grienberger, Ivan Soltesz, Jeffrey C. Magee, Sandro Romani
bioRxiv 2020.02.04.934182; doi: https://doi.org/10.1101/2020.02.04.934182
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Bidirectional synaptic plasticity rapidly modifies hippocampal representations independent of correlated activity
Aaron D. Milstein, Yiding Li, Katie C. Bittner, Christine Grienberger, Ivan Soltesz, Jeffrey C. Magee, Sandro Romani
bioRxiv 2020.02.04.934182; doi: https://doi.org/10.1101/2020.02.04.934182

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