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Optogenetic inhibition-mediated activity-dependent modification of CA1 pyramidal-interneuron connections during behavior

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Cite this article as: eLife 2020;9:e61106 doi: 10.7554/eLife.61106

Abstract

In vitro work revealed that excitatory synaptic inputs to hippocampal inhibitory interneurons could undergo Hebbian, associative or non-associative plasticity. Both behavioral and learning-dependent reorganization of these connections has also been demonstrated by measuring spike transmission probabilities in pyramidal cell-interneuron spike cross-correlations that indicate monosynaptic connections. Here we investigated the activity-dependent modification of these connections during exploratory behavior in rats by optogenetically inhibiting pyramidal cell and interneuron subpopulations. Light application and associated firing alteration of pyramidal and interneuron populations led to lasting changes of pyramidal-interneuron connection weights as indicated by spike transmission changes. Spike transmission alterations were predicted by the light-mediated changes in the number of pre- and postsynaptic spike pairing events and by firing rate changes of interneurons but not pyramidal cells. This work demonstrates the presence of activity-dependent associative and non-associative reorganization of pyramidal-interneuron connections triggered by the optogenetic modification of the firing rate and spike synchrony of cells.

Data availability

Original data and programs are available in the scientific repository of the Institute of Science and Technology Austria upon publications.(https://research-explorer.app.ist.ac.at/ IST-REx-ID: 8563)

Article and author information

Author details

  1. Igor Gridchyn

    Neuroscience, IST Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Philipp Schoenenberger

    Neuroscience, IST Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Joseph O'Neill

    Neuroscience, IST Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Jozsef Csicsvari

    Neuroscience, IST Austria, Klosterneuburg, Austria
    For correspondence
    jozsef.csicsvari@ist.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5193-4036

Funding

Austrian Science Fund (I02072 & I03713)

  • Jozsef Csicsvari

Swiss National Science Foundation

  • Philipp Schoenenberger

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures involving experimental animals were carried out inaccordance with Austrian (Austrian federal Law for experiments with liveanimals) animal law under a project license (BMBWF-66.018/0015-WF/V/3b/2014, BMBWF-66.018/0018-WF/V/3b/2019) approved by the Austrian FederalScience Ministry (BMWFW).

Reviewing Editor

  1. Laura L Colgin, University of Texas at Austin, United States

Publication history

  1. Received: July 15, 2020
  2. Accepted: October 3, 2020
  3. Accepted Manuscript published: October 5, 2020 (version 1)
  4. Version of Record published: October 20, 2020 (version 2)

Copyright

© 2020, Gridchyn 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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