Paradoxical response reversal of top-down modulation in cortical circuits with three interneuron types

Abstract

Pyramidal cells and interneurons expressing parvalbumin (PV), somatostatin (SST), and vasoactive intestinal peptide (VIP) show cell type-specific connectivity patterns leading to a canonical microcircuit across cortex. Experiments recording from this circuit often report counterintuitive and seemingly contradictory findings. For example, the response of SST cells in mouse V1 to top-down behavioral modulation can change its sign when the visual input changes, a phenomenon that we call response reversal. We developed a theoretical framework to explain these seemingly contradictory effects as emerging phenomena in circuits with two key features: interactions between multiple neural populations and a nonlinear neuronal input-output relationship. Furthermore, we built a cortical circuit model which reproduces counterintuitive dynamics observed in mouse V1. Our analytical calculations pinpoint connection properties critical to response reversal, and predict additional novel types of complex dynamics that could be tested in future experiments.

Article and author information

Author details

  1. Luis Carlos Garcia del Molino

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Guangyu Robert Yang

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jorge F Mejias

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Xiao-Jing Wang

    Center for Neural Science, New York University, New York, United States
    For correspondence
    xjwang@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3124-8474

Funding

Office of Naval Research (N00014-17-1-2041)

  • Xiao-Jing Wang

Science and Technology Commission of Shanghai Municipality (14JC1404900)

  • Xiao-Jing Wang

NIH Blueprint for Neuroscience Research (R01MH062349)

  • Xiao-Jing Wang

Science and Technology Commission of Shanghai Municipality (15JC1400104)

  • Xiao-Jing Wang

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

Reviewing Editor

  1. Peter Latham, University College London, United Kingdom

Version history

  1. Received: June 19, 2017
  2. Accepted: December 2, 2017
  3. Accepted Manuscript published: December 19, 2017 (version 1)
  4. Version of Record published: January 22, 2018 (version 2)
  5. Version of Record updated: August 2, 2018 (version 3)
  6. Version of Record updated: March 13, 2020 (version 4)

Copyright

© 2017, Garcia del Molino 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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  1. Luis Carlos Garcia del Molino
  2. Guangyu Robert Yang
  3. Jorge F Mejias
  4. Xiao-Jing Wang
(2017)
Paradoxical response reversal of top-down modulation in cortical circuits with three interneuron types
eLife 6:e29742.
https://doi.org/10.7554/eLife.29742

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https://doi.org/10.7554/eLife.29742

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