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.

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.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

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

Further reading

    1. Neuroscience
    David Richter, Dirk van Moorselaar, Jan Theeuwes
    Research Article

    Avoiding distraction by salient yet irrelevant stimuli is critical when accomplishing daily tasks. One possible mechanism to accomplish this is by suppressing stimuli that may be distracting such that they no longer compete for attention. While the behavioral benefits of distractor suppression are well established, its neural underpinnings are not yet fully understood. In a functional MRI (fMRI) study, we examined whether and how sensory responses in early visual areas show signs of distractor suppression after incidental learning of spatial statistical regularities. Participants were exposed to an additional singleton task where, unbeknownst to them, one location more frequently contained a salient distractor. We analyzed whether visual responses in terms of fMRI BOLD were modulated by this distractor predictability. Our findings indicate that implicit spatial priors shape sensory processing even at the earliest stages of cortical visual processing, evident in early visual cortex as a suppression of stimuli at locations which frequently contained distracting information. Notably, while this suppression was spatially (receptive field) specific, it did extend to nearby neutral locations and occurred regardless of whether distractors, nontarget items, or targets were presented at this location, suggesting that suppression arises before stimulus identification. Crucially, we observed similar spatially specific neural suppression even if search was only anticipated, but no search display was presented. Our results highlight proactive modulations in early visual cortex, where potential distractions are suppressed preemptively, before stimulus onset, based on learned expectations. Combined, our study underscores how the brain leverages implicitly learned prior knowledge to optimize sensory processing and attention allocation.