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A cellular mechanism for inverse effectiveness in multisensory integration

  1. Torrey LS Truszkowski
  2. Oscar A Carrillo
  3. Julia Bleier
  4. Carolina Ramirez-Vizcarrondo
  5. Molly McQuillan
  6. Christopher P Truszkowski
  7. Arseny S Khakhalin
  8. Carlos D Aizenman  Is a corresponding author
  1. Brown University, United States
  2. Bard College, United States
  3. Roger Williams University, United States
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Cite this article as: eLife 2017;6:e25392 doi: 10.7554/eLife.25392

Abstract

To build a coherent view of the external world, an organism needs to integrate multiple types of sensory information from different sources, a process known as multisensory integration (MSI). In a prior study (Felch et al. 2016) we showed that the temporal dependence of MSI in the optic tectum of Xenopus laevis tadpoles is mediated by the network dynamics of the recruitment of local inhibition by sensory input. This was one of the first cellular-level mechanisms described for MSI. Here we expand this cellular level view of MSI by focusing on the principle of inverse effectiveness, another central feature of MSI stating that the amount of multisensory enhancement observed inversely depends on the size of unisensory responses. We show that non-linear summation of crossmodal synaptic responses, mediated by NMDA-type glutamate receptor (NMDARs) activation, form the cellular basis for inverse effectiveness, both at the cellular and behavioral levels.

Article and author information

Author details

  1. Torrey LS Truszkowski

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Oscar A Carrillo

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Julia Bleier

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Carolina Ramirez-Vizcarrondo

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Molly McQuillan

    Bard College, Annandale-On-Hudson, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Christopher P Truszkowski

    Digital Services, Roger Williams University, Bristol, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Arseny S Khakhalin

    Bard College, Annandale-On-Hudson, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0429-1728
  8. Carlos D Aizenman

    Department of Neuroscience, Brown University, Providence, United States
    For correspondence
    Carlos_Aizenman@brown.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7378-7217

Funding

National Institutes of Health (NIH F31 NS09379001)

  • Torrey LS Truszkowski

National Science Foundation (NSF IOS 1353044)

  • Torrey LS Truszkowski
  • Oscar A Carrillo
  • Julia Bleier
  • Carolina Ramirez-Vizcarrondo
  • Christopher P Truszkowski
  • Carlos D Aizenman

American Physiological Society

  • Oscar A Carrillo
  • Carolina Ramirez-Vizcarrondo

Bard Summer Research Institute, Bard College

  • Molly McQuillan
  • Arseny S Khakhalin

Brown University

  • Oscar A Carrillo
  • Julia Bleier
  • Carolina Ramirez-Vizcarrondo

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (1607000219) of Brown University.

Reviewing Editor

  1. Gary L Westbrook, Vollum Institute, United States

Publication history

  1. Received: January 25, 2017
  2. Accepted: March 15, 2017
  3. Accepted Manuscript published: March 18, 2017 (version 1)
  4. Accepted Manuscript updated: March 24, 2017 (version 2)
  5. Version of Record published: March 31, 2017 (version 3)

Copyright

© 2017, Truszkowski 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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