1. Neuroscience

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. Daniel L Felch
  6. Molly McQuillan
  7. Christopher P Truszkowski
  8. Arseny S Khakhalin
  9. Carlos D Aizenman  Is a corresponding author
  1. Brown University, United States
  2. Bard College, United States
  3. Roger Williams University, United States
https://doi.org/10.7554/eLife.25392
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  1. Torrey LS Truszkowski
  2. Oscar A Carrillo
  3. Julia Bleier
  4. Carolina Ramirez-Vizcarrondo
  5. Daniel L Felch
  6. Molly McQuillan
  7. Christopher P Truszkowski
  8. Arseny S Khakhalin
  9. Carlos D Aizenman
(2017)
A cellular mechanism for inverse effectiveness in multisensory integration
eLife 6:e25392.
https://doi.org/10.7554/eLife.25392
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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). Previously 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 (Felch et al., 2016). 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. Daniel L Felch

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

  6. Molly McQuillan

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

  7. Christopher P Truszkowski

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

  8. 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

  9. 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.

Reviewing Editor

  1. Gary L Westbrook, Vollum Institute, United States

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.

Version 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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  1. Torrey LS Truszkowski
  2. Oscar A Carrillo
  3. Julia Bleier
  4. Carolina Ramirez-Vizcarrondo
  5. Daniel L Felch
  6. Molly McQuillan
  7. Christopher P Truszkowski
  8. Arseny S Khakhalin
  9. Carlos D Aizenman
(2017)
A cellular mechanism for inverse effectiveness in multisensory integration
eLife 6:e25392.
https://doi.org/10.7554/eLife.25392

Share this article

https://doi.org/10.7554/eLife.25392

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    Multisensory integration (MSI) is the process that allows the brain to bind together spatiotemporally congruent inputs from different sensory modalities to produce single salient representations. While the phenomenology of MSI in vertebrate brains is well described, relatively little is known about cellular and synaptic mechanisms underlying this phenomenon. Here we use an isolated brain preparation to describe cellular mechanisms underlying development of MSI between visual and mechanosensory inputs in the optic tectum of Xenopus tadpoles. We find MSI is highly dependent on the temporal interval between crossmodal stimulus pairs. Over a key developmental period, the temporal window for MSI significantly narrows and is selectively tuned to specific interstimulus intervals. These changes in MSI correlate with developmental increases in evoked synaptic inhibition, and inhibitory blockade reverses observed developmental changes in MSI. We propose a model in which development of recurrent inhibition mediates development of temporal aspects of MSI in the tectum.

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