1. Neuroscience
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Sensory experience inversely regulates feedforward and feedback excitation-inhibition ratio in rodent visual cortex

  1. Nathaniel J Miska
  2. Leonidas MA Richter
  3. Brian A Cary
  4. Julijana Gjorgjieva
  5. Gina G Turrigiano  Is a corresponding author
  1. Brandeis University, United States
  2. Max Planck Institute for Brain Research, Germany
Research Article
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Cite this article as: eLife 2018;7:e38846 doi: 10.7554/eLife.38846

Abstract

Brief (2-3d) monocular deprivation (MD) during the critical period induces a profound loss of responsiveness within binocular (V1b) and monocular (V1m) regions of rodent primary visual cortex. This has largely been ascribed to long-term depression (LTD) at thalamocortical synapses, while a contribution from intracortical inhibition has been controversial. Here we used optogenetics to isolate and measure feedforward thalamocortical and feedback intracortical excitation-inhibition (E-I) ratios following brief MD. Despite depression at thalamocortical synapses, thalamocortical E-I ratio was unaffected in V1b and shifted toward excitation in V1m, indicating that thalamocortical excitation was not effectively reduced. In contrast, feedback intracortical E-I ratio was shifted toward inhibition in V1m, and a computational model demonstrated that these opposing shifts produced an overall suppression of layer 4 excitability. Thus, feedforward and feedback E-I ratios can be independently tuned by visual experience, and enhanced feedback inhibition is the primary driving force behind loss of visual responsiveness.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Individual data points are plotted over bar graphs of means +/- SEM for each figure.

Article and author information

Author details

  1. Nathaniel J Miska

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8587-4919
  2. Leonidas MA Richter

    Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Brian A Cary

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Julijana Gjorgjieva

    Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7118-4079
  5. Gina G Turrigiano

    Department of Biology, Brandeis University, Waltham, United States
    For correspondence
    turrigiano@brandeis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4476-4059

Funding

National Science Foundation (NSF10604)

  • Nathaniel J Miska

National Institute of Neurological Disorders and Stroke (F31 NS089170)

  • Nathaniel J Miska

National Eye Institute (R01 EY025613)

  • Gina G Turrigiano

Max-Planck-Gesellschaft

  • Julijana Gjorgjieva

National Institute of Neurological Disorders and Stroke (R37 NS092635)

  • Gina G Turrigiano

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 Brandeis University institutional animal care and use committee (IACUC) protocols (#15005 and #18002). All surgery was performed under ketamine-xylazine-acepromazine anesthesia and included sufficient post-operative analgesia to minimize any animal suffering.

Reviewing Editor

  1. Julie A Kauer, Brown University, United States

Publication history

  1. Received: June 1, 2018
  2. Accepted: October 11, 2018
  3. Accepted Manuscript published: October 12, 2018 (version 1)
  4. Version of Record published: November 8, 2018 (version 2)

Copyright

© 2018, Miska 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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