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Optogenetically induced low-frequency correlations impair perception

  1. Anirvan S Nandy  Is a corresponding author
  2. Jonathan J Nassi
  3. Monika P Jadi
  4. John H Reynolds
  1. The Salk Institute for Biological Studies, United States
  2. Yale University, United States
  3. Salk Institute for Biological Studies, United States
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Cite this article as: eLife 2019;8:e35123 doi: 10.7554/eLife.35123

Abstract

Deployment of covert attention to a spatial location can cause large decreases in low-frequency correlated variability among neurons in macaque area V4 whose receptive-fields lie at the attended location. It has been estimated that this reduction accounts for a substantial fraction of the attention-mediated improvement in sensory processing. These estimates depend on assumptions about how population signals are decoded and the conclusion that correlated variability impairs perception, is purely hypothetical. Here we test this proposal directly by optogenetically inducing low-frequency fluctuations, to see if this interferes with performance in an attention-demanding task. We find that low-frequency optical stimulation of neurons in V4 elevates correlations among pairs of neurons and impairs the animal's ability to make fine sensory discriminations. Stimulation at higher frequencies does not impair performance, despite comparable modulation of neuronal responses. These results support the hypothesis that attention-dependent reductions in correlated variability contribute to improved perception of attended stimuli.

Data availability

Data for the main figures are available via Dryad (doi:10.5061/dryad.8v0k1j3).

The following data sets were generated

Article and author information

Author details

  1. Anirvan S Nandy

    Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, La Jolla, United States
    For correspondence
    nandy@snl.salk.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4225-5349
  2. Jonathan J Nassi

    Systems Neurobiological Laboratories, The Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Monika P Jadi

    Department of Neuroscience, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. John H Reynolds

    The Salk Institute for Biological Studies, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

NIH Blueprint for Neuroscience Research

  • John H Reynolds

Brain and Behavior Research Foundation

  • Anirvan S Nandy
  • Jonathan J Nassi

National Institutes of Health (R00EY025026)

  • Monika P Jadi

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 of the Salk Institute. All procedures were approved by the Institutional Animal Care and Use Committee at the Salk Institute (Protocol #14-00014) and conformed to NIH guidelines.

Reviewing Editor

  1. Tatiana Pasternak, University of Rochester, United States

Publication history

  1. Received: January 16, 2018
  2. Accepted: February 6, 2019
  3. Accepted Manuscript published: February 22, 2019 (version 1)
  4. Version of Record published: February 26, 2019 (version 2)
  5. Version of Record updated: March 7, 2019 (version 3)

Copyright

© 2019, Nandy 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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