1. Neuroscience

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
https://doi.org/10.7554/eLife.35123
Share this article
Cite this article
  1. Anirvan S Nandy
  2. Jonathan J Nassi
  3. Monika P Jadi
  4. John H Reynolds
(2019)
Optogenetically induced low-frequency correlations impair perception
eLife 8:e35123.
https://doi.org/10.7554/eLife.35123
  2. Download BibTeX
  3. Download .RIS

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.

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.

Metrics

  • 3,832
    views
  • 554
    downloads
  • 28
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Anirvan S Nandy
  2. Jonathan J Nassi
  3. Monika P Jadi
  4. John H Reynolds
(2019)
Optogenetically induced low-frequency correlations impair perception
eLife 8:e35123.
https://doi.org/10.7554/eLife.35123

Share this article

https://doi.org/10.7554/eLife.35123

Categories and tags

Research organism

Further reading

    1. Computational and Systems Biology
    2. Neuroscience

    A statistical framework for analysis of trial-level temporal dynamics in fiber photometry experiments

    Gabriel Loewinger, Erjia Cui ... Francisco Pereira
    Tools and Resources

    Fiber photometry has become a popular technique to measure neural activity in vivo, but common analysis strategies can reduce the detection of effects because they condense within-trial signals into summary measures, and discard trial-level information by averaging across-trials. We propose a novel photometry statistical framework based on functional linear mixed modeling, which enables hypothesis testing of variable effects at every trial time-point, and uses trial-level signals without averaging. This makes it possible to compare the timing and magnitude of signals across conditions while accounting for between-animal differences. Our framework produces a series of plots that illustrate covariate effect estimates and statistical significance at each trial time-point. By exploiting signal autocorrelation, our methodology yields joint 95% confidence intervals that account for inspecting effects across the entire trial and improve the detection of event-related signal changes over common multiple comparisons correction strategies. We reanalyze data from a recent study proposing a theory for the role of mesolimbic dopamine in reward learning, and show the capability of our framework to reveal significant effects obscured by standard analysis approaches. For example, our method identifies two dopamine components with distinct temporal dynamics in response to reward delivery. In simulation experiments, our methodology yields improved statistical power over common analysis approaches. Finally, we provide an open-source package and analysis guide for applying our framework.

    1. Neuroscience

    Unraveling the impact of congenital deafness on individual brain organization

    Lenia Amaral, Xiaosha Wang ... Ella Striem-Amit
    Research Article

    Research on brain plasticity, particularly in the context of deafness, consistently emphasizes the reorganization of the auditory cortex. But to what extent do all individuals with deafness show the same level of reorganization? To address this question, we examined the individual differences in functional connectivity (FC) from the deprived auditory cortex. Our findings demonstrate remarkable differentiation between individuals deriving from the absence of shared auditory experiences, resulting in heightened FC variability among deaf individuals, compared to more consistent FC in the hearing group. Notably, connectivity to language regions becomes more diverse across individuals with deafness. This does not stem from delayed language acquisition; it is found in deaf native signers, who are exposed to natural language since birth. However, comparing FC diversity between deaf native signers and deaf delayed signers, who were deprived of language in early development, we show that language experience also impacts individual differences, although to a more moderate extent. Overall, our research points out the intricate interplay between brain plasticity and individual differences, shedding light on the diverse ways reorganization manifests among individuals. It joins findings of increased connectivity diversity in blindness and highlights the importance of considering individual differences in personalized rehabilitation for sensory loss.