Large-scale two-photon imaging revealed super-sparse population codes in V1 superficial layer of awake monkeys

  1. Shiming Tang  Is a corresponding author
  2. Yimeng Zhang
  3. Zhihao Li
  4. Ming Li
  5. Fang Liu
  6. Hongfei Jiang
  7. Tai Sing Lee  Is a corresponding author
  1. Peking University, China
  2. Carnegie Mellon University, United States

Abstract

One general principle of sensory information processing is that the brain must optimize efficiency by reducing the number of neurons processing the same information. The sparseness of the sensory representations in a population of neurons reflects the efficiency of the neural code. Here we employ large-scale two-photon calcium imaging to examine the responses of a large population of neurons with single-cell resolution, within the superficial layers of area V1, while simultaneously presenting a large set of natural visual stimuli, to provide the first direct measure of the population sparseness in awake primates. The results show that only 0.5% of neurons respond strongly to any given natural image-indicating a tenfold increase in the inferred sparseness over previous measurements. These population activities are nevertheless necessary and sufficient to discriminate visual stimuli with high accuracy, suggesting that the neural code in the primary visual cortex is both super-sparse and highly efficient.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 2 and 3.

Article and author information

Author details

  1. Shiming Tang

    School of Life Sciences, Peking University, Beijing, China
    For correspondence
    tangshm@pku.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0294-3259
  2. Yimeng Zhang

    Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2248-8951
  3. Zhihao Li

    Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ming Li

    School of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Fang Liu

    School of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Hongfei Jiang

    School of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Tai Sing Lee

    Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, United States
    For correspondence
    tai@cnbc.cmu.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Natural Science Foundation of China (31730109)

  • Shiming Tang

National Natural Science Foundation of China (China Outstanding Young Researcher Award 30525016)

  • Shiming Tang

National Basic Research Program of China (2017YFA0105201)

  • Shiming Tang

Peking University (Project 985 grant)

  • Shiming Tang

Beijing Municipal Commission of Science and Technology (Z151100000915070)

  • Shiming Tang

NIH Office of the Director (1R01EY022247)

  • Tai Sing Lee

National Science Foundation (CISE 1320651)

  • Tai Sing Lee

Intelligence Advanced Research Projects Activity (D16PC00007)

  • Tai Sing Lee

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

Reviewing Editor

  1. Emilio Salinas, Wake Forest School of Medicine, United States

Ethics

Animal experimentation: Animal experimentation: All procedures involving animals were in accordance with the Guide of Institutional Animal Care and Use Committee (IACUC) of Peking University Animals, and approved by the Peking University Animal Care and Use Committee (LSC-TangSM-5). All surgrey was performed under general anesthesia and strictly sterile conditions, and every effort was made to minimize suffering.

Version history

  1. Received: January 24, 2018
  2. Accepted: April 25, 2018
  3. Accepted Manuscript published: April 26, 2018 (version 1)
  4. Version of Record published: May 15, 2018 (version 2)

Copyright

© 2018, Tang 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. Shiming Tang
  2. Yimeng Zhang
  3. Zhihao Li
  4. Ming Li
  5. Fang Liu
  6. Hongfei Jiang
  7. Tai Sing Lee
(2018)
Large-scale two-photon imaging revealed super-sparse population codes in V1 superficial layer of awake monkeys
eLife 7:e33370.
https://doi.org/10.7554/eLife.33370

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https://doi.org/10.7554/eLife.33370

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