Active information maintenance in working memory by a sensory cortex

  1. Xiaoxing Zhang
  2. Wenjun Yan
  3. Wenliang Wang
  4. Hongmei Fan
  5. Ruiqing Hou
  6. Yulei Chen
  7. Zhaoqin Chen
  8. Chaofan Ge
  9. Shumin Duan
  10. Albert Compte
  11. Chengyu T Li  Is a corresponding author
  1. CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, China
  2. Zhejiang University School of Medicine, China
  3. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Spain

Abstract

Working memory is a critical brain function for maintaining and manipulating information over delay periods of seconds. It is debated whether delay-period neural activity in sensory regions is important for the active maintenance of information during the delay period. Here, we tackle this question by examining the anterior piriform cortex (APC), an olfactory sensory cortex, in head-fixed mice performing several olfactory working memory tasks. Active information maintenance is necessary in these tasks, especially in a dual-task paradigm in which mice are required to perform another distracting task while actively maintaining information during the delay period. Optogenetic suppression of neuronal activity in APC during the delay period impaired performance in all the tasks. Furthermore, electrophysiological recordings revealed that APC neuronal populations encoded odor information in the delay period even with an intervening distracting task. Thus, delay activity in APC is important for active information maintenance in olfactory working memory.

Data availability

All data generated or analyzed during this study are available on Dryad under doi:10.5061/dryad.dt5h4m1. Source data files have been provided for Figures 1-4.

The following data sets were generated

Article and author information

Author details

  1. Xiaoxing Zhang

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5229-6091
  2. Wenjun Yan

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Wenliang Wang

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Hongmei Fan

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ruiqing Hou

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yulei Chen

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Zhaoqin Chen

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Chaofan Ge

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Shumin Duan

    Department of Neurobiology, Key Laboratory of Medical Neurobiology of Ministry of Health of China, Key Laboratory of Neurobiology, Zhejiang University School of Medicine, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Albert Compte

    Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  11. Chengyu T Li

    Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
    For correspondence
    tonylicy@ion.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6829-0209

Funding

National Natural Science Foundation of China (Distinguished Young Scholars of China (31525010))

  • Chengyu T Li

Chinese Academy of Agricultural Sciences (Key Research Program of Frontier Sciences QYZDB-SSW-SMC009)

  • Chengyu T Li

Chinese Academy of Agricultural Sciences (Instrument Developing Project YZ201540)

  • Chengyu T Li

Shanghai Science and Technology Commission (No.15JC1400102)

  • Chengyu T Li

Spanish Ministry of Science

  • Albert Compte

Innovation and Universities and the European Regional Development Fund (BFU2015-65318-R)

  • Albert Compte

CERCA Programme/Generalitat de Catalunya

  • Albert Compte

Shanghai Municipal Science and Technology Major Project (2018SHZDZX05)

  • Chengyu T Li

National Natural Science Foundation of China (General Program 31471049)

  • Chengyu T Li

Shanghei Science and Technology Commission (16JC1400101)

  • Chengyu T Li

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

Reviewing Editor

  1. Upinder Singh Bhalla, Tata Institute of Fundamental Research, India

Ethics

Animal experimentation: All experiments were performed in compliance with the animal care standards set by the U.S. National Institutes of Health and have been approved by the Institutional Animal Care and Use Committee of the Institute of Neuroscience, Chinese Academy of Sciences (ION-2018010).

Version history

  1. Received: October 28, 2018
  2. Accepted: June 20, 2019
  3. Accepted Manuscript published: June 24, 2019 (version 1)
  4. Version of Record published: July 16, 2019 (version 2)

Copyright

© 2019, Zhang 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. Xiaoxing Zhang
  2. Wenjun Yan
  3. Wenliang Wang
  4. Hongmei Fan
  5. Ruiqing Hou
  6. Yulei Chen
  7. Zhaoqin Chen
  8. Chaofan Ge
  9. Shumin Duan
  10. Albert Compte
  11. Chengyu T Li
(2019)
Active information maintenance in working memory by a sensory cortex
eLife 8:e43191.
https://doi.org/10.7554/eLife.43191

Share this article

https://doi.org/10.7554/eLife.43191

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