1. Neuroscience
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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
Research Article
  • Cited 11
  • Views 3,672
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Cite this article as: eLife 2019;8:e43191 doi: 10.7554/eLife.43191

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.

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).

Reviewing Editor

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

Publication 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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Further reading

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    Gordon H Petty et al.
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    Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

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