Anterior insular cortex plays a critical role in interoceptive attention

  1. Xingchao Wang
  2. Qiong Wu
  3. Laura Egan
  4. Xiaosi Gu
  5. Pinan Liu
  6. Hong Gu
  7. Yihong Yang
  8. Jing Luo
  9. Yanhong Wu  Is a corresponding author
  10. Zhixian Gao  Is a corresponding author
  11. Jin Fan  Is a corresponding author
  1. Beijing Tiantan Hospital, Capital Medical University, China
  2. Capital Normal University, China
  3. Queens College, The City University of New York, United States
  4. Icahn School of Medicine at Mount Sinai, United States
  5. National Institute on Drug Abuse, United States
  6. Peking University, China

Abstract

Accumulating evidence indicates that the anterior insular cortex (AIC) mediates interoceptive attention, which refers to attention towards physiological signals arising from the body. However, the necessity of the AIC in this process has not been demonstrated. Using a novel task that directs attention toward breathing rhythm, we assessed the involvement of the AIC in interoceptive attention in healthy participants using functional magnetic resonance imaging and examined the necessity of the AIC in interoceptive attention in patients with AIC lesions. Results showed that interoceptive attention was associated with increased AIC activation, as well as enhanced coupling between the AIC and somatosensory areas along with reduced coupling between the AIC and visual sensory areas. In addition, AIC activation was predictive of individual differences in interoceptive accuracy. Importantly, AIC lesion patients showed disrupted interoceptive discrimination accuracy and sensitivity. These results provide compelling evidence that AIC plays a critical role in interoceptive attention.

Data availability

Source data have been deposited in Dyrad, including behavioral data, fMRI data, and lesion patient data. Our Dyrad DOI is: doi:10.5061/dryad.5sj852c

The following data sets were generated

Article and author information

Author details

  1. Xingchao Wang

    Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Qiong Wu

    School of Psychology, Capital Normal University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Laura Egan

    Department of Psychology, Queens College, The City University of New York, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Xiaosi Gu

    Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Pinan Liu

    Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Hong Gu

    Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Yihong Yang

    Neuroimaging Research Branch, Intramural Research Program, National Institute on Drug Abuse, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jing Luo

    School of Psychology, Capital Normal University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Yanhong Wu

    School of Psychological and Cognitive Sciences, Peking University, Beijing, China
    For correspondence
    wuyh@pku.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  10. Zhixian Gao

    Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
    For correspondence
    gaozx@ccmu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  11. Jin Fan

    Department of Psychology, Queens College, The City University of New York, New York, United States
    For correspondence
    jin.fan@qc.cuny.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9630-8330

Funding

National Natural Science Foundation of China (81729001)

  • Jin Fan

China Postdoctoral Science Foundation (2016M600835)

  • Qiong Wu

National Institute on Drug Abuse (1R01DA043695)

  • Xiaosi Gu

National Natural Science Foundation of China (81328008)

  • Jin Fan

National Natural Science Foundation of China (61690205)

  • Yanhong Wu

National Institute of Mental Health (R01MH094305)

  • Jin Fan

Research grant of 973 (973-2015CB351800)

  • Yanhong Wu

National Natural Science Foundation of China (31771205)

  • Yanhong Wu

National Institute on Drug Abuse (Intramul Research Program)

  • Yihong Yang

Brain research Project of Beijing (Z16110002616014)

  • Pinan Liu

Beijing Municipal Administration of Hospital Youth programs (QML20170503)

  • Xingchao Wang

National Natural Science Foundation of China (81600931)

  • Xingchao Wang

Capital Health Development Research Project of Beijing (2016-4-1074)

  • Xingchao Wang

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

Reviewing Editor

  1. Klaas Enno Stephan, University of Zurich and ETH Zurich, Switzerland

Ethics

Human subjects: All participants in fMRI study and in lesion study were gave written informed consent in accordance with the procedures and protocols approved by The Human Subjects Review Committee of Peking University and by The Institutional Review Board of the Beijing Tiantan Hospital, Capital Medical University, respectively.

Version history

  1. Received: September 24, 2018
  2. Accepted: April 13, 2019
  3. Accepted Manuscript published: April 15, 2019 (version 1)
  4. Version of Record published: April 29, 2019 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Xingchao Wang
  2. Qiong Wu
  3. Laura Egan
  4. Xiaosi Gu
  5. Pinan Liu
  6. Hong Gu
  7. Yihong Yang
  8. Jing Luo
  9. Yanhong Wu
  10. Zhixian Gao
  11. Jin Fan
(2019)
Anterior insular cortex plays a critical role in interoceptive attention
eLife 8:e42265.
https://doi.org/10.7554/eLife.42265

Share this article

https://doi.org/10.7554/eLife.42265

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