Threat of shock increases excitability and connectivity of the intraparietal sulcus

  1. Nicholas L Balderston  Is a corresponding author
  2. Elizabeth Hale
  3. Abigail Hsiung
  4. Salvatore Torrisi
  5. Tom Holroyd
  6. Frederick W Carver
  7. Richard Coppola
  8. Monique Ernst
  9. Christian Grillon
  1. National Institutes of Health, United States
  2. National Institute of Mental Health, United States

Abstract

Anxiety disorders affect approximately 1 in 5 (18%) Americans within a given 1 year period, placing a substantial burden on the national health care system. Therefore, there is a critical need to understand the neural mechanisms mediating anxiety symptoms. We used unbiased, multimodal, data-driven, whole-brain measures of neural activity (magnetoencephalography) and connectivity (fMRI) to identify the regions of the brain that contribute most prominently to sustained anxiety. We report that a single brain region, the intraparietal sulcus (IPS), shows both elevated neural activity and global brain connectivity during threat. The IPS plays a key role in attention orienting, and may contribute to the hypervigilance that is a common symptom of pathological anxiety. Hyperactivation of this region during elevated state anxiety may account for the paradoxical facilitation of performance on tasks that require an external focus of attention, and impairment of performance on tasks that require an internal focus of attention.

Article and author information

Author details

  1. Nicholas L Balderston

    Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, United States
    For correspondence
    nicholas.balderston@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8565-1544
  2. Elizabeth Hale

    Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Abigail Hsiung

    Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Salvatore Torrisi

    Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Tom Holroyd

    MEG Core Facility, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Frederick W Carver

    MEG Core Facility, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Richard Coppola

    MEG Core Facility, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Monique Ernst

    Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Christian Grillon

    Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Mental Health (ZIAMH002798)

  • Christian Grillon

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

Reviewing Editor

  1. Matthew J Brookes, University of Nottingham, United Kingdom

Ethics

Human subjects: All participants gave written informed consent approved by the National Institute of Mental Health (NIMH) Combined Neuroscience Institutional Review Board and received compensation for participating.

Version history

  1. Received: November 28, 2016
  2. Accepted: May 29, 2017
  3. Accepted Manuscript published: May 30, 2017 (version 1)
  4. Version of Record published: June 20, 2017 (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. Nicholas L Balderston
  2. Elizabeth Hale
  3. Abigail Hsiung
  4. Salvatore Torrisi
  5. Tom Holroyd
  6. Frederick W Carver
  7. Richard Coppola
  8. Monique Ernst
  9. Christian Grillon
(2017)
Threat of shock increases excitability and connectivity of the intraparietal sulcus
eLife 6:e23608.
https://doi.org/10.7554/eLife.23608

Share this article

https://doi.org/10.7554/eLife.23608

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