Ultra-high field imaging reveals increased whole brain connectivity underpins cognitive strategies that attenuate pain

  1. Enrico Schulz  Is a corresponding author
  2. Anne Stankewitz
  3. Anderson M Winkler
  4. Stephanie Irving
  5. Viktor Witkovský
  6. Irene Tracey
  1. Ludwig-Maximilians-Universität München, Germany
  2. University of Oxford, United Kingdom
  3. Institute of Measurement Science, Slovak Academy of Sciences, Slovakia

Abstract

We investigated how the attenuation of pain with cognitive interventions affects brain connectivity using neuroimaging and a whole brain novel analysis approach. While receiving tonic cold pain, 20 healthy participants performed three different pain attenuation strategies during simultaneous collection of functional imaging data at 7 tesla. Participants were asked to rate their pain after each trial. We related the trial-by-trial variability of the attenuation performance to the trial-by-trial functional connectivity strength change of brain data. Across all conditions, we found that a higher performance of pain attenuation was predominantly associated with higher functional connectivity. Of note, we observed an association between low pain and high connectivity for regions that belong to brain regions long associated with pain processing, i.e. the insular and cingulate cortices. For one of the cognitive strategies (safe place), the performance of pain attenuation was explained by diffusion tensor imaging metrics of increased white matter integrity.

Data availability

The dataset has been made available at Open Science Framework (https://osf.io/tbc2u/). The source data files to generate the figures are included in the submission (Source data 1 - 7).

The following data sets were generated
    1. Enrico Schulz
    (2020) Pain Attentuation
    OSF, doi:10.17605/OSF.IO/TBC2U.

Article and author information

Author details

  1. Enrico Schulz

    Department of Neurology, Ludwig-Maximilians-Universität München, Martinsried, Germany
    For correspondence
    es@pain.sc
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8188-380X
  2. Anne Stankewitz

    Department of Neurology, Ludwig-Maximilians-Universität München, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Anderson M Winkler

    Wellcome Centre For Integrative Neuroimaging, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Stephanie Irving

    Department of Neurology, Ludwig-Maximilians-Universität München, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Viktor Witkovský

    Department of Theoretical Methods, Institute of Measurement Science, Slovak Academy of Sciences, Bratislava, Slovakia
    Competing interests
    The authors declare that no competing interests exist.
  6. Irene Tracey

    FMRIB Centre, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (2879/1-1)

  • Enrico Schulz

Wellcome (090955/Z/09/Z)

  • Irene Tracey

Wellcome (083259/Z/07/Z)

  • Irene Tracey

Medical Research Council (G0700399)

  • Irene Tracey

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

Ethics

Human subjects: Informed consent and consent to publish was obtained in accordance with ethical standards set out by the Declaration of Helsinki (1964) and with procedures approved by the Medical Sciences Interdivisional Research Ethics Committee of the University of Oxford (REC ref: MSD-IDREC- C1-2014-157).

Reviewing Editor

  1. Rohini Kuner, Universität Heidelberg, Germany

Publication history

  1. Received: January 9, 2020
  2. Accepted: August 28, 2020
  3. Accepted Manuscript published: September 2, 2020 (version 1)
  4. Version of Record published: September 17, 2020 (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. Enrico Schulz
  2. Anne Stankewitz
  3. Anderson M Winkler
  4. Stephanie Irving
  5. Viktor Witkovský
  6. Irene Tracey
(2020)
Ultra-high field imaging reveals increased whole brain connectivity underpins cognitive strategies that attenuate pain
eLife 9:e55028.
https://doi.org/10.7554/eLife.55028
  1. Further reading

Further reading

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    Funding: Deutsche Forschungsgesellschaft (410169619, 424778381), Deutsches Zentrum für Luftund Raumfahrt (DynaSti), National Institutes of Health (2R01 MH113929), Foundation for OCD Research (FFOR).