1. Neuroscience
Download icon

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
Research Article
  • Cited 0
  • Views 1,489
  • Annotations
Cite this article as: eLife 2020;9:e55028 doi: 10.7554/eLife.55028

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.

Metrics

  • 1,489
    Page views
  • 182
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Debora Fusca, Peter Kloppenburg
    Research Article

    Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

    1. Neuroscience
    Wanhui Sheng et al.
    Research Article Updated

    Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here, we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes; however, activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.