Functional dissociation of stimulus intensity encoding and predictive coding of pain in the insula

  1. Stephan Geuter  Is a corresponding author
  2. Sabrina Boll
  3. Falk Eippert
  4. Christian Büchel
  1. University Medical Center Hamburg Eppendorf, Germany
  2. University of Oxford, United Kingdom

Abstract

The computational principles by which the brain creates a painful experience from nociception are still unknown. Classic theories suggest that cortical regions either reflect stimulus intensity or additive effects of intensity and expectations, respectively. By contrast, predictive coding theories provide a unified framework explaining how perception is shaped by the integration of beliefs about the world with mismatches resulting from the comparison of these believes against sensory input. Using functional magnetic resonance imaging during a probabilistic heat pain paradigm, we investigated which computations underlie pain perception. Skin conductance, pupil dilation, and anterior insula responses to cued pain stimuli strictly followed the response patterns hypothesized by the predictive coding model, whereas posterior insula encoded stimulus intensity. This novel functional dissociation of pain processing within the insula together with previously observed alterations in chronic pain offer a novel interpretation of aberrant pain processing as disturbed weighting of predictions and prediction errors.

Article and author information

Author details

  1. Stephan Geuter

    Department of Systems Neuroscience, University Medical Center Hamburg Eppendorf, Hamburg, Germany
    For correspondence
    stephan.geuter@colorado.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4935-5692
  2. Sabrina Boll

    Department of Systems Neuroscience, University Medical Center Hamburg Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Falk Eippert

    Centre for Functional Magnetic Resonance Imaging of the Brain, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3986-1719
  4. Christian Büchel

    Department of Systems Neuroscience, University Medical Center Hamburg Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (SFB 936 A06)

  • Christian Büchel

European Commission (ERC Advanced Investigator Grant 2010-AdG_20100407)

  • Christian Büchel

Deutsche Forschungsgemeinschaft (Fellowship GE 2774/1-1)

  • Stephan Geuter

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

Reviewing Editor

  1. Heidi Johansen-Berg, University of Oxford, United Kingdom

Ethics

Human subjects: The study was approved by and conducted in accordance with the ethics guidelines of the Medical Chamber Hamburg (PV4745). All participants provided informed consent to participate and to publish.

Version history

  1. Received: January 19, 2017
  2. Accepted: May 18, 2017
  3. Accepted Manuscript published: May 19, 2017 (version 1)
  4. Version of Record published: June 14, 2017 (version 2)

Copyright

© 2017, Geuter 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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  1. Stephan Geuter
  2. Sabrina Boll
  3. Falk Eippert
  4. Christian Büchel
(2017)
Functional dissociation of stimulus intensity encoding and predictive coding of pain in the insula
eLife 6:e24770.
https://doi.org/10.7554/eLife.24770

Share this article

https://doi.org/10.7554/eLife.24770

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