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Research Articles, Behavioral/Cognitive

Opioid-Independent and Opioid-Mediated Modes of Pain Modulation

Chantal Berna, Siri Leknes, Asma H. Ahmad, Roisin N. Mhuircheartaigh, Guy M. Goodwin and Irene Tracey
Journal of Neuroscience 17 October 2018, 38 (42) 9047-9058; DOI: https://doi.org/10.1523/JNEUROSCI.0854-18.2018
Chantal Berna
1Pain Center, Division of Anesthesiology, Lausanne University Hospital (CHUV), 1011 Lausanne, Switzerland,
2Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom,
3Department of Psychiatry, University of Oxford and Oxford Health NHS Trust, Warneford Hospital, Oxford OX3 7JX, United Kingdom, and
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Siri Leknes
2Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom,
4Department of Psychology, University of Oslo, 0317 OSLO, Norway
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Asma H. Ahmad
2Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom,
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Roisin N. Mhuircheartaigh
2Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom,
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Guy M. Goodwin
3Department of Psychiatry, University of Oxford and Oxford Health NHS Trust, Warneford Hospital, Oxford OX3 7JX, United Kingdom, and
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Irene Tracey
2Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom,
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Abstract

Pain is regulated endogenously through both opioid and non-opioid mechanisms. We hypothesized that two novel pain modulation tasks, one drawing on context/expectations and one using voluntary reappraisal, would show differing levels of opioid dependence. Specifically, we expected that naloxone would block context-related analgesia, whereas mental imagery-based pain reappraisal would be opioid-independent.

A double-blind, placebo-controlled intravenous naloxone versus saline crossover design was used. Twenty healthy volunteers completed the two modulation tasks with acute heat stimuli calibrated to induce moderate pain. In the mental imagery task, participants imagined either a “pleasant” or a “comparison” scenario during painful heat. In the relative relief task, moderate heat stimuli coincided with visual cues eliciting relief from the expectation of intense pain, and were compared with moderate heat stimuli delivered under the expectation of non-painful warmth. Both “pleasant imagery” and “relative relief” conditions significantly improved ratings of pain intensity and pleasantness during saline treatment. Indeed, the target stimuli in both tasks, which had been calibrated to induce moderate pain, were rated as mildly pleasant. Furthermore, consistently with the main hypothesis, blocking endogenous opioid signaling with naloxone did not significantly affect imagery-induced regulation of pain intensity or pleasantness. In contrast, the relative relief-induced pain regulation (i.e., context/expectation) was blocked by naloxone. We conclude that endogenous opioid signaling is necessary for expectation-related relative relief analgesia, but not for pain reappraisal through mental imagery. These results support mental imagery as a powerful and clinically relevant strategy for regulating pain affect also in patients where endogenous opioid mechanisms might be compromised.

SIGNIFICANCE STATEMENT Neurotransmitter systems in the human brain can be probed through antagonist drugs. Studies using the opioid antagonist naloxone have demonstrated that the brain relies on both opioid and non-opioid mechanisms to downregulate pain. This holds clinical relevance given altered endogenous opioid processes in many chronic pain conditions. The present study used a double-blinded, placebo-controlled naloxone blockage of endogenous opioids in healthy humans to show differential opioid involvement in two pain modulation tasks. Context/expectation-driven (relative relief-related) analgesia was blocked by naloxone. In contrast, pain reappraisal through mental imagery was intact despite opioid receptor blockade, suggesting opioid independence. These results support mental imagery as a powerful, clinically relevant strategy for regulating pain as it does not rely on a functioning opioidergic system.

  • descending pain modulation
  • expectation
  • mental imagery
  • naloxone
  • pain modulation
  • pain relief
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The Journal of Neuroscience: 38 (42)
Journal of Neuroscience
Vol. 38, Issue 42
17 Oct 2018
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Opioid-Independent and Opioid-Mediated Modes of Pain Modulation
Chantal Berna, Siri Leknes, Asma H. Ahmad, Roisin N. Mhuircheartaigh, Guy M. Goodwin, Irene Tracey
Journal of Neuroscience 17 October 2018, 38 (42) 9047-9058; DOI: 10.1523/JNEUROSCI.0854-18.2018

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Opioid-Independent and Opioid-Mediated Modes of Pain Modulation
Chantal Berna, Siri Leknes, Asma H. Ahmad, Roisin N. Mhuircheartaigh, Guy M. Goodwin, Irene Tracey
Journal of Neuroscience 17 October 2018, 38 (42) 9047-9058; DOI: 10.1523/JNEUROSCI.0854-18.2018
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Keywords

  • descending pain modulation
  • expectation
  • mental imagery
  • naloxone
  • pain modulation
  • pain relief

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