Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study
BackgroundPain is a complex experience that involves sensory-discriminative and cognitive-emotional neuronal processes. It has long been known across cultures that pain can be relieved by mindful breathing (MB). There is a common assumption that MB exerts its analgesic effect...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
JMIR Publications
2021-10-01
|
Series: | Journal of Medical Internet Research |
Online Access: | https://www.jmir.org/2021/10/e27298 |
_version_ | 1797735661756743680 |
---|---|
author | Xiao-Su Hu Katherine Beard Mary Catherine Sherbel Thiago D Nascimento Sean Petty Eddie Pantzlaff David Schwitzer Niko Kaciroti Eric Maslowski Lawrence M Ashman Stephen E Feinberg Alexandre F DaSilva |
author_facet | Xiao-Su Hu Katherine Beard Mary Catherine Sherbel Thiago D Nascimento Sean Petty Eddie Pantzlaff David Schwitzer Niko Kaciroti Eric Maslowski Lawrence M Ashman Stephen E Feinberg Alexandre F DaSilva |
author_sort | Xiao-Su Hu |
collection | DOAJ |
description |
BackgroundPain is a complex experience that involves sensory-discriminative and cognitive-emotional neuronal processes. It has long been known across cultures that pain can be relieved by mindful breathing (MB). There is a common assumption that MB exerts its analgesic effect through interoception. Interoception refers to consciously refocusing the mind’s attention to the physical sensation of internal organ function.
ObjectiveIn this study, we dissect the cortical analgesic processes by imaging the brains of healthy subjects exposed to traditional MB (TMB) and compare them with another group for which we augmented MB to an outside sensory experience via virtual reality breathing (VRB).
MethodsThe VRB protocol involved in-house–developed virtual reality 3D lungs that synchronized with the participants’ breathing cycles in real time, providing them with an immersive visual-auditory exteroception of their breathing.
ResultsWe found that both breathing interventions led to a significant increase in pain thresholds after week-long practices, as measured by a thermal quantitative sensory test. However, the underlying analgesic brain mechanisms were opposite, as revealed by functional near-infrared spectroscopy data. In the TMB practice, the anterior prefrontal cortex uniquely modulated the premotor cortex. This increased its functional connection with the primary somatosensory cortex (S1), thereby facilitating the S1-based sensory-interoceptive processing of breathing but inhibiting its other role in sensory-discriminative pain processing. In contrast, virtual reality induced an immersive 3D exteroception with augmented visual-auditory cortical activations, which diminished the functional connection with the S1 and consequently weakened the pain processing function of the S1.
ConclusionsIn summary, our study suggested two analgesic neuromechanisms of VRB and TMB practices—exteroception and interoception—that distinctively modulated the S1 processing of the ascending noxious inputs. This is in line with the concept of dualism (Yin and Yang). |
first_indexed | 2024-03-12T13:01:17Z |
format | Article |
id | doaj.art-47552e0fb2034570a4b13af558179504 |
institution | Directory Open Access Journal |
issn | 1438-8871 |
language | English |
last_indexed | 2024-03-12T13:01:17Z |
publishDate | 2021-10-01 |
publisher | JMIR Publications |
record_format | Article |
series | Journal of Medical Internet Research |
spelling | doaj.art-47552e0fb2034570a4b13af5581795042023-08-28T19:31:02ZengJMIR PublicationsJournal of Medical Internet Research1438-88712021-10-012310e2729810.2196/27298Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy StudyXiao-Su Huhttps://orcid.org/0000-0003-1401-000XKatherine Beardhttps://orcid.org/0000-0002-9211-9046Mary Catherine Sherbelhttps://orcid.org/0000-0002-1988-717XThiago D Nascimentohttps://orcid.org/0000-0003-0910-9005Sean Pettyhttps://orcid.org/0000-0002-6226-3434Eddie Pantzlaffhttps://orcid.org/0000-0002-6771-2411David Schwitzerhttps://orcid.org/0000-0002-0165-1919Niko Kacirotihttps://orcid.org/0000-0001-8843-8231Eric Maslowskihttps://orcid.org/0000-0001-5431-3350Lawrence M Ashmanhttps://orcid.org/0000-0003-4334-6717Stephen E Feinberghttps://orcid.org/0000-0003-3292-8797Alexandre F DaSilvahttps://orcid.org/0000-0003-3138-7781 BackgroundPain is a complex experience that involves sensory-discriminative and cognitive-emotional neuronal processes. It has long been known across cultures that pain can be relieved by mindful breathing (MB). There is a common assumption that MB exerts its analgesic effect through interoception. Interoception refers to consciously refocusing the mind’s attention to the physical sensation of internal organ function. ObjectiveIn this study, we dissect the cortical analgesic processes by imaging the brains of healthy subjects exposed to traditional MB (TMB) and compare them with another group for which we augmented MB to an outside sensory experience via virtual reality breathing (VRB). MethodsThe VRB protocol involved in-house–developed virtual reality 3D lungs that synchronized with the participants’ breathing cycles in real time, providing them with an immersive visual-auditory exteroception of their breathing. ResultsWe found that both breathing interventions led to a significant increase in pain thresholds after week-long practices, as measured by a thermal quantitative sensory test. However, the underlying analgesic brain mechanisms were opposite, as revealed by functional near-infrared spectroscopy data. In the TMB practice, the anterior prefrontal cortex uniquely modulated the premotor cortex. This increased its functional connection with the primary somatosensory cortex (S1), thereby facilitating the S1-based sensory-interoceptive processing of breathing but inhibiting its other role in sensory-discriminative pain processing. In contrast, virtual reality induced an immersive 3D exteroception with augmented visual-auditory cortical activations, which diminished the functional connection with the S1 and consequently weakened the pain processing function of the S1. ConclusionsIn summary, our study suggested two analgesic neuromechanisms of VRB and TMB practices—exteroception and interoception—that distinctively modulated the S1 processing of the ascending noxious inputs. This is in line with the concept of dualism (Yin and Yang).https://www.jmir.org/2021/10/e27298 |
spellingShingle | Xiao-Su Hu Katherine Beard Mary Catherine Sherbel Thiago D Nascimento Sean Petty Eddie Pantzlaff David Schwitzer Niko Kaciroti Eric Maslowski Lawrence M Ashman Stephen E Feinberg Alexandre F DaSilva Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study Journal of Medical Internet Research |
title | Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study |
title_full | Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study |
title_fullStr | Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study |
title_full_unstemmed | Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study |
title_short | Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study |
title_sort | brain mechanisms of virtual reality breathing versus traditional mindful breathing in pain modulation observational functional near infrared spectroscopy study |
url | https://www.jmir.org/2021/10/e27298 |
work_keys_str_mv | AT xiaosuhu brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT katherinebeard brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT marycatherinesherbel brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT thiagodnascimento brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT seanpetty brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT eddiepantzlaff brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT davidschwitzer brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT nikokaciroti brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT ericmaslowski brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT lawrencemashman brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT stephenefeinberg brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy AT alexandrefdasilva brainmechanismsofvirtualrealitybreathingversustraditionalmindfulbreathinginpainmodulationobservationalfunctionalnearinfraredspectroscopystudy |