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...

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Main Authors: 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
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
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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).
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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
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