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Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study

BACKGROUND: Pain 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...

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Autores principales: Hu, Xiao-Su, Beard, Katherine, Sherbel, Mary Catherine, Nascimento, Thiago D, Petty, Sean, Pantzlaff, Eddie, Schwitzer, David, Kaciroti, Niko, Maslowski, Eric, Ashman, Lawrence M, Feinberg, Stephen E, DaSilva, Alexandre F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: JMIR Publications 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8548979/
https://www.ncbi.nlm.nih.gov/pubmed/34636731
http://dx.doi.org/10.2196/27298
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author Hu, Xiao-Su
Beard, Katherine
Sherbel, Mary Catherine
Nascimento, Thiago D
Petty, Sean
Pantzlaff, Eddie
Schwitzer, David
Kaciroti, Niko
Maslowski, Eric
Ashman, Lawrence M
Feinberg, Stephen E
DaSilva, Alexandre F
author_facet Hu, Xiao-Su
Beard, Katherine
Sherbel, Mary Catherine
Nascimento, Thiago D
Petty, Sean
Pantzlaff, Eddie
Schwitzer, David
Kaciroti, Niko
Maslowski, Eric
Ashman, Lawrence M
Feinberg, Stephen E
DaSilva, Alexandre F
author_sort Hu, Xiao-Su
collection PubMed
description BACKGROUND: Pain 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. OBJECTIVE: In 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). METHODS: The 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. RESULTS: We 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. CONCLUSIONS: In 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 pubmed-85489792021-11-10 Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study Hu, Xiao-Su Beard, Katherine Sherbel, Mary Catherine Nascimento, Thiago D Petty, Sean Pantzlaff, Eddie Schwitzer, David Kaciroti, Niko Maslowski, Eric Ashman, Lawrence M Feinberg, Stephen E DaSilva, Alexandre F J Med Internet Res Original Paper BACKGROUND: Pain 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. OBJECTIVE: In 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). METHODS: The 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. RESULTS: We 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. CONCLUSIONS: In 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). JMIR Publications 2021-10-12 /pmc/articles/PMC8548979/ /pubmed/34636731 http://dx.doi.org/10.2196/27298 Text en ©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. Originally published in the Journal of Medical Internet Research (https://www.jmir.org), 12.10.2021. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work, first published in the Journal of Medical Internet Research, is properly cited. The complete bibliographic information, a link to the original publication on https://www.jmir.org/, as well as this copyright and license information must be included.
spellingShingle Original Paper
Hu, Xiao-Su
Beard, Katherine
Sherbel, Mary Catherine
Nascimento, Thiago D
Petty, Sean
Pantzlaff, Eddie
Schwitzer, David
Kaciroti, Niko
Maslowski, Eric
Ashman, Lawrence M
Feinberg, Stephen E
DaSilva, Alexandre F
Brain Mechanisms of Virtual Reality Breathing Versus Traditional Mindful Breathing in Pain Modulation: Observational Functional Near-infrared Spectroscopy Study
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
topic Original Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8548979/
https://www.ncbi.nlm.nih.gov/pubmed/34636731
http://dx.doi.org/10.2196/27298
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