Skip to main content
Top
Gepubliceerd in:

13-07-2023 | ORIGINAL PAPER

Neural and Psychological Mechanisms in the Relationship Between Resting Breathing Rate and Pain

Auteurs: Valeria Oliva, Jennifer N. Baumgartner, Suzan R. Farris, Gabriel Riegner, Lora Khatib, Youngkyoo Jung, Robert C. Coghill, Fadel Zeidan

Gepubliceerd in: Mindfulness | Uitgave 7/2023

Log in om toegang te krijgen
share
DELEN

Deel dit onderdeel of sectie (kopieer de link)

  • Optie A:
    Klik op de rechtermuisknop op de link en selecteer de optie “linkadres kopiëren”
  • Optie B:
    Deel de link per e-mail

Abstract

Objectives

Breathing rate and pain are influenced by a spectrum of cognitive, affective, and physiological interactions. Yet, it is unknown if an individual’s resting breathing rate is associated with pain.

Methods

Continuous cerebral blood flow (CBF) and respiration rate were collected in 74 healthy participants during innocuous (35 °C) and noxious (49 °C) stimulation. Mindfulness and anxiety were assessed before acquiring perfusion fMRI data. Visual analog scale pain ratings were collected after pain testing.

Results

Slower resting respiration rate during noxious (r = 0.26, p = 0.03) and innocuous (r = 0.28, p = 0.02) heat was associated with lower pain sensitivity. Analyses of the whole-brain fMRI data revealed that higher CBF in the supramarginal gyrus, a central node of the ventral attention network, was associated with a slower breathing rate during noxious heat (r =  − 0.51, p < 0.001) and lower reported pain levels (r =  − 0.24, p = 0.04). Higher levels of dispositional mindfulness, but not anxiety (p > 0.20), were associated with slower breathing rate (r =  − 0.28, p = 0.02) and lower pain (r =  − 0.25, p = 0.03).

Conclusions

These findings demonstrate that individuals who naturally breathe slower report lower pain and engage unique mechanisms, suggesting the allocation of attention to physical bodily processes.
Literatuur
go back to reference Buxton, R. B., Wong, E. C., & Frank, L. R. (1998). Dynamics of blood flow and oxygenation changes during brain activation: The balloon model. Magnetic Resonance in Medicine, 39(6), 855–864.CrossRefPubMed Buxton, R. B., Wong, E. C., & Frank, L. R. (1998). Dynamics of blood flow and oxygenation changes during brain activation: The balloon model. Magnetic Resonance in Medicine, 39(6), 855–864.CrossRefPubMed
go back to reference Chan, P. S., Cheng, C. H., Wu, Y. T., Wu, C. W., Liu, H. A., Shaw, F. Z., Liu, C. Y., & Davenport, P. W. (2018). Cortical and subcortical neural correlates for respiratory sensation in response to transient inspiratory occlusions in humans. Frontiers in Physiology, 9, 1804. https://doi.org/10.3389/fphys.2018.01804 Chan, P. S., Cheng, C. H., Wu, Y. T., Wu, C. W., Liu, H. A., Shaw, F. Z., Liu, C. Y., & Davenport, P. W. (2018). Cortical and subcortical neural correlates for respiratory sensation in response to transient inspiratory occlusions in humans. Frontiers in Physiology, 9, 1804. https://​doi.​org/​10.​3389/​fphys.​2018.​01804
go back to reference Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M. P., & Shulman, G. L. (2000). Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neuroscience, 3(3), 292–297. https://doi.org/10.1038/73009 Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M. P., & Shulman, G. L. (2000). Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neuroscience, 3(3), 292–297. https://​doi.​org/​10.​1038/​73009
go back to reference Garfinkel, S. N., Manassei, M. F., Hamilton-Fletcher, G., In den Bosch, Y., Critchley, H. D., & Engels, M. (2016). Interoceptive dimensions across cardiac and respiratory axes. Philosophy Transactions of the Royal Societyof London. Series B: Biological Science, 371(1708). https://doi.org/10.1098/rstb.2016.0014 Garfinkel, S. N., Manassei, M. F., Hamilton-Fletcher, G., In den Bosch, Y., Critchley, H. D., & Engels, M. (2016). Interoceptive dimensions across cardiac and respiratory axes. Philosophy Transactions of the Royal Societyof London. Series B: Biological Science, 371(1708). https://​doi.​org/​10.​1098/​rstb.​2016.​0014
go back to reference Garland, E. L., Gaylord, S. A., Palsson, O., Faurot, K., Douglas Mann, J., & Whitehead, W. E. (2012). Therapeutic mechanisms of a mindfulness-based treatment for IBS: Effects on visceral sensitivity, catastrophizing, and affective processing of pain sensations. Journal of Behavioral Medicine, 35(6), 591–602. https://doi.org/10.1007/s10865-011-9391-zCrossRefPubMed Garland, E. L., Gaylord, S. A., Palsson, O., Faurot, K., Douglas Mann, J., & Whitehead, W. E. (2012). Therapeutic mechanisms of a mindfulness-based treatment for IBS: Effects on visceral sensitivity, catastrophizing, and affective processing of pain sensations. Journal of Behavioral Medicine, 35(6), 591–602. https://​doi.​org/​10.​1007/​s10865-011-9391-zCrossRefPubMed
go back to reference Garland, E. L., Manusov, E. G., Froeliger, B., Kelly, A., Williams, J. M., & Howard, M. O. (2014). Mindfulness-oriented recovery enhancement for chronic pain and prescription opioid misuse: Results from an early-stage randomized controlled trial. Journal of Consulting and Clinical Psychology, 82(3), 448–459. https://doi.org/10.1037/a0035798CrossRefPubMedPubMedCentral Garland, E. L., Manusov, E. G., Froeliger, B., Kelly, A., Williams, J. M., & Howard, M. O. (2014). Mindfulness-oriented recovery enhancement for chronic pain and prescription opioid misuse: Results from an early-stage randomized controlled trial. Journal of Consulting and Clinical Psychology, 82(3), 448–459. https://​doi.​org/​10.​1037/​a0035798CrossRefPubMedPubMedCentral
go back to reference Gholamrezaei, A., Van Diest, I., Aziz, Q., Pauwels, A., Tack, J., Vlaeyen, J. W. S., & Van Oudenhove, L. (2022). Effect of slow, deep breathing on visceral pain perception and its underlying psychophysiological mechanisms. Neurogastroenterology Motility, 34(4), e14242. https://doi.org/10.1111/nmo.14242CrossRefPubMed Gholamrezaei, A., Van Diest, I., Aziz, Q., Pauwels, A., Tack, J., Vlaeyen, J. W. S., & Van Oudenhove, L. (2022). Effect of slow, deep breathing on visceral pain perception and its underlying psychophysiological mechanisms. Neurogastroenterology Motility, 34(4), e14242. https://​doi.​org/​10.​1111/​nmo.​14242CrossRefPubMed
go back to reference Joseph, A. E., Moman, R. N., Barman, R. A., Kleppel, D. J., Eberhart, N. D., Gerberi, D. J., Murad, M. H., & Hooten, W. M. (2022). Effects of slow deep breathing on acute clinical pain in adults: A systematic review and meta-analysis of randomized controlled trials. Journal of Evidence-Based Integrative Medicine, 27, 2515690X221078006. https://doi.org/10.1177/2515690X221078006 Joseph, A. E., Moman, R. N., Barman, R. A., Kleppel, D. J., Eberhart, N. D., Gerberi, D. J., Murad, M. H., & Hooten, W. M. (2022). Effects of slow deep breathing on acute clinical pain in adults: A systematic review and meta-analysis of randomized controlled trials. Journal of Evidence-Based Integrative Medicine, 27, 2515690X221078006. https://​doi.​org/​10.​1177/​2515690X22107800​6
go back to reference Khalsa, S. S., Feinstein, J. S., Li, W., Feusner, J. D., Adolphs, R., & Hurlemann, R. (2016). Panic anxiety in humans with bilateral amygdala lesions: Pharmacological induction via cardiorespiratory interoceptive pathways. Journal of Neuroscience, 36(12), 3559–3566. https://doi.org/10.1523/JNEUROSCI.4109-15.2016 Khalsa, S. S., Feinstein, J. S., Li, W., Feusner, J. D., Adolphs, R., & Hurlemann, R. (2016). Panic anxiety in humans with bilateral amygdala lesions: Pharmacological induction via cardiorespiratory interoceptive pathways. Journal of Neuroscience, 36(12), 3559–3566. https://​doi.​org/​10.​1523/​JNEUROSCI.​4109-15.​2016
go back to reference Khalsa, S. S., Adolphs, R., Cameron, O. G., Critchley, H. D., Davenport, P. W., Feinstein, J. S., Feusner, J. D., Garfinkel, S. N., Lane, R. D., Mehling, W. E., Meuret, A. E., Nemeroff, C. B., Oppenheimer, S., Petzschner, F. H., Pollatos, O., Rhudy, J. L., Schramm, L. P., Simmons, W. K., Stein, M. B., . . . participants, I. S. (2018a). Interoception and mental health: A roadmap. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(6), 501–513. https://doi.org/10.1016/j.bpsc.2017.12.004 Khalsa, S. S., Adolphs, R., Cameron, O. G., Critchley, H. D., Davenport, P. W., Feinstein, J. S., Feusner, J. D., Garfinkel, S. N., Lane, R. D., Mehling, W. E., Meuret, A. E., Nemeroff, C. B., Oppenheimer, S., Petzschner, F. H., Pollatos, O., Rhudy, J. L., Schramm, L. P., Simmons, W. K., Stein, M. B., . . . participants, I. S. (2018a). Interoception and mental health: A roadmap. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(6), 501–513. https://​doi.​org/​10.​1016/​j.​bpsc.​2017.​12.​004
go back to reference Ploghaus, A., Narain, C., Beckmann, C. F., Clare, S., Bantick, S., Wise, R., Matthews, P. M., Rawlins, J. N., & Tracey, I. (2001). Exacerbation of pain by anxiety is associated with activity in a hippocampal network. Journal of Neuroscience, 21(24), 9896–9903. https://www.ncbi.nlm.nih.gov/pubmed/11739597 Ploghaus, A., Narain, C., Beckmann, C. F., Clare, S., Bantick, S., Wise, R., Matthews, P. M., Rawlins, J. N., & Tracey, I. (2001). Exacerbation of pain by anxiety is associated with activity in a hippocampal network. Journal of Neuroscience, 21(24), 9896–9903. https://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​11739597
go back to reference Spielberger, C. D. (1983). Manual for the State-Trait Anxiety Inventory (STAI-Form Y). Consulting Psychology Press. Spielberger, C. D. (1983). Manual for the State-Trait Anxiety Inventory (STAI-Form Y). Consulting Psychology Press.
go back to reference Zeidan, F., Emerson, N. M., Farris, S. R., Ray, J. N., Jung, Y., McHaffie, J. G., & Coghill, R. C. (2015a). Mindfulness meditation-based pain relief employs different neural mechanisms than placebo and sham mindfulness meditation-induced analgesia. Journal of Neuroscience, 35(46), 15307–15325. https://doi.org/10.1523/JNEUROSCI.2542-15.2015 Zeidan, F., Emerson, N. M., Farris, S. R., Ray, J. N., Jung, Y., McHaffie, J. G., & Coghill, R. C. (2015a). Mindfulness meditation-based pain relief employs different neural mechanisms than placebo and sham mindfulness meditation-induced analgesia. Journal of Neuroscience, 35(46), 15307–15325. https://​doi.​org/​10.​1523/​JNEUROSCI.​2542-15.​2015
Metagegevens
Titel
Neural and Psychological Mechanisms in the Relationship Between Resting Breathing Rate and Pain
Auteurs
Valeria Oliva
Jennifer N. Baumgartner
Suzan R. Farris
Gabriel Riegner
Lora Khatib
Youngkyoo Jung
Robert C. Coghill
Fadel Zeidan
Publicatiedatum
13-07-2023
Uitgeverij
Springer US
Gepubliceerd in
Mindfulness / Uitgave 7/2023
Print ISSN: 1868-8527
Elektronisch ISSN: 1868-8535
DOI
https://doi.org/10.1007/s12671-023-02176-7