Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks
There are bi-directional interactions between the autonomic nervous system (ANS) and pain. This is likely underpinned by a substantial overlap between brain areas of the central autonomic network and areas involved in pain processing and modulation. To date, however, relatively little is known about...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-02-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2020.00147/full |
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| author | David Johannes Hohenschurz-Schmidt David Johannes Hohenschurz-Schmidt Giovanni Calcagnini Ottavia Dipasquale Jade B. Jackson Jade B. Jackson Sonia Medina Sonia Medina Owen O’Daly Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Alfonso de Lara Rubio Steven C. R. Williams Stephen B. McMahon Elena Makovac Elena Makovac Matthew A. Howard |
| author_facet | David Johannes Hohenschurz-Schmidt David Johannes Hohenschurz-Schmidt Giovanni Calcagnini Ottavia Dipasquale Jade B. Jackson Jade B. Jackson Sonia Medina Sonia Medina Owen O’Daly Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Alfonso de Lara Rubio Steven C. R. Williams Stephen B. McMahon Elena Makovac Elena Makovac Matthew A. Howard |
| author_sort | David Johannes Hohenschurz-Schmidt |
| collection | DOAJ |
| description | There are bi-directional interactions between the autonomic nervous system (ANS) and pain. This is likely underpinned by a substantial overlap between brain areas of the central autonomic network and areas involved in pain processing and modulation. To date, however, relatively little is known about the neuronal substrates of the ANS-pain association. Here, we acquired resting state fMRI scans in 21 healthy subjects at rest and during tonic noxious cold stimulation. As indicators of autonomic function, we examined how heart rate variability (HRV) frequency measures were influenced by tonic noxious stimulation and how these variables related to participants’ pain perception and to brain functional connectivity in regions known to play a role in both ANS regulation and pain perception, namely the right dorsal anterior cingulate cortex (dACC) and periaqueductal gray (PAG). Our findings support a role of the cardiac ANS in brain connectivity during pain, linking functional connections of the dACC and PAG with measurements of low frequency (LF)-HRV. In particular, we identified a three-way relationship between the ANS, cortical brain networks known to underpin pain processing, and participants’ subjectively reported pain experiences. LF-HRV both at rest and during pain correlated with functional connectivity between the seed regions and other cortical areas including the right dorsolateral prefrontal cortex (dlPFC), left anterior insula (AI), and the precuneus. Our findings link cardiovascular autonomic parameters to brain activity changes involved in the elaboration of nociceptive information, thus beginning to elucidate underlying brain mechanisms associated with the reciprocal relationship between autonomic and pain-related systems. |
| first_indexed | 2024-12-10T16:10:52Z |
| format | Article |
| id | doaj.art-ae58bf13f8b442c585331f77d9127ef3 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-10T16:10:52Z |
| publishDate | 2020-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-ae58bf13f8b442c585331f77d9127ef32022-12-22T01:42:07ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2020-02-011410.3389/fnins.2020.00147493080Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State NetworksDavid Johannes Hohenschurz-Schmidt0David Johannes Hohenschurz-Schmidt1Giovanni Calcagnini2Ottavia Dipasquale3Jade B. Jackson4Jade B. Jackson5Sonia Medina6Sonia Medina7Owen O’Daly8Jonathan O’Muircheartaigh9Jonathan O’Muircheartaigh10Jonathan O’Muircheartaigh11Jonathan O’Muircheartaigh12Alfonso de Lara Rubio13Steven C. R. Williams14Stephen B. McMahon15Elena Makovac16Elena Makovac17Matthew A. Howard18Department of Neuroimaging, King’s College London, London, United KingdomDepartment of Surgery and Cancer, Imperial College London, London, United KingdomDepartment of Technology and Health, Italian National Institute of Health, Rome, ItalyDepartment of Neuroimaging, King’s College London, London, United KingdomDepartment of Neuroimaging, King’s College London, London, United KingdomWolfson Centre for Age Related Diseases, King’s College London, London, United KingdomDepartment of Neuroimaging, King’s College London, London, United KingdomWolfson Centre for Age Related Diseases, King’s College London, London, United KingdomDepartment of Neuroimaging, King’s College London, London, United KingdomDepartment of Neuroimaging, King’s College London, London, United KingdomSackler Institute for Translational Neurodevelopment, King’s College London, London, United KingdomCentre for the Developing Brain, King’s College London, London, United KingdomMRC Centre for Neurodevelopmental Disorders, King’s College London, London, United KingdomDepartment of Neuroimaging, King’s College London, London, United KingdomDepartment of Neuroimaging, King’s College London, London, United KingdomDepartment of Technology and Health, Italian National Institute of Health, Rome, ItalyDepartment of Neuroimaging, King’s College London, London, United KingdomDepartment of Technology and Health, Italian National Institute of Health, Rome, ItalyDepartment of Neuroimaging, King’s College London, London, United KingdomThere are bi-directional interactions between the autonomic nervous system (ANS) and pain. This is likely underpinned by a substantial overlap between brain areas of the central autonomic network and areas involved in pain processing and modulation. To date, however, relatively little is known about the neuronal substrates of the ANS-pain association. Here, we acquired resting state fMRI scans in 21 healthy subjects at rest and during tonic noxious cold stimulation. As indicators of autonomic function, we examined how heart rate variability (HRV) frequency measures were influenced by tonic noxious stimulation and how these variables related to participants’ pain perception and to brain functional connectivity in regions known to play a role in both ANS regulation and pain perception, namely the right dorsal anterior cingulate cortex (dACC) and periaqueductal gray (PAG). Our findings support a role of the cardiac ANS in brain connectivity during pain, linking functional connections of the dACC and PAG with measurements of low frequency (LF)-HRV. In particular, we identified a three-way relationship between the ANS, cortical brain networks known to underpin pain processing, and participants’ subjectively reported pain experiences. LF-HRV both at rest and during pain correlated with functional connectivity between the seed regions and other cortical areas including the right dorsolateral prefrontal cortex (dlPFC), left anterior insula (AI), and the precuneus. Our findings link cardiovascular autonomic parameters to brain activity changes involved in the elaboration of nociceptive information, thus beginning to elucidate underlying brain mechanisms associated with the reciprocal relationship between autonomic and pain-related systems.https://www.frontiersin.org/article/10.3389/fnins.2020.00147/fullpainautonomic nervous systemheart rate variabilityfMRIresting stateperiaqueductal gray |
| spellingShingle | David Johannes Hohenschurz-Schmidt David Johannes Hohenschurz-Schmidt Giovanni Calcagnini Ottavia Dipasquale Jade B. Jackson Jade B. Jackson Sonia Medina Sonia Medina Owen O’Daly Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Jonathan O’Muircheartaigh Alfonso de Lara Rubio Steven C. R. Williams Stephen B. McMahon Elena Makovac Elena Makovac Matthew A. Howard Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks Frontiers in Neuroscience pain autonomic nervous system heart rate variability fMRI resting state periaqueductal gray |
| title | Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks |
| title_full | Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks |
| title_fullStr | Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks |
| title_full_unstemmed | Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks |
| title_short | Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks |
| title_sort | linking pain sensation to the autonomic nervous system the role of the anterior cingulate and periaqueductal gray resting state networks |
| topic | pain autonomic nervous system heart rate variability fMRI resting state periaqueductal gray |
| url | https://www.frontiersin.org/article/10.3389/fnins.2020.00147/full |
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