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...

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Published in	Frontiers in neuroscience Vol. 14; p. 147
Main Authors	Hohenschurz-Schmidt, David Johannes, Calcagnini, Giovanni, Dipasquale, Ottavia, Jackson, Jade B., Medina, Sonia, O’Daly, Owen, O’Muircheartaigh, Jonathan, de Lara Rubio, Alfonso, Williams, Steven C. R., McMahon, Stephen B., Makovac, Elena, Howard, Matthew A.
Format	Journal Article
Language	English
Published	Switzerland Frontiers Research Foundation 27.02.2020 Frontiers Media S.A
Subjects	Autonomic nervous system Brain Brain mapping Cold Cortex (cingulate) Cortex (parietal) fMRI Functional magnetic resonance imaging Heart rate heart rate variability Nervous system Neural networks Neuroscience Pain Pain perception periaqueductal gray Periaqueductal gray area Prefrontal cortex resting state fMRI pain resting state autonomic nervous system heart rate variability anterior cingulate cortex periaqueductal gray
Online Access	Get full text
ISSN	1662-453X 1662-4548 1662-453X
DOI	10.3389/fnins.2020.00147

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Abstract	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.
AbstractList	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. 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.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. 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 grey (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 autonomic nervous system, 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.
Author	Makovac, Elena Howard, Matthew A. Calcagnini, Giovanni McMahon, Stephen B. Hohenschurz-Schmidt, David Johannes Medina, Sonia O’Daly, Owen Williams, Steven C. R. Jackson, Jade B. O’Muircheartaigh, Jonathan de Lara Rubio, Alfonso Dipasquale, Ottavia
AuthorAffiliation	7 MRC Centre for Neurodevelopmental Disorders, King’s College London , London , United Kingdom 2 Department of Surgery and Cancer, Imperial College London , London , United Kingdom 1 Department of Neuroimaging, King’s College London , London , United Kingdom 5 Sackler Institute for Translational Neurodevelopment, King’s College London , London , United Kingdom 3 Department of Technology and Health, Italian National Institute of Health , Rome , Italy 4 Wolfson Centre for Age Related Diseases, King’s College London , London , United Kingdom 6 Centre for the Developing Brain, King’s College London , London , United Kingdom
AuthorAffiliation_xml	– name: 6 Centre for the Developing Brain, King’s College London , London , United Kingdom – name: 4 Wolfson Centre for Age Related Diseases, King’s College London , London , United Kingdom – name: 1 Department of Neuroimaging, King’s College London , London , United Kingdom – name: 5 Sackler Institute for Translational Neurodevelopment, King’s College London , London , United Kingdom – name: 3 Department of Technology and Health, Italian National Institute of Health , Rome , Italy – name: 2 Department of Surgery and Cancer, Imperial College London , London , United Kingdom – name: 7 MRC Centre for Neurodevelopmental Disorders, King’s College London , London , United Kingdom
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Copyright	Copyright © 2020 Hohenschurz-Schmidt, Calcagnini, Dipasquale, Jackson, Medina, O’Daly, O’Muircheartaigh, de Lara Rubio, Williams, McMahon, Makovac and Howard. 2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2020 Hohenschurz-Schmidt, Calcagnini, Dipasquale, Jackson, Medina, O’Daly, O’Muircheartaigh, de Lara Rubio, Williams, McMahon, Makovac and Howard. 2020 Hohenschurz-Schmidt, Calcagnini, Dipasquale, Jackson, Medina, O’Daly, O’Muircheartaigh, de Lara Rubio, Williams, McMahon, Makovac and Howard
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Keywords	fMRI pain resting state autonomic nervous system heart rate variability anterior cingulate cortex periaqueductal gray
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Edited by: Luke Henderson, The University of Sydney, Australia Reviewed by: Giris Jacob, Tel Aviv Sourasky Medical Center, Israel; Vaughan G. Macefield, Baker Heart and Diabetes Institute, Australia This article was submitted to Autonomic Neuroscience, a section of the journal Frontiers in Neuroscience
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PublicationTitle	Frontiers in neuroscience
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Snippet	There are bi-directional interactions between the autonomic nervous system (ANS) and pain. This is likely underpinned by a substantial overlap between brain...
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SubjectTerms	Autonomic nervous system Brain Brain mapping Cold Cortex (cingulate) Cortex (parietal) fMRI Functional magnetic resonance imaging Heart rate heart rate variability Nervous system Neural networks Neuroscience Pain Pain perception periaqueductal gray Periaqueductal gray area Prefrontal cortex resting state
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Title	Linking Pain Sensation to the Autonomic Nervous System: The Role of the Anterior Cingulate and Periaqueductal Gray Resting-State Networks
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