Sustained perturbation in functional connectivity induced by cold pain

Background Functional connectivity (FC) perturbations have been reported in multiple chronic pain phenotypes, but the nature of reported changes varies between cohorts and may relate to the consequences of living with chronic‐pain related comorbidities, such as anxiety and depression. Healthy volunt...

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Published inEuropean journal of pain Vol. 24; no. 9; pp. 1850 - 1861
Main Authors Makovac, Elena, Dipasquale, Ottavia, Jackson, Jade B., Medina, Sonia, O'Daly, Owen, O'Muircheartaigh, Jonathan, Lara Rubio, Alfonso, Williams, Steven C. R., McMahon, Stephen B., Howard, Matthew A.
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LanguageEnglish
Published England 01.10.2020
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Abstract Background Functional connectivity (FC) perturbations have been reported in multiple chronic pain phenotypes, but the nature of reported changes varies between cohorts and may relate to the consequences of living with chronic‐pain related comorbidities, such as anxiety and depression. Healthy volunteer studies provide opportunities to study the effects of tonic noxious stimulation independently of these sequelae. Connectivity changes in task negative and positive networks, for example, the default mode and salience networks (DMN/SN), respectively, have been described, but how these and other connectivity networks, for example, those governing descending pain control are affected by the presence of tonic, noxious stimulation in healthy, pain‐free individuals, remains unknown. Method In 20 healthy volunteers, we assessed FC prior to, during, and following tonic cold painful stimulation in the ventromedial prefrontal cortex (vmPFC), rostral anterior insula (rAI), subgenual anterior cingulate cortex (ACC) and periaqueductal grey (PAG). We also recorded subjectively reported pain using a computerised visual analogue scale. Results We saw DMN FC changes during painful stimulation and that inter‐network connectivity between the rAI with the vmPFC increased during pain, whereas PAG‐precuneus FC decreased. Pain‐induced FC alterations persisted following noxious stimulation. FC changes related to the magnitude of individuals' subjectively reported pain. Conclusions We demonstrate FC changes during and following tonic cold‐pain in healthy participants. Similarities between our findings and reports of patients with chronic pain suggest that some FC changes observed in these patients may relate to the presence of an ongoing afferent nociceptive drive. Significance How pain‐related resting state networks are affected by tonic cold‐pain remains unknown. We investigated functional connectivity alterations during and following tonic cold pain in healthy volunteers. Cold pain perturbed the functional connectivity of the ventro‐medial prefrontal cortex, anterior insula, and the periacquaductal grey area. These connectivity changes were associated with the magnitude of individuals’ reported pain. We suggest that some connectivity changes described in chronic pain patients may be due to an ongoing afferent peripheral drive.
AbstractList Functional connectivity (FC) perturbations have been reported in multiple chronic pain phenotypes, but the nature of reported changes varies between cohorts and may relate to the consequences of living with chronic-pain related comorbidities, such as anxiety and depression. Healthy volunteer studies provide opportunities to study the effects of tonic noxious stimulation independently of these sequelae. Connectivity changes in task negative and positive networks, for example, the default mode and salience networks (DMN/SN), respectively, have been described, but how these and other connectivity networks, for example, those governing descending pain control are affected by the presence of tonic, noxious stimulation in healthy, pain-free individuals, remains unknown. In 20 healthy volunteers, we assessed FC prior to, during, and following tonic cold painful stimulation in the ventromedial prefrontal cortex (vmPFC), rostral anterior insula (rAI), subgenual anterior cingulate cortex (ACC) and periaqueductal grey (PAG). We also recorded subjectively reported pain using a computerised visual analogue scale. We saw DMN FC changes during painful stimulation and that inter-network connectivity between the rAI with the vmPFC increased during pain, whereas PAG-precuneus FC decreased. Pain-induced FC alterations persisted following noxious stimulation. FC changes related to the magnitude of individuals' subjectively reported pain. We demonstrate FC changes during and following tonic cold-pain in healthy participants. Similarities between our findings and reports of patients with chronic pain suggest that some FC changes observed in these patients may relate to the presence of an ongoing afferent nociceptive drive. How pain-related resting state networks are affected by tonic cold-pain remains unknown. We investigated functional connectivity alterations during and following tonic cold pain in healthy volunteers. Cold pain perturbed the functional connectivity of the ventro-medial prefrontal cortex, anterior insula, and the periacquaductal grey area. These connectivity changes were associated with the magnitude of individuals' reported pain. We suggest that some connectivity changes described in chronic pain patients may be due to an ongoing afferent peripheral drive.
Background Functional connectivity (FC) perturbations have been reported in multiple chronic pain phenotypes, but the nature of reported changes varies between cohorts and may relate to the consequences of living with chronic‐pain related comorbidities, such as anxiety and depression. Healthy volunteer studies provide opportunities to study the effects of tonic noxious stimulation independently of these sequelae. Connectivity changes in task negative and positive networks, for example, the default mode and salience networks (DMN/SN), respectively, have been described, but how these and other connectivity networks, for example, those governing descending pain control are affected by the presence of tonic, noxious stimulation in healthy, pain‐free individuals, remains unknown. Method In 20 healthy volunteers, we assessed FC prior to, during, and following tonic cold painful stimulation in the ventromedial prefrontal cortex (vmPFC), rostral anterior insula (rAI), subgenual anterior cingulate cortex (ACC) and periaqueductal grey (PAG). We also recorded subjectively reported pain using a computerised visual analogue scale. Results We saw DMN FC changes during painful stimulation and that inter‐network connectivity between the rAI with the vmPFC increased during pain, whereas PAG‐precuneus FC decreased. Pain‐induced FC alterations persisted following noxious stimulation. FC changes related to the magnitude of individuals' subjectively reported pain. Conclusions We demonstrate FC changes during and following tonic cold‐pain in healthy participants. Similarities between our findings and reports of patients with chronic pain suggest that some FC changes observed in these patients may relate to the presence of an ongoing afferent nociceptive drive. Significance How pain‐related resting state networks are affected by tonic cold‐pain remains unknown. We investigated functional connectivity alterations during and following tonic cold pain in healthy volunteers. Cold pain perturbed the functional connectivity of the ventro‐medial prefrontal cortex, anterior insula, and the periacquaductal grey area. These connectivity changes were associated with the magnitude of individuals’ reported pain. We suggest that some connectivity changes described in chronic pain patients may be due to an ongoing afferent peripheral drive.
Author Makovac, Elena
O'Muircheartaigh, Jonathan
Howard, Matthew A.
McMahon, Stephen B.
Medina, Sonia
Williams, Steven C. R.
Lara Rubio, Alfonso
Jackson, Jade B.
Dipasquale, Ottavia
O'Daly, Owen
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  givenname: Matthew A.
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  organization: King's College London
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CitedBy_id crossref_primary_10_1113_JP282013
crossref_primary_10_3389_fneur_2023_1136367
crossref_primary_10_1002_ejp_2097
crossref_primary_10_1016_j_neuropharm_2021_108765
crossref_primary_10_3390_jcm13061645
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Copyright 2020 The Authors. European Journal of Pain published by John Wiley & Sons Ltd on behalf of European Pain Federation EFIC
2020 The Authors. European Journal of Pain published by John Wiley & Sons Ltd on behalf of European Pain Federation EFIC ®.
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Notes Funding information
This work was funded by a Medical Research Council Experimental Medicine Challenge Grant (MR/N026969/1). MAH, SM, OO and SW are also supported by the NIHR Biomedical Research Centre for Mental Health at the South London and Maudsley NHS Trust. JOM is supported by a Sir Henry Dale Fellowship jointly funded by the Welcome Trust and the Royal Society (grant number 206675/Z/17/Z) and a Medical Research Council (MRC) Centre grant (MR/N026063/1).
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Snippet Background Functional connectivity (FC) perturbations have been reported in multiple chronic pain phenotypes, but the nature of reported changes varies between...
Functional connectivity (FC) perturbations have been reported in multiple chronic pain phenotypes, but the nature of reported changes varies between cohorts...
SourceID pubmed
wiley
SourceType Index Database
Publisher
StartPage 1850
SubjectTerms Brain Mapping
Chronic Pain - diagnostic imaging
Humans
Magnetic Resonance Imaging
Neural Pathways - diagnostic imaging
Prefrontal Cortex - diagnostic imaging
Title Sustained perturbation in functional connectivity induced by cold pain
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fejp.1633
https://www.ncbi.nlm.nih.gov/pubmed/32648623
Volume 24
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