Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.

Cognitive self-regulation can strongly modulate pain and emotion. However, it is unclear whether self-regulation primarily influences primary nociceptive and affective processes or evaluative ones. In this study, participants engaged in self-regulation to increase or decrease pain while experiencing...

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Main Authors: Choong-Wan Woo, Mathieu Roy, Jason T Buhle, Tor D Wager
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.1002036
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spelling doaj-096fcba9f8ca402fb6da9bd8a530c87e2021-07-02T16:28:53ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852015-01-01131e100203610.1371/journal.pbio.1002036Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.Choong-Wan WooMathieu RoyJason T BuhleTor D WagerCognitive self-regulation can strongly modulate pain and emotion. However, it is unclear whether self-regulation primarily influences primary nociceptive and affective processes or evaluative ones. In this study, participants engaged in self-regulation to increase or decrease pain while experiencing multiple levels of painful heat during functional magnetic resonance imaging (fMRI) imaging. Both heat intensity and self-regulation strongly influenced reported pain, but they did so via two distinct brain pathways. The effects of stimulus intensity were mediated by the neurologic pain signature (NPS), an a priori distributed brain network shown to predict physical pain with over 90% sensitivity and specificity across four studies. Self-regulation did not influence NPS responses; instead, its effects were mediated through functional connections between the nucleus accumbens and ventromedial prefrontal cortex. This pathway was unresponsive to noxious input, and has been broadly implicated in valuation, emotional appraisal, and functional outcomes in pain and other types of affective processes. These findings provide evidence that pain reports are associated with two dissociable functional systems: nociceptive/affective aspects mediated by the NPS, and evaluative/functional aspects mediated by a fronto-striatal system.https://doi.org/10.1371/journal.pbio.1002036
collection DOAJ
language English
format Article
sources DOAJ
author Choong-Wan Woo
Mathieu Roy
Jason T Buhle
Tor D Wager
spellingShingle Choong-Wan Woo
Mathieu Roy
Jason T Buhle
Tor D Wager
Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
PLoS Biology
author_facet Choong-Wan Woo
Mathieu Roy
Jason T Buhle
Tor D Wager
author_sort Choong-Wan Woo
title Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
title_short Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
title_full Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
title_fullStr Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
title_full_unstemmed Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
title_sort distinct brain systems mediate the effects of nociceptive input and self-regulation on pain.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2015-01-01
description Cognitive self-regulation can strongly modulate pain and emotion. However, it is unclear whether self-regulation primarily influences primary nociceptive and affective processes or evaluative ones. In this study, participants engaged in self-regulation to increase or decrease pain while experiencing multiple levels of painful heat during functional magnetic resonance imaging (fMRI) imaging. Both heat intensity and self-regulation strongly influenced reported pain, but they did so via two distinct brain pathways. The effects of stimulus intensity were mediated by the neurologic pain signature (NPS), an a priori distributed brain network shown to predict physical pain with over 90% sensitivity and specificity across four studies. Self-regulation did not influence NPS responses; instead, its effects were mediated through functional connections between the nucleus accumbens and ventromedial prefrontal cortex. This pathway was unresponsive to noxious input, and has been broadly implicated in valuation, emotional appraisal, and functional outcomes in pain and other types of affective processes. These findings provide evidence that pain reports are associated with two dissociable functional systems: nociceptive/affective aspects mediated by the NPS, and evaluative/functional aspects mediated by a fronto-striatal system.
url https://doi.org/10.1371/journal.pbio.1002036
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