Brain mechanisms of social touch-induced analgesia in females
Supportive touch has remarkable benefits in childbirth and during painful medical procedures. But does social touch influence pain neurophysiology, ie, the brain processes linked to nociception and primary pain experience? What other brain processes beyond primary pain systems mediate their analgesi...
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Veröffentlicht in: | Pain (Amsterdam) 2019-09, Vol.160 (9), p.2072-2085 |
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description | Supportive touch has remarkable benefits in childbirth and during painful medical procedures. But does social touch influence pain neurophysiology, ie, the brain processes linked to nociception and primary pain experience? What other brain processes beyond primary pain systems mediate their analgesic effects? In this study, women (N = 30) experienced thermal pain while holding their romantic partner's hand or an inert device. Social touch reduced pain and attenuated functional magnetic resonance imaging activity in the Neurologic Pain Signature (NPS)-a multivariate brain pattern sensitive and specific to somatic pain-and increased connectivity between the NPS and both somatosensory and "default mode" regions. Brain correlates of touch-induced analgesia included reduced pain-related activation in (1) regions targeted by primary nociceptive afferents (eg, posterior insula, and anterior cingulate cortex); and (b) regions associated with affective value (orbitofrontal cortex), meaning (ventromedial prefrontal cortex [PFC]), and attentional regulation (dorsolateral PFC). Activation reductions during handholding (vs holding a rubber device) significantly mediated reductions in pain intensity and unpleasantness; greater pain reductions during handholding correlated with greater increases in emotional comfort, which correlated with higher perceived relationship quality and (a trend toward) greater perceived closeness with the romantic partner. The strongest mediators of analgesia were activity reductions in a brain circuit traditionally associated with stress and defensive behavior in mammals, including ventromedial and dorsomedial PFC, rostral anterior cingulate cortex, amygdala/hippocampus, hypothalamus, and periaqueductal gray matter. Social touch affects core brain processes that contribute to pain and pain-related affective distress in females, and should be considered alongside other treatments in medical and caregiving contexts. |
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But does social touch influence pain neurophysiology, ie, the brain processes linked to nociception and primary pain experience? What other brain processes beyond primary pain systems mediate their analgesic effects? In this study, women (N = 30) experienced thermal pain while holding their romantic partner's hand or an inert device. Social touch reduced pain and attenuated functional magnetic resonance imaging activity in the Neurologic Pain Signature (NPS)-a multivariate brain pattern sensitive and specific to somatic pain-and increased connectivity between the NPS and both somatosensory and "default mode" regions. Brain correlates of touch-induced analgesia included reduced pain-related activation in (1) regions targeted by primary nociceptive afferents (eg, posterior insula, and anterior cingulate cortex); and (b) regions associated with affective value (orbitofrontal cortex), meaning (ventromedial prefrontal cortex [PFC]), and attentional regulation (dorsolateral PFC). Activation reductions during handholding (vs holding a rubber device) significantly mediated reductions in pain intensity and unpleasantness; greater pain reductions during handholding correlated with greater increases in emotional comfort, which correlated with higher perceived relationship quality and (a trend toward) greater perceived closeness with the romantic partner. The strongest mediators of analgesia were activity reductions in a brain circuit traditionally associated with stress and defensive behavior in mammals, including ventromedial and dorsomedial PFC, rostral anterior cingulate cortex, amygdala/hippocampus, hypothalamus, and periaqueductal gray matter. Social touch affects core brain processes that contribute to pain and pain-related affective distress in females, and should be considered alongside other treatments in medical and caregiving contexts.</description><identifier>ISSN: 0304-3959</identifier><identifier>EISSN: 1872-6623</identifier><identifier>DOI: 10.1097/j.pain.0000000000001599</identifier><identifier>PMID: 31241496</identifier><language>eng</language><publisher>United States: Wolters Kluwer</publisher><subject>Adolescent ; Adult ; Analgesia - methods ; Analgesia - psychology ; Brain - diagnostic imaging ; Brain - physiology ; Cognitive Sciences ; Female ; Humans ; Interpersonal Relations ; Life Sciences ; Male ; Neurons and Cognition ; Pain - diagnostic imaging ; Pain - psychology ; Pain Management - methods ; Pain Management - psychology ; Pain Measurement - methods ; Pain Measurement - psychology ; Sex Factors ; Sexual Partners - psychology ; Touch - physiology ; Touch Perception - physiology ; Young Adult</subject><ispartof>Pain (Amsterdam), 2019-09, Vol.160 (9), p.2072-2085</ispartof><rights>Wolters Kluwer</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4587-17955bb31292782f73b0bd41ef4bff095a1d29c0b162be0b526274468c9cb4bb3</citedby><cites>FETCH-LOGICAL-c4587-17955bb31292782f73b0bd41ef4bff095a1d29c0b162be0b526274468c9cb4bb3</cites><orcidid>0000-0002-3121-6491</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31241496$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04756900$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>López-Solà, Marina</creatorcontrib><creatorcontrib>Geuter, Stephan</creatorcontrib><creatorcontrib>Koban, Leonie</creatorcontrib><creatorcontrib>Coan, James A.</creatorcontrib><creatorcontrib>Wager, Tor D.</creatorcontrib><title>Brain mechanisms of social touch-induced analgesia in females</title><title>Pain (Amsterdam)</title><addtitle>Pain</addtitle><description>Supportive touch has remarkable benefits in childbirth and during painful medical procedures. But does social touch influence pain neurophysiology, ie, the brain processes linked to nociception and primary pain experience? What other brain processes beyond primary pain systems mediate their analgesic effects? In this study, women (N = 30) experienced thermal pain while holding their romantic partner's hand or an inert device. Social touch reduced pain and attenuated functional magnetic resonance imaging activity in the Neurologic Pain Signature (NPS)-a multivariate brain pattern sensitive and specific to somatic pain-and increased connectivity between the NPS and both somatosensory and "default mode" regions. Brain correlates of touch-induced analgesia included reduced pain-related activation in (1) regions targeted by primary nociceptive afferents (eg, posterior insula, and anterior cingulate cortex); and (b) regions associated with affective value (orbitofrontal cortex), meaning (ventromedial prefrontal cortex [PFC]), and attentional regulation (dorsolateral PFC). Activation reductions during handholding (vs holding a rubber device) significantly mediated reductions in pain intensity and unpleasantness; greater pain reductions during handholding correlated with greater increases in emotional comfort, which correlated with higher perceived relationship quality and (a trend toward) greater perceived closeness with the romantic partner. The strongest mediators of analgesia were activity reductions in a brain circuit traditionally associated with stress and defensive behavior in mammals, including ventromedial and dorsomedial PFC, rostral anterior cingulate cortex, amygdala/hippocampus, hypothalamus, and periaqueductal gray matter. Social touch affects core brain processes that contribute to pain and pain-related affective distress in females, and should be considered alongside other treatments in medical and caregiving contexts.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Analgesia - methods</subject><subject>Analgesia - psychology</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - physiology</subject><subject>Cognitive Sciences</subject><subject>Female</subject><subject>Humans</subject><subject>Interpersonal Relations</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Neurons and Cognition</subject><subject>Pain - diagnostic imaging</subject><subject>Pain - psychology</subject><subject>Pain Management - methods</subject><subject>Pain Management - psychology</subject><subject>Pain Measurement - methods</subject><subject>Pain Measurement - psychology</subject><subject>Sex Factors</subject><subject>Sexual Partners - psychology</subject><subject>Touch - physiology</subject><subject>Touch Perception - physiology</subject><subject>Young Adult</subject><issn>0304-3959</issn><issn>1872-6623</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkMtOwzAQRS0EgvL4BcgSFiljx496waJUQJEqsYG1ZTsOSXGSEicg_h6HAkLMxtLo3DPWRegMwxSDFJfr6UZXzRT-DGZS7qAJngmSck6yXTSBDGiaSSYP0GEI6wgRQuQ-OsgwoZhKPkFX110UJbWzpW6qUIekLZLQ2kr7pG8HW6ZVkw_W5YlutH92odJJ5AtXa-_CMdortA_u5Ps9Qk-3N4-LZbp6uLtfzFeppWwmUiwkY8bEq5KIGSlEZsDkFLuCmqIAyTTOibRgMCfGgWGEE0Epn1lpDY3BI3Sx9Zbaq01X1br7UK2u1HK-UuMOqGBcArzhyJ5v2U3Xvg4u9KqugnXe68a1Q1CxAUYFiGxExRa1XRtC54pfNwY19qzWauxZ_e85Jk-_jwymdvlv7qfYCNAt8N763nXhxQ_vrlOl074vv3w8kzwlgCXEf0M6mkX2CdVRh2k</recordid><startdate>20190901</startdate><enddate>20190901</enddate><creator>López-Solà, Marina</creator><creator>Geuter, Stephan</creator><creator>Koban, Leonie</creator><creator>Coan, James A.</creator><creator>Wager, Tor D.</creator><general>Wolters Kluwer</general><general>Lippincott, Williams & Wilkins</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-3121-6491</orcidid></search><sort><creationdate>20190901</creationdate><title>Brain mechanisms of social touch-induced analgesia in females</title><author>López-Solà, Marina ; 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Activation reductions during handholding (vs holding a rubber device) significantly mediated reductions in pain intensity and unpleasantness; greater pain reductions during handholding correlated with greater increases in emotional comfort, which correlated with higher perceived relationship quality and (a trend toward) greater perceived closeness with the romantic partner. The strongest mediators of analgesia were activity reductions in a brain circuit traditionally associated with stress and defensive behavior in mammals, including ventromedial and dorsomedial PFC, rostral anterior cingulate cortex, amygdala/hippocampus, hypothalamus, and periaqueductal gray matter. 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subjects | Adolescent Adult Analgesia - methods Analgesia - psychology Brain - diagnostic imaging Brain - physiology Cognitive Sciences Female Humans Interpersonal Relations Life Sciences Male Neurons and Cognition Pain - diagnostic imaging Pain - psychology Pain Management - methods Pain Management - psychology Pain Measurement - methods Pain Measurement - psychology Sex Factors Sexual Partners - psychology Touch - physiology Touch Perception - physiology Young Adult |
title | Brain mechanisms of social touch-induced analgesia in females |
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