Neural mechanisms of pain processing differ between endurance athletes and nonathletes: A functional connectivity magnetic resonance imaging study
Pain perception and the ability to modulate arising pain vary tremendously between individuals. It has been shown that endurance athletes possess higher pain tolerance thresholds and a greater effect of conditioned pain modulation than nonathletes, both indicating a more efficient system of endogeno...
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| Veröffentlicht in: | Human brain mapping 2021-12, Vol.42 (18), p.5927-5942 |
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| creator | Geisler, Maria Ritter, Alexander Herbsleb, Marco Bär, Karl‐Jürgen Weiss, Thomas |
| description | Pain perception and the ability to modulate arising pain vary tremendously between individuals. It has been shown that endurance athletes possess higher pain tolerance thresholds and a greater effect of conditioned pain modulation than nonathletes, both indicating a more efficient system of endogenous pain inhibition. The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. We found lower pain ratings in endurance athletes compared to nonathletes to physically identical painful stimulation. Furthermore, brain activations of athletes versus nonathletes during painful heat stimulation revealed reduced activation in several brain regions that are typically activated by nociceptive stimulation. This included the thalamus, primary and secondary somatosensory cortex, insula, anterior cingulate cortex, midcingulate cortex, dorsolateral prefrontal cortex, and brain stem (BS). Functional connectivity analyses revealed stronger network during painful heat stimulation in athletes between the analyzed brain regions except for connections with the BS that showed reduced functional connectivity in athletes. Post hoc correlation analyses revealed associations of the subject's fitness level and the brain activation strengths, subject's fitness level and functional connectivity, and brain activation strengths and functional connectivity. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat.
The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat. |
| doi_str_mv | 10.1002/hbm.25659 |
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The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat.</description><identifier>ISSN: 1065-9471</identifier><identifier>ISSN: 1097-0193</identifier><identifier>EISSN: 1097-0193</identifier><identifier>DOI: 10.1002/hbm.25659</identifier><identifier>PMID: 34524716</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adult ; Athletes ; Brain ; Brain mapping ; Brain stem ; Brain Stem - diagnostic imaging ; Brain Stem - physiology ; Cerebral Cortex - diagnostic imaging ; Cerebral Cortex - physiology ; Connectome ; Cortex (cingulate) ; Cortex (somatosensory) ; Endurance ; endurance sport ; Fitness ; Functional magnetic resonance imaging ; functional magnetic resonance imaging (fMRI) ; Heat ; heat pain ; Humans ; Information processing ; Life Sciences & Biomedicine ; Magnetic Resonance Imaging ; Male ; Males ; Neural networks ; Neuroimaging ; Neurosciences ; Neurosciences & Neurology ; neurosignature of physical pain ; Pain ; Pain Measurement ; pain modulation ; Pain perception ; Pain Perception - physiology ; Prefrontal cortex ; Radiology, Nuclear Medicine & Medical Imaging ; Resonance ; Science & Technology ; Stimulation ; Thalamus ; Thalamus - diagnostic imaging ; Thalamus - physiology ; Young Adult</subject><ispartof>Human brain mapping, 2021-12, Vol.42 (18), p.5927-5942</ispartof><rights>2021 The Authors. published by Wiley Periodicals LLC.</rights><rights>2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.</rights><rights>2021. This work is published 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.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>14</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000695998100001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c4979-d4ae6af46cd782795db938aa1f26d87426a934099d02f4bff332a9cb38a9b4213</citedby><cites>FETCH-LOGICAL-c4979-d4ae6af46cd782795db938aa1f26d87426a934099d02f4bff332a9cb38a9b4213</cites><orcidid>0000-0001-8190-5175 ; 0000-0003-3861-5679 ; 0000-0002-0321-2119 ; 0000-0002-1312-1018</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8596969/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8596969/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,1418,2115,11567,27929,27930,39263,45579,45580,46057,46481,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34524716$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Geisler, Maria</creatorcontrib><creatorcontrib>Ritter, Alexander</creatorcontrib><creatorcontrib>Herbsleb, Marco</creatorcontrib><creatorcontrib>Bär, Karl‐Jürgen</creatorcontrib><creatorcontrib>Weiss, Thomas</creatorcontrib><title>Neural mechanisms of pain processing differ between endurance athletes and nonathletes: A functional connectivity magnetic resonance imaging study</title><title>Human brain mapping</title><addtitle>HUM BRAIN MAPP</addtitle><addtitle>Hum Brain Mapp</addtitle><description>Pain perception and the ability to modulate arising pain vary tremendously between individuals. It has been shown that endurance athletes possess higher pain tolerance thresholds and a greater effect of conditioned pain modulation than nonathletes, both indicating a more efficient system of endogenous pain inhibition. The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. We found lower pain ratings in endurance athletes compared to nonathletes to physically identical painful stimulation. Furthermore, brain activations of athletes versus nonathletes during painful heat stimulation revealed reduced activation in several brain regions that are typically activated by nociceptive stimulation. This included the thalamus, primary and secondary somatosensory cortex, insula, anterior cingulate cortex, midcingulate cortex, dorsolateral prefrontal cortex, and brain stem (BS). Functional connectivity analyses revealed stronger network during painful heat stimulation in athletes between the analyzed brain regions except for connections with the BS that showed reduced functional connectivity in athletes. Post hoc correlation analyses revealed associations of the subject's fitness level and the brain activation strengths, subject's fitness level and functional connectivity, and brain activation strengths and functional connectivity. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat.
The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat.</description><subject>Adult</subject><subject>Athletes</subject><subject>Brain</subject><subject>Brain mapping</subject><subject>Brain stem</subject><subject>Brain Stem - diagnostic imaging</subject><subject>Brain Stem - physiology</subject><subject>Cerebral Cortex - diagnostic imaging</subject><subject>Cerebral Cortex - physiology</subject><subject>Connectome</subject><subject>Cortex (cingulate)</subject><subject>Cortex (somatosensory)</subject><subject>Endurance</subject><subject>endurance sport</subject><subject>Fitness</subject><subject>Functional magnetic resonance imaging</subject><subject>functional magnetic resonance imaging (fMRI)</subject><subject>Heat</subject><subject>heat pain</subject><subject>Humans</subject><subject>Information processing</subject><subject>Life Sciences & Biomedicine</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Males</subject><subject>Neural networks</subject><subject>Neuroimaging</subject><subject>Neurosciences</subject><subject>Neurosciences & Neurology</subject><subject>neurosignature of physical pain</subject><subject>Pain</subject><subject>Pain Measurement</subject><subject>pain modulation</subject><subject>Pain perception</subject><subject>Pain Perception - physiology</subject><subject>Prefrontal cortex</subject><subject>Radiology, Nuclear Medicine & Medical Imaging</subject><subject>Resonance</subject><subject>Science & Technology</subject><subject>Stimulation</subject><subject>Thalamus</subject><subject>Thalamus - diagnostic imaging</subject><subject>Thalamus - physiology</subject><subject>Young Adult</subject><issn>1065-9471</issn><issn>1097-0193</issn><issn>1097-0193</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><recordid>eNqNkt2KFDEQhRtR3B-98AUk4I0is5ukf8sLYR3UFVa90euQTldmsnQnYye9y7zGPrHVzuyggiB9kU7lq5NDnWTZM8HPBOfyfN0OZ7KsSniQHQsO9YILyB_O_1W5gKIWR9lJjNecC1Fy8Tg7yotSUrk6zu6-4DTqng1o1tq7OEQWLNto59lmDAZjdH7FOmctjqzFdIvoGfqOmrxBptO6x4SRad8xH_z9_g27YHbyJjmq9cwE75E2Ny5t2aBXHpMzbMRIp7OMo9p8T0xTt32SPbK6j_h0v55m3z-8_7a8XFx9_fhpeXG1MAXUsOgKjZW2RWW6upE1lF0LeaO1sLLqmrqQlYa84AAdl7Zorc1zqcG0xEBbSJGfZm93upupHbAz6BNNQm1GcjNuVdBO_Xni3Vqtwo1qSqjoI4GXe4Ex_JgwJjW4aLDvtccwRSXLWkJOgy4JffEXeh2mkUYzU9BwCcALol7tKDOGGEe0BzOCqzlpRUmrX0kT-_x39wfyPloCXu-AW2yDjcYhTfqAcc4rKAEakqV3QXTz__TSJT0nuwyTT9R6vm91PW7_bVldvvu88_4T6EjXjw</recordid><startdate>20211215</startdate><enddate>20211215</enddate><creator>Geisler, Maria</creator><creator>Ritter, Alexander</creator><creator>Herbsleb, Marco</creator><creator>Bär, Karl‐Jürgen</creator><creator>Weiss, Thomas</creator><general>John Wiley & Sons, Inc</general><general>Wiley</general><scope>24P</scope><scope>WIN</scope><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</scope><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>3V.</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>8FD</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8190-5175</orcidid><orcidid>https://orcid.org/0000-0003-3861-5679</orcidid><orcidid>https://orcid.org/0000-0002-0321-2119</orcidid><orcidid>https://orcid.org/0000-0002-1312-1018</orcidid></search><sort><creationdate>20211215</creationdate><title>Neural mechanisms of pain processing differ between endurance athletes and nonathletes: A functional connectivity magnetic resonance imaging study</title><author>Geisler, Maria ; Ritter, Alexander ; Herbsleb, Marco ; Bär, Karl‐Jürgen ; Weiss, Thomas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4979-d4ae6af46cd782795db938aa1f26d87426a934099d02f4bff332a9cb38a9b4213</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adult</topic><topic>Athletes</topic><topic>Brain</topic><topic>Brain mapping</topic><topic>Brain stem</topic><topic>Brain Stem - diagnostic imaging</topic><topic>Brain Stem - physiology</topic><topic>Cerebral Cortex - diagnostic imaging</topic><topic>Cerebral Cortex - physiology</topic><topic>Connectome</topic><topic>Cortex (cingulate)</topic><topic>Cortex (somatosensory)</topic><topic>Endurance</topic><topic>endurance sport</topic><topic>Fitness</topic><topic>Functional magnetic resonance imaging</topic><topic>functional magnetic resonance imaging (fMRI)</topic><topic>Heat</topic><topic>heat pain</topic><topic>Humans</topic><topic>Information processing</topic><topic>Life Sciences & Biomedicine</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Males</topic><topic>Neural networks</topic><topic>Neuroimaging</topic><topic>Neurosciences</topic><topic>Neurosciences & Neurology</topic><topic>neurosignature of physical pain</topic><topic>Pain</topic><topic>Pain Measurement</topic><topic>pain modulation</topic><topic>Pain perception</topic><topic>Pain Perception - physiology</topic><topic>Prefrontal cortex</topic><topic>Radiology, Nuclear Medicine & Medical Imaging</topic><topic>Resonance</topic><topic>Science & Technology</topic><topic>Stimulation</topic><topic>Thalamus</topic><topic>Thalamus - diagnostic imaging</topic><topic>Thalamus - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Geisler, Maria</creatorcontrib><creatorcontrib>Ritter, Alexander</creatorcontrib><creatorcontrib>Herbsleb, Marco</creatorcontrib><creatorcontrib>Bär, Karl‐Jürgen</creatorcontrib><creatorcontrib>Weiss, Thomas</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Web of Science - Science Citation Index Expanded - 2021</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Technology Research Database</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Proquest Central</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human brain mapping</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Geisler, Maria</au><au>Ritter, Alexander</au><au>Herbsleb, Marco</au><au>Bär, Karl‐Jürgen</au><au>Weiss, Thomas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural mechanisms of pain processing differ between endurance athletes and nonathletes: A functional connectivity magnetic resonance imaging study</atitle><jtitle>Human brain mapping</jtitle><stitle>HUM BRAIN MAPP</stitle><addtitle>Hum Brain Mapp</addtitle><date>2021-12-15</date><risdate>2021</risdate><volume>42</volume><issue>18</issue><spage>5927</spage><epage>5942</epage><pages>5927-5942</pages><issn>1065-9471</issn><issn>1097-0193</issn><eissn>1097-0193</eissn><abstract>Pain perception and the ability to modulate arising pain vary tremendously between individuals. It has been shown that endurance athletes possess higher pain tolerance thresholds and a greater effect of conditioned pain modulation than nonathletes, both indicating a more efficient system of endogenous pain inhibition. The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. We found lower pain ratings in endurance athletes compared to nonathletes to physically identical painful stimulation. Furthermore, brain activations of athletes versus nonathletes during painful heat stimulation revealed reduced activation in several brain regions that are typically activated by nociceptive stimulation. This included the thalamus, primary and secondary somatosensory cortex, insula, anterior cingulate cortex, midcingulate cortex, dorsolateral prefrontal cortex, and brain stem (BS). Functional connectivity analyses revealed stronger network during painful heat stimulation in athletes between the analyzed brain regions except for connections with the BS that showed reduced functional connectivity in athletes. Post hoc correlation analyses revealed associations of the subject's fitness level and the brain activation strengths, subject's fitness level and functional connectivity, and brain activation strengths and functional connectivity. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat.
The aim of the present study was to focus on the neural mechanisms of pain processing in endurance athletes that have not been investigated yet. Therefore, we analyzed the pain processing of 18 male athletes and 19 healthy male nonathletes using functional magnetic resonance imaging. Together, our results demonstrate for the first time that endurance athletes do not only differ in behavioral variables compared to nonathletes, but also in the neural processing of pain elicited by noxious heat.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>34524716</pmid><doi>10.1002/hbm.25659</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-8190-5175</orcidid><orcidid>https://orcid.org/0000-0003-3861-5679</orcidid><orcidid>https://orcid.org/0000-0002-0321-2119</orcidid><orcidid>https://orcid.org/0000-0002-1312-1018</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adult Athletes Brain Brain mapping Brain stem Brain Stem - diagnostic imaging Brain Stem - physiology Cerebral Cortex - diagnostic imaging Cerebral Cortex - physiology Connectome Cortex (cingulate) Cortex (somatosensory) Endurance endurance sport Fitness Functional magnetic resonance imaging functional magnetic resonance imaging (fMRI) Heat heat pain Humans Information processing Life Sciences & Biomedicine Magnetic Resonance Imaging Male Males Neural networks Neuroimaging Neurosciences Neurosciences & Neurology neurosignature of physical pain Pain Pain Measurement pain modulation Pain perception Pain Perception - physiology Prefrontal cortex Radiology, Nuclear Medicine & Medical Imaging Resonance Science & Technology Stimulation Thalamus Thalamus - diagnostic imaging Thalamus - physiology Young Adult |
| title | Neural mechanisms of pain processing differ between endurance athletes and nonathletes: A functional connectivity magnetic resonance imaging study |
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