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Brain (re)organisation following amputation: Implications for phantom limb pain
Following arm amputation the region that represented the missing hand in primary somatosensory cortex (S1) becomes deprived of its primary input, resulting in changed boundaries of the S1 body map. This remapping process has been termed ‘reorganisation’ and has been attributed to multiple mechanisms...
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Published in: | NeuroImage (Orlando, Fla.) Fla.), 2020-09, Vol.218, p.116943-116943, Article 116943 |
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description | Following arm amputation the region that represented the missing hand in primary somatosensory cortex (S1) becomes deprived of its primary input, resulting in changed boundaries of the S1 body map. This remapping process has been termed ‘reorganisation’ and has been attributed to multiple mechanisms, including increased expression of previously masked inputs. In a maladaptive plasticity model, such reorganisation has been associated with phantom limb pain (PLP). Brain activity associated with phantom hand movements is also correlated with PLP, suggesting that preserved limb functional representation may serve as a complementary process. Here we review some of the most recent evidence for the potential drivers and consequences of brain (re)organisation following amputation, based on human neuroimaging. We emphasise other perceptual and behavioural factors consequential to arm amputation, such as non-painful phantom sensations, perceived limb ownership, intact hand compensatory behaviour or prosthesis use, which have also been related to both cortical changes and PLP. We also discuss new findings based on interventions designed to alter the brain representation of the phantom limb, including augmented/virtual reality applications and brain computer interfaces. These studies point to a close interaction of sensory changes and alterations in brain regions involved in body representation, pain processing and motor control. Finally, we review recent evidence based on methodological advances such as high field neuroimaging and multivariate techniques that provide new opportunities to interrogate somatosensory representations in the missing hand cortical territory. Collectively, this research highlights the need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP.
•Technological advancements provide new insight into the neural basis of phantom pain.•Traditional mechanistic accounts of remapping in somatosensory cortex are incomplete.•Related contextual factors such as adaptive behaviour will contribute to brain plasticity.•A broader mechanistic focus beyond primary sensorimotor cortex is needed.•Plasticity and stability of the sensorimotor body maps may vary across time scales. |
doi_str_mv | 10.1016/j.neuroimage.2020.116943 |
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•Technological advancements provide new insight into the neural basis of phantom pain.•Traditional mechanistic accounts of remapping in somatosensory cortex are incomplete.•Related contextual factors such as adaptive behaviour will contribute to brain plasticity.•A broader mechanistic focus beyond primary sensorimotor cortex is needed.•Plasticity and stability of the sensorimotor body maps may vary across time scales.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2020.116943</identifier><identifier>PMID: 32428706</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adult ; Amputation ; Amputation, Surgical ; Amputees ; Arm ; Brain - diagnostic imaging ; Brain - physiopathology ; Brain Mapping ; Brain research ; Computer applications ; Cortex (somatosensory) ; Cortical reorganisation ; Female ; Hand ; Humans ; Interfaces ; Male ; Medical imaging ; Middle Aged ; Motor task performance ; Multivariate analysis ; Neuroimaging ; Pain ; Pain - diagnostic imaging ; Pain - etiology ; Pain - physiopathology ; Pain treatment ; Phantom limb ; Phantom Limb - complications ; Phantom Limb - diagnostic imaging ; Phantom Limb - physiopathology ; Phantom limb pain ; Preserved function ; Somatosensory Cortex - diagnostic imaging ; Somatosensory Cortex - physiopathology ; Spinal cord ; Topography ; Use-dependent plasticity</subject><ispartof>NeuroImage (Orlando, Fla.), 2020-09, Vol.218, p.116943-116943, Article 116943</ispartof><rights>2020 The Author(s)</rights><rights>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><rights>2020. The Author(s)</rights><rights>2020 The Author(s) 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c573t-74c9cc5a841b66edf11ab9e43cf1cfdcdcde4347fb2e928ffef95c610d5c1f003</citedby><cites>FETCH-LOGICAL-c573t-74c9cc5a841b66edf11ab9e43cf1cfdcdcde4347fb2e928ffef95c610d5c1f003</cites><orcidid>0000-0002-5816-8979</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32428706$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Makin, Tamar R.</creatorcontrib><creatorcontrib>Flor, Herta</creatorcontrib><title>Brain (re)organisation following amputation: Implications for phantom limb pain</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>Following arm amputation the region that represented the missing hand in primary somatosensory cortex (S1) becomes deprived of its primary input, resulting in changed boundaries of the S1 body map. This remapping process has been termed ‘reorganisation’ and has been attributed to multiple mechanisms, including increased expression of previously masked inputs. In a maladaptive plasticity model, such reorganisation has been associated with phantom limb pain (PLP). Brain activity associated with phantom hand movements is also correlated with PLP, suggesting that preserved limb functional representation may serve as a complementary process. Here we review some of the most recent evidence for the potential drivers and consequences of brain (re)organisation following amputation, based on human neuroimaging. We emphasise other perceptual and behavioural factors consequential to arm amputation, such as non-painful phantom sensations, perceived limb ownership, intact hand compensatory behaviour or prosthesis use, which have also been related to both cortical changes and PLP. We also discuss new findings based on interventions designed to alter the brain representation of the phantom limb, including augmented/virtual reality applications and brain computer interfaces. These studies point to a close interaction of sensory changes and alterations in brain regions involved in body representation, pain processing and motor control. Finally, we review recent evidence based on methodological advances such as high field neuroimaging and multivariate techniques that provide new opportunities to interrogate somatosensory representations in the missing hand cortical territory. Collectively, this research highlights the need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP.
•Technological advancements provide new insight into the neural basis of phantom pain.•Traditional mechanistic accounts of remapping in somatosensory cortex are incomplete.•Related contextual factors such as adaptive behaviour will contribute to brain plasticity.•A broader mechanistic focus beyond primary sensorimotor cortex is needed.•Plasticity and stability of the sensorimotor body maps may vary across time scales.</description><subject>Adult</subject><subject>Amputation</subject><subject>Amputation, Surgical</subject><subject>Amputees</subject><subject>Arm</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - physiopathology</subject><subject>Brain Mapping</subject><subject>Brain research</subject><subject>Computer applications</subject><subject>Cortex (somatosensory)</subject><subject>Cortical reorganisation</subject><subject>Female</subject><subject>Hand</subject><subject>Humans</subject><subject>Interfaces</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Middle Aged</subject><subject>Motor task performance</subject><subject>Multivariate analysis</subject><subject>Neuroimaging</subject><subject>Pain</subject><subject>Pain - diagnostic imaging</subject><subject>Pain - etiology</subject><subject>Pain - physiopathology</subject><subject>Pain treatment</subject><subject>Phantom limb</subject><subject>Phantom Limb - complications</subject><subject>Phantom Limb - diagnostic imaging</subject><subject>Phantom Limb - physiopathology</subject><subject>Phantom limb pain</subject><subject>Preserved function</subject><subject>Somatosensory Cortex - diagnostic imaging</subject><subject>Somatosensory Cortex - physiopathology</subject><subject>Spinal cord</subject><subject>Topography</subject><subject>Use-dependent plasticity</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqFkk1v1DAQhiMEoqXwF1AkLuWwi-3Ysc0Bqa34WKlSL3C2nMl461ViBzsp4t_j3S2FckE-2DN-5rXno6pqStaU0Pbdbh1wSdGPdotrRlhx01bz5kl1SokWKy0ke7o_i2alKNUn1Yucd4QQTbl6Xp00jDMlSXta3Vwm60N9nvBtTFsbfLazj6F2cRjiDx-2tR2nZT4439ebcRo8HIxckFRPtzbMcawHP3b1VJReVs-cHTK-ut_Pqm-fPn69-rK6vvm8ubq4XoGQzbySHDSAsIrTrm2xd5TaTiNvwFFwPZRVDC5dx1Az5Rw6LaClpBdAHSHNWbU56vbR7syUSinSTxOtNwdHycXYNHsY0IAkXEoHhErBuePa8U4oZlslUGvoi9aHo9a0dCP2gGFOdngk-vgm-FuzjXdGcsZUw4rA-b1Ait8XzLMZfQYcBhswLtkwXhpBWENVQd_8g-7ikkIpVaGYJlxLJQqljhSkmHNC9_AZSsx-AszO_JkAs58Ac5yAEvr672QeAn-3vACXRwBLe-48JpPBYwDsfUKYS_38_1_5Bex4yOM</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Makin, Tamar R.</creator><creator>Flor, Herta</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><general>Academic Press</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</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>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-5816-8979</orcidid></search><sort><creationdate>202009</creationdate><title>Brain (re)organisation following amputation: Implications for phantom limb pain</title><author>Makin, Tamar R. ; Flor, Herta</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c573t-74c9cc5a841b66edf11ab9e43cf1cfdcdcde4347fb2e928ffef95c610d5c1f003</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Amputation</topic><topic>Amputation, Surgical</topic><topic>Amputees</topic><topic>Arm</topic><topic>Brain - diagnostic imaging</topic><topic>Brain - physiopathology</topic><topic>Brain Mapping</topic><topic>Brain research</topic><topic>Computer applications</topic><topic>Cortex (somatosensory)</topic><topic>Cortical reorganisation</topic><topic>Female</topic><topic>Hand</topic><topic>Humans</topic><topic>Interfaces</topic><topic>Male</topic><topic>Medical imaging</topic><topic>Middle Aged</topic><topic>Motor task performance</topic><topic>Multivariate analysis</topic><topic>Neuroimaging</topic><topic>Pain</topic><topic>Pain - diagnostic imaging</topic><topic>Pain - etiology</topic><topic>Pain - physiopathology</topic><topic>Pain treatment</topic><topic>Phantom limb</topic><topic>Phantom Limb - complications</topic><topic>Phantom Limb - diagnostic imaging</topic><topic>Phantom Limb - physiopathology</topic><topic>Phantom limb pain</topic><topic>Preserved function</topic><topic>Somatosensory Cortex - diagnostic imaging</topic><topic>Somatosensory Cortex - physiopathology</topic><topic>Spinal cord</topic><topic>Topography</topic><topic>Use-dependent plasticity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Makin, Tamar R.</creatorcontrib><creatorcontrib>Flor, Herta</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</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)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</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>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Open Access: DOAJ - Directory of Open Access Journals</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Makin, Tamar R.</au><au>Flor, Herta</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brain (re)organisation following amputation: Implications for phantom limb pain</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2020-09</date><risdate>2020</risdate><volume>218</volume><spage>116943</spage><epage>116943</epage><pages>116943-116943</pages><artnum>116943</artnum><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>Following arm amputation the region that represented the missing hand in primary somatosensory cortex (S1) becomes deprived of its primary input, resulting in changed boundaries of the S1 body map. This remapping process has been termed ‘reorganisation’ and has been attributed to multiple mechanisms, including increased expression of previously masked inputs. In a maladaptive plasticity model, such reorganisation has been associated with phantom limb pain (PLP). Brain activity associated with phantom hand movements is also correlated with PLP, suggesting that preserved limb functional representation may serve as a complementary process. Here we review some of the most recent evidence for the potential drivers and consequences of brain (re)organisation following amputation, based on human neuroimaging. We emphasise other perceptual and behavioural factors consequential to arm amputation, such as non-painful phantom sensations, perceived limb ownership, intact hand compensatory behaviour or prosthesis use, which have also been related to both cortical changes and PLP. We also discuss new findings based on interventions designed to alter the brain representation of the phantom limb, including augmented/virtual reality applications and brain computer interfaces. These studies point to a close interaction of sensory changes and alterations in brain regions involved in body representation, pain processing and motor control. Finally, we review recent evidence based on methodological advances such as high field neuroimaging and multivariate techniques that provide new opportunities to interrogate somatosensory representations in the missing hand cortical territory. Collectively, this research highlights the need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP.
•Technological advancements provide new insight into the neural basis of phantom pain.•Traditional mechanistic accounts of remapping in somatosensory cortex are incomplete.•Related contextual factors such as adaptive behaviour will contribute to brain plasticity.•A broader mechanistic focus beyond primary sensorimotor cortex is needed.•Plasticity and stability of the sensorimotor body maps may vary across time scales.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>32428706</pmid><doi>10.1016/j.neuroimage.2020.116943</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-5816-8979</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Amputation Amputation, Surgical Amputees Arm Brain - diagnostic imaging Brain - physiopathology Brain Mapping Brain research Computer applications Cortex (somatosensory) Cortical reorganisation Female Hand Humans Interfaces Male Medical imaging Middle Aged Motor task performance Multivariate analysis Neuroimaging Pain Pain - diagnostic imaging Pain - etiology Pain - physiopathology Pain treatment Phantom limb Phantom Limb - complications Phantom Limb - diagnostic imaging Phantom Limb - physiopathology Phantom limb pain Preserved function Somatosensory Cortex - diagnostic imaging Somatosensory Cortex - physiopathology Spinal cord Topography Use-dependent plasticity |
title | Brain (re)organisation following amputation: Implications for phantom limb pain |
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