Preservation of hand movement representation in the sensorimotor areas of amputees
Denervation due to amputation is known to induce cortical reorganization in the sensorimotor cortex. Although there is evidence that reorganization does not lead to a complete loss of the representation of the phantom limb, it is unclear to what extent detailed, finger-specific activation patterns a...
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Veröffentlicht in: | Brain (London, England : 1878) England : 1878), 2017-12, Vol.140 (12), p.3166-3178 |
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description | Denervation due to amputation is known to induce cortical reorganization in the sensorimotor cortex. Although there is evidence that reorganization does not lead to a complete loss of the representation of the phantom limb, it is unclear to what extent detailed, finger-specific activation patterns are preserved in motor cortex, an issue that is also relevant for development of brain-computer interface solutions for paralysed people. We applied machine learning to obtain a quantitative measure for the functional organization within the motor and adjacent cortices in amputees, using high resolution functional MRI and attempted hand gestures. Subjects with above-elbow arm amputation (n = 8) and non-amputated controls (n = 9) made several gestures with either their right or left hand. Amputees attempted to make gestures with their amputated hand. Images were acquired using 7 T functional MRI. The sensorimotor cortex was divided into four regions, and activity patterns were classified in individual subjects using a support vector machine. Classification scores were significantly above chance for all subjects and all hands, and were highly similar between amputees and controls in most regions. Decodability of phantom movements from primary motor cortex reached the levels of right hand movements in controls. Attempted movements were successfully decoded from primary sensory cortex in amputees, albeit lower than in controls but well above chance level despite absence of somatosensory feedback. There was no significant correlation between decodability and years since amputation, or age. The ability to decode attempted gestures demonstrates that the detailed hand representation is preserved in motor cortex and adjacent regions after denervation. This encourages targeting sensorimotor activity patterns for development of brain-computer interfaces. |
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Although there is evidence that reorganization does not lead to a complete loss of the representation of the phantom limb, it is unclear to what extent detailed, finger-specific activation patterns are preserved in motor cortex, an issue that is also relevant for development of brain-computer interface solutions for paralysed people. We applied machine learning to obtain a quantitative measure for the functional organization within the motor and adjacent cortices in amputees, using high resolution functional MRI and attempted hand gestures. Subjects with above-elbow arm amputation (n = 8) and non-amputated controls (n = 9) made several gestures with either their right or left hand. Amputees attempted to make gestures with their amputated hand. Images were acquired using 7 T functional MRI. The sensorimotor cortex was divided into four regions, and activity patterns were classified in individual subjects using a support vector machine. Classification scores were significantly above chance for all subjects and all hands, and were highly similar between amputees and controls in most regions. Decodability of phantom movements from primary motor cortex reached the levels of right hand movements in controls. Attempted movements were successfully decoded from primary sensory cortex in amputees, albeit lower than in controls but well above chance level despite absence of somatosensory feedback. There was no significant correlation between decodability and years since amputation, or age. The ability to decode attempted gestures demonstrates that the detailed hand representation is preserved in motor cortex and adjacent regions after denervation. This encourages targeting sensorimotor activity patterns for development of brain-computer interfaces.</description><identifier>ISSN: 0006-8950</identifier><identifier>EISSN: 1460-2156</identifier><identifier>DOI: 10.1093/brain/awx274</identifier><identifier>PMID: 29088322</identifier><language>eng</language><publisher>England</publisher><subject>Adult ; Aged ; Amputation ; Case-Control Studies ; Female ; Forearm ; Functional Neuroimaging ; Hand ; Humans ; Machine Learning ; Magnetic Resonance Imaging ; Male ; Middle Aged ; Motor Cortex - physiopathology ; Phantom Limb - physiopathology ; Sensorimotor Cortex - physiopathology ; Time Factors ; Young Adult</subject><ispartof>Brain (London, England : 1878), 2017-12, Vol.140 (12), p.3166-3178</ispartof><rights>The Author (2017). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c384t-5a8579c0839399f10581563ea5d61b268d3ad1e066ba09b72745f19742d8413f3</citedby><cites>FETCH-LOGICAL-c384t-5a8579c0839399f10581563ea5d61b268d3ad1e066ba09b72745f19742d8413f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29088322$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bruurmijn, Mark L C M</creatorcontrib><creatorcontrib>Pereboom, Isabelle P L</creatorcontrib><creatorcontrib>Vansteensel, Mariska J</creatorcontrib><creatorcontrib>Raemaekers, Mathijs A H</creatorcontrib><creatorcontrib>Ramsey, Nick F</creatorcontrib><title>Preservation of hand movement representation in the sensorimotor areas of amputees</title><title>Brain (London, England : 1878)</title><addtitle>Brain</addtitle><description>Denervation due to amputation is known to induce cortical reorganization in the sensorimotor cortex. Although there is evidence that reorganization does not lead to a complete loss of the representation of the phantom limb, it is unclear to what extent detailed, finger-specific activation patterns are preserved in motor cortex, an issue that is also relevant for development of brain-computer interface solutions for paralysed people. We applied machine learning to obtain a quantitative measure for the functional organization within the motor and adjacent cortices in amputees, using high resolution functional MRI and attempted hand gestures. Subjects with above-elbow arm amputation (n = 8) and non-amputated controls (n = 9) made several gestures with either their right or left hand. Amputees attempted to make gestures with their amputated hand. Images were acquired using 7 T functional MRI. The sensorimotor cortex was divided into four regions, and activity patterns were classified in individual subjects using a support vector machine. Classification scores were significantly above chance for all subjects and all hands, and were highly similar between amputees and controls in most regions. Decodability of phantom movements from primary motor cortex reached the levels of right hand movements in controls. Attempted movements were successfully decoded from primary sensory cortex in amputees, albeit lower than in controls but well above chance level despite absence of somatosensory feedback. There was no significant correlation between decodability and years since amputation, or age. The ability to decode attempted gestures demonstrates that the detailed hand representation is preserved in motor cortex and adjacent regions after denervation. This encourages targeting sensorimotor activity patterns for development of brain-computer interfaces.</description><subject>Adult</subject><subject>Aged</subject><subject>Amputation</subject><subject>Case-Control Studies</subject><subject>Female</subject><subject>Forearm</subject><subject>Functional Neuroimaging</subject><subject>Hand</subject><subject>Humans</subject><subject>Machine Learning</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Motor Cortex - physiopathology</subject><subject>Phantom Limb - physiopathology</subject><subject>Sensorimotor Cortex - physiopathology</subject><subject>Time Factors</subject><subject>Young Adult</subject><issn>0006-8950</issn><issn>1460-2156</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUU1LxDAQDaK46-rNs_TowbqZpkmTiyCLX7CgiJ5D2k7dStvUpF3139u1uuhpYN6bN2_mEXIM9ByoYvPUmbKZm_ePKIl3yBRiQcMIuNglU0qpCKXidEIOvH-lFGIWiX0yiRSVkkXRlDw-OPTo1qYrbRPYIliZJg9qu8Yamy5w2G7wphvxsgm6FQZDw1tX1razLjAOjd9MmrrtO0R_SPYKU3k8-qkz8nx99bS4DZf3N3eLy2WYMRl3ITeSJyqjkimmVAGUy8E1Q8NzAWkkZM5MDkiFSA1VaTKcxwtQSRzlMgZWsBm5GHXbPq0xzwaXzlS6HYwZ96mtKfV_pClX-sWutYgBgIlB4PRHwNm3Hn2n69JnWFWmQdt7DYpLHjMAOVDPRmrmrPcOi-0aoHoTg_6OQY8xDPSTv9a25N-_sy-_fYaa</recordid><startdate>20171201</startdate><enddate>20171201</enddate><creator>Bruurmijn, Mark L C M</creator><creator>Pereboom, Isabelle P L</creator><creator>Vansteensel, Mariska J</creator><creator>Raemaekers, Mathijs A H</creator><creator>Ramsey, Nick F</creator><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>5PM</scope></search><sort><creationdate>20171201</creationdate><title>Preservation of hand movement representation in the sensorimotor areas of amputees</title><author>Bruurmijn, Mark L C M ; Pereboom, Isabelle P L ; Vansteensel, Mariska J ; Raemaekers, Mathijs A H ; Ramsey, Nick F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c384t-5a8579c0839399f10581563ea5d61b268d3ad1e066ba09b72745f19742d8413f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Amputation</topic><topic>Case-Control Studies</topic><topic>Female</topic><topic>Forearm</topic><topic>Functional Neuroimaging</topic><topic>Hand</topic><topic>Humans</topic><topic>Machine Learning</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Motor Cortex - physiopathology</topic><topic>Phantom Limb - physiopathology</topic><topic>Sensorimotor Cortex - physiopathology</topic><topic>Time Factors</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bruurmijn, Mark L C M</creatorcontrib><creatorcontrib>Pereboom, Isabelle P L</creatorcontrib><creatorcontrib>Vansteensel, Mariska J</creatorcontrib><creatorcontrib>Raemaekers, Mathijs A H</creatorcontrib><creatorcontrib>Ramsey, Nick F</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Brain (London, England : 1878)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bruurmijn, Mark L C M</au><au>Pereboom, Isabelle P L</au><au>Vansteensel, Mariska J</au><au>Raemaekers, Mathijs A H</au><au>Ramsey, Nick F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Preservation of hand movement representation in the sensorimotor areas of amputees</atitle><jtitle>Brain (London, England : 1878)</jtitle><addtitle>Brain</addtitle><date>2017-12-01</date><risdate>2017</risdate><volume>140</volume><issue>12</issue><spage>3166</spage><epage>3178</epage><pages>3166-3178</pages><issn>0006-8950</issn><eissn>1460-2156</eissn><abstract>Denervation due to amputation is known to induce cortical reorganization in the sensorimotor cortex. Although there is evidence that reorganization does not lead to a complete loss of the representation of the phantom limb, it is unclear to what extent detailed, finger-specific activation patterns are preserved in motor cortex, an issue that is also relevant for development of brain-computer interface solutions for paralysed people. We applied machine learning to obtain a quantitative measure for the functional organization within the motor and adjacent cortices in amputees, using high resolution functional MRI and attempted hand gestures. Subjects with above-elbow arm amputation (n = 8) and non-amputated controls (n = 9) made several gestures with either their right or left hand. Amputees attempted to make gestures with their amputated hand. Images were acquired using 7 T functional MRI. The sensorimotor cortex was divided into four regions, and activity patterns were classified in individual subjects using a support vector machine. Classification scores were significantly above chance for all subjects and all hands, and were highly similar between amputees and controls in most regions. Decodability of phantom movements from primary motor cortex reached the levels of right hand movements in controls. Attempted movements were successfully decoded from primary sensory cortex in amputees, albeit lower than in controls but well above chance level despite absence of somatosensory feedback. There was no significant correlation between decodability and years since amputation, or age. The ability to decode attempted gestures demonstrates that the detailed hand representation is preserved in motor cortex and adjacent regions after denervation. This encourages targeting sensorimotor activity patterns for development of brain-computer interfaces.</abstract><cop>England</cop><pmid>29088322</pmid><doi>10.1093/brain/awx274</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adult Aged Amputation Case-Control Studies Female Forearm Functional Neuroimaging Hand Humans Machine Learning Magnetic Resonance Imaging Male Middle Aged Motor Cortex - physiopathology Phantom Limb - physiopathology Sensorimotor Cortex - physiopathology Time Factors Young Adult |
title | Preservation of hand movement representation in the sensorimotor areas of amputees |
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