Motor hyperactivation during cognitive tasks: An endophenotype of juvenile myoclonic epilepsy
Objective Juvenile myoclonic epilepsy (JME) is the most common genetic generalized epilepsy syndrome. Myoclonus may relate to motor system hyperexcitability and can be provoked by cognitive activities. To aid genetic mapping in complex neuropsychiatric disorders, recent research has utilized imaging...
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| Veröffentlicht in: | Epilepsia (Copenhagen) 2020-07, Vol.61 (7), p.1438-1452 |
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| creator | Caciagli, Lorenzo Wandschneider, Britta Centeno, Maria Vollmar, Christian Vos, Sjoerd B. Trimmel, Karin Long, Lili Xiao, Fenglai Lowe, Alexander J. Sidhu, Meneka K. Thompson, Pamela J. Winston, Gavin P. Duncan, John S. Koepp, Matthias J. |
| description | Objective
Juvenile myoclonic epilepsy (JME) is the most common genetic generalized epilepsy syndrome. Myoclonus may relate to motor system hyperexcitability and can be provoked by cognitive activities. To aid genetic mapping in complex neuropsychiatric disorders, recent research has utilized imaging intermediate phenotypes (endophenotypes). Here, we aimed to (a) characterize activation profiles of the motor system during different cognitive tasks in patients with JME and their unaffected siblings, and (b) validate those as endophenotypes of JME.
Methods
This prospective cross‐sectional investigation included 32 patients with JME, 12 unaffected siblings, and 26 controls, comparable for age, sex, handedness, language laterality, neuropsychological performance, and anxiety and depression scores. We investigated patterns of motor system activation during episodic memory encoding and verb generation functional magnetic resonance imaging (fMRI) tasks.
Results
During both tasks, patients and unaffected siblings showed increased activation of motor system areas compared to controls. Effects were more prominent during memory encoding, which entailed hand motion via joystick responses. Subgroup analyses identified stronger activation of the motor cortex in JME patients with ongoing seizures compared to seizure‐free patients. Receiver‐operating characteristic curves, based on measures of motor activation, accurately discriminated both patients with JME and their siblings from healthy controls (area under the curve: 0.75 and 0.77, for JME and a combined patient‐sibling group against controls, respectively; P |
| doi_str_mv | 10.1111/epi.16575 |
| format | Article |
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Juvenile myoclonic epilepsy (JME) is the most common genetic generalized epilepsy syndrome. Myoclonus may relate to motor system hyperexcitability and can be provoked by cognitive activities. To aid genetic mapping in complex neuropsychiatric disorders, recent research has utilized imaging intermediate phenotypes (endophenotypes). Here, we aimed to (a) characterize activation profiles of the motor system during different cognitive tasks in patients with JME and their unaffected siblings, and (b) validate those as endophenotypes of JME.
Methods
This prospective cross‐sectional investigation included 32 patients with JME, 12 unaffected siblings, and 26 controls, comparable for age, sex, handedness, language laterality, neuropsychological performance, and anxiety and depression scores. We investigated patterns of motor system activation during episodic memory encoding and verb generation functional magnetic resonance imaging (fMRI) tasks.
Results
During both tasks, patients and unaffected siblings showed increased activation of motor system areas compared to controls. Effects were more prominent during memory encoding, which entailed hand motion via joystick responses. Subgroup analyses identified stronger activation of the motor cortex in JME patients with ongoing seizures compared to seizure‐free patients. Receiver‐operating characteristic curves, based on measures of motor activation, accurately discriminated both patients with JME and their siblings from healthy controls (area under the curve: 0.75 and 0.77, for JME and a combined patient‐sibling group against controls, respectively; P < .005).
Significance
Motor system hyperactivation represents a cognitive, domain‐independent endophenotype of JME. We propose measures of motor system activation as quantitative traits for future genetic imaging studies in this syndrome.</description><identifier>ISSN: 0013-9580</identifier><identifier>EISSN: 1528-1167</identifier><identifier>DOI: 10.1111/epi.16575</identifier><identifier>PMID: 32584424</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Adolescent ; Adult ; cognition ; Cognition - physiology ; Cognitive ability ; Cortex (motor) ; Cross-Sectional Studies ; endophenotype ; Endophenotypes ; Epilepsy ; Female ; fMRI ; Full Length Original Research Paper ; Full‐length Original Research ; Functional magnetic resonance imaging ; Gene mapping ; Handedness ; Humans ; Hyperkinesis - diagnostic imaging ; Hyperkinesis - physiopathology ; Hyperkinesis - psychology ; juvenile myoclonic epilepsy ; Male ; Memory ; Mental disorders ; Middle Aged ; motor system ; Myoclonic Epilepsy, Juvenile - diagnostic imaging ; Myoclonic Epilepsy, Juvenile - physiopathology ; Myoclonic Epilepsy, Juvenile - psychology ; Myoclonus ; Neuroimaging ; Phenotypes ; Prospective Studies ; Psychomotor Performance - physiology ; Seizures ; Siblings ; Young Adult</subject><ispartof>Epilepsia (Copenhagen), 2020-07, Vol.61 (7), p.1438-1452</ispartof><rights>2020 The Authors. published by Wiley Periodicals LLC on behalf of International League Against Epilepsy</rights><rights>2020 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.</rights><rights>2020. This article 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>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4435-fa637c74e2abc95f71d4630495afeed8764b152f63b3896a69eb54171f2f14f83</citedby><cites>FETCH-LOGICAL-c4435-fa637c74e2abc95f71d4630495afeed8764b152f63b3896a69eb54171f2f14f83</cites><orcidid>0000-0002-8502-4487 ; 0000-0002-4277-8000 ; 0000-0002-1373-0681 ; 0000-0001-7189-9699 ; 0000-0003-1308-6539 ; 0000-0002-4630-7484 ; 0000-0003-4801-4535 ; 0000-0001-7181-2637 ; 0000-0003-3267-9348 ; 0000-0001-9395-1478 ; 0000-0002-9203-5344 ; 0000-0001-5078-8770</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fepi.16575$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fepi.16575$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32584424$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Caciagli, Lorenzo</creatorcontrib><creatorcontrib>Wandschneider, Britta</creatorcontrib><creatorcontrib>Centeno, Maria</creatorcontrib><creatorcontrib>Vollmar, Christian</creatorcontrib><creatorcontrib>Vos, Sjoerd B.</creatorcontrib><creatorcontrib>Trimmel, Karin</creatorcontrib><creatorcontrib>Long, Lili</creatorcontrib><creatorcontrib>Xiao, Fenglai</creatorcontrib><creatorcontrib>Lowe, Alexander J.</creatorcontrib><creatorcontrib>Sidhu, Meneka K.</creatorcontrib><creatorcontrib>Thompson, Pamela J.</creatorcontrib><creatorcontrib>Winston, Gavin P.</creatorcontrib><creatorcontrib>Duncan, John S.</creatorcontrib><creatorcontrib>Koepp, Matthias J.</creatorcontrib><title>Motor hyperactivation during cognitive tasks: An endophenotype of juvenile myoclonic epilepsy</title><title>Epilepsia (Copenhagen)</title><addtitle>Epilepsia</addtitle><description>Objective
Juvenile myoclonic epilepsy (JME) is the most common genetic generalized epilepsy syndrome. Myoclonus may relate to motor system hyperexcitability and can be provoked by cognitive activities. To aid genetic mapping in complex neuropsychiatric disorders, recent research has utilized imaging intermediate phenotypes (endophenotypes). Here, we aimed to (a) characterize activation profiles of the motor system during different cognitive tasks in patients with JME and their unaffected siblings, and (b) validate those as endophenotypes of JME.
Methods
This prospective cross‐sectional investigation included 32 patients with JME, 12 unaffected siblings, and 26 controls, comparable for age, sex, handedness, language laterality, neuropsychological performance, and anxiety and depression scores. We investigated patterns of motor system activation during episodic memory encoding and verb generation functional magnetic resonance imaging (fMRI) tasks.
Results
During both tasks, patients and unaffected siblings showed increased activation of motor system areas compared to controls. Effects were more prominent during memory encoding, which entailed hand motion via joystick responses. Subgroup analyses identified stronger activation of the motor cortex in JME patients with ongoing seizures compared to seizure‐free patients. Receiver‐operating characteristic curves, based on measures of motor activation, accurately discriminated both patients with JME and their siblings from healthy controls (area under the curve: 0.75 and 0.77, for JME and a combined patient‐sibling group against controls, respectively; P < .005).
Significance
Motor system hyperactivation represents a cognitive, domain‐independent endophenotype of JME. We propose measures of motor system activation as quantitative traits for future genetic imaging studies in this syndrome.</description><subject>Adolescent</subject><subject>Adult</subject><subject>cognition</subject><subject>Cognition - physiology</subject><subject>Cognitive ability</subject><subject>Cortex (motor)</subject><subject>Cross-Sectional Studies</subject><subject>endophenotype</subject><subject>Endophenotypes</subject><subject>Epilepsy</subject><subject>Female</subject><subject>fMRI</subject><subject>Full Length Original Research Paper</subject><subject>Full‐length Original Research</subject><subject>Functional magnetic resonance imaging</subject><subject>Gene mapping</subject><subject>Handedness</subject><subject>Humans</subject><subject>Hyperkinesis - diagnostic imaging</subject><subject>Hyperkinesis - physiopathology</subject><subject>Hyperkinesis - psychology</subject><subject>juvenile myoclonic epilepsy</subject><subject>Male</subject><subject>Memory</subject><subject>Mental disorders</subject><subject>Middle Aged</subject><subject>motor system</subject><subject>Myoclonic Epilepsy, Juvenile - diagnostic imaging</subject><subject>Myoclonic Epilepsy, Juvenile - physiopathology</subject><subject>Myoclonic Epilepsy, Juvenile - psychology</subject><subject>Myoclonus</subject><subject>Neuroimaging</subject><subject>Phenotypes</subject><subject>Prospective Studies</subject><subject>Psychomotor Performance - physiology</subject><subject>Seizures</subject><subject>Siblings</subject><subject>Young Adult</subject><issn>0013-9580</issn><issn>1528-1167</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kU-LFDEQxYMo7rh68AtIwIseejfp_G0PwrKsurCiBz1KSGcqMxl7kjbpHulvb3TWRQVzKUh-9fKqHkJPKTmj9ZzDGM6oFErcQysqWt1QKtV9tCKEsqYTmpygR6XsCCFKKvYQnbBWaM5bvkJf3qcpZbxdRsjWTeFgp5AiXs85xA12aRNDvQQ82fK1vMIXEUNcp3ELMU21ByePd_MBYhgA75fkhhSDw9XQAGNZHqMH3g4FntzWU_T5zdWny3fNzYe315cXN43jnInGW8mUUxxa27tOeEXXXDLCO2E9wForyfs6l5esZ7qTVnbQC04V9a2n3Gt2il4fdce538PaQZyyHcyYw97mxSQbzN8vMWzNJh2Mkpq2oq0CL24Fcvo2Q5nMPhQHw2AjpLmYtv7GOs0Fq-jzf9BdmnOs41WqlUpozUilXh4pl1MpGfydGUrMz9BM3ZH5FVpln_3p_o78nVIFzo_A97rW5f9K5urj9VHyB5WHoug</recordid><startdate>202007</startdate><enddate>202007</enddate><creator>Caciagli, Lorenzo</creator><creator>Wandschneider, Britta</creator><creator>Centeno, Maria</creator><creator>Vollmar, Christian</creator><creator>Vos, Sjoerd B.</creator><creator>Trimmel, Karin</creator><creator>Long, Lili</creator><creator>Xiao, Fenglai</creator><creator>Lowe, Alexander J.</creator><creator>Sidhu, Meneka K.</creator><creator>Thompson, Pamela J.</creator><creator>Winston, Gavin P.</creator><creator>Duncan, John S.</creator><creator>Koepp, Matthias J.</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>7TK</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8502-4487</orcidid><orcidid>https://orcid.org/0000-0002-4277-8000</orcidid><orcidid>https://orcid.org/0000-0002-1373-0681</orcidid><orcidid>https://orcid.org/0000-0001-7189-9699</orcidid><orcidid>https://orcid.org/0000-0003-1308-6539</orcidid><orcidid>https://orcid.org/0000-0002-4630-7484</orcidid><orcidid>https://orcid.org/0000-0003-4801-4535</orcidid><orcidid>https://orcid.org/0000-0001-7181-2637</orcidid><orcidid>https://orcid.org/0000-0003-3267-9348</orcidid><orcidid>https://orcid.org/0000-0001-9395-1478</orcidid><orcidid>https://orcid.org/0000-0002-9203-5344</orcidid><orcidid>https://orcid.org/0000-0001-5078-8770</orcidid></search><sort><creationdate>202007</creationdate><title>Motor hyperactivation during cognitive tasks: An endophenotype of juvenile myoclonic epilepsy</title><author>Caciagli, Lorenzo ; Wandschneider, Britta ; Centeno, Maria ; Vollmar, Christian ; Vos, Sjoerd B. ; Trimmel, Karin ; Long, Lili ; Xiao, Fenglai ; Lowe, Alexander J. ; Sidhu, Meneka K. ; Thompson, Pamela J. ; Winston, Gavin P. ; Duncan, John S. ; Koepp, Matthias J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4435-fa637c74e2abc95f71d4630495afeed8764b152f63b3896a69eb54171f2f14f83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>cognition</topic><topic>Cognition - physiology</topic><topic>Cognitive ability</topic><topic>Cortex (motor)</topic><topic>Cross-Sectional Studies</topic><topic>endophenotype</topic><topic>Endophenotypes</topic><topic>Epilepsy</topic><topic>Female</topic><topic>fMRI</topic><topic>Full Length Original Research Paper</topic><topic>Full‐length Original Research</topic><topic>Functional magnetic resonance imaging</topic><topic>Gene mapping</topic><topic>Handedness</topic><topic>Humans</topic><topic>Hyperkinesis - diagnostic imaging</topic><topic>Hyperkinesis - physiopathology</topic><topic>Hyperkinesis - psychology</topic><topic>juvenile myoclonic epilepsy</topic><topic>Male</topic><topic>Memory</topic><topic>Mental disorders</topic><topic>Middle Aged</topic><topic>motor system</topic><topic>Myoclonic Epilepsy, Juvenile - diagnostic imaging</topic><topic>Myoclonic Epilepsy, Juvenile - physiopathology</topic><topic>Myoclonic Epilepsy, Juvenile - psychology</topic><topic>Myoclonus</topic><topic>Neuroimaging</topic><topic>Phenotypes</topic><topic>Prospective Studies</topic><topic>Psychomotor Performance - physiology</topic><topic>Seizures</topic><topic>Siblings</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Caciagli, Lorenzo</creatorcontrib><creatorcontrib>Wandschneider, Britta</creatorcontrib><creatorcontrib>Centeno, Maria</creatorcontrib><creatorcontrib>Vollmar, Christian</creatorcontrib><creatorcontrib>Vos, Sjoerd B.</creatorcontrib><creatorcontrib>Trimmel, Karin</creatorcontrib><creatorcontrib>Long, Lili</creatorcontrib><creatorcontrib>Xiao, Fenglai</creatorcontrib><creatorcontrib>Lowe, Alexander J.</creatorcontrib><creatorcontrib>Sidhu, Meneka K.</creatorcontrib><creatorcontrib>Thompson, Pamela J.</creatorcontrib><creatorcontrib>Winston, Gavin P.</creatorcontrib><creatorcontrib>Duncan, John S.</creatorcontrib><creatorcontrib>Koepp, Matthias J.</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Epilepsia (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Caciagli, Lorenzo</au><au>Wandschneider, Britta</au><au>Centeno, Maria</au><au>Vollmar, Christian</au><au>Vos, Sjoerd B.</au><au>Trimmel, Karin</au><au>Long, Lili</au><au>Xiao, Fenglai</au><au>Lowe, Alexander J.</au><au>Sidhu, Meneka K.</au><au>Thompson, Pamela J.</au><au>Winston, Gavin P.</au><au>Duncan, John S.</au><au>Koepp, Matthias J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Motor hyperactivation during cognitive tasks: An endophenotype of juvenile myoclonic epilepsy</atitle><jtitle>Epilepsia (Copenhagen)</jtitle><addtitle>Epilepsia</addtitle><date>2020-07</date><risdate>2020</risdate><volume>61</volume><issue>7</issue><spage>1438</spage><epage>1452</epage><pages>1438-1452</pages><issn>0013-9580</issn><eissn>1528-1167</eissn><abstract>Objective
Juvenile myoclonic epilepsy (JME) is the most common genetic generalized epilepsy syndrome. Myoclonus may relate to motor system hyperexcitability and can be provoked by cognitive activities. To aid genetic mapping in complex neuropsychiatric disorders, recent research has utilized imaging intermediate phenotypes (endophenotypes). Here, we aimed to (a) characterize activation profiles of the motor system during different cognitive tasks in patients with JME and their unaffected siblings, and (b) validate those as endophenotypes of JME.
Methods
This prospective cross‐sectional investigation included 32 patients with JME, 12 unaffected siblings, and 26 controls, comparable for age, sex, handedness, language laterality, neuropsychological performance, and anxiety and depression scores. We investigated patterns of motor system activation during episodic memory encoding and verb generation functional magnetic resonance imaging (fMRI) tasks.
Results
During both tasks, patients and unaffected siblings showed increased activation of motor system areas compared to controls. Effects were more prominent during memory encoding, which entailed hand motion via joystick responses. Subgroup analyses identified stronger activation of the motor cortex in JME patients with ongoing seizures compared to seizure‐free patients. Receiver‐operating characteristic curves, based on measures of motor activation, accurately discriminated both patients with JME and their siblings from healthy controls (area under the curve: 0.75 and 0.77, for JME and a combined patient‐sibling group against controls, respectively; P < .005).
Significance
Motor system hyperactivation represents a cognitive, domain‐independent endophenotype of JME. We propose measures of motor system activation as quantitative traits for future genetic imaging studies in this syndrome.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>32584424</pmid><doi>10.1111/epi.16575</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-8502-4487</orcidid><orcidid>https://orcid.org/0000-0002-4277-8000</orcidid><orcidid>https://orcid.org/0000-0002-1373-0681</orcidid><orcidid>https://orcid.org/0000-0001-7189-9699</orcidid><orcidid>https://orcid.org/0000-0003-1308-6539</orcidid><orcidid>https://orcid.org/0000-0002-4630-7484</orcidid><orcidid>https://orcid.org/0000-0003-4801-4535</orcidid><orcidid>https://orcid.org/0000-0001-7181-2637</orcidid><orcidid>https://orcid.org/0000-0003-3267-9348</orcidid><orcidid>https://orcid.org/0000-0001-9395-1478</orcidid><orcidid>https://orcid.org/0000-0002-9203-5344</orcidid><orcidid>https://orcid.org/0000-0001-5078-8770</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Free Content; Wiley Online Library All Journals; Alma/SFX Local Collection |
| subjects | Adolescent Adult cognition Cognition - physiology Cognitive ability Cortex (motor) Cross-Sectional Studies endophenotype Endophenotypes Epilepsy Female fMRI Full Length Original Research Paper Full‐length Original Research Functional magnetic resonance imaging Gene mapping Handedness Humans Hyperkinesis - diagnostic imaging Hyperkinesis - physiopathology Hyperkinesis - psychology juvenile myoclonic epilepsy Male Memory Mental disorders Middle Aged motor system Myoclonic Epilepsy, Juvenile - diagnostic imaging Myoclonic Epilepsy, Juvenile - physiopathology Myoclonic Epilepsy, Juvenile - psychology Myoclonus Neuroimaging Phenotypes Prospective Studies Psychomotor Performance - physiology Seizures Siblings Young Adult |
| title | Motor hyperactivation during cognitive tasks: An endophenotype of juvenile myoclonic epilepsy |
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