Brain plasticity underlying sleep-dependent motor consolidation after motor imagery
Abstract Motor imagery can, similarly to physical practice, improve motor performance through experience-based plasticity. Using magnetoencephalography, we investigated changes in brain activity associated with offline consolidation of motor sequence learning through physical practice or motor image...
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| Veröffentlicht in: | Cerebral cortex (New York, N.Y. 1991) N.Y. 1991), 2023-11, Vol.33 (23), p.11431-11445 |
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| container_title | Cerebral cortex (New York, N.Y. 1991) |
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| creator | Di Rienzo, Franck Debarnot, Ursula Daligault, Sébastien Delpuech, Claude Doyon, Julien Guillot, Aymeric |
| description | Abstract
Motor imagery can, similarly to physical practice, improve motor performance through experience-based plasticity. Using magnetoencephalography, we investigated changes in brain activity associated with offline consolidation of motor sequence learning through physical practice or motor imagery. After an initial training session with either physical practice or motor imagery, participants underwent overnight consolidation. As control condition, participants underwent wake-related consolidation after training with motor imagery. Behavioral analyses revealed that overnight consolidation of motor learning through motor imagery outperformed wake-related consolidation (95% CI [0.02, 0.07], P |
| doi_str_mv | 10.1093/cercor/bhad379 |
| format | Article |
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Motor imagery can, similarly to physical practice, improve motor performance through experience-based plasticity. Using magnetoencephalography, we investigated changes in brain activity associated with offline consolidation of motor sequence learning through physical practice or motor imagery. After an initial training session with either physical practice or motor imagery, participants underwent overnight consolidation. As control condition, participants underwent wake-related consolidation after training with motor imagery. Behavioral analyses revealed that overnight consolidation of motor learning through motor imagery outperformed wake-related consolidation (95% CI [0.02, 0.07], P < 0.001, RP2 = 0.05). As regions of interest, we selected the generators of event-related synchronization/desynchronization of alpha (8–12 Hz) and beta (15–30 Hz) oscillations, which predicted the level of performance on the motor sequence. This yielded a primary sensorimotor-premotor network for alpha oscillations and a cortico-cerebellar network for beta oscillations. The alpha network exhibited increased neural desynchronization after overnight consolidation compared to wake-related consolidation. By contrast, the beta network exhibited an increase in neural synchronization after wake-related consolidation compared to overnight consolidation. We provide the first evidence of parallel brain plasticity underlying behavioral changes associated with sleep-dependent consolidation of motor skill learning through motor imagery and physical practice.</description><identifier>ISSN: 1047-3211</identifier><identifier>EISSN: 1460-2199</identifier><identifier>DOI: 10.1093/cercor/bhad379</identifier><identifier>PMID: 37814365</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Alpha rhythm ; Beta rhythm ; Cerebellum ; Cognitive Sciences ; Humans ; Learning ; Life Sciences ; Magentoencephalography ; Memory Consolidation ; Motor imagery ; Motor learning ; Motor Skills ; Neuronal Plasticity ; Neurons and Cognition ; Neuroplasticity ; Psychomotor Performance ; Sleep</subject><ispartof>Cerebral cortex (New York, N.Y. 1991), 2023-11, Vol.33 (23), p.11431-11445</ispartof><rights>The Author(s) 2023. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>Attribution - NonCommercial</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c318t-79e43b596b627162ce93c429e1d7cb1d5d51160d47ce3eb78e922420a585e303</cites><orcidid>0000-0001-7920-8709 ; 0000-0003-1081-7375</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,777,781,882,1579,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37814365$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04744498$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Di Rienzo, Franck</creatorcontrib><creatorcontrib>Debarnot, Ursula</creatorcontrib><creatorcontrib>Daligault, Sébastien</creatorcontrib><creatorcontrib>Delpuech, Claude</creatorcontrib><creatorcontrib>Doyon, Julien</creatorcontrib><creatorcontrib>Guillot, Aymeric</creatorcontrib><title>Brain plasticity underlying sleep-dependent motor consolidation after motor imagery</title><title>Cerebral cortex (New York, N.Y. 1991)</title><addtitle>Cereb Cortex</addtitle><description>Abstract
Motor imagery can, similarly to physical practice, improve motor performance through experience-based plasticity. Using magnetoencephalography, we investigated changes in brain activity associated with offline consolidation of motor sequence learning through physical practice or motor imagery. After an initial training session with either physical practice or motor imagery, participants underwent overnight consolidation. As control condition, participants underwent wake-related consolidation after training with motor imagery. Behavioral analyses revealed that overnight consolidation of motor learning through motor imagery outperformed wake-related consolidation (95% CI [0.02, 0.07], P < 0.001, RP2 = 0.05). As regions of interest, we selected the generators of event-related synchronization/desynchronization of alpha (8–12 Hz) and beta (15–30 Hz) oscillations, which predicted the level of performance on the motor sequence. This yielded a primary sensorimotor-premotor network for alpha oscillations and a cortico-cerebellar network for beta oscillations. The alpha network exhibited increased neural desynchronization after overnight consolidation compared to wake-related consolidation. By contrast, the beta network exhibited an increase in neural synchronization after wake-related consolidation compared to overnight consolidation. We provide the first evidence of parallel brain plasticity underlying behavioral changes associated with sleep-dependent consolidation of motor skill learning through motor imagery and physical practice.</description><subject>Alpha rhythm</subject><subject>Beta rhythm</subject><subject>Cerebellum</subject><subject>Cognitive Sciences</subject><subject>Humans</subject><subject>Learning</subject><subject>Life Sciences</subject><subject>Magentoencephalography</subject><subject>Memory Consolidation</subject><subject>Motor imagery</subject><subject>Motor learning</subject><subject>Motor Skills</subject><subject>Neuronal Plasticity</subject><subject>Neurons and Cognition</subject><subject>Neuroplasticity</subject><subject>Psychomotor Performance</subject><subject>Sleep</subject><issn>1047-3211</issn><issn>1460-2199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkD1PwzAQhi0EoqWwMqKMMKT1V-J4LBVfUiUGuluOfW2N0jjYCVL-Palaysjk0_nxe74HoVuCpwRLNjMQjA-zcqstE_IMjQnPcUqJlOdDjblIGSVkhK5i_MSYCJrRSzRioiCc5dkYfTwG7eqkqXRsnXFtn3S1hVD1rt4ksQJoUgsNDL26TXa-9SExvo6-cla3zteJXrcQjjdupzcQ-mt0sdZVhJvjOUGr56fV4jVdvr-8LebL1DBStKmQwFmZybzMqSA5NSCZ4VQCscKUxGY2IyTHlgsDDEpRgKSUU6yzIgOG2QQ9HGK3ulJNGIaHXnnt1Ot8qfa9YXvOuSy-ycDeH9gm-K8OYqt2LhqoKl2D76KihchYMWijAzo9oCb4GAOsT9kEq71zdXCujs6HB3fH7K7cgT3hv5L_Puq75r-wH5yrjXM</recordid><startdate>20231127</startdate><enddate>20231127</enddate><creator>Di Rienzo, Franck</creator><creator>Debarnot, Ursula</creator><creator>Daligault, Sébastien</creator><creator>Delpuech, Claude</creator><creator>Doyon, Julien</creator><creator>Guillot, Aymeric</creator><general>Oxford University Press</general><general>Oxford University Press (OUP)</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/0000-0001-7920-8709</orcidid><orcidid>https://orcid.org/0000-0003-1081-7375</orcidid></search><sort><creationdate>20231127</creationdate><title>Brain plasticity underlying sleep-dependent motor consolidation after motor imagery</title><author>Di Rienzo, Franck ; Debarnot, Ursula ; Daligault, Sébastien ; Delpuech, Claude ; Doyon, Julien ; Guillot, Aymeric</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c318t-79e43b596b627162ce93c429e1d7cb1d5d51160d47ce3eb78e922420a585e303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Alpha rhythm</topic><topic>Beta rhythm</topic><topic>Cerebellum</topic><topic>Cognitive Sciences</topic><topic>Humans</topic><topic>Learning</topic><topic>Life Sciences</topic><topic>Magentoencephalography</topic><topic>Memory Consolidation</topic><topic>Motor imagery</topic><topic>Motor learning</topic><topic>Motor Skills</topic><topic>Neuronal Plasticity</topic><topic>Neurons and Cognition</topic><topic>Neuroplasticity</topic><topic>Psychomotor Performance</topic><topic>Sleep</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Di Rienzo, Franck</creatorcontrib><creatorcontrib>Debarnot, Ursula</creatorcontrib><creatorcontrib>Daligault, Sébastien</creatorcontrib><creatorcontrib>Delpuech, Claude</creatorcontrib><creatorcontrib>Doyon, Julien</creatorcontrib><creatorcontrib>Guillot, Aymeric</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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Cerebral cortex (New York, N.Y. 1991)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Di Rienzo, Franck</au><au>Debarnot, Ursula</au><au>Daligault, Sébastien</au><au>Delpuech, Claude</au><au>Doyon, Julien</au><au>Guillot, Aymeric</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brain plasticity underlying sleep-dependent motor consolidation after motor imagery</atitle><jtitle>Cerebral cortex (New York, N.Y. 1991)</jtitle><addtitle>Cereb Cortex</addtitle><date>2023-11-27</date><risdate>2023</risdate><volume>33</volume><issue>23</issue><spage>11431</spage><epage>11445</epage><pages>11431-11445</pages><issn>1047-3211</issn><eissn>1460-2199</eissn><abstract>Abstract
Motor imagery can, similarly to physical practice, improve motor performance through experience-based plasticity. Using magnetoencephalography, we investigated changes in brain activity associated with offline consolidation of motor sequence learning through physical practice or motor imagery. After an initial training session with either physical practice or motor imagery, participants underwent overnight consolidation. As control condition, participants underwent wake-related consolidation after training with motor imagery. Behavioral analyses revealed that overnight consolidation of motor learning through motor imagery outperformed wake-related consolidation (95% CI [0.02, 0.07], P < 0.001, RP2 = 0.05). As regions of interest, we selected the generators of event-related synchronization/desynchronization of alpha (8–12 Hz) and beta (15–30 Hz) oscillations, which predicted the level of performance on the motor sequence. This yielded a primary sensorimotor-premotor network for alpha oscillations and a cortico-cerebellar network for beta oscillations. The alpha network exhibited increased neural desynchronization after overnight consolidation compared to wake-related consolidation. By contrast, the beta network exhibited an increase in neural synchronization after wake-related consolidation compared to overnight consolidation. We provide the first evidence of parallel brain plasticity underlying behavioral changes associated with sleep-dependent consolidation of motor skill learning through motor imagery and physical practice.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>37814365</pmid><doi>10.1093/cercor/bhad379</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-7920-8709</orcidid><orcidid>https://orcid.org/0000-0003-1081-7375</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
| subjects | Alpha rhythm Beta rhythm Cerebellum Cognitive Sciences Humans Learning Life Sciences Magentoencephalography Memory Consolidation Motor imagery Motor learning Motor Skills Neuronal Plasticity Neurons and Cognition Neuroplasticity Psychomotor Performance Sleep |
| title | Brain plasticity underlying sleep-dependent motor consolidation after motor imagery |
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