Neural correlates of motor learning: Network communication versus local oscillations
Learning new motor skills through training, also termed motor learning, is central for everyday life. Current training strategies recommend intensive task-repetitions aimed at inducing local activation of motor areas, associated with changes in oscillation amplitudes (“event-related power”) during t...
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description | Learning new motor skills through training, also termed motor learning, is central for everyday life. Current training strategies recommend intensive task-repetitions aimed at inducing local activation of motor areas, associated with changes in oscillation amplitudes (“event-related power”) during training. More recently, another neural mechanism was suggested to influence motor learning: modulation of functional connectivity (FC), that is, how much spatially separated brain regions communicate with each other before and during training. The goal of the present study was to compare the impact of these two neural processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that training gain, long-term expertise (i.e., average motor performance), and consolidation were all predicted by whole-brain alpha- and beta-band FC at motor areas, striatum, and mediotemporal lobe (MTL). Local power changes during training did not predict any dependent variable. Thus, network dynamics seem more crucial than local activity for motor sequence learning, and training techniques should attempt to facilitate network interactions rather than local cortical activation.
Both, local and network processing mechanisms support motor sequence learning. The aim of the present study was to compare the impact of these two processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that only network dynamics, measured with functional connectivity, could predict learning, long-term expertise, and consolidation. Conversely, local activity, measured with event-related power decrease, did not predict any dependent measure. Specifically, network interactions of the primary motor area, the striatum, and the medial temporal lobe correlated with learning performance. Therefore, network dynamics seem more crucial than local activity for motor sequence learning and training techniques should facilitate network interactions rather than local cortical activation. |
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Both, local and network processing mechanisms support motor sequence learning. The aim of the present study was to compare the impact of these two processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that only network dynamics, measured with functional connectivity, could predict learning, long-term expertise, and consolidation. Conversely, local activity, measured with event-related power decrease, did not predict any dependent measure. Specifically, network interactions of the primary motor area, the striatum, and the medial temporal lobe correlated with learning performance. Therefore, network dynamics seem more crucial than local activity for motor sequence learning and training techniques should facilitate network interactions rather than local cortical activation.</description><identifier>ISSN: 2472-1751</identifier><identifier>EISSN: 2472-1751</identifier><identifier>EISSN: 2644-2353</identifier><identifier>DOI: 10.1162/netn_a_00374</identifier><identifier>PMID: 39355447</identifier><language>eng</language><publisher>255 Main Street, 9th Floor, Cambridge, Massachusetts 02142, USA: MIT Press</publisher><subject>Brain ; Communication ; Consolidation ; Dependent variables ; EEG ; Electroencephalography ; Functional connectivity ; Information processing ; Learning ; Motor sequence learning ; Motor skill ; Motor skill learning ; Motor task performance ; Neostriatum ; Neural networks ; Neural plasticity ; Neurosciences ; Oscillations ; Software utilities ; Temporal lobe ; Training</subject><ispartof>Harvard data science review, 2024-10, Vol.8 (3), p.714-733</ispartof><rights>2024 Massachusetts Institute of Technology.</rights><rights>Copyright MIT Press Journals, The 2024</rights><rights>2024 Massachusetts Institute of Technology 2024 Massachusetts Institute of Technology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c361t-876be0d045e6739e031bcae8712b0f91a8e8b2afd7eac3aec222bd192f21585b3</cites><orcidid>0000-0001-7178-7793 ; 0000-0002-5912-2438</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/PMC11340994/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3100586345?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,21387,27923,27924,33743,33744,43804,53790,53792,64384,64386,64388,72240</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39355447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mottaz, Anaïs</creatorcontrib><creatorcontrib>Savic, Branislav</creatorcontrib><creatorcontrib>Allaman, Leslie</creatorcontrib><creatorcontrib>Guggisberg, Adrian G.</creatorcontrib><title>Neural correlates of motor learning: Network communication versus local oscillations</title><title>Harvard data science review</title><addtitle>Netw Neurosci</addtitle><description>Learning new motor skills through training, also termed motor learning, is central for everyday life. Current training strategies recommend intensive task-repetitions aimed at inducing local activation of motor areas, associated with changes in oscillation amplitudes (“event-related power”) during training. More recently, another neural mechanism was suggested to influence motor learning: modulation of functional connectivity (FC), that is, how much spatially separated brain regions communicate with each other before and during training. The goal of the present study was to compare the impact of these two neural processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that training gain, long-term expertise (i.e., average motor performance), and consolidation were all predicted by whole-brain alpha- and beta-band FC at motor areas, striatum, and mediotemporal lobe (MTL). Local power changes during training did not predict any dependent variable. Thus, network dynamics seem more crucial than local activity for motor sequence learning, and training techniques should attempt to facilitate network interactions rather than local cortical activation.
Both, local and network processing mechanisms support motor sequence learning. The aim of the present study was to compare the impact of these two processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that only network dynamics, measured with functional connectivity, could predict learning, long-term expertise, and consolidation. Conversely, local activity, measured with event-related power decrease, did not predict any dependent measure. Specifically, network interactions of the primary motor area, the striatum, and the medial temporal lobe correlated with learning performance. Therefore, network dynamics seem more crucial than local activity for motor sequence learning and training techniques should facilitate network interactions rather than local cortical activation.</description><subject>Brain</subject><subject>Communication</subject><subject>Consolidation</subject><subject>Dependent variables</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>Functional connectivity</subject><subject>Information processing</subject><subject>Learning</subject><subject>Motor sequence learning</subject><subject>Motor skill</subject><subject>Motor skill learning</subject><subject>Motor task performance</subject><subject>Neostriatum</subject><subject>Neural networks</subject><subject>Neural plasticity</subject><subject>Neurosciences</subject><subject>Oscillations</subject><subject>Software utilities</subject><subject>Temporal lobe</subject><subject>Training</subject><issn>2472-1751</issn><issn>2472-1751</issn><issn>2644-2353</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptkU1PFTEUhhsjEYLsXJtJ3Ljwaj-nHTeGED9ICGxg3ZzpnLn2OtNi28H47y1cxIth1abnydNz3kPIK0bfM9byDwFLsGApFVo-Iwdcar5iWrHnO_d9cpTzhlLKGWdUmhdkX3RCKSn1Abk8xyXB1LiYEk5QMDdxbOZYYmomhBR8WH9szrH8iulHpeZ5Cd5B8TE0N5jykpspuiqI2flpuivkl2RvhCnj0f15SK6-fL48-bY6u_h6enJ8tnKiZWVldNsjHahU2GrRIRWsd4BGM97TsWNg0PQcxkEjOAHoOOf9wDo-cqaM6sUhOd16hwgbe538DOm3jeDt3UNMawupeDehVU6PLYDjQnSywxGEMVLSUcuWG-lkdX3auq6XfsbBYSg1l0fSx5Xgv9t1vLGMCUm77tbw9t6Q4s8Fc7Gzzw5rKAHjkq1gNf-6NM4r-uY_dBOXFGpWlaJUmVZIVal3W8qlmHPC8aEbRu2tye6uv-Kvdyd4gP8u-1-Ds9_58EnXH6moulM</recordid><startdate>20241001</startdate><enddate>20241001</enddate><creator>Mottaz, Anaïs</creator><creator>Savic, Branislav</creator><creator>Allaman, Leslie</creator><creator>Guggisberg, Adrian G.</creator><general>MIT Press</general><general>MIT Press Journals, The</general><general>The MIT Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>JQ2</scope><scope>K7-</scope><scope>LK8</scope><scope>M7P</scope><scope>P62</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-7178-7793</orcidid><orcidid>https://orcid.org/0000-0002-5912-2438</orcidid></search><sort><creationdate>20241001</creationdate><title>Neural correlates of motor learning: Network communication versus local oscillations</title><author>Mottaz, Anaïs ; Savic, Branislav ; Allaman, Leslie ; Guggisberg, Adrian G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c361t-876be0d045e6739e031bcae8712b0f91a8e8b2afd7eac3aec222bd192f21585b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Brain</topic><topic>Communication</topic><topic>Consolidation</topic><topic>Dependent variables</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>Functional connectivity</topic><topic>Information processing</topic><topic>Learning</topic><topic>Motor sequence learning</topic><topic>Motor skill</topic><topic>Motor skill learning</topic><topic>Motor task performance</topic><topic>Neostriatum</topic><topic>Neural networks</topic><topic>Neural plasticity</topic><topic>Neurosciences</topic><topic>Oscillations</topic><topic>Software utilities</topic><topic>Temporal lobe</topic><topic>Training</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mottaz, Anaïs</creatorcontrib><creatorcontrib>Savic, Branislav</creatorcontrib><creatorcontrib>Allaman, Leslie</creatorcontrib><creatorcontrib>Guggisberg, Adrian G.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Computer Science Collection</collection><collection>Computer Science Database</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Publicly Available Content Database</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><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Harvard data science review</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mottaz, Anaïs</au><au>Savic, Branislav</au><au>Allaman, Leslie</au><au>Guggisberg, Adrian G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural correlates of motor learning: Network communication versus local oscillations</atitle><jtitle>Harvard data science review</jtitle><addtitle>Netw Neurosci</addtitle><date>2024-10-01</date><risdate>2024</risdate><volume>8</volume><issue>3</issue><spage>714</spage><epage>733</epage><pages>714-733</pages><issn>2472-1751</issn><eissn>2472-1751</eissn><eissn>2644-2353</eissn><abstract>Learning new motor skills through training, also termed motor learning, is central for everyday life. Current training strategies recommend intensive task-repetitions aimed at inducing local activation of motor areas, associated with changes in oscillation amplitudes (“event-related power”) during training. More recently, another neural mechanism was suggested to influence motor learning: modulation of functional connectivity (FC), that is, how much spatially separated brain regions communicate with each other before and during training. The goal of the present study was to compare the impact of these two neural processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that training gain, long-term expertise (i.e., average motor performance), and consolidation were all predicted by whole-brain alpha- and beta-band FC at motor areas, striatum, and mediotemporal lobe (MTL). Local power changes during training did not predict any dependent variable. Thus, network dynamics seem more crucial than local activity for motor sequence learning, and training techniques should attempt to facilitate network interactions rather than local cortical activation.
Both, local and network processing mechanisms support motor sequence learning. The aim of the present study was to compare the impact of these two processing types on motor learning. We measured EEG before, during, and after a finger-tapping task (FTT) in 20 healthy subjects. The results showed that only network dynamics, measured with functional connectivity, could predict learning, long-term expertise, and consolidation. Conversely, local activity, measured with event-related power decrease, did not predict any dependent measure. Specifically, network interactions of the primary motor area, the striatum, and the medial temporal lobe correlated with learning performance. Therefore, network dynamics seem more crucial than local activity for motor sequence learning and training techniques should facilitate network interactions rather than local cortical activation.</abstract><cop>255 Main Street, 9th Floor, Cambridge, Massachusetts 02142, USA</cop><pub>MIT Press</pub><pmid>39355447</pmid><doi>10.1162/netn_a_00374</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0001-7178-7793</orcidid><orcidid>https://orcid.org/0000-0002-5912-2438</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Brain Communication Consolidation Dependent variables EEG Electroencephalography Functional connectivity Information processing Learning Motor sequence learning Motor skill Motor skill learning Motor task performance Neostriatum Neural networks Neural plasticity Neurosciences Oscillations Software utilities Temporal lobe Training |
title | Neural correlates of motor learning: Network communication versus local oscillations |
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