Prefrontal-subthalamic theta signaling mediates delayed responses during conflict processing
While medial frontal cortex (MFC) and subthalamic nucleus (STN) have been implicated in conflict monitoring and action inhibition, respectively, an integrated understanding of the spatiotemporal and spectral interaction of these nodes and how they interact with motor cortex (M1) to definitively modi...
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Veröffentlicht in: | Progress in neurobiology 2024-05, Vol.236, p.102613-102613, Article 102613 |
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creator | Choi, Jeong Woo Malekmohammadi, Mahsa Niketeghad, Soroush Cross, Katy A. Ebadi, Hamasa Alijanpourotaghsara, Amirreza Aron, Adam Rutishauser, Ueli Pouratian, Nader |
description | While medial frontal cortex (MFC) and subthalamic nucleus (STN) have been implicated in conflict monitoring and action inhibition, respectively, an integrated understanding of the spatiotemporal and spectral interaction of these nodes and how they interact with motor cortex (M1) to definitively modify motor behavior during conflict is lacking. We recorded neural signals intracranially across presupplementary motor area (preSMA), M1, STN, and globus pallidus internus (GPi), during a flanker task in 20 patients undergoing deep brain stimulation implantation surgery for Parkinson disease or dystonia. Conflict is associated with sequential and causal increases in local theta power from preSMA to STN to M1 with movement delays directly correlated with increased STN theta power, indicating preSMA is the MFC locus that monitors conflict and signals STN to implement a ‘break.’ Transmission of theta from STN-to-M1 subsequently results in a transient increase in M1-to-GPi beta flow immediately prior to movement, modulating the motor network to actuate the conflict-related action inhibition (i.e., delayed response). Action regulation during conflict relies on two distinct circuits, the conflict-related theta and movement-related beta networks, that are separated spatially, spectrally, and temporally, but which interact dynamically to mediate motor performance, highlighting complex parallel yet interacting networks regulating movement.
•PreSMA is the MFC locus monitoring for conflict, generating conflict-mediated theta.•Theta flows from preSMA to STN to M1 in conflict processing.•STN-mediated theta changes are required for delayed response in conflict processing.•STN-to-M1 theta flow during conflict is contemporaneous with M1-to-GPi beta flow increases.•Conflict-related theta network modulates movement-related beta networks. |
doi_str_mv | 10.1016/j.pneurobio.2024.102613 |
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•PreSMA is the MFC locus monitoring for conflict, generating conflict-mediated theta.•Theta flows from preSMA to STN to M1 in conflict processing.•STN-mediated theta changes are required for delayed response in conflict processing.•STN-to-M1 theta flow during conflict is contemporaneous with M1-to-GPi beta flow increases.•Conflict-related theta network modulates movement-related beta networks.</description><identifier>ISSN: 0301-0082</identifier><identifier>EISSN: 1873-5118</identifier><identifier>DOI: 10.1016/j.pneurobio.2024.102613</identifier><identifier>PMID: 38631480</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Action regulation ; Basal-ganglia cortical network ; Conflict processing ; Conflict-related theta network ; Intracranial neural recordings ; Movement-related beta network</subject><ispartof>Progress in neurobiology, 2024-05, Vol.236, p.102613-102613, Article 102613</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024. Published by Elsevier Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c317t-3292055e5c5478be51709f94a0c8bf923ab0d53ad775e1aca4976102b294da593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.pneurobio.2024.102613$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38631480$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Choi, Jeong Woo</creatorcontrib><creatorcontrib>Malekmohammadi, Mahsa</creatorcontrib><creatorcontrib>Niketeghad, Soroush</creatorcontrib><creatorcontrib>Cross, Katy A.</creatorcontrib><creatorcontrib>Ebadi, Hamasa</creatorcontrib><creatorcontrib>Alijanpourotaghsara, Amirreza</creatorcontrib><creatorcontrib>Aron, Adam</creatorcontrib><creatorcontrib>Rutishauser, Ueli</creatorcontrib><creatorcontrib>Pouratian, Nader</creatorcontrib><title>Prefrontal-subthalamic theta signaling mediates delayed responses during conflict processing</title><title>Progress in neurobiology</title><addtitle>Prog Neurobiol</addtitle><description>While medial frontal cortex (MFC) and subthalamic nucleus (STN) have been implicated in conflict monitoring and action inhibition, respectively, an integrated understanding of the spatiotemporal and spectral interaction of these nodes and how they interact with motor cortex (M1) to definitively modify motor behavior during conflict is lacking. We recorded neural signals intracranially across presupplementary motor area (preSMA), M1, STN, and globus pallidus internus (GPi), during a flanker task in 20 patients undergoing deep brain stimulation implantation surgery for Parkinson disease or dystonia. Conflict is associated with sequential and causal increases in local theta power from preSMA to STN to M1 with movement delays directly correlated with increased STN theta power, indicating preSMA is the MFC locus that monitors conflict and signals STN to implement a ‘break.’ Transmission of theta from STN-to-M1 subsequently results in a transient increase in M1-to-GPi beta flow immediately prior to movement, modulating the motor network to actuate the conflict-related action inhibition (i.e., delayed response). Action regulation during conflict relies on two distinct circuits, the conflict-related theta and movement-related beta networks, that are separated spatially, spectrally, and temporally, but which interact dynamically to mediate motor performance, highlighting complex parallel yet interacting networks regulating movement.
•PreSMA is the MFC locus monitoring for conflict, generating conflict-mediated theta.•Theta flows from preSMA to STN to M1 in conflict processing.•STN-mediated theta changes are required for delayed response in conflict processing.•STN-to-M1 theta flow during conflict is contemporaneous with M1-to-GPi beta flow increases.•Conflict-related theta network modulates movement-related beta networks.</description><subject>Action regulation</subject><subject>Basal-ganglia cortical network</subject><subject>Conflict processing</subject><subject>Conflict-related theta network</subject><subject>Intracranial neural recordings</subject><subject>Movement-related beta network</subject><issn>0301-0082</issn><issn>1873-5118</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkEtLAzEUhYMotlb_gs7SzdSbZDKPZSm-oKAL3Qkhk7nTpkwnNckI_femtHbrKnD4bg7nI-SOwpQCzR_W022Pg7O1sVMGLIspyyk_I2NaFjwVlJbnZAwcaApQshG58n4NADkHfklGvMw5zUoYk693h62zfVBd6oc6rFSnNkYnYYVBJd4se9WZfplssDEqoE8a7NQOm8Sh39re75PB7Qlt-7YzOiRbZzV6H7NrctGqzuPN8Z2Qz6fHj_lLunh7fp3PFqnmtAgpZxUDIVBokRVljYIWULVVpkCXdVsxrmpoBFdNUQikSqusKvI4uGZV1ihR8Qm5P_wbq78H9EFujNfYdapHO3jJIaMslpQiosUB1c56H7fLrTMb5XaSgtyrlWt5Uiv3auVBbby8PZYMdbRxuvtzGYHZAcA49cegk14b7HU051AH2Vjzb8kv1feQCQ</recordid><startdate>20240501</startdate><enddate>20240501</enddate><creator>Choi, Jeong Woo</creator><creator>Malekmohammadi, Mahsa</creator><creator>Niketeghad, Soroush</creator><creator>Cross, Katy A.</creator><creator>Ebadi, Hamasa</creator><creator>Alijanpourotaghsara, Amirreza</creator><creator>Aron, Adam</creator><creator>Rutishauser, Ueli</creator><creator>Pouratian, Nader</creator><general>Elsevier Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20240501</creationdate><title>Prefrontal-subthalamic theta signaling mediates delayed responses during conflict processing</title><author>Choi, Jeong Woo ; Malekmohammadi, Mahsa ; Niketeghad, Soroush ; Cross, Katy A. ; Ebadi, Hamasa ; Alijanpourotaghsara, Amirreza ; Aron, Adam ; Rutishauser, Ueli ; Pouratian, Nader</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c317t-3292055e5c5478be51709f94a0c8bf923ab0d53ad775e1aca4976102b294da593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Action regulation</topic><topic>Basal-ganglia cortical network</topic><topic>Conflict processing</topic><topic>Conflict-related theta network</topic><topic>Intracranial neural recordings</topic><topic>Movement-related beta network</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Choi, Jeong Woo</creatorcontrib><creatorcontrib>Malekmohammadi, Mahsa</creatorcontrib><creatorcontrib>Niketeghad, Soroush</creatorcontrib><creatorcontrib>Cross, Katy A.</creatorcontrib><creatorcontrib>Ebadi, Hamasa</creatorcontrib><creatorcontrib>Alijanpourotaghsara, Amirreza</creatorcontrib><creatorcontrib>Aron, Adam</creatorcontrib><creatorcontrib>Rutishauser, Ueli</creatorcontrib><creatorcontrib>Pouratian, Nader</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Progress in neurobiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Choi, Jeong Woo</au><au>Malekmohammadi, Mahsa</au><au>Niketeghad, Soroush</au><au>Cross, Katy A.</au><au>Ebadi, Hamasa</au><au>Alijanpourotaghsara, Amirreza</au><au>Aron, Adam</au><au>Rutishauser, Ueli</au><au>Pouratian, Nader</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prefrontal-subthalamic theta signaling mediates delayed responses during conflict processing</atitle><jtitle>Progress in neurobiology</jtitle><addtitle>Prog Neurobiol</addtitle><date>2024-05-01</date><risdate>2024</risdate><volume>236</volume><spage>102613</spage><epage>102613</epage><pages>102613-102613</pages><artnum>102613</artnum><issn>0301-0082</issn><eissn>1873-5118</eissn><abstract>While medial frontal cortex (MFC) and subthalamic nucleus (STN) have been implicated in conflict monitoring and action inhibition, respectively, an integrated understanding of the spatiotemporal and spectral interaction of these nodes and how they interact with motor cortex (M1) to definitively modify motor behavior during conflict is lacking. We recorded neural signals intracranially across presupplementary motor area (preSMA), M1, STN, and globus pallidus internus (GPi), during a flanker task in 20 patients undergoing deep brain stimulation implantation surgery for Parkinson disease or dystonia. Conflict is associated with sequential and causal increases in local theta power from preSMA to STN to M1 with movement delays directly correlated with increased STN theta power, indicating preSMA is the MFC locus that monitors conflict and signals STN to implement a ‘break.’ Transmission of theta from STN-to-M1 subsequently results in a transient increase in M1-to-GPi beta flow immediately prior to movement, modulating the motor network to actuate the conflict-related action inhibition (i.e., delayed response). Action regulation during conflict relies on two distinct circuits, the conflict-related theta and movement-related beta networks, that are separated spatially, spectrally, and temporally, but which interact dynamically to mediate motor performance, highlighting complex parallel yet interacting networks regulating movement.
•PreSMA is the MFC locus monitoring for conflict, generating conflict-mediated theta.•Theta flows from preSMA to STN to M1 in conflict processing.•STN-mediated theta changes are required for delayed response in conflict processing.•STN-to-M1 theta flow during conflict is contemporaneous with M1-to-GPi beta flow increases.•Conflict-related theta network modulates movement-related beta networks.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>38631480</pmid><doi>10.1016/j.pneurobio.2024.102613</doi><tpages>1</tpages></addata></record> |
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subjects | Action regulation Basal-ganglia cortical network Conflict processing Conflict-related theta network Intracranial neural recordings Movement-related beta network |
title | Prefrontal-subthalamic theta signaling mediates delayed responses during conflict processing |
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