Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography
Transcranial magnetic stimulation (TMS) is increasingly used as a noninvasive technique for neuromodulation in research and clinical applications, yet its mechanisms are not well understood. Here, we present the neurophysiological effects of TMS using intracranial electrocorticography (iEEG) in neur...
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| Veröffentlicht in: | Molecular psychiatry 2024-05, Vol.29 (5), p.1228-1240 |
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| creator | Wang, Jeffrey B. Hassan, Umair Bruss, Joel E. Oya, Hiroyuki Uitermarkt, Brandt D. Trapp, Nicholas T. Gander, Phillip E. Howard, Matthew A. Keller, Corey J. Boes, Aaron D. |
| description | Transcranial magnetic stimulation (TMS) is increasingly used as a noninvasive technique for neuromodulation in research and clinical applications, yet its mechanisms are not well understood. Here, we present the neurophysiological effects of TMS using intracranial electrocorticography (iEEG) in neurosurgical patients. We first evaluated safety in a gel-based phantom. We then performed TMS-iEEG in 22 neurosurgical participants with no adverse events. We next evaluated intracranial responses to single pulses of TMS to the dorsolateral prefrontal cortex (dlPFC) (
N
= 10, 1414 electrodes). We demonstrate that TMS is capable of inducing evoked potentials both locally within the dlPFC and in downstream regions functionally connected to the dlPFC, including the anterior cingulate and insular cortex. These downstream effects were not observed when stimulating other distant brain regions. Intracranial dlPFC electrical stimulation had similar timing and downstream effects as TMS. These findings support the safety and promise of TMS-iEEG in humans to examine local and network-level effects of TMS with higher spatiotemporal resolution than currently available methods. |
| doi_str_mv | 10.1038/s41380-024-02405-y |
| format | Article |
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N
= 10, 1414 electrodes). We demonstrate that TMS is capable of inducing evoked potentials both locally within the dlPFC and in downstream regions functionally connected to the dlPFC, including the anterior cingulate and insular cortex. These downstream effects were not observed when stimulating other distant brain regions. Intracranial dlPFC electrical stimulation had similar timing and downstream effects as TMS. These findings support the safety and promise of TMS-iEEG in humans to examine local and network-level effects of TMS with higher spatiotemporal resolution than currently available methods.</description><identifier>ISSN: 1359-4184</identifier><identifier>ISSN: 1476-5578</identifier><identifier>EISSN: 1476-5578</identifier><identifier>DOI: 10.1038/s41380-024-02405-y</identifier><identifier>PMID: 38317012</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378 ; 692/699/476/1414 ; 9/30 ; Adult ; Behavioral Sciences ; Biological Psychology ; Brain - physiology ; Brain - physiopathology ; Brain Mapping - methods ; Cortex (insular) ; Dorsolateral Prefrontal Cortex - physiology ; Electric Stimulation - methods ; Electrical stimuli ; Electrocorticography - methods ; Evoked Potentials - physiology ; Female ; Humans ; Magnetic fields ; Male ; Medicine ; Medicine & Public Health ; Middle Aged ; Neuromodulation ; Neurosciences ; Neurosurgery ; Pharmacotherapy ; Prefrontal cortex ; Psychiatry ; Transcranial magnetic stimulation ; Transcranial Magnetic Stimulation - methods ; Young Adult</subject><ispartof>Molecular psychiatry, 2024-05, Vol.29 (5), p.1228-1240</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2024. The Author(s), under exclusive licence to Springer Nature Limited.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-16991f45d0c5a859ca7cf1289909474076746cf78682b16f64967594f39763bf3</citedby><cites>FETCH-LOGICAL-c375t-16991f45d0c5a859ca7cf1289909474076746cf78682b16f64967594f39763bf3</cites><orcidid>0000-0002-1733-5478 ; 0000-0002-8933-9822 ; 0000-0002-7865-9257 ; 0000-0003-0529-3490 ; 0000-0003-3945-8820</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41380-024-02405-y$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41380-024-02405-y$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38317012$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Jeffrey B.</creatorcontrib><creatorcontrib>Hassan, Umair</creatorcontrib><creatorcontrib>Bruss, Joel E.</creatorcontrib><creatorcontrib>Oya, Hiroyuki</creatorcontrib><creatorcontrib>Uitermarkt, Brandt D.</creatorcontrib><creatorcontrib>Trapp, Nicholas T.</creatorcontrib><creatorcontrib>Gander, Phillip E.</creatorcontrib><creatorcontrib>Howard, Matthew A.</creatorcontrib><creatorcontrib>Keller, Corey J.</creatorcontrib><creatorcontrib>Boes, Aaron D.</creatorcontrib><title>Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography</title><title>Molecular psychiatry</title><addtitle>Mol Psychiatry</addtitle><addtitle>Mol Psychiatry</addtitle><description>Transcranial magnetic stimulation (TMS) is increasingly used as a noninvasive technique for neuromodulation in research and clinical applications, yet its mechanisms are not well understood. Here, we present the neurophysiological effects of TMS using intracranial electrocorticography (iEEG) in neurosurgical patients. We first evaluated safety in a gel-based phantom. We then performed TMS-iEEG in 22 neurosurgical participants with no adverse events. We next evaluated intracranial responses to single pulses of TMS to the dorsolateral prefrontal cortex (dlPFC) (
N
= 10, 1414 electrodes). We demonstrate that TMS is capable of inducing evoked potentials both locally within the dlPFC and in downstream regions functionally connected to the dlPFC, including the anterior cingulate and insular cortex. These downstream effects were not observed when stimulating other distant brain regions. Intracranial dlPFC electrical stimulation had similar timing and downstream effects as TMS. These findings support the safety and promise of TMS-iEEG in humans to examine local and network-level effects of TMS with higher spatiotemporal resolution than currently available methods.</description><subject>631/378</subject><subject>692/699/476/1414</subject><subject>9/30</subject><subject>Adult</subject><subject>Behavioral Sciences</subject><subject>Biological Psychology</subject><subject>Brain - physiology</subject><subject>Brain - physiopathology</subject><subject>Brain Mapping - methods</subject><subject>Cortex (insular)</subject><subject>Dorsolateral Prefrontal Cortex - physiology</subject><subject>Electric Stimulation - methods</subject><subject>Electrical stimuli</subject><subject>Electrocorticography - methods</subject><subject>Evoked Potentials - physiology</subject><subject>Female</subject><subject>Humans</subject><subject>Magnetic fields</subject><subject>Male</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Middle Aged</subject><subject>Neuromodulation</subject><subject>Neurosciences</subject><subject>Neurosurgery</subject><subject>Pharmacotherapy</subject><subject>Prefrontal cortex</subject><subject>Psychiatry</subject><subject>Transcranial magnetic stimulation</subject><subject>Transcranial Magnetic Stimulation - methods</subject><subject>Young Adult</subject><issn>1359-4184</issn><issn>1476-5578</issn><issn>1476-5578</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUtrGzEUhUVJiZ00f6CLIMimm2ml0XsZTNoUAt20ayHLki0zIzmShuB_H7m2G8iioBeccz9d7gHgM0ZfMSLyW6GYSNShnh42Yt3-A5hjKnjHmJAX7U2Y6iiWdAauStkidBDZJZgRSbBAuJ-D9OC9s7XA5GHNJhbbjmAGOJp1dDVYWGoYp8HUkCJsq24c3EyjiXCZTYgwO5vyyq3gS6gbGGKDnBFuaOScmt44aZ3NbrP_BD56MxR3c7qvwZ_vD78Xj93Trx8_F_dPnSWC1Q5zpbCnbIUsM5Ipa4T1uJdKIUUFRYILyq0Xkst-ibnnVHHBFPVECU6WnlyDL0fuLqfnyZWqx1CsGwYTXZqK7lXfNxITrFnv3lm3acqxdacJOkwJtwaaqz-6bE6lZOf1LofR5L3GSB_i0Mc4dItC_41D71vR7Qk9LUe3-ldynn8zkKOhNCmuXX77-z_YV9r2lm0</recordid><startdate>20240501</startdate><enddate>20240501</enddate><creator>Wang, Jeffrey B.</creator><creator>Hassan, Umair</creator><creator>Bruss, Joel E.</creator><creator>Oya, Hiroyuki</creator><creator>Uitermarkt, Brandt D.</creator><creator>Trapp, Nicholas T.</creator><creator>Gander, Phillip E.</creator><creator>Howard, Matthew A.</creator><creator>Keller, Corey J.</creator><creator>Boes, Aaron D.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>7TK</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-1733-5478</orcidid><orcidid>https://orcid.org/0000-0002-8933-9822</orcidid><orcidid>https://orcid.org/0000-0002-7865-9257</orcidid><orcidid>https://orcid.org/0000-0003-0529-3490</orcidid><orcidid>https://orcid.org/0000-0003-3945-8820</orcidid></search><sort><creationdate>20240501</creationdate><title>Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography</title><author>Wang, Jeffrey B. ; Hassan, Umair ; Bruss, Joel E. ; Oya, Hiroyuki ; Uitermarkt, Brandt D. ; Trapp, Nicholas T. ; Gander, Phillip E. ; Howard, Matthew A. ; Keller, Corey J. ; Boes, Aaron D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-16991f45d0c5a859ca7cf1289909474076746cf78682b16f64967594f39763bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>631/378</topic><topic>692/699/476/1414</topic><topic>9/30</topic><topic>Adult</topic><topic>Behavioral Sciences</topic><topic>Biological Psychology</topic><topic>Brain - physiology</topic><topic>Brain - physiopathology</topic><topic>Brain Mapping - methods</topic><topic>Cortex (insular)</topic><topic>Dorsolateral Prefrontal Cortex - physiology</topic><topic>Electric Stimulation - methods</topic><topic>Electrical stimuli</topic><topic>Electrocorticography - methods</topic><topic>Evoked Potentials - physiology</topic><topic>Female</topic><topic>Humans</topic><topic>Magnetic fields</topic><topic>Male</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Middle Aged</topic><topic>Neuromodulation</topic><topic>Neurosciences</topic><topic>Neurosurgery</topic><topic>Pharmacotherapy</topic><topic>Prefrontal cortex</topic><topic>Psychiatry</topic><topic>Transcranial magnetic stimulation</topic><topic>Transcranial Magnetic Stimulation - methods</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Jeffrey B.</creatorcontrib><creatorcontrib>Hassan, Umair</creatorcontrib><creatorcontrib>Bruss, Joel E.</creatorcontrib><creatorcontrib>Oya, Hiroyuki</creatorcontrib><creatorcontrib>Uitermarkt, Brandt D.</creatorcontrib><creatorcontrib>Trapp, Nicholas T.</creatorcontrib><creatorcontrib>Gander, Phillip E.</creatorcontrib><creatorcontrib>Howard, Matthew A.</creatorcontrib><creatorcontrib>Keller, Corey J.</creatorcontrib><creatorcontrib>Boes, Aaron D.</creatorcontrib><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>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Jeffrey B.</au><au>Hassan, Umair</au><au>Bruss, Joel E.</au><au>Oya, Hiroyuki</au><au>Uitermarkt, Brandt D.</au><au>Trapp, Nicholas T.</au><au>Gander, Phillip E.</au><au>Howard, Matthew A.</au><au>Keller, Corey J.</au><au>Boes, Aaron D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography</atitle><jtitle>Molecular psychiatry</jtitle><stitle>Mol Psychiatry</stitle><addtitle>Mol Psychiatry</addtitle><date>2024-05-01</date><risdate>2024</risdate><volume>29</volume><issue>5</issue><spage>1228</spage><epage>1240</epage><pages>1228-1240</pages><issn>1359-4184</issn><issn>1476-5578</issn><eissn>1476-5578</eissn><abstract>Transcranial magnetic stimulation (TMS) is increasingly used as a noninvasive technique for neuromodulation in research and clinical applications, yet its mechanisms are not well understood. Here, we present the neurophysiological effects of TMS using intracranial electrocorticography (iEEG) in neurosurgical patients. We first evaluated safety in a gel-based phantom. We then performed TMS-iEEG in 22 neurosurgical participants with no adverse events. We next evaluated intracranial responses to single pulses of TMS to the dorsolateral prefrontal cortex (dlPFC) (
N
= 10, 1414 electrodes). We demonstrate that TMS is capable of inducing evoked potentials both locally within the dlPFC and in downstream regions functionally connected to the dlPFC, including the anterior cingulate and insular cortex. These downstream effects were not observed when stimulating other distant brain regions. Intracranial dlPFC electrical stimulation had similar timing and downstream effects as TMS. These findings support the safety and promise of TMS-iEEG in humans to examine local and network-level effects of TMS with higher spatiotemporal resolution than currently available methods.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>38317012</pmid><doi>10.1038/s41380-024-02405-y</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-1733-5478</orcidid><orcidid>https://orcid.org/0000-0002-8933-9822</orcidid><orcidid>https://orcid.org/0000-0002-7865-9257</orcidid><orcidid>https://orcid.org/0000-0003-0529-3490</orcidid><orcidid>https://orcid.org/0000-0003-3945-8820</orcidid></addata></record> |
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| subjects | 631/378 692/699/476/1414 9/30 Adult Behavioral Sciences Biological Psychology Brain - physiology Brain - physiopathology Brain Mapping - methods Cortex (insular) Dorsolateral Prefrontal Cortex - physiology Electric Stimulation - methods Electrical stimuli Electrocorticography - methods Evoked Potentials - physiology Female Humans Magnetic fields Male Medicine Medicine & Public Health Middle Aged Neuromodulation Neurosciences Neurosurgery Pharmacotherapy Prefrontal cortex Psychiatry Transcranial magnetic stimulation Transcranial Magnetic Stimulation - methods Young Adult |
| title | Effects of transcranial magnetic stimulation on the human brain recorded with intracranial electrocorticography |
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