A causal role of anterior prefrontal-putamen circuit for response inhibition revealed by transcranial ultrasound stimulation in humans
Stopping an inappropriate response requires the involvement of the prefrontal-subthalamic hyperdirect pathway. However, how the prefrontal-striatal indirect pathway contributes to stopping is poorly understood. In this study, transcranial ultrasound stimulation is used to perform interventions in a...
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Veröffentlicht in: | Cell reports (Cambridge) 2022-08, Vol.40 (7), p.111197-111197, Article 111197 |
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creator | Nakajima, Koji Osada, Takahiro Ogawa, Akitoshi Tanaka, Masaki Oka, Satoshi Kamagata, Koji Aoki, Shigeki Oshima, Yasushi Tanaka, Sakae Konishi, Seiki |
description | Stopping an inappropriate response requires the involvement of the prefrontal-subthalamic hyperdirect pathway. However, how the prefrontal-striatal indirect pathway contributes to stopping is poorly understood. In this study, transcranial ultrasound stimulation is used to perform interventions in a task-related region in the striatum. Functional magnetic resonance imaging (MRI) reveals activation in the right anterior part of the putamen during response inhibition, and ultrasound stimulation to the anterior putamen, as well as the subthalamic nucleus, results in significant impairments in stopping performance. Diffusion imaging further reveals prominent structural connections between the anterior putamen and the right anterior part of the inferior frontal cortex (IFC), and ultrasound stimulation to the anterior IFC also shows significant impaired stopping performance. These results demonstrate that the right anterior putamen and right anterior IFC causally contribute to stopping and suggest that the anterior IFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping.
[Display omitted]
•The human subthalamic nucleus and striatum are stimulated by ultrasound•The right anterior putamen in the striatum shows a causal contribution to stopping•The right anterior IFC is a cortical counterpart of the anterior putamen•The anterior IFC-anterior putamen circuit works as an essential route for stopping
Nakajima et al. find that ultrasound stimulation to the right anterior putamen and the right anterior inferior frontal cortex (aIFC), a cortical counterpart of the anterior putamen, elicits impaired stopping performance. The aIFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping. |
doi_str_mv | 10.1016/j.celrep.2022.111197 |
format | Article |
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[Display omitted]
•The human subthalamic nucleus and striatum are stimulated by ultrasound•The right anterior putamen in the striatum shows a causal contribution to stopping•The right anterior IFC is a cortical counterpart of the anterior putamen•The anterior IFC-anterior putamen circuit works as an essential route for stopping
Nakajima et al. find that ultrasound stimulation to the right anterior putamen and the right anterior inferior frontal cortex (aIFC), a cortical counterpart of the anterior putamen, elicits impaired stopping performance. The aIFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2022.111197</identifier><language>eng</language><publisher>Elsevier Inc</publisher><subject>basal ganglia ; fMRI ; neuroimaging ; noninvasive brain stimulation ; response inhibition ; stop-signal task ; transcranial ultrasound stimulation ; TUS</subject><ispartof>Cell reports (Cambridge), 2022-08, Vol.40 (7), p.111197-111197, Article 111197</ispartof><rights>2022 The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-1a75b1546f9045f2e17791f4635ea3b20599fe294772bb26b072c0b30c3cf73f3</citedby><cites>FETCH-LOGICAL-c451t-1a75b1546f9045f2e17791f4635ea3b20599fe294772bb26b072c0b30c3cf73f3</cites><orcidid>0000-0002-3743-3200</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,860,27901,27902</link.rule.ids></links><search><creatorcontrib>Nakajima, Koji</creatorcontrib><creatorcontrib>Osada, Takahiro</creatorcontrib><creatorcontrib>Ogawa, Akitoshi</creatorcontrib><creatorcontrib>Tanaka, Masaki</creatorcontrib><creatorcontrib>Oka, Satoshi</creatorcontrib><creatorcontrib>Kamagata, Koji</creatorcontrib><creatorcontrib>Aoki, Shigeki</creatorcontrib><creatorcontrib>Oshima, Yasushi</creatorcontrib><creatorcontrib>Tanaka, Sakae</creatorcontrib><creatorcontrib>Konishi, Seiki</creatorcontrib><title>A causal role of anterior prefrontal-putamen circuit for response inhibition revealed by transcranial ultrasound stimulation in humans</title><title>Cell reports (Cambridge)</title><description>Stopping an inappropriate response requires the involvement of the prefrontal-subthalamic hyperdirect pathway. However, how the prefrontal-striatal indirect pathway contributes to stopping is poorly understood. In this study, transcranial ultrasound stimulation is used to perform interventions in a task-related region in the striatum. Functional magnetic resonance imaging (MRI) reveals activation in the right anterior part of the putamen during response inhibition, and ultrasound stimulation to the anterior putamen, as well as the subthalamic nucleus, results in significant impairments in stopping performance. Diffusion imaging further reveals prominent structural connections between the anterior putamen and the right anterior part of the inferior frontal cortex (IFC), and ultrasound stimulation to the anterior IFC also shows significant impaired stopping performance. These results demonstrate that the right anterior putamen and right anterior IFC causally contribute to stopping and suggest that the anterior IFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping.
[Display omitted]
•The human subthalamic nucleus and striatum are stimulated by ultrasound•The right anterior putamen in the striatum shows a causal contribution to stopping•The right anterior IFC is a cortical counterpart of the anterior putamen•The anterior IFC-anterior putamen circuit works as an essential route for stopping
Nakajima et al. find that ultrasound stimulation to the right anterior putamen and the right anterior inferior frontal cortex (aIFC), a cortical counterpart of the anterior putamen, elicits impaired stopping performance. The aIFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping.</description><subject>basal ganglia</subject><subject>fMRI</subject><subject>neuroimaging</subject><subject>noninvasive brain stimulation</subject><subject>response inhibition</subject><subject>stop-signal task</subject><subject>transcranial ultrasound stimulation</subject><subject>TUS</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kMtOxCAUhhujiROdN3DB0k1HoLTYjYkx3pJJ3OiaUOaQYUKhcplkXsDnlrEuXHkWcIDv_AlfVV0RvCKYdDe7lQIbYFpRTOmKlOr5SbWglJCaUMZP__Tn1TLGHS7V4cKxRfV1j5TMUVoUvAXkNZIuQTA-oCmADt4laespJzmCQ8oElU1CujwHiJN3EZBxWzOYZLwrd3uQFjZoOKAUpIuqLKaEZ1uO0We3QTGZMVv5wxuHtnks3GV1pqWNsPzdL6qPp8f3h5d6_fb8-nC_rhVrSaqJ5O1AWtbpHrNWUyCc90SzrmlBNgPFbd9roD3jnA4D7QbMqcJDg1WjNG90c1Fdz7lT8J8ZYhKjicWflQ58joJy3PS3nDJaUDajKvgYiwsxBTPKcBAEi6N5sROzeXE0L2bzZexuHoPyjb2BIKIy4BRsTACVxMab_wO-AUkdkME</recordid><startdate>20220816</startdate><enddate>20220816</enddate><creator>Nakajima, Koji</creator><creator>Osada, Takahiro</creator><creator>Ogawa, Akitoshi</creator><creator>Tanaka, Masaki</creator><creator>Oka, Satoshi</creator><creator>Kamagata, Koji</creator><creator>Aoki, Shigeki</creator><creator>Oshima, Yasushi</creator><creator>Tanaka, Sakae</creator><creator>Konishi, Seiki</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3743-3200</orcidid></search><sort><creationdate>20220816</creationdate><title>A causal role of anterior prefrontal-putamen circuit for response inhibition revealed by transcranial ultrasound stimulation in humans</title><author>Nakajima, Koji ; Osada, Takahiro ; Ogawa, Akitoshi ; Tanaka, Masaki ; Oka, Satoshi ; Kamagata, Koji ; Aoki, Shigeki ; Oshima, Yasushi ; Tanaka, Sakae ; Konishi, Seiki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-1a75b1546f9045f2e17791f4635ea3b20599fe294772bb26b072c0b30c3cf73f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>basal ganglia</topic><topic>fMRI</topic><topic>neuroimaging</topic><topic>noninvasive brain stimulation</topic><topic>response inhibition</topic><topic>stop-signal task</topic><topic>transcranial ultrasound stimulation</topic><topic>TUS</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nakajima, Koji</creatorcontrib><creatorcontrib>Osada, Takahiro</creatorcontrib><creatorcontrib>Ogawa, Akitoshi</creatorcontrib><creatorcontrib>Tanaka, Masaki</creatorcontrib><creatorcontrib>Oka, Satoshi</creatorcontrib><creatorcontrib>Kamagata, Koji</creatorcontrib><creatorcontrib>Aoki, Shigeki</creatorcontrib><creatorcontrib>Oshima, Yasushi</creatorcontrib><creatorcontrib>Tanaka, Sakae</creatorcontrib><creatorcontrib>Konishi, Seiki</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nakajima, Koji</au><au>Osada, Takahiro</au><au>Ogawa, Akitoshi</au><au>Tanaka, Masaki</au><au>Oka, Satoshi</au><au>Kamagata, Koji</au><au>Aoki, Shigeki</au><au>Oshima, Yasushi</au><au>Tanaka, Sakae</au><au>Konishi, Seiki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A causal role of anterior prefrontal-putamen circuit for response inhibition revealed by transcranial ultrasound stimulation in humans</atitle><jtitle>Cell reports (Cambridge)</jtitle><date>2022-08-16</date><risdate>2022</risdate><volume>40</volume><issue>7</issue><spage>111197</spage><epage>111197</epage><pages>111197-111197</pages><artnum>111197</artnum><issn>2211-1247</issn><eissn>2211-1247</eissn><abstract>Stopping an inappropriate response requires the involvement of the prefrontal-subthalamic hyperdirect pathway. However, how the prefrontal-striatal indirect pathway contributes to stopping is poorly understood. In this study, transcranial ultrasound stimulation is used to perform interventions in a task-related region in the striatum. Functional magnetic resonance imaging (MRI) reveals activation in the right anterior part of the putamen during response inhibition, and ultrasound stimulation to the anterior putamen, as well as the subthalamic nucleus, results in significant impairments in stopping performance. Diffusion imaging further reveals prominent structural connections between the anterior putamen and the right anterior part of the inferior frontal cortex (IFC), and ultrasound stimulation to the anterior IFC also shows significant impaired stopping performance. These results demonstrate that the right anterior putamen and right anterior IFC causally contribute to stopping and suggest that the anterior IFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping.
[Display omitted]
•The human subthalamic nucleus and striatum are stimulated by ultrasound•The right anterior putamen in the striatum shows a causal contribution to stopping•The right anterior IFC is a cortical counterpart of the anterior putamen•The anterior IFC-anterior putamen circuit works as an essential route for stopping
Nakajima et al. find that ultrasound stimulation to the right anterior putamen and the right anterior inferior frontal cortex (aIFC), a cortical counterpart of the anterior putamen, elicits impaired stopping performance. The aIFC-anterior putamen circuit in the indirect pathway serves as an essential route for stopping.</abstract><pub>Elsevier Inc</pub><doi>10.1016/j.celrep.2022.111197</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-3743-3200</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | basal ganglia fMRI neuroimaging noninvasive brain stimulation response inhibition stop-signal task transcranial ultrasound stimulation TUS |
title | A causal role of anterior prefrontal-putamen circuit for response inhibition revealed by transcranial ultrasound stimulation in humans |
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