Deep brain stimulation induces BOLD activation in motor and non-motor networks: An fMRI comparison study of STN and EN/GPi DBS in large animals
The combination of deep brain stimulation (DBS) and functional MRI (fMRI) is a powerful means of tracing brain circuitry and testing the modulatory effects of electrical stimulation on a neuronal network in vivo. The goal of this study was to trace DBS-induced global neuronal network activation in a...
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| Veröffentlicht in: | NeuroImage (Orlando, Fla.) Fla.), 2012-11, Vol.63 (3), p.1408-1420 |
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| creator | Min, Hoon-Ki Hwang, Sun-Chul Marsh, Michael P. Kim, Inyong Knight, Emily Striemer, Bryan Felmlee, Joel P. Welker, Kirk M. Blaha, Charles D. Chang, Su-Youne Bennet, Kevin E. Lee, Kendall H. |
| description | The combination of deep brain stimulation (DBS) and functional MRI (fMRI) is a powerful means of tracing brain circuitry and testing the modulatory effects of electrical stimulation on a neuronal network in vivo. The goal of this study was to trace DBS-induced global neuronal network activation in a large animal model by monitoring the blood oxygenation level-dependent (BOLD) response on fMRI. We conducted DBS in normal anesthetized pigs, targeting the subthalamic nucleus (STN) (n=7) and the entopeduncular nucleus (EN), the non-primate analog of the primate globus pallidus interna (n=4). Using a normalized functional activation map for group analysis and the application of general linear modeling across subjects, we found that both STN and EN/GPi DBS significantly increased BOLD activation in the ipsilateral sensorimotor network (FDR |
| doi_str_mv | 10.1016/j.neuroimage.2012.08.006 |
| format | Article |
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► First report to set up a fMRI group analysis method for pigs ► STN vs EN/GPi stimulation show common sensorimotor network activation. ► PCA data also show that each target activates a distinctive neural network. ► Swine model may be a useful platform for global neuromodulatory DBS studies.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2012.08.006</identifier><identifier>PMID: 22967832</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Anatomy ; Animal cognition ; Animals ; Behavior ; Brain ; Brain - physiology ; Brain Mapping ; Deep Brain Stimulation ; Deep brain stimulation (DBS) ; Entopeduncular nucleus (EN) ; Experiments ; Functional magnetic resonance imaging (fMRI) ; Globus pallidus interna (GPi) ; Hogs ; Laboratory animals ; Magnetic Resonance Imaging ; Neural circuitry ; Neural networks ; Neural Pathways - physiology ; Parkinson's disease ; Parkinson's disease (PD) ; Pedunculopontine nucleus (PPN) ; Primates ; Studies ; Subthalamic nucleus (STN) ; Swine ; Swine model</subject><ispartof>NeuroImage (Orlando, Fla.), 2012-11, Vol.63 (3), p.1408-1420</ispartof><rights>2012 Elsevier Inc.</rights><rights>Copyright © 2012 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Nov 15, 2012</rights><rights>2012 Elsevier Inc. All rights reserved. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-5df652799d46c8aa683f69175ab54d77988452459e4b9b50359458da2c618f9a3</citedby><cites>FETCH-LOGICAL-c540t-5df652799d46c8aa683f69175ab54d77988452459e4b9b50359458da2c618f9a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/1507245963?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995,64385,64387,64389,72469</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22967832$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Min, Hoon-Ki</creatorcontrib><creatorcontrib>Hwang, Sun-Chul</creatorcontrib><creatorcontrib>Marsh, Michael P.</creatorcontrib><creatorcontrib>Kim, Inyong</creatorcontrib><creatorcontrib>Knight, Emily</creatorcontrib><creatorcontrib>Striemer, Bryan</creatorcontrib><creatorcontrib>Felmlee, Joel P.</creatorcontrib><creatorcontrib>Welker, Kirk M.</creatorcontrib><creatorcontrib>Blaha, Charles D.</creatorcontrib><creatorcontrib>Chang, Su-Youne</creatorcontrib><creatorcontrib>Bennet, Kevin E.</creatorcontrib><creatorcontrib>Lee, Kendall H.</creatorcontrib><title>Deep brain stimulation induces BOLD activation in motor and non-motor networks: An fMRI comparison study of STN and EN/GPi DBS in large animals</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>The combination of deep brain stimulation (DBS) and functional MRI (fMRI) is a powerful means of tracing brain circuitry and testing the modulatory effects of electrical stimulation on a neuronal network in vivo. The goal of this study was to trace DBS-induced global neuronal network activation in a large animal model by monitoring the blood oxygenation level-dependent (BOLD) response on fMRI. We conducted DBS in normal anesthetized pigs, targeting the subthalamic nucleus (STN) (n=7) and the entopeduncular nucleus (EN), the non-primate analog of the primate globus pallidus interna (n=4). Using a normalized functional activation map for group analysis and the application of general linear modeling across subjects, we found that both STN and EN/GPi DBS significantly increased BOLD activation in the ipsilateral sensorimotor network (FDR<0.001). In addition, we found differential, target-specific, non-motor network effects. In each group the activated brain areas showed a distinctive correlation pattern forming a group of network connections. Results suggest that the scope of DBS extends beyond an ablation-like effect and that it may have modulatory effects not only on circuits that facilitate motor function but also on those involved in higher cognitive and emotional processing. Taken together, our results show that the swine model for DBS fMRI, which conforms to human implanted DBS electrode configurations and human neuroanatomy, may be a useful platform for translational studies investigating the global neuromodulatory effects of DBS.
► First report to set up a fMRI group analysis method for pigs ► STN vs EN/GPi stimulation show common sensorimotor network activation. ► PCA data also show that each target activates a distinctive neural network. ► Swine model may be a useful platform for global neuromodulatory DBS studies.</description><subject>Anatomy</subject><subject>Animal cognition</subject><subject>Animals</subject><subject>Behavior</subject><subject>Brain</subject><subject>Brain - physiology</subject><subject>Brain Mapping</subject><subject>Deep Brain Stimulation</subject><subject>Deep brain stimulation (DBS)</subject><subject>Entopeduncular nucleus (EN)</subject><subject>Experiments</subject><subject>Functional magnetic resonance imaging (fMRI)</subject><subject>Globus pallidus interna (GPi)</subject><subject>Hogs</subject><subject>Laboratory animals</subject><subject>Magnetic Resonance Imaging</subject><subject>Neural circuitry</subject><subject>Neural networks</subject><subject>Neural Pathways - physiology</subject><subject>Parkinson's disease</subject><subject>Parkinson's disease (PD)</subject><subject>Pedunculopontine nucleus (PPN)</subject><subject>Primates</subject><subject>Studies</subject><subject>Subthalamic nucleus (STN)</subject><subject>Swine</subject><subject>Swine model</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkk1v1DAQhiMEoqXwF5AlLlyytZ34iwNSt1tKpW2LaDlbju0sXhJ7ayeL-iv4yzhsP4BLT2OPn3k9M3qLAiA4QxDRw_XM2zEG16uVnWGI8AzyGYT0WbGPoCClIAw_n86kKjlCYq94ldIaQihQzV8WexgLyniF94tfC2s3oInKeZAG14-dGlzwwHkzapvA_HK5AEoPbnufB30YQgTKG-CDL3c3b4efIf5IH8CRB-351zOgQ79R0aUw6Y7mFoQWXF1f_Kk7uTg8_eLAYn416XUqrmzO52m69Lp40eZg39zFg-Lbp5Pr48_l8vL07PhoWWpSw6EkpqUEMyFMTTVXivKqpQIxohpSG8YE5zXBNRG2bkRDYEVETbhRWFPEW6Gqg-LjTnczNr012vohqk5uYu4i3sqgnPz3xbvvchW2sqo5IwJmgfd3AjHcjDYNsndJ265T3oYxSUQgZAwhRp9GEcJVJQRDGX33H7oOY_R5E5MgmyaiVab4jtIxpBRt-9A3gnIyiFzLR4PIySAScpkNkkvf_j33Q-G9IzIw3wE2b3_rbJRJO-u1NS5aPUgT3NO__AYJfNEQ</recordid><startdate>20121115</startdate><enddate>20121115</enddate><creator>Min, Hoon-Ki</creator><creator>Hwang, Sun-Chul</creator><creator>Marsh, Michael P.</creator><creator>Kim, Inyong</creator><creator>Knight, Emily</creator><creator>Striemer, Bryan</creator><creator>Felmlee, Joel P.</creator><creator>Welker, Kirk M.</creator><creator>Blaha, Charles D.</creator><creator>Chang, Su-Youne</creator><creator>Bennet, Kevin E.</creator><creator>Lee, Kendall H.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><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>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>7QO</scope><scope>5PM</scope></search><sort><creationdate>20121115</creationdate><title>Deep brain stimulation induces BOLD activation in motor and non-motor networks: An fMRI comparison study of STN and EN/GPi DBS in large animals</title><author>Min, Hoon-Ki ; Hwang, Sun-Chul ; Marsh, Michael P. ; Kim, Inyong ; Knight, Emily ; Striemer, Bryan ; Felmlee, Joel P. ; Welker, Kirk M. ; Blaha, Charles D. ; Chang, Su-Youne ; Bennet, Kevin E. ; Lee, Kendall H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c540t-5df652799d46c8aa683f69175ab54d77988452459e4b9b50359458da2c618f9a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Anatomy</topic><topic>Animal cognition</topic><topic>Animals</topic><topic>Behavior</topic><topic>Brain</topic><topic>Brain - physiology</topic><topic>Brain Mapping</topic><topic>Deep Brain Stimulation</topic><topic>Deep brain stimulation (DBS)</topic><topic>Entopeduncular nucleus (EN)</topic><topic>Experiments</topic><topic>Functional magnetic resonance imaging (fMRI)</topic><topic>Globus pallidus interna (GPi)</topic><topic>Hogs</topic><topic>Laboratory animals</topic><topic>Magnetic Resonance Imaging</topic><topic>Neural circuitry</topic><topic>Neural networks</topic><topic>Neural Pathways - physiology</topic><topic>Parkinson's disease</topic><topic>Parkinson's disease (PD)</topic><topic>Pedunculopontine nucleus (PPN)</topic><topic>Primates</topic><topic>Studies</topic><topic>Subthalamic nucleus (STN)</topic><topic>Swine</topic><topic>Swine model</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Min, Hoon-Ki</creatorcontrib><creatorcontrib>Hwang, Sun-Chul</creatorcontrib><creatorcontrib>Marsh, Michael P.</creatorcontrib><creatorcontrib>Kim, Inyong</creatorcontrib><creatorcontrib>Knight, Emily</creatorcontrib><creatorcontrib>Striemer, Bryan</creatorcontrib><creatorcontrib>Felmlee, Joel P.</creatorcontrib><creatorcontrib>Welker, Kirk M.</creatorcontrib><creatorcontrib>Blaha, Charles D.</creatorcontrib><creatorcontrib>Chang, Su-Youne</creatorcontrib><creatorcontrib>Bennet, Kevin E.</creatorcontrib><creatorcontrib>Lee, Kendall H.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Biotechnology Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Min, Hoon-Ki</au><au>Hwang, Sun-Chul</au><au>Marsh, Michael P.</au><au>Kim, Inyong</au><au>Knight, Emily</au><au>Striemer, Bryan</au><au>Felmlee, Joel P.</au><au>Welker, Kirk M.</au><au>Blaha, Charles D.</au><au>Chang, Su-Youne</au><au>Bennet, Kevin E.</au><au>Lee, Kendall H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Deep brain stimulation induces BOLD activation in motor and non-motor networks: An fMRI comparison study of STN and EN/GPi DBS in large animals</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2012-11-15</date><risdate>2012</risdate><volume>63</volume><issue>3</issue><spage>1408</spage><epage>1420</epage><pages>1408-1420</pages><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>The combination of deep brain stimulation (DBS) and functional MRI (fMRI) is a powerful means of tracing brain circuitry and testing the modulatory effects of electrical stimulation on a neuronal network in vivo. The goal of this study was to trace DBS-induced global neuronal network activation in a large animal model by monitoring the blood oxygenation level-dependent (BOLD) response on fMRI. We conducted DBS in normal anesthetized pigs, targeting the subthalamic nucleus (STN) (n=7) and the entopeduncular nucleus (EN), the non-primate analog of the primate globus pallidus interna (n=4). Using a normalized functional activation map for group analysis and the application of general linear modeling across subjects, we found that both STN and EN/GPi DBS significantly increased BOLD activation in the ipsilateral sensorimotor network (FDR<0.001). In addition, we found differential, target-specific, non-motor network effects. In each group the activated brain areas showed a distinctive correlation pattern forming a group of network connections. Results suggest that the scope of DBS extends beyond an ablation-like effect and that it may have modulatory effects not only on circuits that facilitate motor function but also on those involved in higher cognitive and emotional processing. Taken together, our results show that the swine model for DBS fMRI, which conforms to human implanted DBS electrode configurations and human neuroanatomy, may be a useful platform for translational studies investigating the global neuromodulatory effects of DBS.
► First report to set up a fMRI group analysis method for pigs ► STN vs EN/GPi stimulation show common sensorimotor network activation. ► PCA data also show that each target activates a distinctive neural network. ► Swine model may be a useful platform for global neuromodulatory DBS studies.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22967832</pmid><doi>10.1016/j.neuroimage.2012.08.006</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Anatomy Animal cognition Animals Behavior Brain Brain - physiology Brain Mapping Deep Brain Stimulation Deep brain stimulation (DBS) Entopeduncular nucleus (EN) Experiments Functional magnetic resonance imaging (fMRI) Globus pallidus interna (GPi) Hogs Laboratory animals Magnetic Resonance Imaging Neural circuitry Neural networks Neural Pathways - physiology Parkinson's disease Parkinson's disease (PD) Pedunculopontine nucleus (PPN) Primates Studies Subthalamic nucleus (STN) Swine Swine model |
| title | Deep brain stimulation induces BOLD activation in motor and non-motor networks: An fMRI comparison study of STN and EN/GPi DBS in large animals |
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