Vagal nerve stimulation triggers widespread responses and alters large-scale functional connectivity in the rat brain
Vagus nerve stimulation (VNS) is a therapy for epilepsy and depression. However, its efficacy varies and its mechanism remains unclear. Prior studies have used functional magnetic resonance imaging (fMRI) to map brain activations with VNS in human brains, but have reported inconsistent findings. The...
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| description | Vagus nerve stimulation (VNS) is a therapy for epilepsy and depression. However, its efficacy varies and its mechanism remains unclear. Prior studies have used functional magnetic resonance imaging (fMRI) to map brain activations with VNS in human brains, but have reported inconsistent findings. The source of inconsistency is likely attributable to the complex temporal characteristics of VNS-evoked fMRI responses that cannot be fully explained by simplified response models in the conventional model-based analysis for activation mapping. To address this issue, we acquired 7-Tesla blood oxygenation level dependent fMRI data from anesthetized Sprague-Dawley rats receiving electrical stimulation at the left cervical vagus nerve. Using spatially independent component analysis, we identified 20 functional brain networks and detected the network-wise activations with VNS in a data-driven manner. Our results showed that VNS activated 15 out of 20 brain networks, and the activated regions covered >76% of the brain volume. The time course of the evoked response was complex and distinct across regions and networks. In addition, VNS altered the strengths and patterns of correlations among brain networks relative to those in the resting state. The most notable changes in network-network interactions were related to the limbic system. Together, such profound and widespread effects of VNS may underlie its unique potential for a wide range of therapeutics to relieve central or peripheral conditions. |
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However, its efficacy varies and its mechanism remains unclear. Prior studies have used functional magnetic resonance imaging (fMRI) to map brain activations with VNS in human brains, but have reported inconsistent findings. The source of inconsistency is likely attributable to the complex temporal characteristics of VNS-evoked fMRI responses that cannot be fully explained by simplified response models in the conventional model-based analysis for activation mapping. To address this issue, we acquired 7-Tesla blood oxygenation level dependent fMRI data from anesthetized Sprague-Dawley rats receiving electrical stimulation at the left cervical vagus nerve. Using spatially independent component analysis, we identified 20 functional brain networks and detected the network-wise activations with VNS in a data-driven manner. Our results showed that VNS activated 15 out of 20 brain networks, and the activated regions covered >76% of the brain volume. The time course of the evoked response was complex and distinct across regions and networks. In addition, VNS altered the strengths and patterns of correlations among brain networks relative to those in the resting state. The most notable changes in network-network interactions were related to the limbic system. Together, such profound and widespread effects of VNS may underlie its unique potential for a wide range of therapeutics to relieve central or peripheral conditions.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0189518</identifier><identifier>PMID: 29240833</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal cognition ; Animal models ; Animals ; Biology and Life Sciences ; Biomedical engineering ; Brain ; Brain - diagnostic imaging ; Brain - physiology ; Brain mapping ; Brain Mapping - methods ; Brain research ; Computer and Information Sciences ; Computer engineering ; Electrical stimuli ; Epilepsy ; Evaluation ; Evoked response (psychophysiology) ; Functional magnetic resonance imaging ; Independent component analysis ; Laboratory animals ; Limbic system ; Magnetic resonance ; Magnetic Resonance Imaging ; Male ; Medical imaging ; Medicine and Health Sciences ; Mental depression ; Methods ; Models, Biological ; Networks ; Neural networks ; Neural stimulation ; Neuroimaging ; Neurosciences ; NMR ; Nuclear magnetic resonance ; Oxygenation ; Rats ; Rats, Sprague-Dawley ; Research and Analysis Methods ; Rodents ; Stimulation ; Studies ; Tomography ; Vagus nerve ; Vagus Nerve Stimulation - methods</subject><ispartof>PloS one, 2017-12, Vol.12 (12), p.e0189518-e0189518</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Cao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Cao et al 2017 Cao et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-d814d5fc73023b6383082161d414f861b12a1e4d010f99b5e5effd87376a6793</citedby><cites>FETCH-LOGICAL-c692t-d814d5fc73023b6383082161d414f861b12a1e4d010f99b5e5effd87376a6793</cites><orcidid>0000-0002-8773-4204</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/PMC5730194/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5730194/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29240833$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cao, Jiayue</creatorcontrib><creatorcontrib>Lu, Kun-Han</creatorcontrib><creatorcontrib>Powley, Terry L</creatorcontrib><creatorcontrib>Liu, Zhongming</creatorcontrib><title>Vagal nerve stimulation triggers widespread responses and alters large-scale functional connectivity in the rat brain</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Vagus nerve stimulation (VNS) is a therapy for epilepsy and depression. However, its efficacy varies and its mechanism remains unclear. Prior studies have used functional magnetic resonance imaging (fMRI) to map brain activations with VNS in human brains, but have reported inconsistent findings. The source of inconsistency is likely attributable to the complex temporal characteristics of VNS-evoked fMRI responses that cannot be fully explained by simplified response models in the conventional model-based analysis for activation mapping. To address this issue, we acquired 7-Tesla blood oxygenation level dependent fMRI data from anesthetized Sprague-Dawley rats receiving electrical stimulation at the left cervical vagus nerve. Using spatially independent component analysis, we identified 20 functional brain networks and detected the network-wise activations with VNS in a data-driven manner. Our results showed that VNS activated 15 out of 20 brain networks, and the activated regions covered >76% of the brain volume. The time course of the evoked response was complex and distinct across regions and networks. In addition, VNS altered the strengths and patterns of correlations among brain networks relative to those in the resting state. The most notable changes in network-network interactions were related to the limbic system. Together, such profound and widespread effects of VNS may underlie its unique potential for a wide range of therapeutics to relieve central or peripheral conditions.</description><subject>Animal cognition</subject><subject>Animal models</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Biomedical engineering</subject><subject>Brain</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - physiology</subject><subject>Brain mapping</subject><subject>Brain Mapping - methods</subject><subject>Brain research</subject><subject>Computer and Information Sciences</subject><subject>Computer engineering</subject><subject>Electrical stimuli</subject><subject>Epilepsy</subject><subject>Evaluation</subject><subject>Evoked response (psychophysiology)</subject><subject>Functional magnetic resonance imaging</subject><subject>Independent component analysis</subject><subject>Laboratory animals</subject><subject>Limbic system</subject><subject>Magnetic resonance</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Medicine and Health Sciences</subject><subject>Mental depression</subject><subject>Methods</subject><subject>Models, Biological</subject><subject>Networks</subject><subject>Neural networks</subject><subject>Neural stimulation</subject><subject>Neuroimaging</subject><subject>Neurosciences</subject><subject>NMR</subject><subject>Nuclear magnetic resonance</subject><subject>Oxygenation</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Research and Analysis Methods</subject><subject>Rodents</subject><subject>Stimulation</subject><subject>Studies</subject><subject>Tomography</subject><subject>Vagus nerve</subject><subject>Vagus Nerve Stimulation - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cao, Jiayue</au><au>Lu, Kun-Han</au><au>Powley, Terry L</au><au>Liu, Zhongming</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vagal nerve stimulation triggers widespread responses and alters large-scale functional connectivity in the rat brain</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-12-14</date><risdate>2017</risdate><volume>12</volume><issue>12</issue><spage>e0189518</spage><epage>e0189518</epage><pages>e0189518-e0189518</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Vagus nerve stimulation (VNS) is a therapy for epilepsy and depression. However, its efficacy varies and its mechanism remains unclear. Prior studies have used functional magnetic resonance imaging (fMRI) to map brain activations with VNS in human brains, but have reported inconsistent findings. The source of inconsistency is likely attributable to the complex temporal characteristics of VNS-evoked fMRI responses that cannot be fully explained by simplified response models in the conventional model-based analysis for activation mapping. To address this issue, we acquired 7-Tesla blood oxygenation level dependent fMRI data from anesthetized Sprague-Dawley rats receiving electrical stimulation at the left cervical vagus nerve. Using spatially independent component analysis, we identified 20 functional brain networks and detected the network-wise activations with VNS in a data-driven manner. Our results showed that VNS activated 15 out of 20 brain networks, and the activated regions covered >76% of the brain volume. The time course of the evoked response was complex and distinct across regions and networks. In addition, VNS altered the strengths and patterns of correlations among brain networks relative to those in the resting state. The most notable changes in network-network interactions were related to the limbic system. Together, such profound and widespread effects of VNS may underlie its unique potential for a wide range of therapeutics to relieve central or peripheral conditions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29240833</pmid><doi>10.1371/journal.pone.0189518</doi><tpages>e0189518</tpages><orcidid>https://orcid.org/0000-0002-8773-4204</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animal cognition Animal models Animals Biology and Life Sciences Biomedical engineering Brain Brain - diagnostic imaging Brain - physiology Brain mapping Brain Mapping - methods Brain research Computer and Information Sciences Computer engineering Electrical stimuli Epilepsy Evaluation Evoked response (psychophysiology) Functional magnetic resonance imaging Independent component analysis Laboratory animals Limbic system Magnetic resonance Magnetic Resonance Imaging Male Medical imaging Medicine and Health Sciences Mental depression Methods Models, Biological Networks Neural networks Neural stimulation Neuroimaging Neurosciences NMR Nuclear magnetic resonance Oxygenation Rats Rats, Sprague-Dawley Research and Analysis Methods Rodents Stimulation Studies Tomography Vagus nerve Vagus Nerve Stimulation - methods |
| title | Vagal nerve stimulation triggers widespread responses and alters large-scale functional connectivity in the rat brain |
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