The voxel-wise analysis of false negative fMRI activation in regions of provoked impaired cerebrovascular reactivity
Task-evoked Blood-oxygenation-level-dependent (BOLD-fMRI) signal activation is widely used to interrogate eloquence of brain areas. However, data interpretation can be improved, especially in regions with absent BOLD-fMRI signal activation. Absent BOLD-fMRI signal activation may actually represent f...
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| creator | van Niftrik, Christiaan Hendrik Bas Piccirelli, Marco Muscas, Giovanni Sebök, Martina Fisher, Joseph Arnold Bozinov, Oliver Stippich, Christoph Valavanis, Antonios Regli, Luca Fierstra, Jorn |
| description | Task-evoked Blood-oxygenation-level-dependent (BOLD-fMRI) signal activation is widely used to interrogate eloquence of brain areas. However, data interpretation can be improved, especially in regions with absent BOLD-fMRI signal activation. Absent BOLD-fMRI signal activation may actually represent false-negative activation due to impaired cerebrovascular reactivity (BOLD-CVR) of the vascular bed. The relationship between impaired BOLD-CVR and BOLD-fMRI signal activation may be better studied in healthy subjects where neurovascular coupling is known to be intact. Using a model-based prospective end-tidal carbon dioxide (CO2) targeting algorithm, we performed two controlled 3 tesla BOLD-CVR studies on 17 healthy subjects: 1: at the subjects' individual resting end-tidal CO2 baseline. 2: Around +6.0 mmHg CO2 above the subjects' individual resting baseline. Two BOLD-fMRI finger-tapping experiments were performed at similar normo- and hypercapnic levels. Relative BOLD fMRI signal activation and t-values were calculated for BOLD-CVR and BOLD-fMRI data. For each component of the cerebral motor-network (precentral gyrus, postcentral gyrus, supplementary motor area, cerebellum und fronto-operculum), the correlation between BOLD-CVR and BOLD-fMRI signal changes and t-values was investigated. Finally, a voxel-wise quantitative analysis of the impact of BOLD-CVR on BOLD-fMRI was performed. For the motor-network, the linear correlation coefficient between BOLD-CVR and BOLD-fMRI t-values were significant (p |
| doi_str_mv | 10.1371/journal.pone.0215294 |
| format | Article |
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However, data interpretation can be improved, especially in regions with absent BOLD-fMRI signal activation. Absent BOLD-fMRI signal activation may actually represent false-negative activation due to impaired cerebrovascular reactivity (BOLD-CVR) of the vascular bed. The relationship between impaired BOLD-CVR and BOLD-fMRI signal activation may be better studied in healthy subjects where neurovascular coupling is known to be intact. Using a model-based prospective end-tidal carbon dioxide (CO2) targeting algorithm, we performed two controlled 3 tesla BOLD-CVR studies on 17 healthy subjects: 1: at the subjects' individual resting end-tidal CO2 baseline. 2: Around +6.0 mmHg CO2 above the subjects' individual resting baseline. Two BOLD-fMRI finger-tapping experiments were performed at similar normo- and hypercapnic levels. Relative BOLD fMRI signal activation and t-values were calculated for BOLD-CVR and BOLD-fMRI data. For each component of the cerebral motor-network (precentral gyrus, postcentral gyrus, supplementary motor area, cerebellum und fronto-operculum), the correlation between BOLD-CVR and BOLD-fMRI signal changes and t-values was investigated. Finally, a voxel-wise quantitative analysis of the impact of BOLD-CVR on BOLD-fMRI was performed. For the motor-network, the linear correlation coefficient between BOLD-CVR and BOLD-fMRI t-values were significant (p<0.01) and in the range 0.33-0.55, similar to the correlations between the CVR and fMRI Δ%signal (p<0.05; range 0.34-0.60). The linear relationship between CVR and fMRI is challenged by our voxel-wise analysis of Δ%signal and t-value change between normo- and hypercapnia. Our main finding is that BOLD fMRI signal activation maps are markedly dampened in the presence of impaired BOLD-CVR and highlights the importance of a complementary BOLD-CVR assessment in addition to a task-evoked BOLD fMRI to identify brain areas at risk for false-negative BOLD-fMRI signal activation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0215294</identifier><identifier>PMID: 31059517</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Algorithms ; Biology and Life Sciences ; Brain ; Brain - blood supply ; Brain - diagnostic imaging ; Brain cancer ; Brain mapping ; Carbon dioxide ; Cerebellum ; Cerebrovascular Circulation ; Cerebrovascular disorders ; Computer and Information Sciences ; Correlation ; Correlation coefficient ; Correlation coefficients ; Data interpretation ; Earth Sciences ; Ecology and Environmental Sciences ; Engineering and Technology ; Female ; Functional magnetic resonance imaging ; Humans ; Hypercapnia ; Hypercapnia - diagnostic imaging ; Image Processing, Computer-Assisted ; Impact analysis ; Magnetic resonance imaging ; Magnetic Resonance Imaging - methods ; Male ; Medicine and Health Sciences ; Motor task performance ; Neuroimaging ; Neurosciences ; Neurosurgery ; Neurovascular Coupling ; NMR ; Nuclear magnetic resonance ; Operculum ; Oxygenation ; Physical Sciences ; Postcentral gyrus ; Precentral gyrus ; Quantitative analysis ; Research and Analysis Methods ; Supplementary motor area</subject><ispartof>PloS one, 2019-05, Vol.14 (5), p.e0215294</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 van Niftrik 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>2019 van Niftrik et al 2019 van Niftrik et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c659t-f8d5a47f72baabf093ebc61fe51b672c55aa068ed4229289fa686100a388da623</citedby><cites>FETCH-LOGICAL-c659t-f8d5a47f72baabf093ebc61fe51b672c55aa068ed4229289fa686100a388da623</cites><orcidid>0000-0003-0930-8717 ; 0000-0003-4639-4474</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/PMC6502350/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6502350/$$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/31059517$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van Niftrik, Christiaan Hendrik Bas</creatorcontrib><creatorcontrib>Piccirelli, Marco</creatorcontrib><creatorcontrib>Muscas, Giovanni</creatorcontrib><creatorcontrib>Sebök, Martina</creatorcontrib><creatorcontrib>Fisher, Joseph Arnold</creatorcontrib><creatorcontrib>Bozinov, Oliver</creatorcontrib><creatorcontrib>Stippich, Christoph</creatorcontrib><creatorcontrib>Valavanis, Antonios</creatorcontrib><creatorcontrib>Regli, Luca</creatorcontrib><creatorcontrib>Fierstra, Jorn</creatorcontrib><title>The voxel-wise analysis of false negative fMRI activation in regions of provoked impaired cerebrovascular reactivity</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Task-evoked Blood-oxygenation-level-dependent (BOLD-fMRI) signal activation is widely used to interrogate eloquence of brain areas. However, data interpretation can be improved, especially in regions with absent BOLD-fMRI signal activation. Absent BOLD-fMRI signal activation may actually represent false-negative activation due to impaired cerebrovascular reactivity (BOLD-CVR) of the vascular bed. The relationship between impaired BOLD-CVR and BOLD-fMRI signal activation may be better studied in healthy subjects where neurovascular coupling is known to be intact. Using a model-based prospective end-tidal carbon dioxide (CO2) targeting algorithm, we performed two controlled 3 tesla BOLD-CVR studies on 17 healthy subjects: 1: at the subjects' individual resting end-tidal CO2 baseline. 2: Around +6.0 mmHg CO2 above the subjects' individual resting baseline. Two BOLD-fMRI finger-tapping experiments were performed at similar normo- and hypercapnic levels. Relative BOLD fMRI signal activation and t-values were calculated for BOLD-CVR and BOLD-fMRI data. For each component of the cerebral motor-network (precentral gyrus, postcentral gyrus, supplementary motor area, cerebellum und fronto-operculum), the correlation between BOLD-CVR and BOLD-fMRI signal changes and t-values was investigated. Finally, a voxel-wise quantitative analysis of the impact of BOLD-CVR on BOLD-fMRI was performed. For the motor-network, the linear correlation coefficient between BOLD-CVR and BOLD-fMRI t-values were significant (p<0.01) and in the range 0.33-0.55, similar to the correlations between the CVR and fMRI Δ%signal (p<0.05; range 0.34-0.60). The linear relationship between CVR and fMRI is challenged by our voxel-wise analysis of Δ%signal and t-value change between normo- and hypercapnia. Our main finding is that BOLD fMRI signal activation maps are markedly dampened in the presence of impaired BOLD-CVR and highlights the importance of a complementary BOLD-CVR assessment in addition to a task-evoked BOLD fMRI to identify brain areas at risk for false-negative BOLD-fMRI signal activation.</description><subject>Adult</subject><subject>Algorithms</subject><subject>Biology and Life Sciences</subject><subject>Brain</subject><subject>Brain - blood supply</subject><subject>Brain - diagnostic imaging</subject><subject>Brain cancer</subject><subject>Brain mapping</subject><subject>Carbon dioxide</subject><subject>Cerebellum</subject><subject>Cerebrovascular Circulation</subject><subject>Cerebrovascular disorders</subject><subject>Computer and Information Sciences</subject><subject>Correlation</subject><subject>Correlation coefficient</subject><subject>Correlation coefficients</subject><subject>Data interpretation</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Engineering and Technology</subject><subject>Female</subject><subject>Functional magnetic resonance imaging</subject><subject>Humans</subject><subject>Hypercapnia</subject><subject>Hypercapnia - 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However, data interpretation can be improved, especially in regions with absent BOLD-fMRI signal activation. Absent BOLD-fMRI signal activation may actually represent false-negative activation due to impaired cerebrovascular reactivity (BOLD-CVR) of the vascular bed. The relationship between impaired BOLD-CVR and BOLD-fMRI signal activation may be better studied in healthy subjects where neurovascular coupling is known to be intact. Using a model-based prospective end-tidal carbon dioxide (CO2) targeting algorithm, we performed two controlled 3 tesla BOLD-CVR studies on 17 healthy subjects: 1: at the subjects' individual resting end-tidal CO2 baseline. 2: Around +6.0 mmHg CO2 above the subjects' individual resting baseline. Two BOLD-fMRI finger-tapping experiments were performed at similar normo- and hypercapnic levels. Relative BOLD fMRI signal activation and t-values were calculated for BOLD-CVR and BOLD-fMRI data. For each component of the cerebral motor-network (precentral gyrus, postcentral gyrus, supplementary motor area, cerebellum und fronto-operculum), the correlation between BOLD-CVR and BOLD-fMRI signal changes and t-values was investigated. Finally, a voxel-wise quantitative analysis of the impact of BOLD-CVR on BOLD-fMRI was performed. For the motor-network, the linear correlation coefficient between BOLD-CVR and BOLD-fMRI t-values were significant (p<0.01) and in the range 0.33-0.55, similar to the correlations between the CVR and fMRI Δ%signal (p<0.05; range 0.34-0.60). The linear relationship between CVR and fMRI is challenged by our voxel-wise analysis of Δ%signal and t-value change between normo- and hypercapnia. Our main finding is that BOLD fMRI signal activation maps are markedly dampened in the presence of impaired BOLD-CVR and highlights the importance of a complementary BOLD-CVR assessment in addition to a task-evoked BOLD fMRI to identify brain areas at risk for false-negative BOLD-fMRI signal activation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31059517</pmid><doi>10.1371/journal.pone.0215294</doi><tpages>e0215294</tpages><orcidid>https://orcid.org/0000-0003-0930-8717</orcidid><orcidid>https://orcid.org/0000-0003-4639-4474</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2019-05, Vol.14 (5), p.e0215294 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2221080779 |
| source | PLoS; MEDLINE; PubMed Central; Directory of Open Access Journals; Free Full-Text Journals in Chemistry; EZB Electronic Journals Library |
| subjects | Adult Algorithms Biology and Life Sciences Brain Brain - blood supply Brain - diagnostic imaging Brain cancer Brain mapping Carbon dioxide Cerebellum Cerebrovascular Circulation Cerebrovascular disorders Computer and Information Sciences Correlation Correlation coefficient Correlation coefficients Data interpretation Earth Sciences Ecology and Environmental Sciences Engineering and Technology Female Functional magnetic resonance imaging Humans Hypercapnia Hypercapnia - diagnostic imaging Image Processing, Computer-Assisted Impact analysis Magnetic resonance imaging Magnetic Resonance Imaging - methods Male Medicine and Health Sciences Motor task performance Neuroimaging Neurosciences Neurosurgery Neurovascular Coupling NMR Nuclear magnetic resonance Operculum Oxygenation Physical Sciences Postcentral gyrus Precentral gyrus Quantitative analysis Research and Analysis Methods Supplementary motor area |
| title | The voxel-wise analysis of false negative fMRI activation in regions of provoked impaired cerebrovascular reactivity |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-12T04%3A17%3A52IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20voxel-wise%20analysis%20of%20false%20negative%20fMRI%20activation%20in%20regions%20of%20provoked%20impaired%20cerebrovascular%20reactivity&rft.jtitle=PloS%20one&rft.au=van%20Niftrik,%20Christiaan%20Hendrik%20Bas&rft.date=2019-05-06&rft.volume=14&rft.issue=5&rft.spage=e0215294&rft.pages=e0215294-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0215294&rft_dat=%3Cgale_plos_%3EA584560736%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2221080779&rft_id=info:pmid/31059517&rft_galeid=A584560736&rft_doaj_id=oai_doaj_org_article_3059f75c00964c208b54ca458899fce0&rfr_iscdi=true |