Intracranial EEG-fMRI analysis of focal epileptiform discharges in humans

Summary Purpose:  Combining intracranial electroencephalography (iEEG) with functional magnetic resonance imaging (fMRI) is of interest in epilepsy studies as it would allow the detection of much smaller interictal epileptiform discharges than can be recorded using scalp EEG‐fMRI. This may help eluc...

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Veröffentlicht in:Epilepsia (Copenhagen) 2012-09, Vol.53 (9), p.1636-1648
Hauptverfasser: Cunningham, Cameron B. J., Goodyear, Bradley G., Badawy, Radwa, Zaamout, Fateh, Pittman, Daniel J., Beers, Craig A., Federico, Paolo
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container_end_page 1648
container_issue 9
container_start_page 1636
container_title Epilepsia (Copenhagen)
container_volume 53
creator Cunningham, Cameron B. J.
Goodyear, Bradley G.
Badawy, Radwa
Zaamout, Fateh
Pittman, Daniel J.
Beers, Craig A.
Federico, Paolo
description Summary Purpose:  Combining intracranial electroencephalography (iEEG) with functional magnetic resonance imaging (fMRI) is of interest in epilepsy studies as it would allow the detection of much smaller interictal epileptiform discharges than can be recorded using scalp EEG‐fMRI. This may help elucidate the spatiotemporal mechanisms underlying the generation of interictal discharges. To our knowledge, iEEG‐fMRI has never been performed at 3 Tesla (3T) in humans. We report our findings relating to spike‐associated blood oxygen level–dependent (BOLD) signal changes in two subjects. Methods:  iEEG‐fMRI at 3T was performed in two subjects. Twelve channels of iEEG were recorded from subdural strips implanted on the left posterior temporal and middle frontal lobes in a 20‐year‐old female with bilateral periventricular gray matter heterotopia. Twenty channels of iEEG were recorded bilaterally from two subdural strips laid anterior–posterior along mesial temporal surfaces in a 29‐year‐old woman with bilateral temporal seizures and mild left amygdalar enlargement on MRI. Functional MRI (fMRI) statistical maps were generated and thresholded at p = 0.01. Key Findings:  No adverse events were noted. A total of 105 interictal discharges were recorded in the posterior middle temporal gyrus of Subject 1. In Subject 2, 478 discharges were recorded from both mesial temporal surfaces (n = 194 left, 284 right). The right and left discharges were modeled separately, as they were independent. Subject 1 showed spike‐associated BOLD signal increases in the left superior temporal region, left middle frontal gyrus, and right parietal lobe. BOLD decreases were seen in the right frontal and parietal lobes. In Subject 2, BOLD signal increases were seen in both mesial temporal lobes, which when left and right spikes were modeled independently, were greater on the side of the discharge. In addition, striking BOLD signal decreases were observed in the thalamus and posterior cingulate gyrus. Significance:  iEEG‐fMRI can be performed at 3T with low risk. Notably, runs of only 5 or 10 min of EEG‐fMRI were performed as part of our implementation protocol, yet a significant number of epileptiform discharges were recorded, allowing meaningful analyses. With these studies, we have shown that deactivation can be seen in individual subjects with focal epileptiform discharges. These preliminary observations suggest a novel mechanism through which focal interictal discharges may have widespread c
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J. ; Goodyear, Bradley G. ; Badawy, Radwa ; Zaamout, Fateh ; Pittman, Daniel J. ; Beers, Craig A. ; Federico, Paolo</creator><creatorcontrib>Cunningham, Cameron B. J. ; Goodyear, Bradley G. ; Badawy, Radwa ; Zaamout, Fateh ; Pittman, Daniel J. ; Beers, Craig A. ; Federico, Paolo</creatorcontrib><description>Summary Purpose:  Combining intracranial electroencephalography (iEEG) with functional magnetic resonance imaging (fMRI) is of interest in epilepsy studies as it would allow the detection of much smaller interictal epileptiform discharges than can be recorded using scalp EEG‐fMRI. This may help elucidate the spatiotemporal mechanisms underlying the generation of interictal discharges. To our knowledge, iEEG‐fMRI has never been performed at 3 Tesla (3T) in humans. We report our findings relating to spike‐associated blood oxygen level–dependent (BOLD) signal changes in two subjects. Methods:  iEEG‐fMRI at 3T was performed in two subjects. Twelve channels of iEEG were recorded from subdural strips implanted on the left posterior temporal and middle frontal lobes in a 20‐year‐old female with bilateral periventricular gray matter heterotopia. Twenty channels of iEEG were recorded bilaterally from two subdural strips laid anterior–posterior along mesial temporal surfaces in a 29‐year‐old woman with bilateral temporal seizures and mild left amygdalar enlargement on MRI. Functional MRI (fMRI) statistical maps were generated and thresholded at p = 0.01. Key Findings:  No adverse events were noted. A total of 105 interictal discharges were recorded in the posterior middle temporal gyrus of Subject 1. In Subject 2, 478 discharges were recorded from both mesial temporal surfaces (n = 194 left, 284 right). The right and left discharges were modeled separately, as they were independent. Subject 1 showed spike‐associated BOLD signal increases in the left superior temporal region, left middle frontal gyrus, and right parietal lobe. BOLD decreases were seen in the right frontal and parietal lobes. In Subject 2, BOLD signal increases were seen in both mesial temporal lobes, which when left and right spikes were modeled independently, were greater on the side of the discharge. In addition, striking BOLD signal decreases were observed in the thalamus and posterior cingulate gyrus. Significance:  iEEG‐fMRI can be performed at 3T with low risk. Notably, runs of only 5 or 10 min of EEG‐fMRI were performed as part of our implementation protocol, yet a significant number of epileptiform discharges were recorded, allowing meaningful analyses. With these studies, we have shown that deactivation can be seen in individual subjects with focal epileptiform discharges. 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Electric activity recording ; Electroencephalography ; Electroencephalography - instrumentation ; Electroencephalography - methods ; Epilepsies, Partial - diagnosis ; Epilepsies, Partial - metabolism ; Epilepsies, Partial - physiopathology ; Epilepsy ; Female ; Firing pattern ; Focal epilepsy ; frontal gyrus ; Frontal lobe ; Functional magnetic resonance imaging ; Functional MRI ; Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy ; Humans ; Intracranial EEG ; Investigative techniques, diagnostic techniques (general aspects) ; Magnetic Resonance Imaging - instrumentation ; Magnetic Resonance Imaging - methods ; Medical sciences ; Nervous system ; Nervous system (semeiology, syndromes) ; Neurology ; NMR ; Nuclear magnetic resonance ; Oxygen ; Parietal lobe ; Risk factors ; Scalp ; Seizures ; Statistics ; Substantia grisea ; temporal gyrus ; Temporal lobe ; Thalamus ; Young Adult</subject><ispartof>Epilepsia (Copenhagen), 2012-09, Vol.53 (9), p.1636-1648</ispartof><rights>Wiley Periodicals, Inc. © 2012 International League Against Epilepsy</rights><rights>2015 INIST-CNRS</rights><rights>Wiley Periodicals, Inc. © 2012 International League Against Epilepsy.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5641-f7f237a6fb931010886cd10206afada856417a758fe97e628ca50e06b5ab089b3</citedby><cites>FETCH-LOGICAL-c5641-f7f237a6fb931010886cd10206afada856417a758fe97e628ca50e06b5ab089b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1528-1167.2012.03601.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1528-1167.2012.03601.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=26389605$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22881457$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cunningham, Cameron B. J.</creatorcontrib><creatorcontrib>Goodyear, Bradley G.</creatorcontrib><creatorcontrib>Badawy, Radwa</creatorcontrib><creatorcontrib>Zaamout, Fateh</creatorcontrib><creatorcontrib>Pittman, Daniel J.</creatorcontrib><creatorcontrib>Beers, Craig A.</creatorcontrib><creatorcontrib>Federico, Paolo</creatorcontrib><title>Intracranial EEG-fMRI analysis of focal epileptiform discharges in humans</title><title>Epilepsia (Copenhagen)</title><addtitle>Epilepsia</addtitle><description>Summary Purpose:  Combining intracranial electroencephalography (iEEG) with functional magnetic resonance imaging (fMRI) is of interest in epilepsy studies as it would allow the detection of much smaller interictal epileptiform discharges than can be recorded using scalp EEG‐fMRI. This may help elucidate the spatiotemporal mechanisms underlying the generation of interictal discharges. To our knowledge, iEEG‐fMRI has never been performed at 3 Tesla (3T) in humans. We report our findings relating to spike‐associated blood oxygen level–dependent (BOLD) signal changes in two subjects. Methods:  iEEG‐fMRI at 3T was performed in two subjects. Twelve channels of iEEG were recorded from subdural strips implanted on the left posterior temporal and middle frontal lobes in a 20‐year‐old female with bilateral periventricular gray matter heterotopia. Twenty channels of iEEG were recorded bilaterally from two subdural strips laid anterior–posterior along mesial temporal surfaces in a 29‐year‐old woman with bilateral temporal seizures and mild left amygdalar enlargement on MRI. Functional MRI (fMRI) statistical maps were generated and thresholded at p = 0.01. Key Findings:  No adverse events were noted. A total of 105 interictal discharges were recorded in the posterior middle temporal gyrus of Subject 1. In Subject 2, 478 discharges were recorded from both mesial temporal surfaces (n = 194 left, 284 right). The right and left discharges were modeled separately, as they were independent. Subject 1 showed spike‐associated BOLD signal increases in the left superior temporal region, left middle frontal gyrus, and right parietal lobe. BOLD decreases were seen in the right frontal and parietal lobes. In Subject 2, BOLD signal increases were seen in both mesial temporal lobes, which when left and right spikes were modeled independently, were greater on the side of the discharge. In addition, striking BOLD signal decreases were observed in the thalamus and posterior cingulate gyrus. Significance:  iEEG‐fMRI can be performed at 3T with low risk. Notably, runs of only 5 or 10 min of EEG‐fMRI were performed as part of our implementation protocol, yet a significant number of epileptiform discharges were recorded, allowing meaningful analyses. With these studies, we have shown that deactivation can be seen in individual subjects with focal epileptiform discharges. These preliminary observations suggest a novel mechanism through which focal interictal discharges may have widespread cortical and subcortical influences.</description><subject>Adult</subject><subject>Biological and medical sciences</subject><subject>Brain</subject><subject>Brain - metabolism</subject><subject>Brain - physiopathology</subject><subject>Cortex</subject><subject>Deactivation</subject><subject>EEG</subject><subject>EEG-fMRI</subject><subject>Electrodes, Implanted</subject><subject>Electrodiagnosis. Electric activity recording</subject><subject>Electroencephalography</subject><subject>Electroencephalography - instrumentation</subject><subject>Electroencephalography - methods</subject><subject>Epilepsies, Partial - diagnosis</subject><subject>Epilepsies, Partial - metabolism</subject><subject>Epilepsies, Partial - physiopathology</subject><subject>Epilepsy</subject><subject>Female</subject><subject>Firing pattern</subject><subject>Focal epilepsy</subject><subject>frontal gyrus</subject><subject>Frontal lobe</subject><subject>Functional magnetic resonance imaging</subject><subject>Functional MRI</subject><subject>Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy</subject><subject>Humans</subject><subject>Intracranial EEG</subject><subject>Investigative techniques, diagnostic techniques (general aspects)</subject><subject>Magnetic Resonance Imaging - instrumentation</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Medical sciences</subject><subject>Nervous system</subject><subject>Nervous system (semeiology, syndromes)</subject><subject>Neurology</subject><subject>NMR</subject><subject>Nuclear magnetic resonance</subject><subject>Oxygen</subject><subject>Parietal lobe</subject><subject>Risk factors</subject><subject>Scalp</subject><subject>Seizures</subject><subject>Statistics</subject><subject>Substantia grisea</subject><subject>temporal gyrus</subject><subject>Temporal lobe</subject><subject>Thalamus</subject><subject>Young Adult</subject><issn>0013-9580</issn><issn>1528-1167</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkl2LEzEUhoMobl39CzIggjczniTNx1x4oWutA7t-oSx4E85MEzd1PmrSwfbfm9nWCl5tbhI4z3tyyBNCMgoFTevluqCC6ZxSqQoGlBXAJdBid4_MToX7ZAZAeV4KDWfkUYxrAFBS8YfkjDGt6VyoGamqfhuwCdh7bLPFYpm7qy9Vhj22--hjNrjMDU0q2Y1v7Wbr3RC6bOVjc4Phh42Z77ObscM-PiYPHLbRPjnu5-Tbu8XXi_f55cdldfH6Mm-EnNPcKce4QunqklOgoLVsVhQYSHS4Qj1BCpXQzpbKSqYbFGBB1gJr0GXNz8mLQ99NGH6NNm5Nl6axbYu9HcZoKJR8LlMDdQeUa0mlECyhz_5D18MY0iskSlDFJGUgEqUPVBOGGIN1ZhN8h2GfWpnJjFmbSYCZBJjJjLk1Y3Yp-vR4wVh3dnUK_lWRgOdHAGN6cJeUND7-4yTXpbyd4dWB-52E7O88gFl8qqZTyueHvI9buzvlMfw06XMoYa4_LM2b689v4bu-Moz_AQ7VtXA</recordid><startdate>201209</startdate><enddate>201209</enddate><creator>Cunningham, Cameron B. J.</creator><creator>Goodyear, Bradley G.</creator><creator>Badawy, Radwa</creator><creator>Zaamout, Fateh</creator><creator>Pittman, Daniel J.</creator><creator>Beers, Craig A.</creator><creator>Federico, Paolo</creator><general>Blackwell Publishing Ltd</general><general>Wiley-Blackwell</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>IQODW</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>7TK</scope><scope>7X8</scope></search><sort><creationdate>201209</creationdate><title>Intracranial EEG-fMRI analysis of focal epileptiform discharges in humans</title><author>Cunningham, Cameron B. J. ; Goodyear, Bradley G. ; Badawy, Radwa ; Zaamout, Fateh ; Pittman, Daniel J. ; Beers, Craig A. ; Federico, Paolo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5641-f7f237a6fb931010886cd10206afada856417a758fe97e628ca50e06b5ab089b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adult</topic><topic>Biological and medical sciences</topic><topic>Brain</topic><topic>Brain - metabolism</topic><topic>Brain - physiopathology</topic><topic>Cortex</topic><topic>Deactivation</topic><topic>EEG</topic><topic>EEG-fMRI</topic><topic>Electrodes, Implanted</topic><topic>Electrodiagnosis. Electric activity recording</topic><topic>Electroencephalography</topic><topic>Electroencephalography - instrumentation</topic><topic>Electroencephalography - methods</topic><topic>Epilepsies, Partial - diagnosis</topic><topic>Epilepsies, Partial - metabolism</topic><topic>Epilepsies, Partial - physiopathology</topic><topic>Epilepsy</topic><topic>Female</topic><topic>Firing pattern</topic><topic>Focal epilepsy</topic><topic>frontal gyrus</topic><topic>Frontal lobe</topic><topic>Functional magnetic resonance imaging</topic><topic>Functional MRI</topic><topic>Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy</topic><topic>Humans</topic><topic>Intracranial EEG</topic><topic>Investigative techniques, diagnostic techniques (general aspects)</topic><topic>Magnetic Resonance Imaging - instrumentation</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Medical sciences</topic><topic>Nervous system</topic><topic>Nervous system (semeiology, syndromes)</topic><topic>Neurology</topic><topic>NMR</topic><topic>Nuclear magnetic resonance</topic><topic>Oxygen</topic><topic>Parietal lobe</topic><topic>Risk factors</topic><topic>Scalp</topic><topic>Seizures</topic><topic>Statistics</topic><topic>Substantia grisea</topic><topic>temporal gyrus</topic><topic>Temporal lobe</topic><topic>Thalamus</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cunningham, Cameron B. J.</creatorcontrib><creatorcontrib>Goodyear, Bradley G.</creatorcontrib><creatorcontrib>Badawy, Radwa</creatorcontrib><creatorcontrib>Zaamout, Fateh</creatorcontrib><creatorcontrib>Pittman, Daniel J.</creatorcontrib><creatorcontrib>Beers, Craig A.</creatorcontrib><creatorcontrib>Federico, Paolo</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><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>MEDLINE - Academic</collection><jtitle>Epilepsia (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cunningham, Cameron B. J.</au><au>Goodyear, Bradley G.</au><au>Badawy, Radwa</au><au>Zaamout, Fateh</au><au>Pittman, Daniel J.</au><au>Beers, Craig A.</au><au>Federico, Paolo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intracranial EEG-fMRI analysis of focal epileptiform discharges in humans</atitle><jtitle>Epilepsia (Copenhagen)</jtitle><addtitle>Epilepsia</addtitle><date>2012-09</date><risdate>2012</risdate><volume>53</volume><issue>9</issue><spage>1636</spage><epage>1648</epage><pages>1636-1648</pages><issn>0013-9580</issn><eissn>1528-1167</eissn><coden>EPILAK</coden><abstract>Summary Purpose:  Combining intracranial electroencephalography (iEEG) with functional magnetic resonance imaging (fMRI) is of interest in epilepsy studies as it would allow the detection of much smaller interictal epileptiform discharges than can be recorded using scalp EEG‐fMRI. This may help elucidate the spatiotemporal mechanisms underlying the generation of interictal discharges. To our knowledge, iEEG‐fMRI has never been performed at 3 Tesla (3T) in humans. We report our findings relating to spike‐associated blood oxygen level–dependent (BOLD) signal changes in two subjects. Methods:  iEEG‐fMRI at 3T was performed in two subjects. Twelve channels of iEEG were recorded from subdural strips implanted on the left posterior temporal and middle frontal lobes in a 20‐year‐old female with bilateral periventricular gray matter heterotopia. Twenty channels of iEEG were recorded bilaterally from two subdural strips laid anterior–posterior along mesial temporal surfaces in a 29‐year‐old woman with bilateral temporal seizures and mild left amygdalar enlargement on MRI. Functional MRI (fMRI) statistical maps were generated and thresholded at p = 0.01. Key Findings:  No adverse events were noted. A total of 105 interictal discharges were recorded in the posterior middle temporal gyrus of Subject 1. In Subject 2, 478 discharges were recorded from both mesial temporal surfaces (n = 194 left, 284 right). The right and left discharges were modeled separately, as they were independent. Subject 1 showed spike‐associated BOLD signal increases in the left superior temporal region, left middle frontal gyrus, and right parietal lobe. BOLD decreases were seen in the right frontal and parietal lobes. In Subject 2, BOLD signal increases were seen in both mesial temporal lobes, which when left and right spikes were modeled independently, were greater on the side of the discharge. In addition, striking BOLD signal decreases were observed in the thalamus and posterior cingulate gyrus. Significance:  iEEG‐fMRI can be performed at 3T with low risk. Notably, runs of only 5 or 10 min of EEG‐fMRI were performed as part of our implementation protocol, yet a significant number of epileptiform discharges were recorded, allowing meaningful analyses. With these studies, we have shown that deactivation can be seen in individual subjects with focal epileptiform discharges. These preliminary observations suggest a novel mechanism through which focal interictal discharges may have widespread cortical and subcortical influences.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22881457</pmid><doi>10.1111/j.1528-1167.2012.03601.x</doi><tpages>13</tpages></addata></record>
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subjects Adult
Biological and medical sciences
Brain
Brain - metabolism
Brain - physiopathology
Cortex
Deactivation
EEG
EEG-fMRI
Electrodes, Implanted
Electrodiagnosis. Electric activity recording
Electroencephalography
Electroencephalography - instrumentation
Electroencephalography - methods
Epilepsies, Partial - diagnosis
Epilepsies, Partial - metabolism
Epilepsies, Partial - physiopathology
Epilepsy
Female
Firing pattern
Focal epilepsy
frontal gyrus
Frontal lobe
Functional magnetic resonance imaging
Functional MRI
Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy
Humans
Intracranial EEG
Investigative techniques, diagnostic techniques (general aspects)
Magnetic Resonance Imaging - instrumentation
Magnetic Resonance Imaging - methods
Medical sciences
Nervous system
Nervous system (semeiology, syndromes)
Neurology
NMR
Nuclear magnetic resonance
Oxygen
Parietal lobe
Risk factors
Scalp
Seizures
Statistics
Substantia grisea
temporal gyrus
Temporal lobe
Thalamus
Young Adult
title Intracranial EEG-fMRI analysis of focal epileptiform discharges in humans
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