Dynamic analysis of fMRI activation during epileptic spikes can help identify the seizure origin

Journal article

Kowalczyk, Magdalena A., Omidvarnia, Amir, Dhollander, Thijs and Jackson, Graeme D.. (2020). Dynamic analysis of fMRI activation during epileptic spikes can help identify the seizure origin. Epilepsia. 61(11), pp. 2558-2571. https://doi.org/10.1111/epi.16695
AuthorsKowalczyk, Magdalena A., Omidvarnia, Amir, Dhollander, Thijs and Jackson, Graeme D.
Abstract

Objective
We use the dynamic electroencephalography–functional magnetic resonance imaging (EEG-fMRI) method to incorporate variability in the amplitude and field of the interictal epileptic discharges (IEDs) into the fMRI analysis. We ask whether IED variability analysis can (a) identify additional activated brain regions during the course of IEDs, not seen in standard analysis; and (b) demonstrate the origin and spread of epileptic activity. We explore whether these functional changes recapitulate the structural connections and propagation of epileptic activity during seizures.

Methods
Seventeen patients with focal epilepsy and at least 30 IEDs of a single type during simultaneous EEG-fMRI were studied. IED variability and EEG source imaging (ESI) analysis extracted time-varying dynamic changes. General linear modeling (GLM) generated static functional maps. Dynamic maps were compared to static functional maps. The dynamic sequence from IED variability was compared to the ESI results. In a subset of patients, we investigated structural connections between active brain regions using diffusion-based fiber tractography.

Results
IED variability distinguished the origin of epileptic activity from its propagation in 15 of 17 (88%) patients. This included two cases where no result was obtained from the standard GLM analysis. In both of these cases, IED variability revealed activation in line with the presumed epileptic focus. Two cases showed no result from either method. Both had very high spike rates associated with dysplasia in the postcentral gyrus. In all 15 cases with dynamic activation, the observed dynamics were concordant with ESI. Fiber tractography identified specific white matter pathways between brain regions that were active at IED onset and propagation.

Significance
Dynamic techniques involving IED variability can provide additional power for EEG-fMRI analysis, compared to standard analysis, revealing additional biologically plausible information in cases with no result from the standard analysis and gives insight into the origin and spread of IEDs.

KeywordsEEG; fibre tractography; fMRI; focal epilepsy; IED variability; source imaging
Year2020
JournalEpilepsia
Journal citation61 (11), pp. 2558-2571
PublisherWiley-Blackwell Publishing, Inc.
ISSN1528-1167
Digital Object Identifier (DOI)https://doi.org/10.1111/epi.16695
Scopus EID2-s2.0-85091256756
Research or scholarlyResearch
Page range2558-2571
FunderNational Health and Medical Research Council (NHMRC)
Publisher's version
License
All rights reserved
File Access Level
Controlled
Output statusPublished
Publication dates
Online21 Sep 2020
Publication process dates
Accepted25 Aug 2020
Deposited03 Jul 2021
Grant IDNHMRC/1060312
NHMRC/1091593
Permalink -

https://acuresearchbank.acu.edu.au/item/8w4z2/dynamic-analysis-of-fmri-activation-during-epileptic-spikes-can-help-identify-the-seizure-origin

Log in to edit

Restricted files

Publisher's version

  • 87
    total views
  • 0
    total downloads
  • 0
    views this month
  • 0
    downloads this month
These values are for the period from 19th October 2020, when this repository was created.

Export as

Related outputs

Do mindfulness-based interventions change brain function in people with substance dependence? A systematic review of the fMRI evidence
Lorenzetti, Valentina, Gaillard, Alexandra, Beyer, Emillie, Kowalczyk, Magdalena, Kamboj, Sunjeev K., Manning, Victoria and Gleeson, John Francis Martin. (2023). Do mindfulness-based interventions change brain function in people with substance dependence? A systematic review of the fMRI evidence. BMC Psychiatry. 23(1), p. Article 407. https://doi.org/10.1186/s12888-023-04789-7
Structural network alterations in focal and generalized epilepsy assessed in a worldwide ENIGMA study follow axes of epilepsy risk gene expression
Larivière, Sara, Royer, Jessica, Rodríguez-Cruces, Raúl, Paquola, Casey, Caligiuri, Maria Eugenia, Gambardella, Antonio, Concha, Luis, Keller, Simon S., Cendes, Fernando, Yasuda, Clarissa L., Bonilha, Leonardo, Gleichgerrcht, Ezequiel, Focke, Niels K., Domin, Martin, von Podewills, Felix, Langner, Soenke, Rummel, Christian, Wiest, Roland, Martin, Pascal, ... Bernhardt, Boris C.. (2022). Structural network alterations in focal and generalized epilepsy assessed in a worldwide ENIGMA study follow axes of epilepsy risk gene expression. Nature Communications. 13(1), p. Article 4320. https://doi.org/10.1038/s41467-022-31730-5
Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy
Park, Bo-yong, Larivière, Sara, Rodríguez-Cruces, Raul, Royer, Jessica, Tavakol, Shahin, Wang, Yezhou, Caciagli, Lorenzo, Caligiuri, Maria Eugenia, Gambardella, Antonio, Concha, Luis, Keller, Simon S, Cendes, Fernando, Alvim, Marina K M, Yasuda, Clarissa, Bonilha, Leonardo, Gleichgerrcht, Ezequiel, Focke, Niels K, Kreilkamp, Barbara A K, Domin, Martin, ... Bernhardt, Boris C. (2022). Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy. Brain. 145(4), pp. 1285-1298. https://doi.org/10.1093/brain/awab417
Brain anatomical alterations in young cannabis users : Is it all hype? A meta-analysis of structural neuroimaging studies
Lorenzetti, Valentina, Kowalczyk, Magdalena, Duehlmeyer, Leonie, Greenwood, Lisa-Marie, Chye, Yann, Yücel, Murat, Whittle, Sarah and Roberts, Carl A.. (2022). Brain anatomical alterations in young cannabis users : Is it all hype? A meta-analysis of structural neuroimaging studies. Cannabis and Cannabinoid Research. 8(1), pp. 184-196. https://doi.org/10.1089/can.2021.0099
A systems-level analysis highlights microglial activation as a modifying factor in common epilepsies
Altmann, Andre, Ryten, Mina, Di Nunzio, Martina, Ravizza, Teresa, Tolomeo, Daniele, Reynolds, Regina H., Somani, Alyma, Bacigaluppi, Marco, Iori, Valentina, Micotti, Edoardo, Di Sapia, Rossella, Cerovic, Milica, Palma, Eleonora, Ruffolo, Gabriele, Botía, Juan A., Absil, Julie, Alhusaini, Saud, Alvim, Marina K. M., Auvinen, Pia, ... Sisodiya, Sanjay M.. (2022). A systems-level analysis highlights microglial activation as a modifying factor in common epilepsies. Neuropathology and Applied Neurobiology. 48(1), p. Article e12758. https://doi.org/10.1111/nan.12758
Patterns of brain function associated with cannabis cue-reactivity in regular cannabis users : A systematic review of fMRI studies
Sehl, Hannah, Terrett, Gill, Greenwood, Lisa-Marie, Kowalczyk, Magdalena, Thomson, Hannah, Poudel, Govinda, Manning, Victoria and Lorenzetti, Valentina. (2021). Patterns of brain function associated with cannabis cue-reactivity in regular cannabis users : A systematic review of fMRI studies. Psychopharmacology. 238(10), pp. 2709-2728. https://doi.org/10.1007/s00213-021-05973-x
Do comorbid personality disorders in cocaine dependence exacerbate neuroanatomical alterations? A structural neuroimaging study
Roberts, Carl A., Lorenzetti, Valentina, Albein-Urios, Natalia, Kowalczyk, Magdalena A., Martinez-Gonzalez, Jose M. and Verdejo-Garcia, Antonio. (2021). Do comorbid personality disorders in cocaine dependence exacerbate neuroanatomical alterations? A structural neuroimaging study. Progress in Neuropsychopharmacology and Biological Psychiatry. 110, p. 110298. https://doi.org/10.1016/j.pnpbp.2021.110298
Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study
Larivière, Sara, Rodríguez-Cruces, Raúl, Royer, Jessica, Caligiuri, Maria Eugenia, Gambardella, Antonio, Concha, Luis, Keller, Simon S., Cendes, Fernando, Yasuda, Clarissa, Bonilha, Leonardo, Gleichgerrcht, Ezequiel, Focke, Niels K., Domin, Martin, von Podewills, Felix, Langner, Soenke, Rummel, Christian, Wiest, Roland, Martin, Pascal, Kotikalapudi, Raviteja, ... Bernhardt, Boris C.. (2020). Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study. Science Advances. 6(47), p. eabc6457. https://doi.org/10.1126/sciadv.abc6457
Towards fast and reliable simultaneous EEG-fMRI analysis of epilepsy with automatic spike detection
Omidvarnia, Amir, Kowalczyk, Magdalena A., Pedersen, Mangor and Jackson, Graeme D.. (2019). Towards fast and reliable simultaneous EEG-fMRI analysis of epilepsy with automatic spike detection. Clinical Neurophysiology. 130(3), pp. 368-378. https://doi.org/10.1016/j.clinph.2018.11.024
Normal cerebral cortical thickness in first-degree relatives of temporal lobe epilepsy patients
Alhusaini, Saud, Kowalczyk, Magdalena A., Yasuda, Clarissa L., Semmelroch, Mira K., Katsurayama, Marilise, Zabin, Matheus, Zanão, Tamires, Nogueira, Mateus H., Alvim, Marina K. M., Ferraz, Victória R., Tsai, Meng-Han, Fitzsimons, Mary, Lopes-Cendes, Iscia, Doherty, Colin P., Cavalleri, Gianpiero L., Cendes, Fernando, Jackson, Graeme D. and Delanty, Norman. (2019). Normal cerebral cortical thickness in first-degree relatives of temporal lobe epilepsy patients. Neurology. 92(4), pp. e351-e358. https://doi.org/10.1212/WNL.0000000000006834
Human GABRG2 generalized epilepsy : Increased somatosensory and striato-thalamic connectivity
Pedersen, Mangor, Kowalczyk, Magdalena, Omidvarnia, Amir, Perucca, Piero, Gooley, Samuel, Petrou, Steven, Scheffer, Ingrid E., Berkovic, Samuel F. and Jackson, Graeme D.. (2019). Human GABRG2 generalized epilepsy : Increased somatosensory and striato-thalamic connectivity. Neurology Genetics. 5(4), p. e340. https://doi.org/10.1212/NXG.0000000000000340
Clinical benefit of presurgical EEG-fMRI in difficult-to-localize focal epilepsy : A single-institution retrospective review.
Kowalczyk, Magdalena A., Omidvarnia, Amir, Abbott, David F., Tailby, Chris, Vaughan, David N. and Jackson, Graeme D.. (2019). Clinical benefit of presurgical EEG-fMRI in difficult-to-localize focal epilepsy : A single-institution retrospective review. Epilepsia. 61(1), pp. 49-60. https://doi.org/10.1111/epi.16399
Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study
Whelan, Christopher D., Altmann, Andre, Botía, Juan A., Jahanshad, Neda, Hibar, Derrek P., Absil, Julie, Alhusaini, Saud, Alvim, Marina K. M., Auvinen, Pia, Bartolini, Emanuele, Bergo, Felipe P. G., Bernardes, Tauana, Blackmon, Karen, Braga, Barbara, Caligiuri, Maria Eugenia, Calvo, Anna, Carr, Sarah J., Chen, Jian, Chen, Shuai, ... Sisodiya, Sanjay M.. (2018). Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain: a journal of neurology. 141(2), pp. 391-408. https://doi.org/10.1093/brain/awx341
Cognitive impairment in epilepsy : The role of reduced network flexibility
Tailby, Chris, Kowalczyk, Magdalena A. and Jackson, Graeme D.. (2018). Cognitive impairment in epilepsy : The role of reduced network flexibility. Annals of Clinical and Translational Neurology. 5(1), pp. 29-40. https://doi.org/10.1002/acn3.503
Mapping the verbal semantic memory network before anterior temporal lobectomy using a combination of rTMS and fMRI
Sethi, M., Carney, P., Kowalczyk, M., Pedersen, M., Tailby, C. and Jackosn, G.. (2001). Mapping the verbal semantic memory network before anterior temporal lobectomy using a combination of rTMS and fMRI. Epilepsia. 58(Suppl. 5), p. S182. https://doi.org/10.1111/epi.13944