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Localizing confined epileptic foci in patients with an unclear focus or presumed multifocality using a component-based EEG-fMRI method

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Abstract

Precise localization of epileptic foci is an unavoidable prerequisite in epilepsy surgery. Simultaneous EEG-fMRI recording has recently created new horizons to locate foci in patients with epilepsy and, in comparison with single-modality methods, has yielded more promising results although it is still subject to limitations such as lack of access to information between interictal events. This study assesses its potential added value in the presurgical evaluation of patients with complex source localization. Adult candidates considered ineligible for surgery on account of an unclear focus and/or presumed multifocality on the basis of EEG underwent EEG-fMRI. Adopting a component-based approach, this study attempts to identify the neural behavior of the epileptic generators and detect the components-of-interest which will later be used as input in the GLM model, substituting the classical linear regressor. Twenty-eight sets interictal epileptiform discharges (IED) from nine patients were analyzed. In eight patients, at least one BOLD response was significant, positive and topographically related to the IEDs. These patients were rejected for surgery because of an unclear focus in four, presumed multifocality in three, and a combination of the two conditions in two. Component-based EEG-fMRI improved localization in five out of six patients with unclear foci. In patients with presumed multifocality, component-based EEG-fMRI advocated one of the foci in five patients and confirmed multifocality in one of the patients. In seven patients, component-based EEG-fMRI opened new prospects for surgery and in two of these patients, intracranial EEG supported the EEG-fMRI results. In these complex cases, component-based EEG-fMRI either improved source localization or corroborated a negative decision regarding surgical candidacy. As supported by the statistical findings, the developed EEG-fMRI method leads to a more realistic estimation of localization compared to the conventional EEG-fMRI approach, making it a tool of high value in pre-surgical evaluation of patients with refractory epilepsy. To ensure proper implementation, we have included guidelines for the application of component-based EEG-fMRI in clinical practice.

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Acknowledgments

The EEG-fMRI data used in this study were acquired in the National Brain Mapping Laboratory (NBML), Tehran, Iran. The authors would like to show their gratitude to Dr. Paolo Federico (Department of Clinical Neurosciences, University of Calgary, Calgary, Alberta, Canada) and his group for sharing their pearls of wisdom during the course of this research. They are also immensely grateful to Prof. Ali Moti Nasrabadi and Dr. Negar Mohammadi for their valuable comments, although any errors are of our own and should not tarnish the reputation of these esteemed individuals. The first author also expresses his gratitude to the Cognitive Science and Technologies Council (COGC), Tehran, Iran for their tremendous support.

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Authors and Affiliations

  1. CIPCE, School of Electrical and Computer Engineering, College of Engineering, University of Tehran, North Kargar Ave., Tehran, Iran

    Elias Ebrahimzadeh, Mahya Mirbagheri & Hamid Soltanian-Zadeh

  2. Neural Engineering Laboratory, Department of Electrical and Computer Engineering, George Mason University, Fairfax, VA, USA

    Mohammad Shams

  3. Department of Psychological Sciences, University of California, Merced, CA, USA

    Ali Rahimpour Jounghani

  4. Biomedical Engineering Department, School of Electrical Engineering, Payame Noor University of North Tehran, Tehran, Iran

    Farahnaz Fayaz

  5. Division of Neonatology, Department of Pediatrics at UMCU-Wilhelmina Children’s Hospital, Utrecht, The Netherlands

    Naser Hakimi

  6. School of graduate studies, SUNY Empire State College, Manhattan, NY, USA

    Lila Rajabion

  7. Image Analysis Laboratory, Department of Radiology, Henry Ford Hospital, Detroit, MI, USA

    Hamid Soltanian-Zadeh

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  1. Elias Ebrahimzadeh
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  2. Mohammad Shams
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  3. Ali Rahimpour Jounghani
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  4. Farahnaz Fayaz
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  5. Mahya Mirbagheri
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  6. Naser Hakimi
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  7. Lila Rajabion
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  8. Hamid Soltanian-Zadeh
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Contributions

EE and HS conceived of the presented idea. EE developed the theory and performed the computations. Material preparation, data collection and analysis were performed by EE. The first draft of the manuscript was written by EE, ARJ, FF and all authors commented on previous versions of the manuscript. MSH, LR and HS verified the analytical methods. The visualization and validation were done by MM and NH. All authors provided critical feedback and helped shape the research, analysis and manuscript. All authors read and approved the final manuscript. HS supervised the project.

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Correspondence to Elias Ebrahimzadeh.

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Ebrahimzadeh, E., Shams, M., Rahimpour Jounghani, A. et al. Localizing confined epileptic foci in patients with an unclear focus or presumed multifocality using a component-based EEG-fMRI method. Cogn Neurodyn 15, 207–222 (2021). https://doi.org/10.1007/s11571-020-09614-5

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