BOLD mapping of human epileptic spikes recorded during simultaneous intracranial EEG-fMRI: The impact of automated spike classification

• Published in: NeuroImage (Orlando, Fla.) Vol. 184; pp. 981 - 992
• Main Authors: Sharma, Niraj K., Pedreira, Carlos, Chaudhary, Umair J., Centeno, Maria, Carmichael, David W., Yadee, Tinonkorn, Murta, Teresa, Diehl, Beate, Lemieux, Louis
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.01.2019; Elsevier Limited; Academic Press
• Subjects: Adult; Automated IED classification; Automation; BOLD response; Brain - physiopathology; Brain mapping; Brain Mapping - methods; Classification; Cluster Analysis; Data processing; Drug resistance; EEG; EEG-fMRI; Electroencephalography - methods; Epilepsy; Epilepsy - physiopathology; Female; Functional magnetic resonance imaging; Humans; IED; Intracranial EEG; Localization; Magnetic Resonance Imaging - methods; Male; Mapping; Motivation; Neurology; Neurosurgery; Pattern Recognition, Automated; Reproducibility of Results; Signal Processing, Computer-Assisted; Studies; Surgery; United Kingdom > UK; Intracranial EEG; Automated IED classification; CED; SED; EEG-fMRI; EZ; icEEG; IED; BOLD response; BOLD; WC
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2018.09.065

Simultaneous intracranial EEG and functional MRI (icEEG-fMRI) can be used to map the haemodynamic (BOLD) changes associated with the generation of IEDs. Unlike scalp EEG-fMRI, in most patients who undergo icEEG-fMRI, IEDs recorded intracranially are numerous and show variability in terms of field amplitude and morphology. Therefore, visual marking can be highly subjective and time consuming. In this study, we applied an automated spike classification algorithm, Wave_clus (WC), to IEDs marked visually on icEEG data acquired during simultaneous fMRI acquisition. The motivation of this work is to determine whether using a potentially more consistent and unbiased automated approach can produce more biologically meaningful BOLD patterns compared to the BOLD patterns obtained based on the conventional, visual classification. We analysed simultaneous icEEG-fMRI data from eight patients with severe drug resistant epilepsy, and who subsequently underwent resective surgery that resulted in a good outcome: confirmed epileptogenic zone (EZ). For each patient two fMRI analyses were performed: one based on the conventional visual IED classification and the other based on the automated classification. We used the concordance of the IED-related BOLD maps with the confirmed EZ as an indication of their biological meaning, which we compared for the automated and visual classifications for all IED originating in the EZ. Across the group, the visual and automated classifications resulted in 32 and 24 EZ IED classes respectively, for which 75% vs 83% of the corresponding BOLD maps were concordant. At the single-subject level, the BOLD maps for the automated approach had greater concordance in four patients, and less concordance in one patient, compared to those obtained using the conventional visual classification, and equal concordance for three remaining patients. These differences did not reach statistical significance. We found automated IED classification on icEEG data recorded during fMRI to be feasible and to result in IED-related BOLD maps that may contain similar or greater biological meaning compared to the conventional approach in the majority of the cases studied. We anticipate that this approach will help to gain significant new insights into the brain networks associated with IEDs and in relation to postsurgical outcome. •IcEEG-fMRI provides a unique insight into the generators of IEDs.•Visual IED marking can be highly subjective and time consuming.•An automated spike classification algorithm, Wave_clus, can minimise subjectivity.•The BOLD maps associated with IEDs classified using Wave_clus may commonly have equal or greater biological meaning than those obtained using conventional, visual classification.