Spatiotemporal mapping of epileptic spikes using simultaneous EEG-functional MRI.
Epileptic spikes occur on the sub-second timescale and are known to involve not only epileptic foci but also large-scale distributed brain networks. There is likely to be a sequence of neural activity in multiple brain regions that occurs within the duration of a single spike, but standard electroencephalography-functional magnetic resonance imaging analyses, which use only the timing of the spikes to model the functional magnetic resonance imaging data, cannot determine the sequence of these activations. Our aim in this study is to temporally resolve these spatial activations to observe the spatiotemporal dynamics of the spike-related neural activity at a sub-second timescale. We studied eight focal epilepsy patients (age 11-42 years, six female) and used amplitude features of the electroencephalogram specific to different spike components (early and late peaks and troughs) to encode temporal information into our functional magnetic resonance imaging models. This enables us to associate each activation with a specific model of each of the spike components to infer the temporal order of these spike-related spatial activations. In seven of eight patients the distributed networks were associated with the late spike component. The focal activations were more variably coupled with time epochs, but tended to precede the distributed network effects. We also found that incorporating electroencephalogram features into the models increased sensitivity and in six patients revealed additional regions unseen in the standard analysis result. This included strong bilateral thalamus activation in two patients. We demonstrate the clinical utility of this approach in a patient who recently underwent a successful surgical resection of the region where we saw enhanced activation using electroencephalogram amplitude information specific to the early spike component. This focal cluster of activation was larger and more precisely tracked the anatomy compared to what was seen using the standard timing-based analysis. Our novel electroencephalography-functional magnetic resonance imaging data fusion approach, which utilizes information based on the single spike variability across all electroencephalogram channels, has the potential to help us better understand epileptic networks and aid in the interpretation of functional magnetic resonance imaging activation maps during treatment planning.
The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.
Jennifer M
JM
Walz
The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.|The Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, VIC, Australia.
Mangor
M
Pedersen
The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.
Amir
A
Omidvarnia
The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.
Mira
M
Semmelroch
The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.|The Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, VIC, Australia.|Department of Neurology, Austin Health, Melbourne, VIC, Australia.
Graeme D
GD
Jackson
D000293:Adolescent; D000328:Adult; D001931:Brain Mapping / Q000379:methods*; D002648:Child; D004569:Electroencephalography / Q000379:methods*; D004828:Epilepsies, Partial / Q000000981:diagnostic imaging*; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging / Q000379:methods*; D008297:Male; D008953:Models, Anatomic; D064847:Multimodal Imaging / Q000379:methods*; D009415:Nerve Net / Q000000981:diagnostic imaging; D013788:Thalamus / Q000000981:diagnostic imaging / Q000503:physiopathology; D055815:Young Adult
EEG; amplitude variability; focal epilepsy; functional MRI; spikes