Cross-scale effects of neural interactions during human neocortical seizure activity

Small-scale neuronal networks may impose widespread effects on large network dynamics. To unravel this relationship, we analyzed eight multiscale recordings of spontaneous seizures from four patients with epilepsy. During seizures, multiunit spike activity organizes into a submillimeter-sized wavefr...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2017-10, Vol.114 (40), p.10761-10766
Main Authors: Eissa, Tahra L., Dijkstra, Koen, Brune, Christoph, Emerson, Ronald G., van Putten, Michel J. A. M., Goodman, Robert R., McKhann, Guy M., Schevon, Catherine A., van Drongelen, Wim, van Gils, Stephan A.
Format: Article
Language:English
Subjects:
Action potential
Action Potentials - physiology
Bifurcations
Biological Sciences
Brain Waves - physiology
Convulsions & seizures
Drug Resistant Epilepsy - physiopathology
Electroencephalography
Epilepsies, Partial - physiopathology
Epilepsy
Firing pattern
Humans
Inhibition
Multiscale analysis
Neocortex
Neocortex - physiopathology
Neural networks
Nonlinear systems
Physical Sciences
Seizing
Seizures
Seizures - physiopathology
Territory
Wave propagation
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Summary:Small-scale neuronal networks may impose widespread effects on large network dynamics. To unravel this relationship, we analyzed eight multiscale recordings of spontaneous seizures from four patients with epilepsy. During seizures, multiunit spike activity organizes into a submillimeter-sized wavefront, and this activity correlates significantly with low-frequency rhythms from electrocorticographic recordings across a 10-cm-sized neocortical network. Notably, this correlation effect is specific to the ictal wavefront and is absent interictally or from action potential activity outside the wavefront territory. To examine the multiscale interactions, we created a model using a multiscale, nonlinear system and found evidence for a dual role for feedforward inhibition in seizures: while inhibition at the wavefront fails, allowing seizure propagation, feedforward inhibition of the surrounding centimeter-scale networks is activated via long-range excitatory connections. Bifurcation analysis revealed that distinct dynamical pathways for seizure termination depend on the surrounding inhibition strength. Using our model, we found that the mesoscopic, local wavefront acts as the forcing term of the ictal process, while the macroscopic, centimeter-sized network modulates the oscillatory seizure activity.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1702490114