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eNeuro. 2016 May 23;3(2). pii: ENEURO.0141-15.2016. doi: 10.1523/ENEURO.0141-15.2016. eCollection 2016 Mar-Apr.

Multiscale Aspects of Generation of High-Gamma Activity during Seizures in Human Neocortex.

Author information

1
Committee on Neurobiology, The University of Chicago, Chicago, Illinois 60637; Departments of Pediatrics, The University of Chicago, Chicago, Illinois 60637.
2
Departments of Pediatrics, The University of Chicago, Chicago, Illinois 60637; Department Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin 53226.
3
Departments of Pediatrics, The University of Chicago , Chicago, Illinois 60637.
4
Department Physiology, Medical College of Wisconsin , Milwaukee, Wisconsin 53226.
5
Department of Neurological Surgery, Columbia University , New York, New York 10032.
6
Department Neurosurgery, Medical College of Wisconsin , Milwaukee, Wisconsin 53226.
7
Department of Neurosurgery, Mount Sinai Hospital , New York, New York 10029.
8
Departments of Pediatrics, The University of Chicago, Chicago, Illinois 60637; Department Surgery, The University of Chicago, Chicago, Illinois 60637.
9
The Computation Institute, The University of Chicago , Chicago, Illinois 60637.
10
Department of Neurological Surgery, Columbia University, New York, New York 10032; Department of Neurology, Columbia University, New York, New York 10032.
11
Department of Neurology, Columbia University , New York, New York 10032.
12
Committee on Neurobiology, The University of Chicago, Chicago, Illinois 60637; Departments of Pediatrics, The University of Chicago, Chicago, Illinois 60637; The Computation Institute, The University of Chicago, Chicago, Illinois 60637; Committee on Computational Neuroscience, The University of Chicago, Chicago, Illinois 60637.

Abstract

High-gamma (HG; 80-150 Hz) activity in macroscopic clinical records is considered a marker for critical brain regions involved in seizure initiation; it is correlated with pathological multiunit firing during neocortical seizures in the seizure core, an area identified by correlated multiunit spiking and low frequency seizure activity. However, the effects of the spatiotemporal dynamics of seizure on HG power generation are not well understood. Here, we studied HG generation and propagation, using a three-step, multiscale signal analysis and modeling approach. First, we analyzed concurrent neuronal and microscopic network HG activity in neocortical slices from seven intractable epilepsy patients. We found HG activity in these networks, especially when neurons displayed paroxysmal depolarization shifts and network activity was highly synchronized. Second, we examined HG activity acquired with microelectrode arrays recorded during human seizures (n = 8). We confirmed the presence of synchronized HG power across microelectrode records and the macroscale, both specifically associated with the core region of the seizure. Third, we used volume conduction-based modeling to relate HG activity and network synchrony at different network scales. We showed that local HG oscillations require high levels of synchrony to cross scales, and that this requirement is met at the microscopic scale, but not within macroscopic networks. Instead, we present evidence that HG power at the macroscale may result from harmonics of ongoing seizure activity. Ictal HG power marks the seizure core, but the generating mechanism can differ across spatial scales.

KEYWORDS:

HFOs; epilepsy; human; modeling; neocortex; seizure

PMID:
27257623
PMCID:
PMC4876490
DOI:
10.1523/ENEURO.0141-15.2016
[Indexed for MEDLINE]
Free PMC Article

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