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New Research, Disorders of the Nervous System

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

Tahra L. Eissa, Andrew K. Tryba, Charles J. Marcuccilli, Faiza Ben-Mabrouk, Elliot H. Smith, Sean M. Lew, Robert R. Goodman, Guy M. McKhann Jr, David M. Frim, Lorenzo L. Pesce, Michael H. Kohrman, Ronald G. Emerson, Catherine A. Schevon and Wim van Drongelen
eNeuro 26 April 2016, ENEURO.0141-15.2016; https://doi.org/10.1523/ENEURO.0141-15.2016
Tahra L. Eissa
1Committees on Neurobiology, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
3Departments of Pediatrics, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
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Andrew K. Tryba
3Departments of Pediatrics, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
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Charles J. Marcuccilli
3Departments of Pediatrics, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
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Faiza Ben-Mabrouk
6Department Physiology, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226
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Elliot H. Smith
8Department of Neurological Surgery, Columbia University, 710 West 168th Street, New York, NY 10032
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Sean M. Lew
7Department Neurosurgery, Medical College of Wisconsin, 9200 W. Wisconsin Ave., Milwaukee, WI 53226
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Robert R. Goodman
10Department of Neurosurgery, Mt. Sinai, 1468 Madison Avenue, New York, NY 10029
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Guy M. McKhann Jr
8Department of Neurological Surgery, Columbia University, 710 West 168th Street, New York, NY 10032
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David M. Frim
3Departments of Pediatrics, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
4Department Surgery, The University of Chicago 5841 South Maryland Avenue, Chicago, IL 60637
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Lorenzo L. Pesce
5The Computation Institute, The University of Chicago, 5735 South Ellis Avenue, Chicago, IL 60637
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Michael H. Kohrman
3Departments of Pediatrics, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
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Ronald G. Emerson
8Department of Neurological Surgery, Columbia University, 710 West 168th Street, New York, NY 10032
9Department of Neurology, Columbia University, 710 West 168th Street, New York, NY 10032
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Catherine A. Schevon
9Department of Neurology, Columbia University, 710 West 168th Street, New York, NY 10032
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Wim van Drongelen
1Committees on Neurobiology, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
2Computational Neuroscience, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
3Departments of Pediatrics, The University of Chicago, KCBD 900 East 57th Street, Chicago, IL 60637
5The Computation Institute, The University of Chicago, 5735 South Ellis Avenue, Chicago, IL 60637
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Abstract

High gamma (HG, 80-150Hz) 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, where multiunit spiking correlates with seizure activity. However, the effects of the seizure’s spatiotemporal dynamics on HG power generation are not well understood. Here, we studied HG generation and propagation, using a three-step, multi-scale 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 (PDSs) and network activity was highly synchronized. Second, we examined HG activity acquired with microelectrode arrays (MEAs) 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 seizure’s core region. 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.

Significance Statement: We demonstrate that ictal HG power (80-150Hz) in cortical measurements is increased in the seizure core and appears on clinical recordings as a result of volume conduction and synchrony between harmonics generated during ongoing seizure activity. The accuracy of ictal HG activity to localize the core is superior to that of the lower frequency seizure activity since these are generated across much larger cortical areas. Therefore, detection of HG power provides a promising tool for surgical evaluation of patients with epilepsy.

  • epilepsy
  • HFOs
  • human
  • modeling
  • neocortex
  • seizure

Footnotes

  • ↵1 Authors report no conflict of interest.

  • ↵3 This work is funded by NIH Grant 1R01 NS084142, R01 NS095368-01 and Dr. Ralph and Marian Falk Medical Research Trust

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Multiscale Aspects of Generation of High Gamma Activity during Seizures in Human Neocortex
Tahra L. Eissa, Andrew K. Tryba, Charles J. Marcuccilli, Faiza Ben-Mabrouk, Elliot H. Smith, Sean M. Lew, Robert R. Goodman, Guy M. McKhann Jr, David M. Frim, Lorenzo L. Pesce, Michael H. Kohrman, Ronald G. Emerson, Catherine A. Schevon, Wim van Drongelen
eNeuro 26 April 2016, ENEURO.0141-15.2016; DOI: 10.1523/ENEURO.0141-15.2016

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Multiscale Aspects of Generation of High Gamma Activity during Seizures in Human Neocortex
Tahra L. Eissa, Andrew K. Tryba, Charles J. Marcuccilli, Faiza Ben-Mabrouk, Elliot H. Smith, Sean M. Lew, Robert R. Goodman, Guy M. McKhann Jr, David M. Frim, Lorenzo L. Pesce, Michael H. Kohrman, Ronald G. Emerson, Catherine A. Schevon, Wim van Drongelen
eNeuro 26 April 2016, ENEURO.0141-15.2016; DOI: 10.1523/ENEURO.0141-15.2016
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Keywords

  • epilepsy
  • HFOs
  • human
  • modeling
  • neocortex
  • seizure

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