Multiple Oscillatory Push–Pull Antagonisms Constrain Seizure Propagation
Objective Drug‐resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low‐frequency activity (LFA), high‐frequency activity (HFA), or low‐to‐high cross‐frequency coupling. However, the...
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| Published in | Annals of neurology Vol. 86; no. 5; pp. 683 - 694 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken, USA
John Wiley & Sons, Inc
01.11.2019
Wiley Subscription Services, Inc |
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| Online Access | Get full text |
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| Abstract | Objective
Drug‐resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low‐frequency activity (LFA), high‐frequency activity (HFA), or low‐to‐high cross‐frequency coupling. However, the mechanism by which different oscillatory networks constrain the propagation of focal seizures remains unclear.
Methods
We studied focal epilepsy patients with invasive electrocorticography (ECoG) recordings and compared multilayer directional network interactions between focal seizures either with or without secondary generalization. Within‐frequency and cross‐frequency directional connectivity were estimated by an adaptive directed transfer function and cross‐frequency directionality, respectively.
Results
In the within‐frequency epileptic network, we found that the seizure onset zone (SOZ) always sent stronger information flow to the surrounding regions, and secondary generalization was accompanied by weaker information flow in the LFA from the surrounding regions to SOZ. In the cross‐frequency epileptic network, secondary generalization was associated with either decreased information flow from surrounding regions’ HFA to SOZ's LFA or increased information flow from SOZ's LFA to surrounding regions’ HFA.
Interpretation
Our results suggest that the secondary generalization of focal seizures is regulated by numerous within‐ and cross‐frequency push–pull dynamics, potentially reflecting impaired excitation–inhibition interactions of the epileptic network. ANN NEUROL 2019;86:683–694 |
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| AbstractList | ObjectiveDrug‐resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low‐frequency activity (LFA), high‐frequency activity (HFA), or low‐to‐high cross‐frequency coupling. However, the mechanism by which different oscillatory networks constrain the propagation of focal seizures remains unclear.MethodsWe studied focal epilepsy patients with invasive electrocorticography (ECoG) recordings and compared multilayer directional network interactions between focal seizures either with or without secondary generalization. Within‐frequency and cross‐frequency directional connectivity were estimated by an adaptive directed transfer function and cross‐frequency directionality, respectively.ResultsIn the within‐frequency epileptic network, we found that the seizure onset zone (SOZ) always sent stronger information flow to the surrounding regions, and secondary generalization was accompanied by weaker information flow in the LFA from the surrounding regions to SOZ. In the cross‐frequency epileptic network, secondary generalization was associated with either decreased information flow from surrounding regions’ HFA to SOZ's LFA or increased information flow from SOZ's LFA to surrounding regions’ HFA.InterpretationOur results suggest that the secondary generalization of focal seizures is regulated by numerous within‐ and cross‐frequency push–pull dynamics, potentially reflecting impaired excitation–inhibition interactions of the epileptic network. ANN NEUROL 2019;86:683–694 Drug-resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low-frequency activity (LFA), high-frequency activity (HFA), or low-to-high cross-frequency coupling. However, the mechanism by which different oscillatory networks constrain the propagation of focal seizures remains unclear. We studied focal epilepsy patients with invasive electrocorticography (ECoG) recordings and compared multilayer directional network interactions between focal seizures either with or without secondary generalization. Within-frequency and cross-frequency directional connectivity were estimated by an adaptive directed transfer function and cross-frequency directionality, respectively. In the within-frequency epileptic network, we found that the seizure onset zone (SOZ) always sent stronger information flow to the surrounding regions, and secondary generalization was accompanied by weaker information flow in the LFA from the surrounding regions to SOZ. In the cross-frequency epileptic network, secondary generalization was associated with either decreased information flow from surrounding regions' HFA to SOZ's LFA or increased information flow from SOZ's LFA to surrounding regions' HFA. Our results suggest that the secondary generalization of focal seizures is regulated by numerous within- and cross-frequency push-pull dynamics, potentially reflecting impaired excitation-inhibition interactions of the epileptic network. ANN NEUROL 2019;86:683-694. Drug-resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low-frequency activity (LFA), high-frequency activity (HFA), or low-to-high cross-frequency coupling. However, the mechanism by which different oscillatory networks constrain the propagation of focal seizures remains unclear.OBJECTIVEDrug-resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low-frequency activity (LFA), high-frequency activity (HFA), or low-to-high cross-frequency coupling. However, the mechanism by which different oscillatory networks constrain the propagation of focal seizures remains unclear.We studied focal epilepsy patients with invasive electrocorticography (ECoG) recordings and compared multilayer directional network interactions between focal seizures either with or without secondary generalization. Within-frequency and cross-frequency directional connectivity were estimated by an adaptive directed transfer function and cross-frequency directionality, respectively.METHODSWe studied focal epilepsy patients with invasive electrocorticography (ECoG) recordings and compared multilayer directional network interactions between focal seizures either with or without secondary generalization. Within-frequency and cross-frequency directional connectivity were estimated by an adaptive directed transfer function and cross-frequency directionality, respectively.In the within-frequency epileptic network, we found that the seizure onset zone (SOZ) always sent stronger information flow to the surrounding regions, and secondary generalization was accompanied by weaker information flow in the LFA from the surrounding regions to SOZ. In the cross-frequency epileptic network, secondary generalization was associated with either decreased information flow from surrounding regions' HFA to SOZ's LFA or increased information flow from SOZ's LFA to surrounding regions' HFA.RESULTSIn the within-frequency epileptic network, we found that the seizure onset zone (SOZ) always sent stronger information flow to the surrounding regions, and secondary generalization was accompanied by weaker information flow in the LFA from the surrounding regions to SOZ. In the cross-frequency epileptic network, secondary generalization was associated with either decreased information flow from surrounding regions' HFA to SOZ's LFA or increased information flow from SOZ's LFA to surrounding regions' HFA.Our results suggest that the secondary generalization of focal seizures is regulated by numerous within- and cross-frequency push-pull dynamics, potentially reflecting impaired excitation-inhibition interactions of the epileptic network. ANN NEUROL 2019;86:683-694.INTERPRETATIONOur results suggest that the secondary generalization of focal seizures is regulated by numerous within- and cross-frequency push-pull dynamics, potentially reflecting impaired excitation-inhibition interactions of the epileptic network. ANN NEUROL 2019;86:683-694. Objective Drug‐resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal oscillations such as low‐frequency activity (LFA), high‐frequency activity (HFA), or low‐to‐high cross‐frequency coupling. However, the mechanism by which different oscillatory networks constrain the propagation of focal seizures remains unclear. Methods We studied focal epilepsy patients with invasive electrocorticography (ECoG) recordings and compared multilayer directional network interactions between focal seizures either with or without secondary generalization. Within‐frequency and cross‐frequency directional connectivity were estimated by an adaptive directed transfer function and cross‐frequency directionality, respectively. Results In the within‐frequency epileptic network, we found that the seizure onset zone (SOZ) always sent stronger information flow to the surrounding regions, and secondary generalization was accompanied by weaker information flow in the LFA from the surrounding regions to SOZ. In the cross‐frequency epileptic network, secondary generalization was associated with either decreased information flow from surrounding regions’ HFA to SOZ's LFA or increased information flow from SOZ's LFA to surrounding regions’ HFA. Interpretation Our results suggest that the secondary generalization of focal seizures is regulated by numerous within‐ and cross‐frequency push–pull dynamics, potentially reflecting impaired excitation–inhibition interactions of the epileptic network. ANN NEUROL 2019;86:683–694 |
| Author | Jiang, Haiteng He, Bin Worrell, Gregory A. Cai, Zhengxiang |
| AuthorAffiliation | 2 Department of Neurology Mayo Clinic Rochester MN 1 Department of Biomedical Engineering Carnegie Mellon University Pittsburgh PA |
| AuthorAffiliation_xml | – name: 2 Department of Neurology Mayo Clinic Rochester MN – name: 1 Department of Biomedical Engineering Carnegie Mellon University Pittsburgh PA |
| Author_xml | – sequence: 1 givenname: Haiteng surname: Jiang fullname: Jiang, Haiteng organization: Carnegie Mellon University – sequence: 2 givenname: Zhengxiang surname: Cai fullname: Cai, Zhengxiang organization: Carnegie Mellon University – sequence: 3 givenname: Gregory A. orcidid: 0000-0003-2916-0553 surname: Worrell fullname: Worrell, Gregory A. organization: Mayo Clinic – sequence: 4 givenname: Bin orcidid: 0000-0003-2944-8602 surname: He fullname: He, Bin email: bhe1@andrew.cmu.edu organization: Carnegie Mellon University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31566799$$D View this record in MEDLINE/PubMed |
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Drug‐resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different... Drug-resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different neuronal... ObjectiveDrug‐resistant focal epilepsy is widely recognized as a network disease in which epileptic seizure propagation is likely coordinated by different... |
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| SubjectTerms | Adolescent Adult Child Convulsions & seizures Drug Resistant Epilepsy - physiopathology Electrocorticography Epilepsies, Partial - physiopathology Epilepsy Female Humans Information flow Male Middle Aged Multilayers Neural networks Oscillations Propagation Seizures Seizures - physiopathology Transfer functions Young Adult |
| Title | Multiple Oscillatory Push–Pull Antagonisms Constrain Seizure Propagation |
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