WONOEP APPRAISAL: The many facets of epilepsy networks

Scott, Rod C.; Prida, Liset Menéndez de la; Mahoney, J. Matt; Kobow, Katja; Sankar, Raman; Curtis, Marco de

doi:10.1111/epi.14503

Cited by 26 publications

(30 citation statements)

References 56 publications

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“…There is increasing interest in mechanisms of epileptogenesis, as opposed to ictogenesis, and the potential importance of an epileptogenic network. Recent work has emphasized the concept of modeling the brain as a complex system in order to understand the epileptogenic network (Scott et al, 2018). As part of this concept, disturbed signaling pathways and local circuit activity can be associated with an alteration in large-scale brain activity and changes in the behavioral phenotype.…”

Section: The Epileptogenic Networkmentioning

confidence: 99%

Unit firing and oscillations at seizure onset in epileptic rodents

Bragin

Staba

et al. 2019

Neurobiology of Disease

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Epileptic seizures result from a variety of pathophysiological processes, evidenced by different electrographic ictal onset patterns, as seen on direct brain recordings. The two most common electrographic patterns of focal ictal onset in patients are hypersynchronous (HYP) and lowvoltage fast (LVF). Whereas LVF ictal onsets were believed to result from disinhibition; based on similarities with absence seizures, focal HYP ictal onsets were believed to result from increased synchronizing inhibition. Recent findings, however, suggest the differences between these seizure onset types are more complicated and, in some cases, the opposite of these concepts are true. The following review presents evidence that a reduction of tonic inhibition on small pathologically interconnected neuron (PIN) clusters generating pathological high-frequency oscillations (pHFOs), which reflect abnormal synchronously bursting neurons may be the cause of HYP ictal onsets. Increased inhibition preceding LVF ictal onsets are discussed in other reviews in this issue. We postulate that neuronal cell loss following epileptogenic insults can result in structural reorganization, giving rise to small PIN clusters, which generate pHFOs. These clusters have a heterogeneous distribution and are spatially stable over time. Studies have demonstrated that a transient reduction in tonic inhibition causes these clusters to increase in size. This could result in consolidation and synchronization of pHFOs until a critical mass leads to propagation of HYP ictal discharges. Viewed within a network neuroscience framework, local disturbances such as PIN clusters are likely to contribute to large-scale brain network alterations: a better understanding of these epileptogenic networks promises to elucidate mechanisms of ictogenesis, epileptogenesis, and certain comorbidities of epilepsy.

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Section: The Epileptogenic Networkmentioning

confidence: 99%

Unit firing and oscillations at seizure onset in epileptic rodents

Bragin

Staba

et al. 2019

Neurobiology of Disease

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“…There is growing evidence of a network-based nature of epilepsy, meaning the interplay of several regions rather than a single focus is responsible for seizure initiation and propagation (Engel et al, 2013;Kramer & Cash, 2012;Scott et al, 2018;Shih, 2019;van Diessen, Diederen, Braun, Jansen, & Stam, 2013). This motivated efforts to move toward getting a multivariate view by capturing and analyzing dependences between signals and their changes.…”

Section: Introductionmentioning

confidence: 99%

Linear and nonlinear interrelations show fundamentally distinct network structure in preictal intracranial EEG of epilepsy patients

Müller

Caporro

Gast

et al. 2019

Human Brain Mapping

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Resection of the seizure generating tissue can be highly beneficial in patients with drug-resistant epilepsy. However, only about half of all patients undergoing surgery get permanently and completely seizure free. Investigating the dependences between intracranial EEG signals adds a multivariate perspective largely unavailable to visual EEG analysis, which is the current clinical practice. We examined linear and nonlinear interrelations between intracranial EEG signals regarding their spatial distribution and network characteristics. The analyzed signals were recorded immediately before clinical seizure onset in epilepsy patients who received a standardized electrode implantation targeting the mesiotemporal structures. The linear interrelation networks were predominantly locally connected and highly reproducible between patients. In contrast, the nonlinear networks had a clearly centralized structure, which was specific for the individual pathology. The nonlinear interrelations were overrepresented in the focal hemisphere and in patients with no or only rare seizures after surgery specifically in the resected tissue. Connections to the outside were predominantly nonlinear. In all patients without worthwhile improvement after resective treatment, tissue producing strong nonlinear interrelations was left untouched by surgery. Our findings indicate that linear and nonlinear interrelations play fundamentally different roles in preictal intracranial EEG. Moreover, they suggest nonlinear signal interrelations to be a marker of epileptogenic tissue and not a characteristic of the mesiotemporal structures. Our results corroborate the network-based nature of epilepsy and suggest the application of network analysis to support the planning of resective epilepsy surgery. K E Y W O R D S epilepsy, epilepsy surgery, linear, network structure, nonlinear, quantitative EEG Hum Brain Mapp. 2020;41:467-483. wileyonlinelibrary.com/journal/hbm 467 SUPPORTING INFORMATION Additional supporting information may be found online in the Supporting Information section at the end of this article. How to cite this article: Müller M, Caporro M, Gast H, et al. Linear and nonlinear interrelations show fundamentally distinct network structure in preictal intracranial EEG of epilepsy patients. Hum Brain Mapp. 2020;41:467-483.

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“…Redefining the concept of the SOZ network: For many years, seizures and epilepsy have been viewed as a network disorder rather than a focal disorder and significant effort has been invested into the modelling of structural, functional and effective connectivity networks in epilepsy using structural imaging, functional imaging and electrophysiology ( Scott, 2016 ; Wendling et al , 2016 ; Bartolomei et al , 2017 ; Jirsa et al , 2017 ; Scott et al , 2018 ) ( Fig. 2 ).…”

Section: The Future: Single-unit Recordings In the Clinical Contextmentioning

confidence: 99%

Microelectrode recordings in human epilepsy: a case for clinical translation

Chari

Thornton

Tisdall

et al. 2020

Brain Communications

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With their ‘all-or-none’ action potential responses, single neurons (or units) are accepted as the basic computational unit of the brain. There is extensive animal literature to support the mechanistic importance of studying neuronal firing as a way to understand neuronal microcircuits and brain function. Although most studies have emphasized physiology, there is increasing recognition that studying single units provides novel insight into system level mechanisms of disease. Microelectrode recordings are becoming more common in humans, paralleling the increasing use of intracranial electroencephalography recordings in the context of presurgical evaluation in focal epilepsy. In addition to single unit data, microelectrode recordings also record local field potentials and high frequency oscillations, some of which may be different to that recorded by clinical macroelectrodes. However, microelectrodes are being used almost exclusively in research contexts and there are currently no indications for incorporating microelectrode recordings into routine clinical care. In this review, we summarise the lessons learnt from 65 years of microelectrode recordings in human epilepsy patients. We cover the electrode constructs that can be utilised, principles of how to record and process microelectrode data as well as insights into ictal dynamics, interictal dynamics and cognition. We end with a critique on the possibilities of incorporating single unit recordings into clinical care, with a focus on potential clinical indications, each with their specific evidence base and challenges.

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WONOEP APPRAISAL: The many facets of epilepsy networks

Cited by 26 publications

References 56 publications

Unit firing and oscillations at seizure onset in epileptic rodents

Unit firing and oscillations at seizure onset in epileptic rodents

Linear and nonlinear interrelations show fundamentally distinct network structure in preictal intracranial EEG of epilepsy patients

Microelectrode recordings in human epilepsy: a case for clinical translation

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