The Utility of Stereoelectroencephalography in Lesional Epilepsy





Acknowledgments


The author would like to extend sincere thanks to Professor Chauvel and Professor McGonigal for their insightful comments, and invaluable guidance.


Introduction


Epilepsy surgery stands as a transformative therapeutic avenue for patients grappling with drug-resistant epilepsy (DRE). The evolution of neuroimaging has heralded a new era in epilepsy surgery, witnessing a notable surge in surgical procedures performed. However, despite this growth, significant enhancements in surgical outcomes have yet to be realized.


Epilepsy surgery started as an acute procedure performed in the operating room with the guidance of the electrocorticography (ECoG). Subsequently, a phase of extraoperative monitoring was implemented thanks to improvements in technology.


Currently, there are two methods for extraoperative recording:



  • 1.

    Stereoelectroencephalography (SEEG) which was practiced mainly in Europe but has recently become increasingly popular across the globe. SEEG is carried out under the auspice of an anatomo-electro-clinical (AEC) hypothesis driven by the presurgical data. SEEG aims to define the epileptogenic zone and its relation to cortical functions in sampled areas. It guides the therapeutic options, be it resection, ablation or neuromodulation.


  • 2.

    Subdural grids (SDG) with or without depth electrodes, which was practiced mainly in North America. SDG investigates the cortical surface in a two-dimensional manner.



Both approaches are guided by hypotheses and share the common goal of achieving seizure freedom with minimal or no functional deficit. This objective is typically achieved through either complete resection or disconnection of the epileptogenic zone. However, the two methods diverge in their conceptual approach to defining the epileptogenic zone.


The pioneers of SEEG, Bancaud and Talairach, defined the epileptogenic zone as the “site of the beginning and of the primary organization of the epileptic ictal discharge .” Understanding this organization is crucial for interpreting seizure semiology. In essence, SEEG studies the epileptogenic “network,” the spatiotemporal dynamics of the epileptic discharges, and how they evolve and spread in three-dimensional fashion, leading to semiology. The spatial and temporal dynamics of the epileptic discharges and their impact on anatomical structures dictate the repertoire of signs and symptoms. These are then deconstructed, when building the AEC hypothesis to define possible anatomic origins.


In contrast, SDG views the epileptogenic zone as “focus” or “The area of cortex that is necessary and sufficient for initiating seizures and whose removal (or disconnection) is necessary for complete abolition of seizures.” This is rather a surgical and post hoc definition of “what to remove area.” As such, the identification of an epileptogenic lesion or “focus” on imaging became a necessity in the North American school, whereas the advent of neuroimaging did not change the principles of SEEG.


The epileptogenic zone concept is somewhat hypothetical because it cannot be precisely delineated, despite the utility of various methods and interictal data. Achieving high localization accuracy depends on meticulous interpretation of anatomic, clinical, functional, and electrophysiological data. Electrophysiological parameters provide insights into the boundaries of the epileptogenic zone.


The three-channel precept


SEEG exploration provides a three-dimensional insight into brain circuitry, revealing that the epileptogenic zone extends beyond a mere lesion. SEEG compartmentalizes the epileptogenic network into three zones: lesional, interictal, and ictal. This categorization prevents biases in localization and aids in accurate interpretation. The lesional zone is characterized by permanent slow background activity, accentuated by postictal slowing. Its spatial dimension is compared with imaging parameters. The irritative zone comprises sites of abnormal interictal paroxysmal activities that spread within cortico-cortical networks. The accuracy of irritative zone as a marker for epileptogenic zone localization is debated due to its complex waveforms and spread. The Epileptogenic Zone represents the primary organization of ictal discharge. It exhibits reproducible frequency spectra and interareal synchronization during seizures, triggered as a whole by stimulation. SEEG precision in Epileptogenic Zone localization ensures optimal electrode placement and identifies multiple epileptogenic zones if conditions are not met. In contrast to the seizure onset zone in other methods, the operational definition of the epileptogenic zone considers early propagation involving the “early spread network,” which correlates closely with the semiology.


The predicament of localization


In some published series, it has been observed that the presence of a lesion may improve surgical outcomes, but it does not necessarily enhance the localization of the epileptogenic zone. ,


Nevertheless, it will influence the formulation of the presurgical hypothesis. In one study led by Chauvel et al., the investigators studied the experience of using SEEG in presurgical evaluation in two groups: those with visible lesion on magnetic resonance imaging (MRI), and those with MRI-negative epilepsy. No significant difference in localization was found between lesional and MRI-negative groups. We have replicated those findings in an unpublished series of 27 children studied with SEEG (9 lesional, 18 MRI negative). Overall, Engel class I or II outcome was achieved in 83% and 88% of MRI negative group and lesional groups respectively, with P -value of .36.


The localization of the epileptogenic zone can be achieved through a process of indirect inference. This inference is based on studying the semiology, the outward expression of a seizure caused by the interplay between the spatial and temporal evolution of epileptic discharges as they propagate through anatomical structures. While the presence of a lesion identified on MRI may indicate that a specific brain structure plays a role in organizing the epileptogenic zone, the epileptogenic zone itself cannot be solely equated with the lesion.


Lesional zone in SEEG is defined by the presence of continuous or nearly continuous delta activity, along with the disappearance of normal background activity, which can serve as reliable indicators of lesional tissue, particularly in MRI-negative regions.


Analyzing seizure semiology is crucial for localizing the epileptogenic zone, despite inherent limitations and gaps in understanding its generation. It forms the basis for constructing a presurgical anatomo-electro-clinical (AEC) hypothesis, integrating anatomical, electrophysiological, and clinical data. Semiology reflects the intricate interaction between epileptic discharges and cortical and subcortical structures in three-dimensional space and time. As discharges propagate from the seizure onset zone, semiology emerges. Thus, in SEEG, the aim is to sample potential areas or networks capable of producing semiology, regardless of lesion presence. However, it is impractical and unsafe to sample all involved areas, necessitating careful SEEG planning and interpretation within these limitations in mind.


There are essential considerations to take into account when analyzing semiology:



  • 1.

    The type of the cortex being invaded by the epileptic discharges: the expression of elementary signs or symptoms is related to the activation of primary cortices. However, as the discharges spread to association and multimodal cortices, the manifestations become more elaborate and complex. Equally, the presence of complex behavior at the outset of seizure onset may indicate early involvement of polymodal areas. Emotional and autonomic features may point to contributions from the limbic cortex.


  • 2.

    The frequency of the discharges: fast discharges in the gamma range typically deactivate normal function, while slow frequency discharges in the theta discharge can mimic physiologic function. For example, low frequency discharges in delta and theta range in the motor area lead to clonic activity, whereas higher frequency in the gamma range can lead to tonic or negative motor phenomenon.


  • 3.

    Some semiological features can be generated by the synchronization or the desynchronization between anatomically or functionally interconnected structures. Fear, for example can be generated by stimulating the amygdala or by loss of synchrony on the orbitofrontal region. Similarly, ictal humming is generated by increased coherence between the superior temporal gyrus and the inferior frontal gyrus.



Semiologic localization requires sound knowledge of cerebral anatomy and connectivity. Decisions on implantation targets are driven by how functionally or anatomically interconnected regions are assumed to participate in the organization of the epileptic network, and the current understanding of cortical organization, in terms of architecture and connections.


Put simply, cortical zones can be divided into limbic, paralimbic, heteromodal, unimodal and primary areas. Extensive connectivity is typically present between structures within the same zone, and between adjacent zones. Cortical connections can be traced to the concept of dual origin of cortex from two primordial moieties, archicortical (hippocampus) and paleocortical (olfactory cortex), leading to a progressive architectonic trend from periallocortex to proisocortex to isocortex and culminating in pre- and post-Rolandic sensorimotor and association areas. Feedforward connections begin in primary sensory cortices and sequentially terminate in the limbic areas. Conversely, feedback connections are generated from limbic cortices to primary sensory cortices. Inputs and outputs are processed in a serial and parallel fashion in dorsal and ventral streams.


In practical terms, even if a lesion is detected on MRI, an SEEG exploration may still be necessary, depending on its location and the seizure semiology. For example, if the lesion impacts a paralimbic structure like the posterior orbitofrontal area, it might be advisable to explore neighboring paralimbic structures such as the insula, temporal pole, cingulate gyrus, and parahippocampal gyrus during SEEG evaluation. This expanded assessment accounts for the interconnectedness within the paralimbic network, which could influence the epileptogenic zone, regardless of the lesion’s location.


Likewise, if a lesion is identified in the posterior fusiform gyrus and the seizure symptoms suggest an early versive head turn, SEEG investigation should encompass both the dorsal and ventral visual streams, with potential sampling of mesial temporal structures. This comprehensive approach is crucial because seizures may engage not only the visual cortex where the lesion is situated in the ventral stream, but also connected regions responsible for visual processing and motor responses in the dorsal stream.


SEEG in epilepsies with visible lesion on imaging


A lesion should be considered in relation to the epileptogenic network and other presurgical data.


Lesions do not always indicate where the seizures come from. Indeed, the lesion and the epileptogenic zone do not often overlap. In one study, only one third of patients with focal cortical dysplasia or neurodevelopmental tumor had focal epileptogenic zone, while the other two thirds had a more distributed organization of the epileptogenic network. Thus, as discussed earlier, SEEG should be considered if sufficient localization cannot be accomplished with available presurgical data, regardless of the presence of lesion.


SEEG have been traditionally indicated in MRI negative epilepsy, but there are many other circumstances where it should be considered, even if there is a visible lesion. These are supplemented by a clinical examples in the figures below:


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Mar 2, 2025 | Posted by in NEUROSURGERY | Comments Off on The Utility of Stereoelectroencephalography in Lesional Epilepsy

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