Intracranial Monitoring: Stereo-electroencephalography Recording

Brief Historical Perspective of Stereotactic Epilepsy Surgery

The application the stereotactic method in medicine has a long and complex history. The technical and methodologic aspects have evolved with clinical knowledge, innovations, and progress in the basic scientific understanding of different pathologies including epilepsy. Stereotaxy is based on the use of a Cartesian coordinate system first described by Descartes in the 17th century. According to Descartes, a point in a 3D space is represented by the intersection of three planes intersecting at right angles.

In neurosurgery, the history of stereotaxy actually starts with the use of this Cartesian principle by Sir Victor Horsley, a neurosurgeon, and Robert Henry Clarke, a mathematician who described the first stereotactic frame, which was applied on nonhuman subjects in 1905. Ten years later, Mussen, an engineer who worked on the Horsley-Clarke device, designed a conceptually similar device to be applied on human subjects. Unfortunately, the ingenious device did not convince neurosurgeons of its applicability because of its imprecision. Mussen wrapped the apparatus in newspaper and stored it in his attic.

In 1947, almost 30 years after Mussen’s device application failure, Spiegel and Wycis at Temple University developed the first stereotactic frame that was precise and usable on humans. Spiegel developed a stereotactic atlas of the human brain based on internal references obtained by pneumoencephalography; the foramen of Monro, the white anterior commissure (AC), and the pineal gland calcification were used as fiduciary landmarks. In 1952, because of the variability of the pineal gland, mainly in the exploration of diencephalic and pineal gland tumors, a neurosurgeon named Jean Talairach suggested replacing the “repère marker” by the posterior commissure (PC). Subsequently, the same author proposed the proportional grid coordinate concept based on the AC-PC line and the vertical lines from the AC and PC landmarks (vAC and vPC). ^, The first Talairach atlas of the basal ganglia was published in 1957.

After the initial development of the stereotactic frame and the first applications in the treatment of movement disorders, Talairach dedicated most of his activity in the field of cerebral tumors and epilepsy surgery, along with the neurologist Jean Bancaud, who joined him in 1952 at Saint Anne Hospital in the French capital. During years of clinical and academic partnership, Talairach and Bancaud’s views and concepts related to organization of the EZ and surgical approaches led the departure from previous concepts that were limited to cortical surface explorations, as initially preconized by Penfield and Jasper in Montreal. The French novel concept was based on a comprehensive analysis and time-related correlations of the morphology and functionality of the human brain during development of ictal and interictal activities, recorded in situ. A detailed stereotactic atlas that was published in 1967 focused on the human cortex and perfectly illustrated the topographic relations between function and stereotactic coordinates with cortical and subcortical anatomy, demonstrating these relations in 3D stereotactic space rather than 2D superficial planes as previously described ( Fig. 90.1 ).

The new technique, as part of the SEEG methodology, proposed functional exploration using intracortical recordings. The first implantation of intracerebral electrodes using the described methodology was performed on May 3, 1957. Such implantation has allowed clinicians to explore the activity of different brain structures and to record the patient’s spontaneous seizures. The harmonious combination of gross anatomy knowledge, the stereotactic technique, intracortical ictal/interictal recordings, and semiology correlations was named stereo-electro-encephalography in 1962. These explorations were the basis of tailored corticectomies first performed in 1960. Long after, the new method became a worldwide reference for extraoperative invasive monitoring for patients with difficult-to-localize MRE.

The technical aspect of the SEEG methodology was originally described as a multiphase process using the Talairach stereotactic frame and the double-grid system in association with teleangiography. ^{, ,} Despite its long reported successful record, with almost 60 years of clinical use, the technical intricacy regarding the placement of SEEG depth electrodes in addition to the complexity in interpreting the SEEG recordings may have contributed to the limited widespread application of the technique in centers outside France. Taking advantage of new radiologic, computational, and robotic innovations now commonly available in many surgical centers, more modern and less cumbersome methods of stereotactic implantation of SEEG depth electrodes can be applied on a routine basis.

Developing The Hypotheses and Implantation Planning

The development of a SEEG implantation plan requires a clear formulation of precise anatomo-electro-clinical hypotheses to be tested and the possible surgical treatment strategies that the investigation will provide. These hypotheses are typically generated during a multidisciplinary patient management conference based on the results of various noninvasive tests. Intracerebral depth electrodes sample the anatomic lesion (if identified), the more likely structure(s) of ictal onset, early and late propagation regions, and interactions with cortical functional (cognitive, language, sensory, sensory-motor, behavioral) organization, implemented in a clear and well-articulated hypothetical framework for implantation. ^a

References 1, 2, 18, 22, 56, 57.

A 3D “conceptualization” of the cortical areas responsible for emergence of the clinical manifestations, downstream from the hypothesized EZ, is an essential part of the presurgical implantation strategy. Initially, by analyzing the available noninvasive data and the temporal evolution of the ictal clinical manifestations, hypotheses on the anatomic location of the EZ are formulated. The implantation plans are created through collaborative discussions among epileptologists, neurosurgeons, neuropsychologists, and neuroradiologists who, in conjunction, formulate hypotheses for EZ localization. Adequate knowledge of the possible neural systems involved in the primary organization of the epileptogenic process is mandatory. Equally important is to account for the 3D aspects of depth electrode recordings, which despite limited coverage that is largely compensated by the interpolation process made possible by electrophysiologic methodology (i.e., frequencies, Cartesian spatial relations, and latencies analyses) in addition to adequate semiology analysis and correct interpretation of noninvasive data, enable accurate sampling of the structures along its trajectory from its entry site to its tip. Therefore, the trajectory of the recording electrodes are as important as the targets or entry point areas. Expressly, the SEEG electrode “target” can be conceived as the entire trajectory of a specific electrode and not only its most distal end. Consequently, the investigation must account for the lateral and mesial cortices of different lobes and the bottom of sulci between them.

The implantation should also consider the different cortical cytoarchitectonic areas that are involved in seizure primary organization and propagation patterns and their likely connectivity to other cortical and subcortical areas. For instance, the posterior orbito-frontal areas are intimately connected with the temporal pole and the rostral ventral insula cortex, indicating the need to explore these three anatomic areas that are physiologically organized as a single neural unit. It is important to emphasize that the implantation strategy focus is not to map lobes or lobules, but the epileptogenic cortical arrangement, which, in general, involves multiple lobes and sublobar structures.

Lastly, the aim to obtain all the possible information from the SEEG exploration should not be pursued at the expense of an excessive number of electrodes, which will likely increase the morbidity of the implantation. In general, implantations that exceed 15 depth electrodes are rare and likely excessive. In addition, the possible involvement of highly functional regions in the ictal discharge requires their judicious coverage, with the twofold goal to assess their role in the seizure organization and to define the boundaries for safe surgical resections.

In addition to the meticulous analyses of seizure semiology and noninvasive data, the fundamentals and basic principles of adequate SEEG implantation and guided resection are also based on (1) generic anatomo-functional cortical and subcortical organization, (2) 3D recognition of fine sulco-gyral anatomy using subsegmentation in sulcal roots, and (3) the critical role played by the limbic structures in the propagation of seizures. Specifically, the basic knowledge about anatomic circuitry is frequently taken into account in SEEG planning. Some practical and illustrative examples are highlighted in the following paragraphs.

When a temporal pole EZ is suspected, electrodes are systematically placed in the posterior paralimbic part of the orbital frontal cortex (Brodman Area [BA] 13), in general under oblique orientation, and orthogonal lateral electrodes are placed in the anterior superior temporal, anterior insular, limen insulae, and subcallosal cingulate areas (BA 25), which are all paralimbic cortices highly connected to the pole of the temporal lobe. In addition, to better define the involvement (or not) of the adjacent amygdaloid complex and hippocampal formation, depth electrodes are also placed in these respective regions in orthogonal (Cartesian) fashion. It is important to consider that the amygdaloid complex has dense connectivity to the anterior perisylvian areas as well as the rostral portions of the superior temporal gyrus (planum polare) and frontal opercular areas. Consequently, these cortical areas should be explored in patients whose semiology indicates amygdala and peri-amygdala onset. Variations and extensions to this implantation plan will depend primarily on patient semiology and secondarily on the results of other preimplantation methods of localization.

When the EZ hypothesis involves the mesial temporal lobe structures in addition to separate orthogonal electrodes in the amygdaloid complex, the head of the hippocampus, and the body/tail of the hippocampus, electrodes are systematically implanted in the perirhinal and entorhinal cortex as well, mainly because of the known role of these structures in subtypes of mesial temporal lobe epilepsy (MTLE) ^, with vast projections to the frontal cortex.

When involvement of the presupplementary motor area (pre-SMA), supplementary motor area proper (SMA), and frontal eye field (BA 6 to 8) is suspected, electrodes are implanted in the posterior parietal operculum (BA 40) and the anterior border of the superior parietal lobule and rostral positions of the intraparietal sulcus (BA 7a) in addition to other premotor, precentral, and sometimes prefrontal electrodes, depending on the video-EEG or suspicious imaging. All of these structures are known to be densely connected and, on several occasions, rapid propagation of the ictal discharge among these somewhat distant structures has been observed.

The 3D recognition of fine sulco-gyral anatomy using subsegmentation in sulcal roots (or sulcal pits) can be the drive for more precise implantation. In the example of the superior temporal sulcus (STS), the five sulcal roots of this structure have quite different phylogenetic and ontogenetic origins with a clearly different pattern of connectivity that can be used to check potential distant propagation pathways. Based on this, segmentation of the STS and the specific connectivity of each of its sulcal domain–specific distant areas may be implanted.

The critical role played by the limbic structures in the majority of temporal epilepsies is an argument to question the role of the paleocortex and archicortex in general. Thus whether the pre-SEEG hypotheses are pointing in the direction of the frontal, parietal, or occipital lobes, regardless of the presence of a lesion, it is common practice in SEEG planning to systematically investigate the associated limbic cortices. ^{, , ,}

Seeg Implantation Patterns

SEEG implantation patterns are based on a tailored strategy of exploration, which results from the individualized hypotheses of localization. Consequently, standard implantation is not a common practice in SEEG. Nevertheless, a number of typical and similar patterns of electrode coverage can be recognized ( Fig. 90.2 ). This apparent standardization must be practiced and applied with discernment and criteria. Some of the most common patterns of explorations frequently applied in SEEG are discussed in the following sections.