Concepts of Cortical Anatomy and Talairach Stereotaxic Space Applied to the SEEG Method

Stereoelectroencephalography (SEEG) concepts are directed toward the precise identification of the parcel of the cortical ribbon responsible for seizure genesis in patients with drug resistant epilepsy. The phase I preoperative workup (noninvasive phase) based on careful analyses of the electro-clinical and radiological explorations is designed to harvest all information supposed to have “localizing value” of the cortical area (s) generating the ictal discharge. When these “localizing” information are too uncertain to propose an upfront corticectomy but strong enough to propose a coherent hypothesis about the location of the epileptogenic zone (EZ) in the individual anatomy, a phase II can be proposed (SEEG).

How phase I data are translated in terms of anatomical hypotheses and stereotaxic coordinates, how the hypotheses are conceptualized in implantation strategy and how the electroclinical information generated by the SEEG are interpreted, are all aspects that are fundamentally rooted in the understanding of the 3D anatomo-functional organization of the cerebral cortex. In this chapter, we will discuss the fundamentals of cortical anatomy and stereotaxic space applied to the SEEG methodology.

A brief history of cortical anatomy

Raised by the debate between equipotentiality and phrenology in the XVIII century the meticulous study of how specific areas of the cerebral cortex are involved in functional specialization took off with the “modern localizationism” of Paul Broca (1824–80), the renowned French surgeon and anatomist. The systematic study of correlation between neurological symptoms and localization of lesions in the brain (the anatomo-clinical method) created the need for detailed morphological study of the cerebral cortex. In 1854 Louis Pierre Gratiolet published “Mémoire des plis cérébraux de l’homme et des primates” and in 1892 Daniel John Cunningham published “Contribution to the surface anatomy of the cerebral hemispheres”. These two major comprehensive contributions created a base for further studies of the cerebral cortex and have remained unchallenged until now. The discovery by Fritz & Hitzig in 1870 that electricity could stimulate the brain and that specific parts of the cortex were involved in motor function, with different regions of cortex relating to different parts of the body (somatotopy) led rapidly to neurosurgeons like Wilder Penfield (1891–1976) systematically using cortical electrical stimulation as a tool for functional brain mapping in general neurosurgery and epilepsy surgery.

Thanks to the discovery of X-rays by Wilhem Conrad Röntgen in 1895, Remy and Contremoulin introduced the concept of stereotactic frame and stereotaxic image-guided navigation in 1897. Subsequently, the use of stereotactic methodology for human functional neurosurgery by Spiegel and Wycis started at the end of the 1940’s mainly for psychiatric surgery and movement disorders.

The basic concept of stereotaxic neurosurgery was to provide neurosurgeons with a method allowing them to safely navigate in the brain using the “language of numbers” (analytic geometry). The frame allowed the intracranial space of the patients to be represented within an ortho-normed tridimensional Euclidean space with tripolar coordinates defining the position of each point of the patient’s intracranial space. The frame at the same time offered a remarkably stable way of fixation of the skull in addition to a reference to the stereotactic space. Numerous frames have been manufactured, usually relying either on the Cartesian coordinates or on polar coordinates (or both). Some frames combine Cartesian coordinates and analogic targeting capacities.

The stereotaxic approach for brain anatomy: the 3-dimensional space

In the late 1950’s, Jean Talairach and Gerard Guiot went to visit Spiegel and Wycis in Philadelphia and founded stereotactic functional neurosurgery in France. At this time the only types of imaging available were plain X-ray, ventriculography invented by Walter Dandy in 1918 and angiography invented by the Portuguese neurologist Antonio Egas Moniz in 1927, confining neurosurgeons to indirect targeting of the intracerebral targets of functional neurosurgery. However, neurosurgeons had previously rapidly understood that the wide variability of relationship between intracranial targets for functional operations and the bony structures provided by X-rays was far too imprecise to use it as landmarks for trajectories in the brain. The introduction of air ventriculography gave access to the visualization of deep anatomical landmarks like the foramen of Monroe and the pineal gland, used by Spiegel and Wycis as reference structures for the very first stereotactic atlas as early as 1925.

Following the introduction of electroencephalography (EEG) in humans by Hans Berger in 1924, Forster and Altenburger performed the first invasive EEG recording around 5 years later. Then, Wilder Penfield and Herbert Jasper systematically used EEG recording of interictal activities and electrical stimulation of the exposed cortex in awake patients in order to map respectively the epileptic focus around the lesion and surrounding functional areas, in order to guide the resective surgery. Jean Talairach was a meticulous anatomist and the first to use stereotactic methodology for epilepsy. Thanks to the use of stereotactic methodology, Talairach proposed to insert deep electrodes into selected structures, allowing not only recording of interictal activities and mapping of the functional value of the investigated structures but also recording ictal (seizure-related) electrical activity, which was supposed, according to Bancaud, to be a better descriptor of the cortical areas generating seizures, which would be necessary to remove for successful outcome of epilepsy surgery. The first stereoelectroencephalographic recordings using deep electrodes were acute, recording patients while they remained fixed in the stereotactic frame for several hours, waiting for seizures. Then, Talairach and Bancaud moved toward chronic recording with patients keeping their implanted electrodes as long as several weeks. Depending on the pre-SEEG hypotheses the strategy of implantation was shaped based on the range of anatomo-physiological correlations known at this time. This principle of the SEEG methodology challenged the capacity of the neurosurgeons to reach discrete deep critical structures in the pre-CT and pre-MRI era.

Jean Talairach proposed the use of the anterior commissure-posterior commissure (AC-PC) referential system visible on ventriculography, and proportionalization for indirect targeting of deeply seated targets but also cerebral cortex. Talairach published a first atlas summarizing the statistical positions of the main brain structures in the AC-PC reference system in 1957. ^, He introduced the teleradiography technique with an X-ray source at more than 4 m from the receptor and orthogonality of the beam to the receptor. Teleradiography has the advantage of the absence of magnification factor and cushion deformity and allows direct calculation within a 3D space without mathematical transformation, thanks to strictly orthogonal X-rays and thus a high geometrical reliability. His homemade stereotactic frame was a very rigid one, designed to host a grid system specially adapted to multiple trajectories of the SEEG approach ( Fig. 2.1 ).

The fundamental concepts of stereotaxic cortical and subcortical localization, as described above, are intrinsically related to the methods associated with Talairach’s approach and the distinct utilization of direct and indirect stereotaxic localization methods. As a short explanation, the direct method is applied to the intracranial targets, structures and lesions that are visible on MRI. As a complementary method, indirect targeting localization is required in structures that are not MRI-visible such as, for example, the motor cingulate cortical areas and the entorhinal or perirhinal cortices. Despite the significant improvements in imaging modalities, the indirect targeting method and the application of the Talairach stereotaxic space still play an important role in defining important anatomical-functional structures that are not visible with the direct MRI-based methods.

Definitions related to the Talairach stereotaxic space

For the indirect localization of cortical and subcortical structures, Jean Talairach and colleagues developed a method of stereotaxic localization that is based on precise anatomical landmarks. In the Talairach reference system, three reference lines constitute the basis for the three-dimensional proportional grid system. These three lines are: 1. AC-PC, VAC and the midline:

1.

AC-PC line: the reference line passes through the superior edge of the anterior commissure and the posterior edge of the posterior commissure. It follows a path which is parallel to the hypothalamic sulcus, dividing the thalamic from the subthalamic region. The AC-PC line defines the horizontal plane.
2.

VAC: this is a vertical line adjacent to the posterior margin of the anterior commissure. This line is the basis of the vertical frontal plane.
3.

VPC: this is a vertical line adjacent to the anterior margin of the posterior commissure.
4.

Midline: This is the interhemispheric, sagittal plane.

The study of a series of human cadaver hemispheres under formal stereotaxic conditions yielded the concept of the “noyau chirurgical” or surgical nucleus, that portion of the volume of a nucleus possessing the same coordinates in all the hemispheres surveyed. Clearly aware of the importance of stereotaxic neurosurgery for clinical and research, Talairach developed the concept of the “proportional grid system” as the basis of the methodology for the reasoned assembly and comparison of data from successive patients with cerebral hemispheres of individual sizes and proportions.

Distances from these planes and reference points are measured in millimeters. Because of the individuals’ variations in height, length and width of human brains, these measurements are only applicable to one individual. This becomes increasingly true with greater distances from the basal lines. For this reason, highly precise millimetric measurements can only be applied to the gray central nuclei. ^, To deal with this variability, a three-dimension proportional grid system was created, first proposed in 1967. The three-dimensional proportional grid system takes into consideration the maximal dimensions of the brain in three planes of space and, for this reason, adapting to all brains of all dimensions. This proportional localization system marks off the distances separating the basal lines and the cortical periphery defined by lines through:

The highest point of the parietal cortex.

The most posterior point of the occipital cortex.

The lowest point of the temporal lobe.

The most anterior point of the frontal lobe.

The most lateral point of the parietal-temporal cortex.

The volume defined by these planes are then divided into several different blocks:

Above the AC-PC line in eights.

Below the AC-PC line in quarters.

Anterior to the VAC line and posterior to VPC line in quarters.

The space between the two perpendiculars erected through the anterior and the posterior commissures is divided into three zones (E1, E2 and E3), and it consistently defines the localization of the motor cortex.

The AC-PC system turned out to be very reliable for deep nuclei and cerebral cortex. Talairach’s coworker Gabor Szikla (1928–83) developed a methodology that allowed visualization of the 3D anatomy of the cerebral cortex based on its arterial vasculature. Cortical veins remain at the surface of the cortex and go from gyral crown to gyral crown bridging sulci. On the contrary, the arterial supply dives into sulci creating arterial loops in the sulci ( Fig. 2.2 ).

Based on the atlas of arterial loops in sulci published by Gabor Szikla in 1977, a generation of stereotactic neurosurgeons became able to target specific gyri individually with sub-millimetric precision while avoiding vessels, thanks to stereotactic cerebral angiography. The level of precision and safety of this methodology of SEEG implantation, based on in vivo direct visualization of the 3D anatomy of the cerebral cortex long before the CT-scan & MRI era is quite incredible ( Fig. 2.3 ). Then in the 1970’s, Talairach, Bancaud and coworkers provided the epilepsy surgery community with a completely new approach of investigation for drug resistant epilepsies.

The Talairach stereotaxic space applied to SEEG methodology

The application of the proportional Talairach stereotaxic space provides a normalized method that can be applied across different subjects, allowing statistical studies and group analysis, because each individual case can be reduced to a common scale. For example, in the frontal lobe, the primary somatomotor cortical area (Brodmann area 4) contributes to the formation of the pyramidal tract and is intrinsically connected with areas six and 5, sending efferent fibers to the thalamus, lenticular nucleus, substantial nigra and zona incerta. From an anatomical point of view, area four is located at the depth of the central sulcus and not accessible through the dorsolateral aspect of the hemisphere. From a stereotaxic point of view, area four is almost completely located within the stereotactic space between the VAC and VPC.

Area six is known to be involved in motor functions and extrapyramidal syndromes and it contributes to the corticospinal tract. In the mesial surface, it is located between the VAC and VPC. From an anatomical-functional aspect, this area corresponds to the supplementary motor areas.

Area eight represents a large portion of the frontal eye field for voluntary conjugate movements of the eyes. It is connected by long association bundles with other cortical regions, in particular the occipital lobe, and by projection fibers with the brain stem and the oculomotor nerves. In the dorsal lateral surface area eight is located anterior to the VAC, where the frontal eye fields (FEF) cortical area is located. Areas 9 and 10 belong to the pre-frontal area, mainly connecting with the thalamic dorso-medial nucleus.

Patterns of SEEG Explorations

After the authors have discussed some anatomical and stereotaxic landmarks associated with SEEG explorations, we will demonstrate how the theoretical parts are applied to the SEEG implantation strategies, particularly focused on anterior temporal exploration based on Talairach stereotaxic coordinates.

To report a schematic and didactic method of implantation, the authors divided the temporal lobe into four anatomical-functional regions. We report only the orthogonally oriented trajectories due to the consistency of implantation and the adequate exploration of the mesial and lateral compartments in the temporal lobe using the Talairach stereotaxic space.

The temporal pole

In humans, the temporal pole is located ventral to the sylvian fissure, at the rostral tip of the temporal lobe, in the most rostral part of the middle cranial fossa. Rostrally, the temporal pole is in contact with the dura that is adjacent to the sphenoid greater wing. The caudal limits are not well defined, with no clear anatomical separation from other portions of the temporal lobe. Its caudal boundary can be arbitrarily defined as the virtual plane defined by the limitans sulcus of the insula, in continuation with the limen insulae.

From a cytoarchitectonic aspect, the temporal pole contains two areas. The most dorsal aspect, in proximity with the Sylvian fissure, was classified as Area 38 by Brodmann in 1909 and as temporopolar area TG by Von Economo and Koskinas in 1929. This area is mostly constituted of agranular cortex, similar to the most ventral and rostral aspects of the insula cortex and the most posterior aspect of the orbitofrontal cortex. From a structural aspect, these areas are highly connected through the uncinate fascicle ( Fig. 2.4 ). From the Talairach coordinates aspect, the temporal pole is located anterior to the VAC and ventral to the AC-PC line, more precisely at the C10 coordinate in the dorsal aspect and D12 in the ventral aspect ( Fig. 2.4 , panels B and C). The electrode trajectory located in the dorsal aspect of the temporal pole (C10) explores the dorsal lateral and mesial surface (the sylvian surface) of the superior temporal gyrus. Eventually, if vascularity allows, the trajectory can be extended through the sylvian cistern to also explore the most rostral and ventral aspects of the limen insulae, and the more posterior aspect of the orbito-frontal cortex, in the BA25. This trajectory allows the exploration of three different cortical regions (the temporal pole, the limen insulae, and the caudal aspect of the orbito-frontal surface), all corresponding to agranular paralimbic cortex.

The central core

The central core of the temporal lobe corresponds to Brodmann area 21 in the dorsal lateral aspects. BA 21 is located in the rostral aspect of the middle temporal gyrus, lying posterior to the boundaries of the temporal pole (BA 38) and anterior to BA 37, which lies at the posterior limits of the temporal lobe. Dorsally it is limited by the superior temporal sulcus, a deep and well-defined sulcus, which is mostly an uninterrupted sulcus and extends from the temporal pole to the temporal parietal transition. Ventrally, the middle temporal gyrus is separated from the inferior temporal gyrus by the combination of several small and discontinuous sulci, that, in combination, form the so-called inferior temporal sulcus. The projection of BA 21 into the mesial planes corresponds to the temporal horn of the lateral ventricle, the amygdala and the head of hippocampus, and the anterior and posterior mesial surface of the uncus.

From a stereotaxic coordinate perspective, the structures located in the central core of the temporal lobe are located between the VAC and the VPC planes on sagittal orientation, precisely in column E of the Talairach coordinate system. Electrodes implanted in an orthogonal orientation, immediately posterior to VAC, at the most anterior areas of E10, will explore the anterior uncus and the amygdaloid complex in the mesial contacts and the dorsal lateral neocortex (BA 21) in the lateral contacts. In the more lateral contacts, the trajectory trespasses the depths of the rostral aspect of the superior temporal sulcus and the crown of the middle temporal gyrus. The amygdaloid complex is in proximity with VAC, centered approximately at 5 mm posterior or anterior to the vertical line. The anterior uncus is located at the mesial projection of the amygdaloid complex, with the dorsal aspect corresponding to the piriform cortex.

Immediately ventral and posterior to the “amygdala trajectory”, at E10, is the so-called hippocampus trajectory. The hippocampus electrodes explore the more caudal aspect of the uncus, transpassing the head of the hippocampus to finally end at the dorso-lateral aspect of the middle temporal gyrus (Broadman area 21). Immediately ventral to the hippocampus trajectory, in the E column, is the anterior basal temporal electrode that will explore the anterior basal parahippocampal area where the entorhinal and perirhinal cortices are located (Brodmann area 28), in the most mesial aspect of the trajectory. More laterally, the trajectory will pass by the anterior fusiform cortex and the basal and lateral aspects of the temporo-occipital sulcus and inferior temporal gyrus (Brodmann area 20) ( Fig. 2.5 ).