Chapter 3 – Cranial-Cerebral Relationships Applied to Microneurosurgery

Chapter 3 Cranial-Cerebral Relationships Applied to Microneurosurgery

The determination of the exact relations of the primary fissures and convolutions of the brain to the surface of the cranium is of importance to the physician and surgeon, as a guide to the localization and estimation of the effects of diseases and injuries of the brain and its coverings …

David Ferrier, 1843–1928 (Ferrier, 1876 apud Greenblatt, 1997)

3.1 Microneurosurgical Anatomy – General Remarks

Although evident, it is interesting to point out that the neuroimaging and intraoperative identification of intracranial structures, as with other body organs, are done from and based on the initial recognition of their surrounding natural spaces. Intracranially, this is constituted by the cerebrospinal fluid (CSF) filled spaces, and surgery is always preferably done through the same natural spaces, hence also preferably through CSF spaces for intracranial surgery.

This ideal practice became possible only with the advent of microneurosurgery. This was led particularly by the contributions of Yasargil (1999), evolved through the progressive development of initial transfissural and transcisternal approaches, particularly for the removal of extrinsic lesions (Yasargil et al., 1976), to posterior transsulcal approaches for intrinsic lesions (Harkey et al., 1989; Pia, 1986; Yasargil, 1994; Yasargil, 1996; Yasargil et al., 1988a), and with the consequent establishment of the sulci as fundamental anatomical landmarks for its practice.

The brain sulci can be used as microsurgical corridors for the removal of cortical and subcortical lesions, to reach the ventricular cavities, or to serve as landmarks and limiting surgical boundaries for subpial or transgyral approaches (Figure 3.1).

Figure 3.1 Possible transcerebral microneurosurgical routes.

Given the actual brain anatomy with the gyri constituting a real continuum throughout their multiple, and to some extent also variable, superficial, and deep connections that, respectively interrupt and limit the depth of their related sulci, it is important to emphasize that, despite being distinctively named, the gyri should be understood as arbitrary circumscribed regions of the brain surface. They are delimited by sulci that correspond to extensions of the subarachnoid space and that should also be understood as arbitrary circumscribed spaces of the brain surface which can be constituted by single or multiple segments, and with a variable morphology to some extent.

When compared to the subpial and transgyral approaches, besides the obvious advantage of providing a natural closer proximity to deep spaces and lesions, the transsulcal approaches are naturally oriented toward the nearest part of the ventricular cavity, which can be very helpful when dealing with peri- and intraventricular lesions. This unique feature of the radial orientation of sulci in relation to the nearest ventricular space, which is well seen in MRI coronal cuts, is due to the evolutionary fact that the sulci of the superolateral surface of the brain are a product of an infolding process of the cerebral surface. This took place mainly throughout the evolution of mammals in order to increase the cortical surface, and it occurred concomitant to the C-shaped bending of the telencephalon in relation to a center constituted by the thalami, which together carried the morphological modifications of the primitive prosencephalic vesicle that gave rise to the lateral ventricles through the same C-shaped bending process (Sarnat and Netsky, 1981; Squire et al., 2003; Williams and Warwick, 1980). Despite their anatomical variations, the main sulci have then constant topographical relationships with their related ventricular cavities and hence with the deep neural structures (Harkey et al., 1989; Ono et al., 1990; Rhoton, 2003; Seeger, 1978; Ribas et al., 2006).

Once the cortex is thicker over the crest of a convolution and thinner in the depth of a sulcus (Carpenter and Sutin, 1983), theoretically, while the actual transgyral approaches sacrifice a larger number of neurons and of projection fibers, the transsulcal approaches sacrifice a larger number of U fibers (Carpenter and Sutin, 1983; Harkey et al., 1989) (Figure 3.2).

Figure 3.2 (A) Classic sketch by Vogt C, Vogt O, 1919, 1928, (B) cadaveric specimen, and (C) MRI coronal image, showing 1) that while the projection fibers arise from the crest of the gyri, the bottom of the sulci are related mainly to U-fibers, and 2) that while the main sulci of the superolateral and basal brain surfaces point to the nearest ventricular cavity, the sulci of the medial surface are parallel to the corpus callosum, and their organization depends on its normal development.

The subpial approaches can be started either through a transcortical opening just next to a sulcus or be initiated through a more limited sulcal opening.

The major disadvantage of the transsulcal approach is that the surgeon has to deal with intrasulcal vessels with diameters proportional to the dimensions of the sulci, and with occasional cortical veins that can run along the sulci surface (Figure 3.3). Besides the respective vascular impairments, damage to these vessels can cause bleeding that spreads through the adjacent subarachnoid space and that can obliterate the clear microsurgical view. Even small vessels can be critical in eloquent areas of the brain.

Figure 3.3 (A) Classic sketch by Key and Reteius (Key and Reteius, 1875 apud Yasargil, 1984a), 1875, and (B) Microneurosurgical opening of the Sylvian fissure, showing that, while the arteries are loosely attached to arachnoid bands within the intrasulcal spaces, the veins are more firmly attached to the pia mater and brain surface. (C) Microneurosurgical opening of the Sylvian fissure showing the arachnoid space (Arach), artery (Art) and vein (Vein).

In order to avoid stretching and tearing these vessels, and to optimize opening of the sulci, the arachnoid should be divided preferably with sharp instruments and the sulci should be progressively opened along their entire required extent. The running arteries should be freed and protected toward one side after the coagulation and division of their tiny contralateral perforating branches. The coagulation and division of larger veins are dependent on their location, and small intrasulcal veins should usually be coagulated to prevent their posterior bleeding during subsequent maneuvers. Vessels at the sulci depth can be avoided if necessary by entering the white matter before reaching them in order to proceed subpially. Larger sulcal opening extents provide less traction of the sulcal related vessels and walls, easing the transsulcal work by decreasing the need for Stille retractors.

For removal of hemispheric intrinsic lesions, the transsulcal approach can be useful to reach lesions that can then be removed piecemeal or en bloc, and also to delimit the removal of a gyral region that encloses the lesion. In particular, for the infiltrative gliomas that are so common and that frequently remain confined within their site of origin for some time (Yasargil, 1994), the anatomical removal of a gyral or of a lobular sector that encloses the tumor is justified and can facilitate and enhance its radical resection in non-eloquent areas.

In similitude to the brain extrinsic lesions that require complete dissection and exposure for their correct microsurgical treatment, as with the clipping of aneurysms or the removal of benign tumors, the strategy of isolation and removal of a gyral sector that contains an infiltrative tumor provided by its delimiting sulci identification and opening should then be considered when feasible.

In parallel with the significant microneurosurgical (Yasargil, 1999) and intracranial microanatomic knowledge (Rhoton, 2003; Yasargil, 1984a; Yasargil, 1994) gained over the last decades, the current localization of the brain sulci and gyri on the external cranial surface for the correct positioning of supratentorial craniotomies and for general transoperatory orientation (Rhoton, 1999; Seeger, 1978; Uematsu et al., 1992) is still mostly based on cranial-topographic anatomy studies done particularly in the second half of the nineteenth century (Gusmão et al., 2000; Finger, 1994; Kocher, 1907 apud Krause, 1912; Krause, 1912; Krönlein, 1898 apud Krause, 1912; Taylor and Haughton, 1900 apud Uematsu et al., 1992; Testut and Jacob, 1932; Uematsu et al., 1992) or done with the aid of stereotactic (Chin et al., 1999) or sophisticated frameless imaging devices (Watanabe et al., 1987).

The appraisal of the surface projection of intrinsic lesions seen in neuroradiological images frequently performed by neurosurgeons is difficult and error-prone due to the irregular oval shape of the skull and of the brain, and to the obliqueness and variable levels, particularly of axial and coronal images. Special techniques developed for this aim may require specific devices and are based on calculations that are also not free from error (von Economo, 1987; Fernández-Miranda et al., 2008; Hinck and Clifton, 1981; King and Walker, 1980; Krol et al., 1988; O’Leary and Lavyne, 1978; Penning, 1987).

The intraoperative frameless imaging devices developed during the last decade (Watanabe et al., 1987), when available, obviously should not replace the cranial-cerebral anatomic knowledge that every neurosurgeon has to have and has to improve throughout his practice. Moreover, transoperatory brain displacement can affect the accuracy of these navigation systems (Dorward et al., 1999; Roberts et al., 1998; Sure et al., 2000) and, although real-time corrections can nowadays be eventually made by the fusion of ultrasound images with the neuronavigation (Unsgaard et al., 2002) and using intraoperative MRI (Black and Pikul, 1997; Black et al., 1997; Wirtz et al., 1997), correct transoperatory anatomical orientation is of course mandatory for the interpretation and for checking of all these imaging data. The same argument can be made about any new neurosurgical instrument or imaging technique, since the planning, practice, and evaluation of any surgical procedure intrinsically require accurate anatomical knowledge and can be particularly enhanced by a tridimensional understanding.

Regarding the functional reliability of utilizing anatomical sulcal and gyral landmarks for microneurosurgical orientation, it is mandatory to consider that any transoperatory anatomical identification of any eloquent cortical area, even when confirmed by a localizing imaging system, cannot safely replace the knowledge given by transoperatory functional or neurophysiological testing. This is because of common anatomical functional variations, their possible displacements and/or involvement by the underlying pathology (Ebeling and Reulen, 1992b; Ojemann et al., 1989; Simos et al., 1999; Uematsu et al., 1992), or the plasticity more common in long standing lesions (Duffau, 2011b).

On the other hand, it is meaningful to bear in mind that studies on functional neuroimaging and intraoperative cortical stimulation denote findings that, in general, corroborate the expected relationships between elicited functional responses and their respective eloquent anatomical sites (Berger et al., 1990; Boling et al., 1999; Brannen et al., 2001; Ebeling et al., 1992a; Ebeling and Reulen, 1992b; Fitzgerald et al., 1997; Lobel et al., 2001; Ojemann et al., 1989; Quiñones-Hinojosa et al., 2003; Rutten et al., 2002; Schiffbauer et al., 2002; Simos et al., 1999; Uematsu et al., 1992; Yousry et al., 1995).

3.2 The Sulcal, Gyral, and Cranial Key Points

3.2.1 The Concept of Sulcal and Gyral Key Points and Their Cranial-Cerebral Relationships

The knowledge of the primary cortical areas obtained in the second half of the nineteenth century (Broca, 1861 apud Finger, 1994; Ferrier, 1873 apud Finger, 1994; Fritsch and Hitzig, 1960 apud Finger, 1994; Jackson, 1863 apud Finger, 1994) generated the need to relate the brain sulci and gyri to the skull surface in order to properly expose and operate on intracranial lesions diagnosed only through neurological focal findings. This gave rise to several methods to establish the main cranial-cerebral relationships (Bischoff, 1868 apud Broca, 1876; Broca, 1876a apud Stone, 1991; Broca, 1876b; Horsley apud Ebeling et al., 1987; Kocher, 1907; Krause, 1912; Krönlein, 1898 apud Krause, 1912; Taylor and Haughton, 1900 apud Uematsu et al., 1992; Testut and Jacob, 1932). These descriptions were led particularly by Broca in France (Broca, 1876a apud Stone, 1991; Broca, 1876b; Broca, 1861 apud Finger, 1994), and related the brain sulci and gyri mostly to cranial sutures and to craniometric points (Broca, 1861 apud Finger, 1994), and many of these methods are still utilized at the present time.

As already stressed, the development of microneurosurgery established the sulci as the fundamental landmarks of the brain surface and made the subpial and transsulcal microneurosurgical approaches possible (Harkey et al., 1989; Pia, 1986; Yasargil et al., 1988b; Yasargil, 1999; Yasargil, 1994); however, in parallel with the fact that the main sulci and gyri of the brain are currently easily identified in standard magnetic resonance images, their accurate visual transoperative recognition is notoriously difficult because of their common anatomic interruptions and variations, and their arachnoid, cerebrospinal fluid, and frequent vessel coverings.

Upon the exposure of their sites eased by the knowledge of basic cranial-cerebral relationships, the identification of the main sulci may be facilitated by the initial identification of some more remarkable sulci and gyri points constituted by the main sulci extremities and/or intersections, and by the cortical sites that underlie the most prominent cranial points. This identification can then be completed from these starting points through recognition of the exposed sulci and gyri according to previous knowledge of their usual orientations, shapes, and more frequent anatomical variations. Currently, 3D rendering reconstructions of MR images can be very helpful for their preoperative appraisal.

On the superolateral surface of the brain, besides the always evident lateral or Sylvian fissure, the central sulcus, the precentral sulcus, and the postcentral sulcus, the other main sulci are the superior frontal sulcus, the inferior frontal sulcus, the superior temporal sulcus, and the intraparietal sulcus. The essential microneurosurgical sulcal and cortical key points are naturally those constituted by these main sulci extremities and/or intersections, and by the gyral sites that underlie the most prominent cranial points. Besides being anatomically more constant, the sulcal key points constituted by an intersection of two important sulci can be identified usually as a site with a variable enlargement of the subarachnoid space (Ribas et al., 2006).

In order to project a cortical or a subcortical lesion seen on MR images onto the cranial surface for planning of a craniotomy, similar to navigation systems that localize any given point according to its position in relation to points with previously known coordinates, with the aid of these key points, any intrinsic cerebral lesion can be initially understood with regard to the structure and/or the intracranial space that contains the lesion. Then through the known relationships of this site with its most related cortical and sulcal key points, the lesion can have its external cranial projection estimated considering the position of the corresponding cranial points for these key points.

In addition to determining the external projection of the lesion, its most related sulcal key points will also serve as natural references pertinent to the best transsulcal, subpial, or transgyral approach for the target lesion, and hence contribute particularly to the correct placement of the planned craniotomy.

The sulcal and gyral key points described later are divided into fronto-opercular, superior frontal, and central, parietal, posterior temporal, occipital, and basal supratentorial key points which delineate the cerebral base. They are related to their respective cranial points within intervals smaller than 2 cm (Ribas et al., 2006), which is acceptable for the surgical purposes of placement of craniotomies and intraoperative visual identification of sulcal key points.

Altogether, they constitute a cranial-cerebral anatomic framework which can aid the understanding of the location of any intrinsic brain lesion, orient the placement of craniotomies, and ease the identification of brain sulci and gyri.

Since their locations are particularly related to cranial sutures and the most prominent cranial points (Broca, 1861 apud Finger, 1994), the precise initial identification of these cranial landmarks is mandatory (Figure 3.4).

Figure 3.4 Average cranial suture and main midline measurements. (A) and (B), Adult skull with its main sutures and most prominent points; (C), their average distances and their relationships with the sulci and gyri of the brain. Average measurements are from Ribas et al. (2006).

Ast: asterion (meeting point of the lambdoid occipitomastoid and parietomastoid sutures); Br: bregma (meeting point of the sagittal and coronal sutures); CoSut: coronal suture; Eu: euryon (most prominent point of the parietal bossa or tuberosity); In: inion (prominence given by the external occipital protuberance); La: lambda (meeting point of the sagittal and lambdoid sutures); LaSut: lambdoid suture; Na: nasion (intersection of the nasion bones with the frontal bone); OpCr: opisthocranion (most prominent point of the occipital bossa); PaMaSut: parietomastoid suture; PreAuDepr: preauricular depression (upper aspect of the most posterior aspect of the zygomatic arch, anterior to the tragus); Pt: pterion (region where the frontal, parietal, temporal and sphenoid bones join together); SagSut: sagittal suture; SqSut: squamous suture; St: stephanion (meeting point of the coronal suture and superior temporal line); STL: superior temporal line (from Ribas et al., 2006).

While the coronal sutures are usually palpable laterally and above the superior temporal lines, distances from the nasion to the bregma, and from the bregma to the lambda vary roughly from 12 to 14 cm in adults (Ribas et al., 2006). This knowledge is very helpful for the localization of these two important craniometric points along the midline.

3.2.2 Fronto-Opercular Key Points

The frontoparietal operculum generally covers the superior half of the insular surface, with the triangular and opercular parts of the inferior frontal gyrus covering its anterior aspect and with the basal parts of the pre- and postcentral gyri covering its posterior aspect. The fronto-opercular sulcal key points are: 1) the Anterior Sylvian Point, 2) the Inferior Rolandic Point, and 3) the Inferior Frontal and Precentral Sulci Meeting Point.

3.2.2.1 The Anterior Sylvian Point

The lateral or Sylvian fissure (SyF) is definitely the most identifiable feature of the superolateral face of the brain, and constitutes the main microneurosurgical corridor to the base of the brain (Yasargil et al., 1976; Yasargil, 1984a; Yasargil, 1994; Yasargil et al., 1988a; Yasargil et al., 1975; Yasargil et al., 2002a).

The SyF is divided into a proximal segment (stem, sphenoidal, anterior ramus) and a distal segment (lateral, posterior ramus) by the Anterior Sylvian Point (ASyP) (Türe et al., 1999; Yasargil et al., 2002a; Ribas et al., 2005a). This corresponds with a variable but anatomically constant enlargement of the Sylvian fissure located inferior to the triangular part and anterior/inferior to the opercular part of the inferior frontal gyrus (IFG), and which is evident due to an usual retraction of the triangular part (Figure 3.5).

Figure 3.5 Variations of the IFG illustrated by Testut and Jacob, showing the typical enlargement of the SyF beneath its triangular part. (Reprinted from Testut and Jacob, 1932; Ribas et al., 2005b.)

The horizontal and anterior ascending branches of the SyF originate from the ASyP and delineate the triangular part of the IFG, which always harbors a small descending segment of the inferior frontal sulcus (IFS). Anteriorly to it lies the more prominent orbital part of the IFG which is basally continuous with the most lateral orbital gyrus, and posteriorly to it lies the anatomically constant U-shaped opercular part of the IFG, always harboring the most inferior segment of the precentral sulcus (Ribas et al., 2005a).

Given its constant location and striking cisternal appearance as already shown in old illustrations (Krause, 1912; Taylor and Haughton, 1900 apud Uematsu et al., 1992) and in recent publications (Duvernoy, 1991; Krings et al., 2001; Ono et al., 1990; Pernkoff, 1980; Rhoton, 2003; Seeger, 1995; Seeger, 1978; Squire et al., 2003; Tamraz and Comair, 2000; Türe et al., 1999; Yasargil, 1984a; Yasargil, 1994; Yasargil et al., 2002a), the ASyP can be used not only as a starting site to open the SyF but also as an initial landmark to identify intraoperatively other important neural and sulcal structures along the fissure. These structures are usually hidden by their arachnoidal and vascular coverings, features that characterize the ASyP as the prototype of a microneurosurgical sulcal key point.

Taylor and Haughton (1900 apud Uematsu et al., 1992), in their study of the topography of the convolutions and fissures of the brain published in 1900, used the term Sylvian point, defining it as “the point where the main stem of the fissure of Sylvius reaches the outer aspect of the hemisphere.” In his textbook published in 1912, Krause (1912) reproduced illustrations by the German anatomist August von Froriep (1849–1917) (Lockard, 1977) with identification of the Sylvian point and also illustrated an anatomical opening of the SyF for exposure of a superficial insular lesion (Figure 3.6). Recently, Türe et al. (1999) stressed the use of the term Sylvian point.

Figure 3.6 Reproduction of an old illustration of the Sylvian Point by August von Froriep (A), and opening of the Sylvian fissure by F. Krause (B).

(Reprinted from Krause, 1912.)

Nevertheless, its designation as the Anterior Sylvian Point (ASyP) seems more appropriate, and in line with the term Posterior Sylvian Point (Ribas et al., 2005a; Ribas et al., 2005b; Yasargil and Abdulrauf, 2003), which corresponds to the distal extremity of the posterior ramus of the Sylvian fissure, and that is the starting point of the ascending terminal ramus and the occasional descending terminal ramus (Ono et al., 1990).

The ASyP can also be identified intraoperatively as the SyF segment located just posteriorly to the IFG orbital part since this convolution frequently bulges significantly after dural opening, in contrast to its posterior adjacent triangular part (Figure 3.7).

Figure 3.7 Surgical exposure of the stem of the Sylvian fissure (SyF), Anterior Sylvian Point (ASyP), of the Horizontal (HR) and Anterior Ascending Rami (AAR) of the Sylvian fissure which define the Triangular Part of the Inferior Frontal Gyrus (Tr), its posterior Opercular Part (Op), Superior Temporal Gyrus (STG), Carotid artery (CaA), branches of the middle cerebral artery (M1 and M2), and insular apex (Apex).

AAR: Anterior ascending ramus of SyF; Apex: insular apex; ASyP: anterior Sylvian point; CaA: Carotid artery; HR: horizontal ramus of SyF; M1 and M2: branches of the middle cerebral artery; Op: opercular part of the inferior frontal gyrus; STG: superior temporal gyrus; SyF: Sylvian fissure; Tr: Triangular part of the inferior frontal gyrus.

Yasargil and colleagues emphasized that “the Sylvian point is located in the same plane of the IFG triangular part, and 10 to 15 mm anterior to the Sylvian venous confluence constituted by frontal and temporal tributaries veins,” and advised “to begin opening the fissure immediately anterior to this vein confluence at a point where a temporal or frontal artery or where both arteries appear at the surface of the fissure” (Yasargil et al., 2002b), hence at the ASyP area. Upon opening of the Sylvian fissure, the insular apex can be identified just below the ASyP.

Regarding its cranial relationship, the ASyP lies underneath the most anterior aspect of the squamosal suture, hence just posterior to the sphenoparietal suture that corresponds to the H central bar that characterizes the pterion, and just superior to the sphenotemporal suture (Ribas et al., 2005b).

3.2.2.2 The Inferior Rolandic Point

The inferior extremity of the central sulcus is located just above the Sylvian fissure (SyF) in about 80 percent of humans, and inside the Sylvian fissure in the other 20 percent with the subcentral gyrus then completely hidden inside the fissure (Ribas et al., 2006). The so-called Inferior Rolandic Point (IRP) (Taylor and Haughton, 1900 apud Uematsu et al., 1992) corresponds to the projection of the inferior extremity of the central sulcus onto the lateral SyF, or to their intersection when the central sulcus reaches the fissure.

The IRP is located along the lateral (Sylvian) fissure between 2 and 3 cm posteriorly to the ASyP, approximately mid-distance between the ASyP and the Posterior Sylvian Point (PSyP) at the end of the lateral (Sylvian) fissure (Ribas et al., 2005b).

Regarding its cranial relationships, in adults, the IRP lies underneath the point of intersection of the squamous suture with a 4 cm high vertical line originating in the preauricular depression which lies in front of the tragus, and which corresponds to the upper and most posterior aspect of the zygomatic root (Ribas et al., 2006). This intersection point also corresponds to the highest segment of the concave squamous suture, which then indicates that the subcentral gyrus lies underneath the highest part of the squamous suture (Ribas et al., 2005b; Ribas et al., 2006).

It is interesting to note that the early authors also related the inferior extremity of the central sulcus (CS) to the same vertical line originating at the preauricular depression, but none of them studied the relationship of the projection of the inferior extremity of the CS over the Sylvian fissure with the squamous suture level. Poirier described the lower extremity of the central sulcus as being situated over a line perpendicular to the zygomatic arch and located immediately anterior to the tragus, 7 cm superior to the preauricular point which can be characterized as an evident small depression just anterior to the tragus (Testut and Jacob, 1932). In 1900, Taylor and Haughton (1900 apud Uematsu et al., 1992) described the inferior extremity of the central sulcus as being situated at the intersection of this same perpendicular line with the so-called Sylvian line, that for these authors is given by a line drawn from the junction of the third and fourth segments of the Nasion-Inion curvature to the orbito-temporal angle. Championnière positioned the inferior Rolandic point 3.5 cm superiorly to the posterior extremity of a 7 cm line parallel to the zygomatic arch and which initiated at the frontozygomatic point that corresponds to the site of the frontozygomatic suture situated on the lateral orbital rim (Testut and Jacob, 1932). Recently, Rhoton mentioned that the lower Rolandic point is located approximately 2.5 cm posterior to the Pterion on the Sylvian fissure line, which corresponds to a line drawn between the frontozygomatic point and the three-quarter point of the Nasion-Inion distance (Rhoton, 2003).

In relation to the coronal suture, Passet found the inferior extremity of the central sulcus to be situated 25 mm (range: 0–65 mm) posteriorly to the coronal suture (Passet apud Ebeling et al., 1987), Horsley between 20 and 30 mm (Horsley apud Ebeling et al., 1987), and Lang 27.3 mm (range: 17–33 mm) (Lang, 1985 apud Ebeling et al., 1987).

3.2.2.3 The Inferior Frontal and Precentral Sulci Meeting Point

The inferior frontal sulcus is always interrupted and can end in connection with the precentral sulcus or very close to this sulcus. Their connection point, or the point of connection of an inferior frontal sulcus prolongation line with the precentral sulcus when they do not actually connect, is designated as the inferior frontal and precentral sulci meeting point (IFS/PreCS). This is a practical neurosurgical key point that 1) delineates anteriorly the precentral gyrus at its inferior third level which corresponds to the face motor activation area (Penfield and Rasmussen, 1950b; Penfield and Boldrey apud Brodal, 1981) and 2) indicates the posterior and superior limit of the opercular part of the inferior frontal gyrus.

The IFS/PreCS lies underneath the coronal suture and the superior temporal line meeting point, which corresponds to the craniometric point named the Stephanion (St) (Broca, 1876b; Ribas et al., 2006). Its topographic relationship with the inferior frontal sulcus had already been shown by Broca (1876b), and more recently, Seeger (1995) clearly related the inferior aspect of the coronal suture to the inferior aspect of the precentral sulcus.

3.2.2.4 The Frontoparietal Operculum

Identification of the fronto-opercular key points ASyP, IRP, and IFS/PreCS can be helpful for the identification of all the main sulci and convolutions of the frontoparietal suprasylvian operculum both in preoperative radiologic images and intraoperatively (Ribas et al., 2005a), and for the correct placement of craniotomies.

The superior and inferior margins of the SyF constitute, respectively, the cisternal borders of the frontoparietal and temporal operculi (operculum, from Latin: cover, curtain) which cover the superior and inferior aspects of the insula. Once by definition the frontoparietal operculum extends from the anterior to the posterior ascending branch of the SyF (Williams and Warwick, 1980), hence with the orbital part (Orb) of the inferior frontal gyrus (IFG) disposed anteriorly, the suprasylvian structures can be understood as a series of convolutions morphologically roughly arranged as a V-shaped convolution with its vertex constituted by the ASyP, followed by three U-shaped and one C-shaped convolution, all enclosing sulci terminal segments and extremities (Figures 3.8 and 3.9). The bottom of the three U-shaped convolutions and their related sulcal extremities can be situated either superiorly to the SyF or inside the fissure, then causing the false visual impression that their related sulci end at the SyF (Ribas et al., 2005a).

Figure 3.8 (A) Fronto-opercular key points and (B) their corresponding cranial sites: 1) the anterior Sylvian point (ASyP) is characterized by enlargement of the Sylvian fissure inferior to the triangular part (Tr) and anterior to the opercular part (Op) of the inferior frontal gyrus, and lies underneath the most anterior aspect of the squamous suture, just posterior to the pterion; 2) the inferior Rolandic point (IRP) is located along the Sylvian fissure 2 to 3 cm posteriorly to the ASyP, just anteriorly to Heschl’s gyrus (HeG), and lies underneath the highest aspect of the squamous suture, which also corresponds with the intersection of this suture with a vertical line originating at the preauricular depression, about 4 cm high in adults; and 3) the inferior frontal and precentral sulci meeting point (IFS/PreCS), which indicates the superior aspect of the opercular part (Op) of the IFS (up to 3 cm above the Sylvian fissure), which corresponds to the face motor activation/ventral premotor area (VPM), and which lies underneath the craniometric point known as the stephanion (St) which corresponds to the site of intersection of the coronal suture with the superior temporal line (Ribas et al., 2005b; Ribas et al., 2006).

ASyP: anterior Sylvian point; HeG: Heschl’s gyrus; IFG: inferior frontal gyrus; IFS/PreCS: inferior frontal and precentral sulci meeting point; IFS: inferior frontal sulcus; IRP: inferior Rolandic point; Op: opercular part; St: Stephanion (meeting point of the coronal suture and superior temporal line); Tr: triangular part of the inferior frontal gyrus; VPM: ventral premotor area.

Figure 3.9 The frontoparietal operculum. (A) A cadaveric specimen, (B) a sketch of the neural and sulcal morphology, and (C) a MR sagittal image, disclosing the frontoparietal structures and the fronto-opercular key points, and with the identification of 1) the V-shaped convolution constituted by the triangular part of the IFG located just superiorly to the ASyP, and usually containing a descending branch of the IFS; and of its following three U-shaped convolutions, respectively comprised by 2) the opercular part of the IFG, which always harbors the inferior part of the precentral sulcus; 3) the subcentral gyrus or Rolandic operculum composed of the inferior connection of the pre- and postcentral gyri enclosing the inferior part of the central sulcus; 4) the connecting arm between the postcentral and the supramarginal gyri that contains the inferior part of the postcentral sulcus; followed 5) by the C-shaped convolution constituted by the connection of the supramarginal and superior temporal gyri that encircle the posterior end of the SyF. The bottoms of the U-shaped convolutions and their related sulcal extremities can be either superior to or inside the fissure.

AAR: anterior ascending ramus of SyF; ASCR: anterior subcentral ramus of Sylvian fissure; ASyP: anterior Sylvian point; CS: central sulcus; HR: horizontal ramus of SyF; IFS: inferior frontal sulcus; IFS/PreCS: inferior frontal and precentral sulci meeting point; IRP: inferior Rolandic point; PAR: posterior ascending ramus of SyF; PostCS: postcentral sulcus; PreCS: precentral sulcus; PSCR: posterior subcentral ramus of Sylvian fissure; PSyP: posterior Sylvian point. (Adapted from Ribas et al., 2005a.)

The anterior V-shaped convolution is constituted by the triangular part (Tr) of the IFG, and is located just superiorly to the anterior Sylvian point (ASyP) where the horizontal (HR) and the anterior ascending (AAR) rami of the SyF originate, and delineate this convolution. Usually, the Tr contains a descending branch of the inferior frontal sulcus (IFS).

The most anterior U-shaped convolution is the opercular part (Op) of the IFG that encloses the inferior aspect of the precentral sulcus (PreCS) (Ono et al., 1990; Ebeling et al., 1989; Ribas et al., 2005a; Ribas, 2005b). The PreCS ends superiorly or adjacent to the SyF (in 44 percent of humans) or inside the SyF (56 percent) (Ribas et al., 2005a; Ribas, 2005b), always generating an anatomically constant U-shaped convolution which contains the inferior segment of the PreCS inside, and which corresponds anteriorly to the opercular part itself and posteriorly to its connection with the precentral gyrus (PreCG). Anteriorly, the Op is delimited by the anterior ascending ramus (AAR) of the SyF, and posteriorly by the anterior subcentral ramus (ASCR) of the SyF.

The middle U-shaped convolution is composed of the subcentral gyrus (SCG) that is constituted by the pre- (PreCG) and postcentral (PostCG) connection, also called the inferior frontoparietal “plis de passage” of Broca, and the Rolandic operculum that encircles the inferior part of the central sulcus (CS). The position of the base of the U-shaped convolution, here constituted by the SCG, in relation to the SyF varies in accordance with the position of the inferior Rolandic point (IRP) in relation to the SyF, and it can be found to be either superior to or adjacent to the SyF (in 83 percent of humans) or enclosed inside the SyF (17 percent) (Ribas et al., 2005a; Ribas, 2005b). The SCG or Rolandic operculum is delimited by the anterior (ASCR) and posterior (PSCR) subcentral rami of the SyF.

The third U-shaped convolution is composed of the connecting arm between the postcentral gyrus (PostCG) and the supramarginal gyrus (SMG) that contains the inferior part of the postcentral sulcus (PostCS), and which is delimited anteriorly by the posterior subcentral ramus (PSCR) of the SyF, and posteriorly by the posterior ascending ramus (PAR) of the SyF. According to the position of the inferior extremity of the PostCS in relation to the SyF, the bottom of this third U-shaped convolution can be either superior to the SyF (in 61 percent of humans) or inside the SyF (39 percent) (Ribas et al., 2005a; Ribas, 2005b).

The C-shaped convolution that completes the frontoparietal or suprasylvian operculum is constituted by the connecting arm between the postcentral (PostCG) and the superior temporal (STG) gyri, that encircle the posterior end of the SyF. The inferior margin of the SyF is related only to the STG that constitutes the temporal operculum.

The temporal operculum, which covers the inferior half of the insula, is solely comprised by the superior temporal gyrus (STG).

3.2.2.5 Frontotemporal Craniotomies and Exposures

Frontotemporal exposures are currently based on the pterional or fronto-temporo-sphenoidal craniotomy described by Yasargil (Yasargil, 1984a; Yasargil et al., 1975), and probably constitute the most utilized and systematized neurosurgical procedure.

The transsylvian approach (Yasargil et al., 1976; Yasargil et al., 2002b) provided by the pterional craniotomy is particularly useful for all sorts of anterior basal extrinsic lesions and for frontobasal, mesial temporal and insular intrinsic intracranial lesions (Yasargil, 1984a; Yasargil, 1994; Yasargil et al., 2002c). The more recently proposed basal frontotemporal craniotomies derived from pterional and supraorbital (Jane et al., 1967) craniotomies, such as the combined epi- and subdural approach with anterior clinoid removal (Dolenc, 1985; Dolenc, 1989), and the orbitozygomatic extension of pterional craniotomy (Fujitsu and Kuwabara, 1985; Hakuba et al., 1986), enhance the basal approaches and minimize brain retraction but do not disregard the opening of the Sylvian fissure to optimize its ideal exposure.

Once having understood the location of any given lesion in relation to the fronto-opercular key points, their corresponding cranial sites can aid in the correct placement of frontotemporal craniotomies, particularly with regard to their posterior extent (Figure 3.8).

While the most anterior aspect of the squamosal suture covers the always evident ASyP, which allows identification of the triangular and opercular parts of the inferior frontal gyrus, with the U-shaped opercular part always harboring the inferior aspect of the precentral sulcus, the highest segment of the squamosal suture lies over the subcentral gyrus with its highest point corresponding to the IRP. Just posterior to the IRP, there is the prominence formed by Heschl’s gyrus always underlying the postcentral gyrus (Figure 3.10).

Figure 3.10 (A) The wide opening of the Sylvian fissure discloses the insular apex (Ap) located at the anterior Sylvian point coronal level, just posteriorly to the anterior limiting sulcus (ALS) of the insula. The opercular part (Op) of the postcentral gyrus (PostCG) lies over Heschl’s gyrus (HeG), which separates the anterior polar plane from the posterior temporal plane of the temporo-opercular surface. (B) The depth of the anterior limiting sulcus of the insula, superior to the insular apex (Ap) level, is closely related to the most anterior aspect of the anterior horn of the lateral ventricle (AH), having in between mostly fibers of the anterior limb of the internal capsule.

AH: anterior horn of the lateral ventricle; ALS: anterior limiting sulcus; Ap: Sylvian fissure discloses the insular apex; CS: central sulcus; HeG: Heschl’s gyrus; IFS: inferior frontal sulcus; Op: opercular part of inferior frontal gyrus; Orb, inferior frontal gyrus, orbital part; PreCS: precentral sulcus; PreCG, precentral gyrus; PostCG, postcentral gyrus; SubCG, subcentral gyrus (pre- and postcentral gyri inferior connection arm); Tr: triangular part of the inferior frontal gyrus.

With the cortical exposure, the ASyP can usually be easily recognized due to its cisternal aspect, and the IRP lies 2 to 3 cm posteriorly to the ASyP along the mid-third of the horizontal or posterior SyF segment (Ono et al., 1990).

Since the opercular aspect of the postcentral gyrus (PostCG) always lies over Heschl’s gyrus (HeG) (Wen et al., 1999), the IRP also indicates the position of the anterior margin of HeG along the SyF, and hence the limit between the polar (PoPl) and the temporal planum (TePl) of the temporal opercular surface.

The posterior segment of the inferior frontal sulcus (IFS) and the IFS/PreCS key point can confine the superior limit of the opercular part of the IFG (about 3 cm above the Sylvian fissure in adults) (Ribas, 2005b), and indicate the face area of the PreCG, which roughly corresponds to the ventral premotor area (VPM) (Duffau, 2011b). Together with the ASyP and the IRP, they can then constitute important landmarks to estimate intraoperatively the so-called Broca’s area in the dominant hemisphere, and guide restricted removal of the inferior portion of the motor strip, which is safer in the non-dominant hemisphere, and occasionally necessary in vascular, tumor, and in epilepsy surgery (Hansebout, 1982). The frontal or Broca’s speech area occupies one or both frontal opercular convolutions anterior to the precentral gyrus of the dominant hemisphere (Hansebout, 1982; Rasmussen and Milner, 1975 apud Hansebout, 1982), and their removal is not justified. The pre- and postcentral face area can be removed, if pial barriers are respected, in order to preserve the blood supply to the upper Rolandic areas, and this may result in contralateral facial paresis that usually subsequently improves but that may leave some mild facial deficit (Hansebout, 1982; Rasmussen and Milner, 1975 apud Hansebout, 1982).

Considering that the IRP indicates the position of Heschl’s gyrus (HeG), the removal of the superior and middle temporal gyri posteriorly to the IRP in the dominant hemisphere carries a greater risk of permanent dysphasia (Hansebout, 1982; Rasmussen and Milner, 1975 apud Hansebout, 1982).

The opening of the SyF at the ASyP level discloses the apex of the insula at its depth (Türe et al., 1999), and the limen insula and the middle cerebral artery bifurcation are located a little deeper and anteriorly, 10 to 20 mm perpendicular to the ASyP itself (Yasargil et al., 2002b).

Opening of the Sylvian fissure posteriorly to the ASyP exposes the lateral aspect of the insula, and opening of its stem anteriorly to the ASyP leads to the suprasellar cisterns. When both are opened in conjunction with opening of the Sylvian anterior ascending ramus (AAR), this enables exposure of its continuous insular anterior limiting sulcus (ALS) or anterior periinsular sulcus (Türe et al., 1999), and thus of the anterior aspect of the insula situated behind the posterior orbital gyrus. The depth of the superior aspect of the anterior limiting sulcus (ALS) lies very close to the most anterior portion of the anterior horn, just in front of the head of the caudate nucleus, and is separated from the ventricle by local fibers, and by fibers of the anterior arm of the internal capsule (Türe et al., 1999) (Figure 3.11).

Figure 3.11 Frontotemporal craniotomy for exposure of the suprasylvian operculum and debulking of a glioblastoma multiforme within the inferior aspect of the left postcentral gyrus of a 75-year-old woman without focal deficits. (A) Sagittal MR image; and (B) coronal MR image showing the tumor over the flat aspect of the distal Sylvian fissure that corresponds to the temporal plane; (C) patient in the lateral position and intraoperative identification of the most superior aspect of the squamous suture, which corresponds to the intersection site between the squamous suture and a vertical line originating at the preauricular depression and which overlies the inferior Rolandic point (IRP); (D) exposure of the suprasylvian operculum through a frontotemporal craniotomy centered on the most superior segment of the squamous suture, and identification of the IRP, anterior Sylvian point, and the inferior frontal and precentral sulcus meeting point (IFS/PreCS), which enabled estimation of the topography of their related sulci and gyri; (E) surgical image and (F) CT scan image after the PostCG glioblastoma multiforme debulking.

ASyP: anterior Sylvian point; IFS/PreCS: inferior frontal and precentral sulci meeting point; IRP: inferior Rolandic point; Op: inferior frontal gyrus opercular part; PreAuDepr: preauricular depression; PreCG: precentral gyrus; SqSut: squamous suture; SSqSut: most superior aspect of the squamous suture, over IRP; STS: superior temporal sulcus; SyF: Sylvian fissure; TePl: temporal planum; Tr: inferior frontal gyrus triangular part.

3.2.2.6 Anatomical Remarks Pertinent to Common Frontotemporal Transcerebral Procedures

The frontotemporal approaches definitely constitute the most common and standard procedures in neurosurgical practice, given their frequently related extrinsic and intrinsic lesions and the very common use of the transsylvian route for Sylvian, insular, temporal mesial, subfrontal, and suprasellar lesions (Yasargil, 1984a; Yasargil et al., 1985; Yasargil et al., 2002a).

All of these approaches start with exposure of the frontoparietal and temporal opercula, and should have their temporal gyri recognized (Figure 3.9).

This section discusses the main anatomical issues related to the most standardized frontotemporal transcerebral procedures, with a particular focus on the procedures which require exposure of the temporal horn.

Approaches to the Temporal Horn of the Lateral Ventricle

Given the confinement of the temporal horn within the mesial portion of the temporal lobe, currently considered to belong to the limbic lobe (Federative Committee on Anatomical Terminology, 1998), this portion of the lateral ventricle can only be approached surgically through transcerebral routes and for their understanding, it is mandatory to have in mind some key anatomical features.

Although lying along the hippocampus, most of the temporal horn cavity itself lies mainly along the depth of the fusiform gyrus, about 3 cm deep from the temporal lobe lateral surface, and with its tip located also about 3 cm posterior to the temporal pole (Rasmussen and Jasper, 1958 apud Hansebout, 1977; Wiebe et al., 2001; Wen et al., 2006) (Figure 3.12).

Figure 3.12 (A) The fusiform gyrus, between the collateral sulcus and the occipitotemporal sulcus, constitutes the floor of the temporal horn (B).

CollS: collateral sulcus; FuG: fusiform gyrus; OccTeS: occipitotemporal sulcus; TeHorn: temporal horn with its choroid plexus.

Anteriorly to the tip of the temporal horn, while the bulk of the amygdala is enclosed within the anterior half of the uncus which can have its anterior and superior surfaces exposed through wide opening of the stem of the Sylvian fissure since its surfaces lie within the carotid cistern, the head of the hippocampus lies inside the posterior half of the uncus which cannot be exposed through any anterior and/or lateral cisternal approach. The posterior half of the uncus is incorporated in the most lateral aspect of the basal forebrain along a peduncular bundle of structures that pass between the limen insulae and the most anterior aspect of the temporal horn, and which includes the uncinated and the inferior fronto-occipital fascicles, fibers of the anterior commissure, and the upper extension of the amygdala toward the globus pallidus. Medially to them there is the ventral pallidal-striatum region located behind the anterior perforated substance and already within the basal forebrain, which is more medially continuous with the septal region. Posteriorly, this peduncular bundle of structures is continuous with the fibers that are running underneath the inferior limiting sulcus of the insula, which altogether correspond with the sublentiform part of the internal capsule and which spread laterally covering the temporal horn and the ventricular atrium.

While the different bundles of fibers that incorporate the temporal lobe into the rest of the cerebral hemisphere are collectively referred to as the temporal stem (Horel and Misantone, 1974; Cirillo et al., 1989; Türe et al., 1999; Ebeling et al., 1992a; Duvernoy, 1998; Wang et al., 2008; Choi et al., 2010; Yasargil et al., 2004), when passing underneath the inferior limiting sulcus of the insula, the continuous group of bundles of fibers that cover the temporal horn and the atrium more laterally are referred to as the sagittal stratum (Ludwig and Klinger, 1956; Türe et al., 2000). In order to perform an anterior temporal lobectomy, both the temporal stem and the sagittal stratum should then be divided.

Within the temporal horn, the choroidal fissure starts at the inferior choroidal point, between the head and the body of the hippocampus, lies posteriorly along all its medial aspect, and its opening detaches the mesial temporal structures from the thalamus (Nagata et al., 1988).

The approaches to the temporal horn are relatively standardized since they were developed mainly to remove the amygdala and the anterior portion of the hippocampus to treat patients with uncontrollable seizures due to mesial temporal sclerosis, and with good results.

Anterior Temporal Lobectomy and Lateral Approaches for Exposure of the Temporal Horn

Anterior temporal lobectomy for the surgical treatment of temporal lobe epilepsy was the first standardized procedure for the ventricular exposure and removal of deep and mesial temporal structures (Penfield and Flanigin, 1950a apud Maxwell and Tummala, 2004; Spencer et al., 1984), and is still currently used with different modifications. Its rationale is to remove initially the lateral (neocortical) aspect of the temporal lobe in order to expose the temporal horn and ease the removal of the amygdala and hippocampus (allocortical structures) (Figure 3.13).

Figure 3.13 All techniques for temporal lobectomies are based on exposure of the temporal horn, which can be achieved through different routes. (A) View of the insula after removal of the frontoparietal operculum and of the superior temporal gyrus, and exposure of the temporal horn through an opening along the inferior limiting sulcus of the insula. (B) View of the hippocampus within the temporal horn and of the temporal stem, after removal of the neocortical structures of the temporal lobe (temporal gyri and temporal lobe). (C) View of the choroidal fissure medially to the hippocampus. (D) View of the allocortical structures (hippocampus and amygdala) after the division of the temporal stem.

Amyg: amygdala; ChorF: choroidal fissure; HeG: Heschl’s gyrus; Hipp: hippocampus; InfLimS: inferior limiting sulcus; Ins: insula; TeHorn: temporal horn; TS: temporal stem; TePl: temporal planum.

The most original descriptions of standard temporal lobectomies proposed that the subpial dissection should be started along the summit of the superior temporal gyrus, pulling away its gray matter in order to expose the white matter that should then be suctioned until exposure of the pia-arachnoid which covers the insula and the middle cerebral artery branches. Currently, there is a trend to spare at least the most superior aspect of the superior temporal gyrus, initiating the subpial removal along its inferior aspect or immediately next and inferiorly to the superior temporal sulcus (Maxwell et al., 2004). Nevertheless, since the superior temporal gyrus constitutes the temporal operculum which covers the inferior half of the insula, its removal enhances the basal insular exposure and is still proposed by many authors (Wiebe et al., 2001), particularly with awake surgeries when in the dominant hemisphere (Duffau, 2011b). Once the insula and its inferior limiting sulcus are exposed, the suction should proceed through the temporal stem medially toward the middle fossa floor at an angle of 45°, and finally along the fusiform gyrus reaching the middle fossa skull base. The anterior incision should then be carried out anteroinferiorly until it meets the basal temporal incision (Hansebout, 1977).

After the coagulation and division of anterior and basal temporal veins, the whole disconnected anterior temporal lobe is lifted out, usually leaving some white matter overlying the temporal horn (Hansebout, 1977) which is then carefully removed by suction until the hippocampus is exposed.

Further dissection and exposure lead to the identification of the amygdala anteriorly, and of the head and body of the hippocampus within the temporal horn. The choroid plexus is seen as a fringe covering the head of the hippocampus, and its lifting allows the exposure and opening of the choroid fissure. En bloc removal of the amygdala and of the anterior part of the hippocampus within the parahippocampal gyrus can be done through further cutting of the medial temporal stem between the most anterior aspect of the choroidal fissure (anterior choroidal point) and the limen insulae, opening of the choroidal fissure leaving the choroid plexus superiorly attached to the thalamus, and division of the body of the hippocampus usually at the level of the lateral mesencephalic sulcus, which roughly corresponds to 2 cm of its length.

Regarding the posterior extent of the temporal lobectomy, it is interesting to point out that in 1952, Penfield and Baldwin (Penfield and Baldwin, 1952 apud Hansebout, 1977) and in 1955, Falconer and colleagues (Falconer et al., 1955 apud Hansebout, 1977) had suggested that the dominant temporal lobe resection could be extended posteriorly as far as the vein of Labbé. In 1958, Rasmussen and Jasper suggested that this removal could comprise 5 to 6 cm of the dominant temporal lobe (Rasmussen and Jasper, 1958 apud Hansebout, 1977), and in 1975, Rasmussen considered that, due to the variable position of the vein of Labbé, the safest landmark pertinent to the posterior level of the dominant temporal lobe resection would be the junction of the Rolandic and Sylvian fissures (Rasmussen, 1975 apud Hansebout, 1977). This point corresponds to the inferior projection of the central sulcus into the Sylvian fissure, which is known as the Inferior Rolandic Point and which is located underneath the highest aspect of the cranial squamous suture, 4 cm vertically above the preauricular depression (upper surface of the most posterior aspect of the zygomatic root, just anteriorly to the tragus) (Ribas et al., 2005a). The Inferior Rolandic Point is located along the Sylvian fissure about 2.0 to 2.5 cm posteriorly to the Anterior Sylvian Point (Ribas et al., 2005a), and about 5 cm from the temporal pole. Since there might be some difficulty in obtaining intraoperative measurements from the temporal pole, the preauricular depression can then be considered an easier and fairly good landmark to establish the posterior limit of the resection (Figure 3.14).