Subarachnoid space. Subarachnoid space size

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1 80 Subarachnoid space Martin M. Mortazavi 1, Nimer Adeeb 2, Fareed Rizq 2 and R. Shane Tubbs 3 1 University of Washington School of Medicine, Seattle, Washington, United States 2 Children s of Alabama, Birmingham, Alabama, United States 3 Seattle Science Foundation, Seattle, Washington, USA St George s University, School of Medicine, St Georges, Grenada University of Dundee, Dundee, UK Subarachnoid space size Cerebral subarachnoid space Variations the size of the subarachnoid space have been revealed by ultrasonographic (US) measurements mainly in neonates, infants, and children (Libicher and Troger 1992; Frankel et al. 1998; Lam et al. 2001; Narli et al. 2006; Sabouri et al. 2011; Okur et al. 2013); computed tomography (CT) and magnetic resonance (MR) studies have also been conducted. The width of the subarachnoid space correlates positively with weight, height, and head circumference; there is no significant gender difference (Narli et al. 2006; Sabouri et al. 2011). The width also correlates positively with age, peaking at 7 (Lam et al. 2001) or 13 (Okur et al. 2013) months and declining thereafter. This has been related to the development of the arachnoid villi and improved cerebrospinal fluid (CSF) drainage at 6 18 months of age (Sabouri et al. 2011). A wide subarachnoid space is therefore considered an anatomical variation during the first year of life. The site of measurement is also important: the craniocortical (CC) distance (between the cranium and cerebral hemisphere), sinocortical (SC) area (between the cerebral hemisphere and the superior sagittal sinus), or interhemispheric (IH) area (between the two hemispheres), measured from the narrowest to the widest point (Lam et al. 2001) (Fig. 80.1). Libicher and Troger (1992) reported the upper limits of the normal range as 3, 4, and 6 mm at the CC, SC, and IH respectively. Sabouri et al. (2011) reported higher upper limits: 5, 5.8, and 8 mm at the CC, SC, and IH, respectively. These authors also suggested that race, socioeconomic conditions, and dietary regime could affect the width of the subarachnoid space. Okur et al. (2013) reported the narrowest CC width of the subarachnoid space, over the range mm (Okur et al. 2013). Frankel et al. (1998) and Sabouri et al. (2011) reported narrower ranges of mm and 1 4 mm, respectively. However, measurement of the subarachnoid space to ventricular width ratio (SAS:VW ratio) could be a more accurate method for determining a normal value; the ratio between the shortest CC width of the subarachnoid space Figure 80.1 Anatomic landmarks and sonographic variables of the subarachnoid space in the coronal plane. C = cerebral cortex; SSS = superior sagittal sinus; CCW = craniocortical width; IHW = interhemispheral width; SCW = sinocortical width. Source: Lam et al. (2001) and the shortest width of the anterior horn of the lateral ventricle at the foramen of Monro are calculated (Okur et al. 2013). Spinal subarachnoid space The subarachnoid space dimensions measured between the arachnoid and the pia on the anterior and posterior sagittal diameters and the right and left transverse diameters are symmetrical between the right and left sides. In contrast, they are asymmetrical and vary widely on the anterior and posterior sides over the range 1 5 mm, and are larger on the posterior side. These measurements also vary and decrease monotonically from the cervical to the lumbar spine (Zaaroor et al. 2006). Others The subarachnoid space can be absent in locations where the brain is in close proximity or adherent to the arachnoid, and where the nerves and blood vessels exit the brain (Adeeb et al. 2013). Bergman s Comprehensive Encyclopedia of Human Anatomic Variation, First Edition. Edited by R. Shane Tubbs, Mohammadali M. Shoja and Marios Loukas John Wiley & Sons, Inc. Published 2016 by John Wiley & Sons, Inc. 959

2 960 Bergman s Comprehensive Encyclopedia of Human Anatomic Variation Hodges (1970) denied the presence of a sheet like subarachnoid space over the cerebral hemispheres and considered the arachnoid to be in direct contact with the gyri. Instead, he believed this space to be formed where the arachnoid bridges over the sulci, creating a space within each sulcus about 1 2 mm across and 5 10 mm deep (Hodges 1970). Subarachnoid cisterns The basilar cisterns underlie and partially surround the structures on the floor of the skull, and are named according to the major anatomical structures they bathe. The first detailed description and naming of most cisterns was provided by Key and Retzius (1875) and the cisterns have received more attention since. In the following text, deviations from the normal anatomy of the subarachnoid cisterns will be described. Chiasmatic cistern The location of the chiasmatic cistern in relation to the sellae can vary. It usually overlies the diaphragma sella and the sella turcica, but it sometimes lies more posterior over the dorsum sella (post fixed chiasm) or, less commonly, more anterior over the tuberculum sella (prefixed chiasm) (Gulsen et al. 2010). In cases of incompetent diaphragma sella, the chiasmatic cistern can extend into the sella turcica (Yaşargil 1984). Subdiaphragmatic cistern The size of this cistern is determined by the length of the subdiaphragmatic portion of the pituitary stalk, which can be completely supradiaphragmatic in cases where the opening of the diaphragma sellae is huge and the pituitary dome herniates upwards, resulting in a large cistern. It also varies according to: (1) the shape of the diaphragma sellae (flat, concave, or convex); (2) the size of the sellar cavity; (3) the size of the pituitary gland; (4) the location of the pituitary stalk; and (5) the size of the pituitary stalk (Di Ieva et al. 2012). Lamina terminalis (LT) cistern The anteroposterior (AP) length of the cistern s floor ranges from 14.0 to 28.0 mm. Its anterior boundary can extend as far as 5.0 mm anterior to the limbus sphenoidalis. Occasionally there is no significant anterior boundary, and the LT cistern communicates directly with the interhemispheric cistern (Wang et al. 2011a). The LM cistern can also extend inferoanteriorly to form a tent shaped recess above the interspace anterior to the OC, with an AP length of mm. Its superolateral wall is formed by the pia mater under the gyrus rectus (GR), and its inferior wall by the arachnoid between the optic nerves (ON). There are sometimes dividing membranes within this recess (Yaşargil 1984; Wang et al. 2011a). In some cases, the lateral walls partially adhere to each other in the middle part of the cistern (Wang et al. 2011a). The origin of the frontopolar arteries and the median artery of the corpus callosum (CC) (Yaşargil 1984; Wang et al. 2011a), and several (15 40) small subcallosal arteries, might be found within the lamina terminalis cistern in addition to its normal content. The subcallosal arteries have diameters of mm and can arise from the anterior communicating artery (ACoA), the A2 segment of the anterior cerebral artery (ACA), or the median artery of the CC (Wang et al. 2011a). Carotid cistern The medial wall of the carotid cistern can be absent, unilaterally or bilaterally. In such cases the cistern communicates freely with the chiasmatic cistern. In other cases, the arachnoid membranes separating the carotid, interpeduncular, and crural cisterns are absent, creating a confluent area through which cerebrospinal fluid can pass easily via the posterior part of the carotid cistern (Yaşargil 1984; Brasil and Schneider 1993; Froelich et al. 2008). Olfactory cistern The anterior part of this cistern is usually high and broad. Its highest point reaches mm above the olfactory bulb and its most lateral point extends mm beyond the bulb. Its posterior part is usually wide, reaching a maximal width of 1 cm (Wang et al. 2008). There may be a slit like extension of the olfactory cistern (5 13 mm) if the olfactory sulcus is deep (Yaşargil 1984; Wang et al. 2008). The size of the cistern s cavity also varies. It can be very narrow, with walls attaching to the olfactory structures and insufficient communication with the surrounding subarachnoid space (Wang et al. 2008). There are usually openings at the inferior wall of the olfactory cistern through which it communicates with the adjacent carotid and sylvian cisterns. They might be big (reaching up to 5 mm in diameter), small (less than 0.1 mm in diameter), or absent (Wang et al. 2008). There can also be up to four small olfactory arterial branches, mm in diameter. They arise from the main olfactory artery, anterior olfactory artery, posterior olfacorty artery (most common), or recurrent artery of Heubner (least common). The latter does not usually enter the cistern but the small arterial branches do. The course of these branches within the cistern depends on their origin, since they can begin anteriorly or posteriorly if they arise from the anterior or posterior olfactory artery, respectively. Infrequently, the arterial branches are derived from the orbital artery; these often have a more anterior origin and divide repeatedly within the cistern. Olfactory veins within the cistern are usually 1 3 in number and mm in diameter. They drain into the frontopolar vein or the origin of the superior sagittal sinus (Wang et al. 2008). Sylvian cistern The size and shape of this cistern depends on the relationship between the frontal and temporal lobes. In most cases it narrows superiorly as the frontal and temporal lobes approach each other

3 Chapter 80: Subarachnoid space 961 over a length of mm. At this level, the width of the cistern is usually about cm. Occasionally, the frontal and temporal lobes are closely apposed and cover the substance of the cistern. In other cases, part of the frontal lobe herniates into the adjacent temporal lobe or vice versa, distorting the structure of the cistern. In rare cases the cistern is clearly visible on the surface (Yaşargil 1984). In view of the above variations in the size and characteristics of the investing arachnoid trabeculae and membranes, the Sylvian cistern has been categorized into four types: type 1: large cistern, transparent and fragile arachnoid; type 2: small cistern, transparent and fragile arachnoid; type 3: large cistern, thickened and tough arachnoid; type 4: small cistern, thickened and tough arachnoid. The difficulty of microsurgical dissection of the Sylvian cistern increases from type 1 to type 4 (Yaşargil 1984). Some anatomists divide the cistern into anterior (sphenoidal) and posterior compartments in relation to the limen insulae. The anterior compartment extends from the origin of the middle cerebral artery laterally to the insula medially. It is limited superiorly by the posterior part of the orbital gyri and the lateral part of the anterior perforated substance, and inferiorly by the planum temporalis on the superior surface of the temporal lobe. The posterior compartment is located behind the limen insula and opens into the lateral cerebral surface. It is further subdivided into medial and lateral parts by the intermediate Sylvian membrane, which spans the interval between the upper and lower walls of the posterior compartment of the Sylvian fissure. The medial part is located between the medial parts of the opposing surfaces of the frontoparietal and temporal operculae, and extends into the insular cleft located between the insula and the insular surface of the opercula, its floor being formed by the upper surface of the temporal lobe. The lateral part is located in the lateral part of the cleft between the operculae. Its medial wall is formed by the intermediate Sylvian membrane, its lateral wall by the outer arachnoid membrane, and its superior and inferior walls by the lateral part of the opposing operculae (Inoue et al. 2009) (Fig. 80.2). Pericallosal cistern Some authors have subdivided the pericallosal cistern into three compartments: inferior, anterior, and superior. The inferior compartment is positioned above the lamina terminalis cistern and below the rostrum of the corpus callosum, and is bounded anteriorly by the outer arachnoid membrane and laterally by the paraterminal and paraolfactory gyri. The anterior compartment is bounded anteriorly by the outer arachnoid membrane, posteriorly by the genu of the corpus callosum, and laterally by the cingulate gyri. The superior compartment is located between the body of the corpus callosum inferiorly, and the outer arachnoid membrane spanning the interval between the paired cingulated sulci superiorly. It narrows posteriorly and ends on the superior surface of the splenium. There are no distinct divisions between the three compartments (Inoue et al. 2009). Other authors divide this cistern into anterior and posterior portions separated by arachnoid trabeculae at the branching of Figure 80.2 Anterior view of a drawing of a coronal section extending through the left sylvian fissure showing the lateral, intermediate, and medial sylvian membranes. The outer arachnoidal membrane forms the outer wall of the sylvian cistern and fissure. The lateral sylvian membrane spans the lateral part of the sylvian fissure and extends from the frontoparietal to the temporal operculum deep to the superficial sylvian veins. The intermediate sylvian membrane spans the interval between the medial part of the frontoparietal operculum above and the medial side of the superior temporal and Heschl s gyrus below. The medial sylvian membrane extends downward from the medial edge of the frontoparietal operculum and attaches to the insula on the medial side of the M2 segment of middle cerebral artery. Source: Inoue et al. (2009) the callosomarginal and pericallosal arteries, but with no distinct division (Yaşargil 1984). Interpeduncular cistern Lu and Zhu (2005a) have described the presence of two distinct arachnoid membranes within and dividing the interepeduncular cistern: the basilar artery (BA) bifurcation membrane and the posterior perforated membrane. The BA bifurcation membrane attaches caudally to the anterior walls of the BA bifurcation and the proximal segments of the posterior cerebral artery (PCA) and/or superior cerebellar artery (SCA). It spreads obliquely forward and upward and attaches to the anterior edge of the mamillary bodies and the diencephalic leaf of the Liliequist membranes. Laterally, it attaches via the arachnoid trabeculae to the diencephalic mesencephalic leaflets of Liliequist s membrane. It can appear as an intact membrane (most common), a porous and sparse network, or a dense and porous network (least common). It divides the cistern into two portions: a deep part, which communicates with the ambient cistern; and a superficial part which communicates with the oculomotor cistern. The superficial portion contains only the upper part of the basilar artery. The deep portion contains the bifurcation of the BA, the proximal portions of the PCA and the SCA, the oculomotor nerves, the posterior communicating artery (PCoA), the perforating branches of the

4 962 Bergman s Comprehensive Encyclopedia of Human Anatomic Variation Figure 80.3 Drawing demonstrating the sagittal view of the Liliequist membrane and the interpeduncular cistern. The arrows indicate the mesencephalic leaf and the arrowheads the diencephalic leaf of the Liliequist membrane; the star marks the medial and the lateral pontomesencephalic membrane. 1 = infundibulum and pituitary stalk; 2 = interpeduncular cistern; 3 = pons; 4 = mammillary bodies; 5 = prepontine cistern; 6 = optic chiasm; 7 = frontal lobe; 8 = chiasmatic cistern; 9 = BA bifurcation membrane; 10 = posterior perforated membrane. Source: Lu and Zhu (2005). arteries, the posterior perforated substance, and the posterior perforated membrane (Lu and Zhu 2005a). The posterior perforated membrane attaches caudally to the apex of the BA and the superior wall of the proximal segments of the PCA, and rostrally to the posterosuperior margins of both mamillary bodies. Laterally, it attaches to the diencephalicmesencephalic leaflets of the Liliequist membrane by arachnoid trabeculae. This membrane subdivides the deep portion of the cistern into anterior and posterior parts. The anterior part contains only mamillary bodies and the perforating arteries that supply them; the posterior part houses all the other contents (Lu and Zhu 2005a) (Fig. 80.3). Ambient cistern In contrast to the previous descriptions, Qi et al. (2011a) considered the ambient cistern as extending from the posterior edge of the oculomotor nerve anteriorly to the ascending part of the posterior mesencephalic membrane posteromedially (Qi et al. 2011a). The anterior and posterior perimesencephalic membranes of the ambient cistern are mostly discontinuous and are connected by sparse arachnoid trabeculae. However, a complete, intact perimesencephalic membrane (previously known as the superior cerebellar membrane) can sometimes be found (Qi et al. 2011a). In contrast to Yaşargil (1984) and Yaşargil et al. (1976), who divided the ambient cistern into supra and infratentorial compartments, Qi et al. (2011a) considered that the ambient cistern is the compartment extending above rather than across the level of the tentorial incisura, and further divided it into anterior and posterior parts. According to them, this exclusion of the infratentorial compartment is justified by the presence of a perimesencephalic membrane, arising at the level of the tentorial incisura and creating a relatively intact separation between the supra and infratentorial compartments. In contrast, there was no complete membrane except for scattered arachnoid trabeculae in the infratentorial compartment, which was defined as the cerebellopontine cistern anteriorly and the cerebellomesencephalic cistern posteriorly. The anterior part of the supratentorial compartment is located anterolaterally to the cerebral peduncle and superiorly to the anterior perimesencephalic membrane. The lateral wall is formed by the medial surface of the temporal lobe and the superior wall by the pia covering the lateral surface of the upper peduncle, the optic tract, and the uncus. The posterior compartment is located posterolaterally to the midbrain tegmentum and superiorly to the posterior perimesencephalic membrane. The lateral wall is formed by the medial occipital lobe and the superior wall by the pia covering the midbrain tegmentum, the lateral geniculate body, and the medial occipital lobe (Qi et al. 2011a) (Fig. 80.4, Fig. 80.5). On the basis of this description, Qi et al. (2011a) excluded the superior cerebellar artery and the trochlear nerve (which are infratentorial) from the contents of the ambient cistern. They also reported the P2 and P3 segments of the anterior choroidal artery and their branches as among the contents (Qi et al. 2011a). Figure 80.4 The ambient cistern and adjacent cisterns (inferior view). The anterior ambient cistern (light blue) communicates with the carotid cistern (yellow) anteriorly, the interpeduncular cistern (dark blue) medially, the cerebellopontine cistern inferiorly, and the oculomotor cistern (green) inferomedially. The posterior ambient cistern (light blue) borders the cerebellomesencephalic cistern inferiorly and the quadrigeminal cistern (purple) posteromedially. Car. = carotid; Chiasm. = chiasmatic; Interped. = interpeduncular. Source: Qi et al. (2011).

5 Chapter 80: Subarachnoid space 963 Figure 80.5 A C: Coronal schematic diagrams of the anterior and posterior ambient cisterns. A: Anterior ambient cistern. Its superior wall is formed by the pial layers covering the lateral surface of the peduncle, optic tract, and uncus, which merge to form a reflection before entering the choroid fissure. The inferior wall is formed by the anterior perimesencephalic membrane, the medial wall by the lateral surface of the peduncle, and the lateral wall by the parahippocampal gyrus. The anterior ambient cistern is separated from the cerebellopontine cistern inferiorly by the lateral part of the anterior perimesencephalic membrane. B and C: Posterior ambient cistern. Its superior wall is formed by the pial convergence of the midbrain tegmentum, the lateral geniculate body, and the medial occipital lobe. The inferior wall is formed by the posterior perimesencephalic membrane, the medial wall by the upper midbrain tegmentum, and the lateral wall by the medial occipital lobe. The posterior ambient cistern borders the cerebellomesencephalic cistern inferiorly through the horizontal part of the posterior perimesencephalic membrane and the quadrigeminal cistern medially by the ascending part. The medial posterior choroidal artery (PChA) usually passes through the ascending part and enters the quadrigeminal cistern. P.C.A. = posterior cerebral artery; S.C.A: superior cerebellar artery; A.Ch. A: anterior choroidal artery; Call. = callosum; Cer. Mes. = cerebellomesencephalic; Cer. Pon. = cerebellopontine; Chor. = choroidal; Corp. = corpus; Fiss. = fissure; Gen. = geniculate; Gyr. = gyrus; Parahippo. = parahippocampal; Pericall. = pericallosal; Quad. = quadrigeminal; Tra. = tract. Source: Qi et al. (2011). Crural cistern The crural cistern was considered by Qi et al. (2011a) as part of the anterior ambient cistern rather than a separate cistern. This is because there is no definite border or separation between them except for infrequent sparse arachnoid trabeculae (Qi et al. 2011a). It is occasionally divided into upper and lower parts by an intracrural membrane, extending between the posterior segment of the uncus and the cerebral peduncle (Inoue et al. 2009). Prepontine cistern The lower part of the anterior pontine membrane is occasionally absent, and in such cases the anterior inferior cerebellar artery exits the prepontine cistern to the cerebellopontine cistern by passing below (rather than through) the anterior pontine membrane (Matsuno et al. 1988). Cerebellomedullary cistern (cisterna magna) The cistern magna has a variable expansion dorsally (behind the vermis) depending on the degree of development of the falx cerebelli. It usually ends near the lobulus pyramis of the vermis but can extend all the way up the tentorium, mainly in cases of absent or small falx cerebelli (Yaşargil 1984; Matsuno et al. 1988). Occasionally, a median arachnoid sheet divides the cistern into two sagittal compartments. Another two paramedian sheets can extend into the dorsal spinal subarachnoid space, dividing it into separate compartments (Yaşargil 1984). Arachnoid trabeculae The arachnoid fibers and trabeculae that bridge the subarachnoid space and basilar cisterns usually have fine structures. Nevertheless, they tend to be thicker and tougher where the arteries and nerves pass through the trabeculated wall from one cisternal compartment to another. In most individuals, the three cisterns in which the arachnoid trabeculae and membranes are densest and present the greatest obstacles during operations are the interpeduncular and quadrigeminal cisterns and the cisterna magna (Matsuno et al. 1988). Variable arachnoid trabeculae that differ in their strength and density are also seen in other subarachnoid cisterns and elsewhere in the subarachnoid space. They usually enclose small blood vessels and adhere to the surface of larger blood vessels and nerves in the subarachnoid space (Yaşargil 1984). Arachnoid membranes The arachnoid membranes vary greatly in appearance and configuration. Some are reticulated and porous, such as the basilar artery bifurcation membrane; some are intact and dense without foramina, such as the diencephalic leaf of Liliequist s membrane; and others are plexiform or band shaped or cord shaped, such as the anterior cerebral membrane and

6 964 Bergman s Comprehensive Encyclopedia of Human Anatomic Variation the anterior choroidal membrane. Some trabecular arachnoid membranes differ in appearance and configuration among specimens, such as the basilar artery bifurcation membrane, which may be intact, porous, and sparse, or porous and dense (Lu and Zhu 2005b). Arachnoid Liliequist membrane The membrane that is today known as Liliequist s membrane (LM) was first described and illustrated by Key and Retzius (1875). In his pneumoencephalographic studies of the subarachnoid space and cisterns, Liliequist (1956, 1959) provided the first detailed anatomical description of this membrane, which was subsequently named after him. With the advance of neuroendoscopic and microscopic techniques, interest in studying the LM and other subarachnoid membranes and cisterns increased again, pioneered by Yaşargil s studies (Yaşargil et al. 1976). It was reported that failure to open the LM during third ventriculostomy could result in failure of the procedure (Buxton et al. 1998), which further increased the importance of identifying this membrane. However, since the earliest descriptions, controversy regarding the structure of the LM has continued. We therefore provide a detailed review of the various descriptions of it, including variations. Presence of LM The LM is found in most individuals, mainly separating the interpeduncular, prepontine, and chiasmatic cisterns. However, it was reported to be absent in 2 out of 13 cadavers (15.4%) studied by Froelich et al. (2008), and in 15 out of 35 cadavers (43%) studied by Zhang and An (2000). In such cases, free communication among the interpeduncular, prepontine, and chiasmatic cistern is expected, forming one large cistern. A carotid interpeduncular wall separating the interpeduncular and carotid cisterns was added by Brasil and Schneider (1993), which can be absent unilaterally or bilaterally. However, this seems to contradict the description of Froelich et al. (2008), who stated that the interpeduncular cistern communicates anterolaterally with the carotid cistern along the posterior communicating artery. These authors added that in cases of single LM (see Single membrane below), the prepontine cistern can communicate with the carotid cistern anterolaterally around the posterolateral free border of the LM, and with the ambient cistern laterally along the course of the posterior cerebral artery and across the posterolateral free border of the LM (Froelich et al. 2008). Moreover, Brasil and Schneider (1993) described free communication between the carotid and crural cisterns superolateral to the free margin of the LM. Matsuno et al. (1988) also reported communication with the ambient and crural cisterns. Types of LM On the basis of the various descriptions, the LM has been divided into three types. In type A it is composed of two leaves, diencephalic (DL) and mesencephalic (ML), which originate at the dorsum sellae. In type B it appears as one leaf anteriorly and Figure 80.6 variations of Liliequist s membrane (LM). A, the diencephalic leaf (DL) and mesencephalic leaf (ML) originate along the dorsum sellae and course separately toward the diencephalon and basilar bifurcation, respectively. B, with two posterior leaves including the diencephalic leaf attached to the diencephalon and mesencephalic leaf toward the basilar bifurcation. C, as a single membrane attached posterosuperiorly to the diencephalon between the infundibulum and mamillary bodies. Source: Froelich et al. (2008). two leaves posteriorly, the LM arising as a single membrane and then splitting into DL and ML. In type C, the most common, the LM appears as a single (diencepahlic) membrane (Froelich et al. 2008) (Fig. 80.6). Single membrane (Type C) The classic description by Liliequist (1956, 1959) was of a single membrane with forward convexity, extending from the dorsum sellae to the anterior edge of the mamillary bodies (Type C). Brasil and Schneider (1993) gave a similar description. Yaşargil (1984) and Yaşargil et al. (1976) added that this well developed membrane stretches like a curtain from one mesial temporal surface to another. A full description of the type C LM would therefore be of a single, non fenestrated membrane that arises inferiorly from the basilar arachnoid membrane, covering the dorsum sellae and the posterior clinoid processes, curving anteriorly and attaching superiorly to the pia of the hypothalamus just anterior the mamillary bodies, posterior to the infundibulum. Laterally, it attaches to the pia of the mesial surface of the temporal uncus (Vinas and Panigrahi 2001). This lateral extension (at the carotid interpeduncular wall) is perforated by the oculomotor nerve and the posterior communicating artery (Brasil and Schneider 1993). Lateral extension Other authors disagree on the extent of the lateral extension. Epstein (1965) described the LM as a semilunar transverse membrane stretching obliquely between the oculomotor nerves, which is similar to the description by Matsuno et al. (1988). Such a termination would render the LM a continuous, unperforated membrane. On the other hand, Fox (1989) accepted both types of lateral extension and added that it can also end just before (medial to) the oculomotor nerve, to which it is then connected via arachnoid trabeculae. Similar results were reported by Anik

7 Chapter 80: Subarachnoid space 965 et al. (2011) and Fushimi et al. (2003). Froelich et al. (2008) described the different relationships with the oculomotor nerve. In 6 out of 13 specimens (46%) the nerve was surrounded by the lateral aspect of the ML, creating a separate oculomotor cistern. In two specimens (15.4%) it ran between two lateral leaves of the ML. The superior leaf was attached to the pia of the mesial surface of the temporal lobe, and the inferior leaf was continuous with the arachnoid above and below the level of the incisura. In three specimens (23%) the nerve was above the mesencephalic leaf and connected to it by an arachnoidal ring (Froelich et al. 2008). Zhang et al. (2012) agreed that the ventral wall of the oculomotor cistern is partly formed by the lateral extension of the LM (and partly by the basal arachnoid mater), but they regarded the dorsal membrane (oculomotor membrane) as a different entity and differentiated it from the temporal membrane, which they described as the lateral extension of the DL (Zhang et al. 2012). Superior extension Regarding its superior attachment, Vinas and Panigrahi (2001) added that as well as the premamillary attachment described above there can also be a retromamillary attachment. This is surgically important, as in these patients it is less important to fenestrate the LM during third ventriculostomy because the third ventricle will be opened into the interpeduncular cistern following fenestration of the floor (Vinas and Panigrahi 2001). Similar findings were also described by Matsuno et al. (1988) regarding the attachment of the DL. Inoue et al. (2009) also reported both types of superior attachments of the DL; they found that it was attached to the posterior edge of the mamillary bodies (retromamillary) in 47% of brains, the apex of the mamillary bodies in 33%, and the anterior edge of the mamillary bodies (premamillary) in 20%. On the other hand, Anik et al. (2011) reported that direct attachment to the mamillary bodies was the most common type, found in 17 out of 24 specimens (70.8%). Lu and Zhu (2003) described a more anterior superior attachment of the DL on the posterior surface of the infundibulum all over its course, found in four out of eight cadavers (50%). In the other four (50%) the DL had a superior attachment that was mm posterior to the infundibulum (premamillary) (Lu and Zhu 2003). Free border Brasil and Schneider (1993) divided the single LM into three parts (or walls) on the basis of its cisternal relationships: two carotid interpeduncular walls laterally and a chiasmaticinterpeduncular wall medially. Each of these walls could be selectively absent. They also added that, besides its classic superior attachment, the LM attaches to the pia of the inferior surface of the optic tracts. There is a free margin between the inferolateral border of the optic tracts and the uncus. Superolateral to this free margin there is free communication between the carotid and crural cisterns (Brasil and Schneider 1993). The same free margin was also reported by Lu and Zhu (2003) in the DL of the LM. On the other hand, Zhang et al. (2012) observed this free lateral border of the DL between the inferolateral border of the optic tracts and the oculomotor sheath in only 4 out of 24 specimens (16.7%; Zhang et al. 2012). Agreeing about the lateral extension of the LM, Epstein (1965) and Fox (1989) described the presence of free border lateral to or at (medial to) the oculomotor nerve, respectively. Froelich et al. (2008) described the free border as located posterolaterally between the central attachment to the diencephalon and tentorial edge in type C and in the DL of types A and B, and at the posterior end of the ML in front of the basilar bifurcation in types A and B. Zhang and An (2000) claimed that the free border of the LM is located on its superoposterior part. All these authors agree that the free border becomes attached to the surrounding structures via arachnoid trabeculae. With some exceptions, these trabeculae are not considered part of the LM; they also render it otiose to identify the border of an irregular arachnoid trabecular network because it varies greatly and could be the cause of variations in gross anatomical findings. This was also supported by the findings of Anik et al. (2011), who claimed that various free edges were found in the ML in 7 out of 24 specimens (29.2%) while it was totally closed in 12 (50%). The carotid chiasmatic walls Brasil and Schneider (1993) contradicted the previous descriptions by Epstein (1965), Fox (1989), and Yaşargil (1984), indicating that the LM can surround the infundibulum to create a hypophyseal cistern. They suggested that these surrounding membranes represent the carotid chiasmatic walls (or chiasmatic membrane) and added that the LM is always located posterior to the infundibulum (Brasil and Schneider 1993). The same description was offered by Vinas and Panigrahi (2001) who added that, although the chiasmatic membranes arise from the LM, they represent a different entity. These controversies were further clarified by Zhang and An (2000). Using a modified E12 sheet plastination method, cadaveric dissections, and electron microscopy, these authors concluded that the arachnoid membrane like LM has an architecture significantly different from that of the arachnoid trabeculated carotid chiasmatic walls. The LM appears thicker, unperforated, and with a cleaner surface, and is composed of two layers of arachnoid mater (presumed to be the DL and ML described in other studies) that are better visualized in the middle portion. However, no double layers could be found in 15 out of 35 cadavers (43%). On the other hand, the carotid chiasmatic walls are composed of accumulated, irregularly oriented arachnoid trabeculae that extend from the LM to the pia mater covering the surface of the optic chiasm. Unlike the LM, these walls have openings of various sizes and are penetrated by perforating arteries from the posterior communicating and internal carotid arteries, giving them a vascularized appearance. This is surgically important as it suggests that the most suitable site for opening the LM and approaching the interpeduncular cistern is

8 966 Bergman s Comprehensive Encyclopedia of Human Anatomic Variation the part of the LM between the carotid chiasmatic wall and the oculomotor nerve (Zhang and An 2000), with careful attention to the posterior communicating artery and its branches (Lu and Zhu 2003). Regarding the lateral extension and free border, Zhang and An (2000) stated that the free border of the LM is located on its superoposterior part and continues along the entire length, and can be grossly visualized. At this free border, the LM is connected via arachnoid trabeculae to the surrounding structures including the infundibulum and mamillary bodies. Laterally, it attaches to neither the uncus nor the oculomotor nerve. Instead, it fans out near the free edge of the tentorium and continues with the arachnoid mater covering the tentorium below and above the tentorial notch. Zhang and An (2000) did not comment on the anterior attachment of the LM, but regarded the membrane as continuous anteroinferiorly with the arachnoid mater covering the tentorium, the dorsum sellae, and the clivus (Fig. 80.7). Double membranes (Types A, B) The LM was first described as double membranes by Matsuno et al. (1988). Other authors including Inoue et al. (2009) have given similar descriptions. The classic description is of an arachnoid membrane arising from the arachnoid covering of the dorsum sellae and the posterior clinoid processes (some also add the arachnoid covering of the posterior petroclinoid and adjacent tentorial edge; Froelich et al. 2008), extending between the oculomotor nerve and then splitting into two leaves, the DL and ML (type B). According to these authors, the previous description of a single membrane by Liliequist was of the DL; this can be visualized by the pneumatograph due to its unperforated nature, in contrast to the perforated ML (see section The mesencephalic below) which was visualized in later cadaveric studies (Matsuno et al. 1988) (Fig. 80.8). The diencephalic The DL is a thicker and mostly unperforated membrane that attaches to the posterior or anterior edge or to the tips of the mamillary bodies, separating the interpeduncular and chiasmatic cisterns. At its superior end, the DL sends many arachnoid trabeculae to attach to the surrounding structures, including the infundibulum and mamillary bodies (Matsuno et al. 1988; Froelich et al. 2008; Inoue et al. 2009). The DL is thick in most cases (54%: Anik et al. 2011; 75%: Lu and Zhu 2003), but can be thin (25%: Lu and Zhu 2003; 46%: Anik et al. 2011). It is also mostly semitransparent (83.3%: Anik et al. 2011; 87.5%: Lu and Zhu 2003) but can be opaque (12.5%: Lu and Zhu 2003; 16.7%: Anik et al. 2011). It can also be a largely porous trabeculated membrane (Wang et al. 2011b; Zhang et al. 2012), and in these cases it may have only a small crescent shaped dense non porous part in its anteroinferior attachments (Zhang et al. 2012). The Dl was reported to be absent in 3 out of 24 cadavers (12.5%) by Anik et al. (2011), 6 out of 24 cadavers (25%) by Zhang et al. (2012), and 5 out of 15 cadavers (26.7%) by Wang et al. (2011b). In these cases, the chiasmatic and interpeduncular cisterns merge into one (Wang et al. 2011b). As expected from the description of an unperforated DL, the lateral attachment of the LM is related to the arachnoid sheath surrounding the oculomotor nerve, with numerous trabeculae extending from the oculomotor nerve to the uncus and tentorium (Matsuno et al. 1988; Inoue et al. 2009). Lu and Zhu (2003) reported a case with a unilateral window in the DL connecting the posterior communicating cistern with the interpeduncular cistern (Lu and Zhu 2003). The length of the DL from the inferior to the superior edge is within the range mm (mean 10.8 mm). The width at the inferior edge is mm (mean 19.9 mm), and the width at the superior edge is mm (mean 9.5 mm) (Wang et al. 2011b). The mesencephalic The ML is a thinner membrane, mostly perforated (by the basilar artery), that extends backward and attaches to the pontomesencephalic junction, separating the interpeduncular and prepontine cisterns (Matsuno et al. 1988; Froelich et al. 2008; Inoue et al. 2009). Lu and Zhu (2003) described a different course and termination of the ML (see below). Other authors have reported a free posterior border of the ML connected to the basilar bifurcation and surrounding structures by arachnoid trabeculae (Froelich et al. 2008). Occasionally, the ML is thick (or equal in thickness to the DL) and has small perforations. It can also form a tight cuff around the basilar artery, but more commonly it has a large opening through which the basilar artery ascends (Matsuno et al. 1988; Inoue et al. 2009). The length of the ML from the anterior to the posterior end is over the range mm (mean 4.8 mm). The width at its posterior attachment is mm (mean 4.8 mm). In cases of type A LM, the width of the anterior edge of the ML is similar to that of the inferior edge of the DL. In cases of type B, the width of the anterior edge of the ML is mm (mean 12.6 mm; Wang et al. 2011b). Findings of Froelich et al. In the cadaveric study of Froelich et al. (2008), the LM was identified in 11 out of 13 cadavers (85%). When present, it consisted of either one leaf (type C, most common) or two leaves (type A, B). Type A was found in two specimens (15.4%) and, in addition to the classic description, the authors reported a lateral attachment of the DL to the paramedian perforating substance and of the ML to the pia of the parahippocampal gyri (mesial surface of the temporal lobe). Type B was also found in two specimens (15.4%) where the LM arose as a single membrane and then split into two leaves, DL and ML, with connections similar to those in type A. The authors described the free borders of these two types as located in the posterior end of the ML, in front of the basilar bifurcation, but occasionally covering part of the basilar tip. Type C was found in seven specimens (53.8%), with a posterolaterally located free

9 Chapter 80: Subarachnoid space 967 Covering Inferior surface of tentorium Covering superior surface of tentorium Free border of Lillequist s membrane optic dorsum nerves sellae midbrain tentorium Covering dorsum sellae and clivus Covering superior surface of tentorium A anterior and posterior clinoid processes Free border of Lillequist s membrane B Covering Inferior surface of tentorium Petorating vessel Attaching onto the lateral borders of the optic chiasm Carotidchiasmatic wall Trabecular networks C Lillequist s membrane Figure 80.7 Major arachnoid trabeculae within the subarachnoid cisterns. (a) Superior view of the sellar area and tentorial notch. The shaded area represents Liliequist s membrane and its anteroinferior and lateral attachments. (b) Diagrammatic representation of Liliequist s membrane. The free border surrounds the anterior aspect of the brainstem and extends posteriorly to the roots of the trigeminal nerves. (c) Relationship between Liliequist s membrane and the carotidchiasmatic walls. The carotid chiasmatic walls are arachnoid trabecular networks that continue with loose and irregular arachnoid trabecular networks on the surface and along the free border of Liliequist s membrane. Source: Zhang and An (2000). border between the central diencephalic attachment and the tentorial edge. This free border allowed the prepontine and carotid cisterns to communicate with each other (Froelich et al. 2008). The authors added that the LM is continuous with the arachnoid covering the temporal fossa floor and the superior aspect of the tentorium, above the tentorial edge. Below the tentorial edge the membrane was continuous with the arachnoid

10 968 Bergman s Comprehensive Encyclopedia of Human Anatomic Variation Figure 80.8 Side view of Liliequist s membrane. Source: Wang et al. (2011b). covering the inferior aspect of the tentorium and posterior fossa dura (Froelich et al. 2008). They also agreed with other authors that the LM is continuous laterally with the lateral pontomesencephalic membrane (Matsuno et al. 1988), which separates the ambient cistern from the cerebellopontine cistern, and with the caudal oculomotor membrane (Vinas et al. 1994, 1996a, b), as they share a common embryological origin (Froelich et al. 2008). Relation with the posterior communicating artery Froelich et al. (2008) also described the different relationships of the LM with the posterior communicating artery. In specimens with a single membrane (type C) and a posterolateral free border, the posterior communicating artery coursed above the membrane and crossed the free border to join the posterior cerebral artery. In specimens with a DL and ML, the artery coursed between those leaves (Froelich et al. 2008) (Fig. 80.9). Zhang et al. (2012) stated that, in all cases, the posterior communicating artery courses lateral to the lateral border of the DL. On the other hand, Lu and Zhu (2003) stated that the artery penetrates the DL to enter the interpeduncular cistern. They also reported one specimen where a unilateral posterior communicating artery penetrated the DL at its inferior border, coursed within the leaf, and left via the superior border to enter the deep part of the interpeduncular cistern (Lu and Zhu 2003). Zhang et al. (2012) found the LM to be composed of two layers of arachnoid mater, named the basal and attaching layers; this was similar to the description by Zhang and An (2000). The basal layer arises from the basal arachnoid mater covering the dorsum sellae and posterior clinoid processes, which multiplies into several cellular layers at the basal attachments of the LM, then extends superoposteriorly and folds upon itself to form the uninterrupted basal layer of the LM. This basal layer extends as the inferior part of the DL (no comments were made on the ML) and extends laterally beyond the oculomotor nerve to continue with the arachnoid mater covering the tentorium below and above the tentorial notch. In the midsagittal plane, the basal part constituted more than half the entire length of the LM in two out of four specimens (50%) and less than 20% of the length in one (25%). The attaching layer spreads from the posterior border of the basal layer to attach on the surrounding structures. The diencephalic part of this layer (attaching the DL to the mamillary bodies) is composed of accumulated arachnoid trabeculae. In contrast to previous studies (see above), Zhang et al. (2012) therefore considered these arachnoid trabeculae as a part of the LM. Regarding the gross lateral extension, Zhang et al. (2012) described a triangular membrane, found in 14 out of 24 specimens (58.3%), that spread from the lateral free border of the diencephalic membrane to the mesial temporal uncus. They termed it the temporal membrane and considered it to be part of the DL. This membrane separates the carotid from the ambient cistern and sends variable arachnoid trabeculae to attach to the Figure 80.9 Three-dimensional illustration (sagittal cut, oblique view) of Liliequist s membrane composed of two separate diencephalic (aqua) and mesencephalic (pink) leaves that originate at the dorsum sellae (Type A). Note the posterior communicating artery coursing above the mesencephalic leaf. Inset, with removal of the diencephalic leaf, the mesencephalic leaf can be seen surrounding the oculomotor nerve and reflecting onto the tentorial edge. Source: Froelich et al. (2008)..

11 Chapter 80: Subarachnoid space 969 arachnoid sheath surrounding the oculomotor nerve. In contrast to the DL, the temporal membrane is usually porous and trabeculated, and is occasionally sheet like with small openings. When this membrane is present, the posterior communicating artery always courses above it (Zhang et al. 2012). The ML was divided by Zhang et al. (2012) into three parts, one medial ML and two lateral ML. The medial ML extends between the oculomotor nerves and was referred to as the ML in previous studies, separating the interpeduncular and prepontine cisterns (Zhang et al. 2012). A similar division was used by Qi et al. (2011a), who also used the name anterior perimesencephalic membrane to describe the ML. The relationships between the DL and the medial ML are the types described earlier as A, B, or C (the classical classification of the LM). However, Zhang et al. (2012) found type B to be the most common, followed by type A then C. When the DL is absent, the medial mesencephalic membrane is defined as the combination of an anteriorly located crescent shaped dense non porous part, which attaches to the basal arachnoid membrane (exactly the same as that of the DL) and courses between the oculomotor nerves (to which it attaches laterally), and a posteriorly located porous trabeculated part that extends to the caudal end of the medial ML (Zhang et al. 2012) (Fig ). According to Zhang et al. (2012), regardless of the type of medial ML, its caudal end can be above, at, or below the level of the terminal basilar bifurcation. The lateral ML is equivalent to the lateral pontomesencehalic membrane. It separates the ambient and cerebellopontine cisterns and communicates medially with the DL and medial ML below the oculomotor nerve (the part of the LM that forms part of the ventral sheath of the oculomotor), and attaches to the anterior tentorial edge laterally. Anteriorly it attaches to the basal arachnoid mater covering the posterior border of the oculomotor trigone, and posteriorly it sends out variable arachnoid trabeculae to attach to the anterolateral pontomesencephalic junction. The size of the non porous sheet like portion of this membrane varies, and is inversely proportional to the non porous sheet like portion of the DL (or ML when the DL is absent). When the non porous sheet like part of the DL or ML is prominent the counterpart of the lateral ML is smaller, and vice versa (Zhang et al. 2012). On the basis of these findings, Zhang et al. (2012) proposed another classification of the LM according to presence (type I) or absence (type II) of the DL. In type I, most common, the LM appears similar to that previously described as being divided into types A, B, and C. In type II only the medial and lateral ML are present, with a course similar to that described above and with no separation between the interpeduncular cistern and the chiasmatic cistern (Zhang et al. 2012). Regarding the oculomotor membrane, Zhang et al. (2012) distinguished it from the temporal membrane and described three coronal configurations based on its relationship to the carotid membrane: inverted Y shaped (most common); inverted V shaped; and inverted U shaped (least common). In the inverted Y shaped configuration, the lateral carotid membrane constitutes the upper arm of the inverted Y and attaches superiorly on the mesial temporal uncus near the attachment of the temporal membrane. In the inverted V shaped configuration, the lateral carotid membrane is absent and the apex of the inverted V attaches directly to the mesial temporal uncus near the attachment of the temporal membrane. In the inverted U shaped configuration, the dome of the oculomotor membrane adheres to the dorsal surface of the oculomotor nerve and can be connected to the mesial temporal uncus by scattered arachnoid trabeculae, which represents a less well developed lateral carotid membrane. According to the authors, the LM can attach to the mesial temporal uncus either directly by its temporal membrane or indirectly by the oculomotor membrane (Zhang et al. 2012). Triple membranes Diencephalic mesencephalic membrane (DML) The LM was first described as comprising three leaves by Lu and Zhu (2003). These leaves were the DL, ML, and the diencephalic mesencephalic leaf (DML). These authors described the ML (but not the DL) differently from others. In their study of eight cadavers, Lu and Zhu stated that the ML represents an intact, thick, dense, and unperforated membrane that forms the anterioinferior wall of the interpeduncular cistern. According to them, the ML intersects with the DL at the dorsum sellae and posterior clinoid processes rather than originating from this point. Rostrally, it spreads along the surface of the diaphragma sellae and attaches to the posterior surface of the infundibulum, mm above its inferior bottom, and fuses with the basal chiasmatic membrane (the arachnoid covering the floor of the chiasmatic cistern). In most cases (seven out of eight specimens) the ML was totally above the diaphragma sellae and did not enter the intrasellar region. In Figure Schematic drawing of (a, b) type I and (c) type II of Liliequist s membrane. Source: Zhang et al. (2012).