Subarachnoid Space Martin M

80 Subarachnoid space Martin M. Mortazavi1, Nimer Adeeb2, Fareed Rizq2 and R. Shane Tubbs3 1University of Washington School of Medicine, Seattle, Washington, United States 2Children’s of Alabama, Birmingham, Alabama, United States 3Seattle 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) Figure 80.1 Anatomic landmarks and sonographic variables of or 13 (Okur et al. 2013) months and declining thereafter. This the subarachnoid space in the coronal plane. C = cerebral cortex; has been related to the development of the arachnoid villi and SSS = superior sagittal sinus; CCW = craniocortical width; improved cerebrospinal fluid (CSF) drainage at 6–18 months of IHW = interhemispheral width; SCW = sinocortical width. age (Sabouri et al. 2011). A wide subarachnoid space is therefore Source: Lam et al. (2001) 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), and the shortest width of the anterior horn of the lateral ventri- sinocortical (SC) area (between the cerebral hemisphere and the cle at the foramen of Monro are calculated (Okur et al. 2013). superior sagittal sinus), or interhemispheric (IH) area (between the two hemispheres), measured from the narrowest to the Spinal subarachnoid space widest point (Lam et al. 2001) (Fig. 80.1). Libicher and Troger The subarachnoid space dimensions measured between the (1992) reported the upper limits of the normal range as 3, 4, and arachnoid and the pia on the anterior and posterior sagittal 6 mm at the CC, SC, and IH respectively. Sabouri et al. (2011) diameters and the right and left transverse diameters are sym- reported higher upper limits: 5, 5.8, and 8 mm at the CC, SC, metrical between the right and left sides. In contrast, they are and IH, respectively. These authors also suggested that race, asymmetrical and vary widely on the anterior and posterior socioeconomic conditions, and dietary regime could affect the sides over the range 1–5 mm, and are larger on the posterior width of the subarachnoid space. Okur et al. (2013) reported side. These measurements also vary and decrease monotonically the narrowest CC width of the subarachnoid space, over the from the cervical to the lumbar spine (Zaaroor et al. 2006). range 0.5–6 mm (Okur et al. 2013). Frankel et al. (1998) and Sabouri et al. (2011) reported narrower ranges of 1.9–5.7 mm Others and 1–4 mm, respectively. However, measurement of the suba- The subarachnoid space can be absent in locations where the rachnoid space to ventricular width ratio (SAS:VW ratio) could brain is in close proximity or adherent to the arachnoid, and be a more accurate method for determining a normal value; the where the nerves and blood vessels exit the brain (Adeeb et al. ratio between the shortest CC width of the subarachnoid space 2013).

Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation, First Edition. Edited by R. Shane Tubbs, Mohammadali M. Shoja and Marios Loukas. © 2016 John Wiley & Sons, Inc. Published 2016 by John Wiley & Sons, Inc.

959 960 Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation

Hodges (1970) denied the presence of a sheet‐like suba- The origin of the frontopolar arteries and the median artery rachnoid space over the cerebral hemispheres and considered of the corpus callosum (CC) (Yaşargil 1984; Wang et al. 2011a), the arachnoid to be in direct contact with the gyri. Instead, he and several (15–40) small subcallosal arteries, might be found believed this space to be formed where the arachnoid bridges within the lamina terminalis cistern in addition to its normal over the sulci, creating a space within each sulcus about 1–2 mm content. The subcallosal arteries have diameters of 0.1–0.3 mm across and 5–10 mm deep (Hodges 1970). 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). Subarachnoid cisterns Carotid cistern The basilar cisterns underlie and partially surround the struc- The medial wall of the carotid cistern can be absent, unilaterally tures on the floor of the skull, and are named according to or bilaterally. In such cases the cistern communicates freely with the major anatomical structures they bathe. The first detailed the chiasmatic cistern. In other cases, the arachnoid membranes description and naming of most cisterns was provided by Key separating the carotid, interpeduncular, and crural cisterns are and Retzius (1875) and the cisterns have received more atten- absent, creating a confluent area through which cerebrospinal tion since. In the following text, deviations from the normal fluid can pass easily via the posterior part of the carotid cistern anatomy of the subarachnoid cisterns will be described. (Yaşargil 1984; Brasil and Schneider 1993; Froelich et al. 2008).

Chiasmatic cistern Olfactory cistern The location of the chiasmatic cistern in relation to the sellae The anterior part of this cistern is usually high and broad. Its can vary. It usually overlies the diaphragma sella and the sella highest point reaches 3.0–4.0 mm above the olfactory bulb and turcica, but it sometimes lies more posterior over the dorsum its most lateral point extends 2.0–3.0 mm beyond the bulb. Its sella (post‐fixed chiasm) or, less commonly, more anterior over posterior part is usually wide, reaching a maximal width of 1 the tuberculum sella (prefixed chiasm) (Gulsen et al. 2010). In cm (Wang et al. 2008). There may be a slit‐like extension of cases of incompetent diaphragma sella, the chiasmatic cistern the olfactory cistern (5–13 mm) if the olfactory sulcus is deep can extend into the sella turcica (Yaşargil 1984). (Yaşargil 1984; Wang et al. 2008). The size of the cistern’s cavity also varies. It can be very nar- Subdiaphragmatic cistern row, with walls attaching to the olfactory structures and insuffi- The size of this cistern is determined by the length of the sub- cient communication with the surrounding subarachnoid space diaphragmatic portion of the pituitary stalk, which can be com- (Wang et al. 2008). pletely supradiaphragmatic in cases where the opening of the There are usually openings at the inferior wall of the olfac- diaphragma sellae is huge and the pituitary dome herniates tory cistern through which it communicates with the adjacent upwards, resulting in a large cistern. It also varies according to: carotid and sylvian cisterns. They might be big (reaching up to (1) the shape of the diaphragma sellae (flat, concave, or convex); 5 mm in diameter), small (less than 0.1 mm in diameter), or (2) the size of the sellar cavity; (3) the size of the pituitary gland; absent (Wang et al. 2008). (4) the location of the pituitary stalk; and (5) the size of the pitu- There can also be up to four small olfactory arterial branches, itary stalk (Di Ieva et al. 2012). 0.1–0.35 mm in diameter. They arise from the main olfactory artery, anterior olfactory artery, posterior olfacorty artery (most Lamina terminalis (LT) cistern common), or recurrent artery of Heubner (least common). The The anteroposterior (AP) length of the cistern’s floor ranges latter does not usually enter the cistern but the small arterial from 14.0 to 28.0 mm. Its anterior boundary can extend as far as branches do. The course of these branches within the cistern 5.0 mm anterior to the limbus sphenoidalis. Occasionally there depends on their origin, since they can begin anteriorly or is no significant anterior boundary, and the LT cistern commu- posteriorly if they arise from the anterior or posterior olfac- nicates directly with the interhemispheric cistern (Wang et al. tory artery, respectively. Infrequently, the arterial branches are 2011a). derived from the orbital artery; these often have a more anterior The LM cistern can also extend inferoanteriorly to form a origin and divide repeatedly within the cistern. Olfactory veins tent‐shaped recess above the interspace anterior to the OC, with within the cistern are usually 1–3 in number and 0.3–0.5 mm in an AP length of 4.0–12.0 mm. Its superolateral wall is formed diameter. They drain into the frontopolar vein or the origin of by the pia mater under the gyrus rectus (GR), and its inferior the superior sagittal sinus (Wang et al. 2008). wall by the arachnoid between the optic nerves (ON). There are sometimes dividing membranes within this recess (Yaşargil Sylvian cistern 1984; Wang et al. 2011a). The size and shape of this cistern depends on the relationship In some cases, the lateral walls partially adhere to each other between the frontal and temporal lobes. In most cases it narrows in the middle part of the cistern (Wang et al. 2011a). superiorly as the frontal and temporal lobes approach each other Chapter 80: Subarachnoid space 961 over a length of 15–20 mm. At this level, the width of the cistern is usually about 0.5–1.0 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 Syl- vian 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 Figure 80.2 Anterior view of a drawing of a coronal section extending anterior compartment extends from the origin of the middle cer- through the left sylvian fissure showing the lateral, intermediate, and medial sylvian membranes. The outer arachnoidal membrane forms ebral artery laterally to the insula medially. It is limited superiorly the outer wall of the sylvian cistern and fissure. The lateral sylvian by the posterior part of the orbital gyri and the lateral part of the membrane spans the lateral part of the sylvian fissure and extends from the anterior perforated substance, and inferiorly by the planum tem- frontoparietal to the temporal operculum deep to the superficial sylvian poralis on the superior surface of the temporal lobe. The posterior veins. The intermediate sylvian membrane spans the interval between the compartment is located behind the limen insula and opens into medial part of the frontoparietal operculum above and the medial side of the superior temporal and Heschl’s gyrus below. The medial sylvian the lateral cerebral surface. It is further subdivided into medial membrane extends downward from the medial edge of the frontoparietal and lateral parts by the intermediate Sylvian membrane, which operculum and attaches to the insula on the medial side of the M2 segment spans the interval between the upper and lower walls of the poste- of middle cerebral artery. rior compartment of the Sylvian fissure. The medial part is located Source: Inoue et al. (2009) 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, the callosomarginal and pericallosal arteries, but with no dis- its floor being formed by the upper surface of the temporal lobe. tinct division (Yaşargil 1984). The lateral part is located in the lateral part of the cleft between the operculae. Its medial wall is formed by the intermediate Syl- Interpeduncular cistern vian membrane, its lateral wall by the outer arachnoid membrane, Lu and Zhu (2005a) have described the presence of two distinct and its superior and inferior walls by the lateral part of the oppos- arachnoid membranes within and dividing the interepeduncu- ing operculae (Inoue et al. 2009) (Fig. 80.2). lar cistern: the basilar artery (BA) bifurcation membrane and the posterior perforated membrane. Pericallosal cistern The BA bifurcation membrane attaches caudally to the ante- Some authors have subdivided the pericallosal cistern into three rior walls of the BA bifurcation and the proximal segments compartments: inferior, anterior, and superior. The inferior of the posterior cerebral artery (PCA) and/or superior cere- compartment is positioned above the lamina terminalis cistern bellar artery (SCA). It spreads obliquely forward and upward and below the rostrum of the corpus callosum, and is bounded and attaches to the anterior edge of the mamillary bodies and anteriorly by the outer arachnoid membrane and laterally by the the diencephalic leaf of the Liliequist membranes. Laterally, it paraterminal and paraolfactory gyri. The anterior compartment attaches via the arachnoid trabeculae to the diencephalic‐mes- is bounded anteriorly by the outer arachnoid membrane, pos- encephalic leaflets of Liliequist’s membrane. It can appear as an teriorly by the genu of the corpus callosum, and laterally by the intact membrane (most common), a porous and sparse net- cingulate gyri. The superior compartment is located between the work, or a dense and porous network (least common). It divides body of the corpus callosum inferiorly, and the outer arachnoid the cistern into two portions: a deep part, which communicates membrane spanning the interval between the paired cingulated with the ambient cistern; and a superficial part which commu- sulci superiorly. It narrows posteriorly and ends on the superior nicates with the oculomotor cistern. The superficial portion surface of the splenium. There are no distinct divisions between contains only the upper part of the basilar artery. The deep por- the three compartments (Inoue et al. 2009). tion contains the bifurcation of the BA, the proximal portions Other authors divide this cistern into anterior and posterior of the PCA and the SCA, the oculomotor nerves, the posterior portions separated by arachnoid trabeculae at the branching of communicating artery (PCoA), the perforating branches of the 962 Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation

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 Figure 80.3 Drawing demonstrating the sagittal view of the Liliequist and superiorly to the posterior perimesencephalic membrane. membrane and the interpeduncular cistern. The arrows indicate the mesencephalic leaf and the arrowheads the diencephalic leaf of The lateral wall is formed by the medial occipital lobe and the the Liliequist membrane; the star marks the medial and the lateral superior wall by the pia covering the midbrain tegmentum, the pontomesencephalic membrane. 1 = infundibulum and pituitary lateral geniculate body, and the medial occipital lobe (Qi et al. stalk; 2 = interpeduncular cistern; 3 = pons; 4 = mammillary bodies; 2011a) (Fig. 80.4, Fig. 80.5). 5 = prepontine cistern; 6 = optic chiasm; 7 = frontal lobe; 8 = chiasmatic On the basis of this description, Qi et al. (2011a) excluded cistern; 9 = BA bifurcation membrane; 10 = posterior perforated membrane. the superior cerebellar artery and the trochlear nerve (which are infratentorial) from the contents of the ambient cistern. They Source: Lu and Zhu (2005). also reported the P2 and P3 segments of the anterior choroidal artery and their branches as among the contents (Qi et al. arteries, the posterior perforated substance, and the posterior 2011a). 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 diencephalic‐ mesencephalic 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 Figure 80.4 The ambient cistern and adjacent cisterns (inferior view). The cerebellar membrane) can sometimes be found (Qi et al. 2011a). anterior ambient cistern (light blue) communicates with the carotid cistern (yellow) anteriorly, the interpeduncular cistern (dark blue) medially, the In contrast to Yaşargil (1984) and Yaşargil et al. (1976), who cerebellopontine cistern inferiorly, and the oculomotor cistern (green) divided the ambient cistern into supra‐ and infratentorial com- inferomedially. The posterior ambient cistern (light blue) borders partments, Qi et al. (2011a) considered that the ambient cistern the cerebellomesencephalic cistern inferiorly and the quadrigeminal is the compartment extending above rather than across the level cistern (purple) posteromedially. Car. = carotid; Chiasm. = chiasmatic; of the tentorial incisura, and further divided it into anterior Interped. = interpeduncular. and posterior parts. According to them, this exclusion of the Source: Qi et al. (2011). 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 Arachnoid trabeculae The crural cistern was considered by Qi et al. (2011a) as part of the anterior ambient cistern rather than a separate cistern. This The arachnoid fibers and trabeculae that bridge the subarach- is because there is no definite border or separation between noid space and basilar cisterns usually have fine structures. them except for infrequent sparse arachnoid trabeculae (Qi et al. Nevertheless, they tend to be thicker and tougher where the 2011a). It is occasionally divided into upper and lower parts by arteries and nerves pass through the trabeculated wall from one an intracrural membrane, extending between the posterior seg- cisternal compartment to another. In most individuals, the three ment of the uncus and the cerebral peduncle (Inoue et al. 2009). cisterns in which the arachnoid trabeculae and membranes are densest and present the greatest obstacles during operations are Prepontine cistern the interpeduncular and quadrigeminal cisterns and the cis- The lower part of the anterior pontine membrane is occasionally terna magna (Matsuno et al. 1988). absent, and in such cases the anterior inferior cerebellar artery Variable arachnoid trabeculae that differ in their strength and exits the prepontine cistern to the cerebellopontine cistern by density are also seen in other subarachnoid cisterns and else- passing below (rather than through) the anterior pontine mem- where in the subarachnoid space. They usually enclose small brane (Matsuno et al. 1988). blood vessels and adhere to the surface of larger blood vessels and nerves in the subarachnoid space (Yaşargil 1984). Cerebellomedullary cistern (cisterna magna) The cistern magna has a variable expansion dorsally (behind the vermis) depending on the degree of development of the falx Arachnoid membranes cerebelli. It usually ends near the lobulus pyramis of the vermis but can extend all the way up the tentorium, mainly in cases of The arachnoid membranes vary greatly in appearance and absent or small falx cerebelli (Yaşargil 1984; Matsuno et al. 1988). configuration. Some are reticulated and porous, such as the Occasionally, a median arachnoid sheet divides the cistern basilar artery bifurcation membrane; some are intact and into two sagittal compartments. Another two paramedian sheets dense without foramina, such as the diencephalic leaf of Lil- can extend into the dorsal spinal subarachnoid space, dividing it iequist’s membrane; and others are plexiform or band‐shaped into separate compartments (Yaşargil 1984). or cord‐shaped, such as the anterior cerebral membrane and 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 Figure 80.6 variations of Liliequist’s membrane (LM). A, the diencephalic the first detailed anatomical description of this membrane, leaf (DL) and mesencephalic leaf (ML) originate along the dorsum sellae which was subsequently named after him. With the advance of and course separately toward the diencephalon and basilar bifurcation, neuroendoscopic and microscopic techniques, interest in stud- respectively. B, with two posterior leaves including the diencephalic leaf attached to the diencephalon and mesencephalic leaf toward the basilar ying the LM and other subarachnoid membranes and cisterns bifurcation. C, as a single membrane attached posterosuperiorly to the increased again, pioneered by Yaşargil’s studies (Yaşargil et diencephalon between the infundibulum and mamillary bodies. al. 1976). It was reported that failure to open the LM during Source: Froelich et al. (2008). 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 con- two leaves posteriorly, the LM arising as a single membrane and tinued. We therefore provide a detailed review of the various then splitting into DL and ML. In type C, the most common, the descriptions of it, including variations. LM appears as a single (diencepahlic) membrane (Froelich et al. 2008) (Fig. 80.6). Presence of LM The LM is found in most individuals, mainly separating the Single membrane (Type C) interpeduncular, prepontine, and chiasmatic cisterns. However, The classic description by Liliequist (1956, 1959) was of a single it was reported to be absent in 2 out of 13 cadavers (15.4%) membrane with forward convexity, extending from the dorsum studied by Froelich et al. (2008), and in 15 out of 35 cadavers sellae to the anterior edge of the mamillary bodies (Type C). (43%) studied by Zhang and An (2000). In such cases, free Brasil and Schneider (1993) gave a similar description. Yaşargil communication among the interpeduncular, prepontine, and (1984) and Yaşargil et al. (1976) added that this well‐developed chiasmatic cistern is expected, forming one large cistern. A membrane stretches like a curtain from one mesial temporal carotid‐interpeduncular wall separating the interpeduncular surface to another. A full description of the type C LM would and carotid cisterns was added by Brasil and Schneider (1993), therefore be of a single, non‐fenestrated membrane that arises which can be absent unilaterally or bilaterally. However, this inferiorly from the basilar arachnoid membrane, covering the seems to contradict the description of Froelich et al. (2008), dorsum sellae and the posterior clinoid processes, curving ante- who stated that the interpeduncular cistern communicates riorly and attaching superiorly to the pia of the hypothalamus anterolaterally with the carotid cistern along the posterior com- just anterior the mamillary bodies, posterior to the infundib- municating artery. These authors added that in cases of single ulum. Laterally, it attaches to the pia of the mesial surface of LM (see “Single membrane” below), the prepontine cistern can the temporal uncus (Vinas and Panigrahi 2001). This lateral communicate with the carotid cistern anterolaterally around the extension (at the carotid‐interpeduncular wall) is perforated by posterolateral free border of the LM, and with the ambient cis- the oculomotor nerve and the posterior communicating artery tern laterally along the course of the posterior cerebral artery (Brasil and Schneider 1993). and across the posterolateral free border of the LM (Froelich et al. 2008). Moreover, Brasil and Schneider (1993) described free Lateral extension communication between the carotid and crural cisterns super- Other authors disagree on the extent of the lateral extension. olateral to the free margin of the LM. Matsuno et al. (1988) also Epstein (1965) described the LM as a semilunar transverse reported communication with the ambient and crural cisterns. membrane stretching obliquely between the oculomotor nerves, which is similar to the description by Matsuno et al. (1988). Such Types of LM a termination would render the LM a continuous, unperforated On the basis of the various descriptions, the LM has been membrane. On the other hand, Fox (1989) accepted both types divided into three types. In type A it is composed of two leaves, of lateral extension and added that it can also end just before diencephalic (DL) and mesencephalic (ML), which originate at (medial to) the oculomotor nerve, to which it is then connected the dorsum sellae. In type B it appears as one leaf anteriorly and via arachnoid trabeculae. Similar results were reported by Anik Chapter 80: Subarachnoid space 965 et al. (2011) and Fushimi et al. (2003). Froelich et al. (2008) DL of the LM. On the other hand, Zhang et al. (2012) observed described the different relationships with the oculomotor nerve. this free lateral border of the DL between the inferolateral bor- In 6 out of 13 specimens (46%) the nerve was surrounded by the der of the optic tracts and the oculomotor sheath in only 4 out lateral aspect of the ML, creating a separate oculomotor cistern. of 24 specimens (16.7%; Zhang et al. 2012). In two specimens (15.4%) it ran between two lateral leaves of the Agreeing about the lateral extension of the LM, Epstein ML. The superior leaf was attached to the pia of the mesial sur- (1965) and Fox (1989) described the presence of free border face of the temporal lobe, and the inferior leaf was continuous lateral to or at (medial to) the oculomotor nerve, respectively. with the arachnoid above and below the level of the incisura. In Froelich et al. (2008) described the free border as located poste- three specimens (23%) the nerve was above the mesencephalic rolaterally between the central attachment to the diencephalon leaf and connected to it by an arachnoidal ring (Froelich et al. and tentorial edge in type C and in the DL of types A and B, 2008). Zhang et al. (2012) agreed that the ventral wall of the and at the posterior end of the ML in front of the basilar bifur- oculomotor cistern is partly formed by the lateral extension cation in types A and B. Zhang and An (2000) claimed that the of the LM (and partly by the basal arachnoid mater), but they free border of the LM is located on its superoposterior part. All regarded the dorsal membrane (oculomotor membrane) as a these authors agree that the free border becomes attached to the different entity and differentiated it from the temporal mem- surrounding structures via arachnoid trabeculae. With some brane, which they described as the lateral extension of the DL exceptions, these trabeculae are not considered part of the LM; (Zhang et al. 2012). they also render it otiose to identify the border of an irregular arachnoid trabecular network because it varies greatly and Superior extension could be the cause of variations in gross anatomical findings. Regarding its superior attachment, Vinas and Panigrahi (2001) This was also supported by the findings of Anik et al. (2011), added that as well as the premamillary attachment described who claimed that various free edges were found in the ML in above there can also be a retromamillary attachment. This is 7 out of 24 specimens (29.2%) while it was totally closed in 12 surgically important, as in these patients it is less important to (50%). fenestrate the LM during third ventriculostomy because the third ventricle will be opened into the interpeduncular cistern The carotid‐chiasmatic walls following fenestration of the floor (Vinas and Panigrahi 2001). Brasil and Schneider (1993) contradicted the previous descrip- Similar findings were also described by Matsuno et al. (1988) tions by Epstein (1965), Fox (1989), and Yaşargil (1984), indi- regarding the attachment of the DL. Inoue et al. (2009) also cating that the LM can surround the infundibulum to create a reported both types of superior attachments of the DL; they “hypophyseal cistern.” They suggested that these surrounding found that it was attached to the posterior edge of the mamil- membranes represent the carotid‐chiasmatic walls (or chi- lary bodies (retromamillary) in 47% of brains, the apex of the asmatic membrane) and added that the LM is always located mamillary bodies in 33%, and the anterior edge of the mamil- posterior to the infundibulum (Brasil and Schneider 1993). The lary bodies (premamillary) in 20%. On the other hand, Anik same description was offered by Vinas and Panigrahi (2001) et al. (2011) reported that direct attachment to the mamillary who added that, although the chiasmatic membranes arise from bodies was the most common type, found in 17 out of 24 spec- the LM, they represent a different entity. imens (70.8%). Lu and Zhu (2003) described a more anterior These controversies were further clarified by Zhang and superior‐attachment of the DL on the posterior surface of the An (2000). Using a modified E12 sheet plastination method, infundibulum all over its course, found in four out of eight cadaveric dissections, and electron microscopy, these authors cadavers (50%). In the other four (50%) the DL had a superior concluded that the arachnoid membrane‐like LM has an archi- attachment that was 1.96–4.92 mm posterior to the infundibu- tecture significantly different from that of the arachnoid tra- lum (premamillary) (Lu and Zhu 2003). beculated carotid‐chiasmatic walls. The LM appears thicker, unperforated, and with a cleaner surface, and is composed of Free border two layers of arachnoid mater (presumed to be the DL and ML Brasil and Schneider (1993) divided the single LM into three described in other studies) that are better visualized in the mid- parts (or walls) on the basis of its cisternal relationships: two dle portion. However, no double layers could be found in 15 carotid‐interpeduncular walls laterally and a chiasmatic‐ out of 35 cadavers (43%). On the other hand, the carotid‐chias- interpeduncular wall medially. Each of these walls could be matic walls are composed of accumulated, irregularly oriented selectively absent. They also added that, besides its classic arachnoid trabeculae that extend from the LM to the pia mater superior attachment, the LM attaches to the pia of the inferior covering the surface of the optic chiasm. Unlike the LM, these surface of the optic tracts. There is a free margin between the walls have openings of various sizes and are penetrated by per- inferolateral border of the optic tracts and the uncus. Supero- forating arteries from the posterior communicating and internal lateral to this free margin there is free communication between carotid arteries, giving them a vascularized appearance. This is the carotid and crural cisterns (Brasil and Schneider 1993). The surgically important as it suggests that the most suitable site for same free margin was also reported by Lu and Zhu (2003) in the opening the LM and approaching the interpeduncular cistern is 966 Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation the part of the LM between the carotid‐chiasmatic wall and the cases, the chiasmatic and interpeduncular cisterns merge into oculomotor nerve (Zhang and An 2000), with careful attention one (Wang et al. 2011b). to the posterior communicating artery and its branches (Lu and As expected from the description of an unperforated DL, the Zhu 2003). lateral attachment of the LM is related to the arachnoid sheath Regarding the lateral extension and free border, Zhang and surrounding the oculomotor nerve, with numerous trabeculae An (2000) stated that the free border of the LM is located on extending from the oculomotor nerve to the uncus and tento- its superoposterior part and continues along the entire length, rium (Matsuno et al. 1988; Inoue et al. 2009). Lu and Zhu (2003) and can be grossly visualized. At this free border, the LM is con- reported a case with a unilateral window in the DL connecting nected via arachnoid trabeculae to the surrounding structures the posterior communicating cistern with the interpeduncular including the infundibulum and mamillary bodies. Laterally, it cistern (Lu and Zhu 2003). attaches to neither the uncus nor the oculomotor nerve. Instead, The length of the DL from the inferior to the superior edge it fans out near the free edge of the tentorium and continues is within the range 5.0–13.0 mm (mean 10.8 mm). The width at with the arachnoid mater covering the tentorium below and the inferior edge is 10.0–28 mm (mean 19.9 mm), and the width above the tentorial notch. Zhang and An (2000) did not com- at the superior edge is 5.0–14.0 mm (mean 9.5 mm) (Wang et ment on the anterior attachment of the LM, but regarded the al. 2011b). membrane as continuous anteroinferiorly with the arachnoid mater covering the tentorium, the dorsum sellae, and the clivus The mesencephalic (Fig. 80.7). The ML is a thinner membrane, mostly perforated (by the basilar artery), that extends backward and attaches to the pontomes- Double membranes (Types A, B) encephalic junction, separating the interpeduncular and pre- The LM was first described as double membranes by Matsuno et pontine cisterns (Matsuno et al. 1988; Froelich et al. 2008; Inoue al. (1988). Other authors including Inoue et al. (2009) have given et al. 2009). Lu and Zhu (2003) described a different course and similar descriptions. The classic description is of an arachnoid termination of the ML (see below). Other authors have reported membrane arising from the arachnoid covering of the dorsum a free posterior border of the ML connected to the basilar bifur- sellae and the posterior clinoid processes (some also add the cation and surrounding structures by arachnoid trabeculae arachnoid covering of the posterior petroclinoid and adjacent (Froelich et al. 2008). Occasionally, the ML is thick (or equal tentorial edge; Froelich et al. 2008), extending between the ocu- in thickness to the DL) and has small perforations. It can also lomotor nerve and then splitting into two leaves, the DL and ML form a tight cuff around the basilar artery, but more commonly (type B). According to these authors, the previous description of it has a large opening through which the basilar artery ascends a single membrane by Liliequist was of the DL; this can be visu- (Matsuno et al. 1988; Inoue et al. 2009). alized by the pneumatograph due to its unperforated nature, in The length of the ML from the anterior to the posterior end contrast to the perforated ML (see section “The mesencephalic” is over the range 2.5–10.8 mm (mean 4.8 mm). The width at its below) which was visualized in later cadaveric studies (Matsuno posterior attachment is 2.5–10.8 mm (mean 4.8 mm). In cases of et al. 1988) (Fig. 80.8). 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 The diencephalic of the anterior edge of the ML is 3.0–22.0 mm (mean 12.6 mm; The DL is a thicker and mostly unperforated membrane that Wang et al. 2011b). attaches to the posterior or anterior edge or to the tips of the mamillary bodies, separating the interpeduncular and chias- Findings of Froelich et al. matic cisterns. At its superior end, the DL sends many arachnoid In the cadaveric study of Froelich et al. (2008), the LM was trabeculae to attach to the surrounding structures, including the identified in 11 out of 13 cadavers (85%). When present, it con- infundibulum and mamillary bodies (Matsuno et al. 1988; Froe- sisted of either one leaf (type C, most common) or two leaves lich et al. 2008; Inoue et al. 2009). The DL is thick in most cases (type A, B). Type A was found in two specimens (15.4%) and, (54%: Anik et al. 2011; 75%: Lu and Zhu 2003), but can be thin in addition to the classic description, the authors reported a (25%: Lu and Zhu 2003; 46%: Anik et al. 2011). It is also mostly lateral attachment of the DL to the paramedian perforating semitransparent (83.3%: Anik et al. 2011; 87.5%: Lu and Zhu substance and of the ML to the pia of the parahippocampal 2003) but can be opaque (12.5%: Lu and Zhu 2003; 16.7%: Anik gyri (mesial surface of the temporal lobe). Type B was also et al. 2011). It can also be a largely porous trabeculated mem- found in two specimens (15.4%) where the LM arose as a sin- brane (Wang et al. 2011b; Zhang et al. 2012), and in these cases gle membrane and then split into two leaves, DL and ML, with it may have only a small crescent‐shaped dense non‐porous part connections similar to those in type A. The authors described in its anteroinferior attachments (Zhang et al. 2012). The Dl was the free borders of these two types as located in the posterior reported to be absent in 3 out of 24 cadavers (12.5%) by Anik end of the ML, in front of the basilar bifurcation, but occa- et al. (2011), 6 out of 24 cadavers (25%) by Zhang et al. (2012), sionally covering part of the basilar tip. Type C was found in and 5 out of 15 cadavers (26.7%) by Wang et al. (2011b). In these seven specimens (53.8%), with a posterolaterally located free Chapter 80: Subarachnoid space 967

Covering Inferior Covering superior surface surface of tentorium of tentorium

Free border of Lillequist’s membrane

optic dorsum midbrain tentorium nerves sellae Covering dorsum sellae and clivus Covering superior surface of tentorium Covering Inferior anterior and posterior Free border of surface of tentorium clinoid processes Lillequist’s membrane AB

Attaching onto the lateral borders of the optic chiasm Petorating vessel

Carotid- chiasmatic wall

Trabecular networks

Lillequist’s C 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 The authors added that the LM is continuous with the arach- tentorial edge. This free border allowed the prepontine and noid covering the temporal fossa floor and the superior aspect carotid cisterns to communicate with each other (Froelich of the tentorium, above the tentorial edge. Below the tento- et al. 2008). rial edge the membrane was continuous with the arachnoid 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 two out of four specimens (50%) and less than 20% of the length dura (Froelich et al. 2008). They also agreed with other authors in one (25%). The attaching layer spreads from the posterior that the LM is continuous laterally with the lateral pontomes- border of the basal layer to attach on the surrounding struc- encephalic membrane (Matsuno et al. 1988), which separates tures. The diencephalic part of this layer (attaching the DL to the ambient cistern from the cerebellopontine cistern, and with the mamillary bodies) is composed of accumulated arachnoid the caudal oculomotor membrane (Vinas et al. 1994, 1996a, b), trabeculae. In contrast to previous studies (see above), Zhang et as they share a common embryological origin (Froelich et al. al. (2012) therefore considered these arachnoid trabeculae as a 2008). part of the LM. Regarding the gross lateral extension, Zhang et al. (2012) Relation with the posterior communicating artery described a triangular membrane, found in 14 out of 24 spec- Froelich et al. (2008) also described the different relationships imens (58.3%), that spread from the lateral free border of the of the LM with the posterior communicating artery. In spec- diencephalic membrane to the mesial temporal uncus. They imens with a single membrane (type C) and a posterolateral termed it the temporal membrane and considered it to be part of free border, the posterior communicating artery coursed above the DL. This membrane separates the carotid from the ambient the membrane and crossed the free border to join the posterior cistern and sends variable arachnoid trabeculae to attach to the 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, Figure 80.9 then extends superoposteriorly and folds upon itself to form the Three-dimensional illustration (sagittal cut, oblique view) of Liliequist’s membrane composed of two separate diencephalic (aqua) uninterrupted basal layer of the LM. This basal layer extends and mesencephalic (pink) leaves that originate at the dorsum sellae as the inferior part of the DL (no comments were made on the (Type A). Note the posterior communicating artery coursing above the ML) and extends laterally beyond the oculomotor nerve to con- mesencephalic leaf. Inset, with removal of the diencephalic leaf, the tinue with the arachnoid mater covering the tentorium below mesencephalic leaf can be seen surrounding the oculomotor nerve and and above the tentorial notch. In the midsagittal plane, the basal reﬂecting onto the tentorial edge. part constituted more than half the entire length of the LM in Source: Froelich et al. (2008).. Chapter 80: Subarachnoid space 969 arachnoid sheath surrounding the oculomotor nerve. In con- appears similar to that previously described as being divided trast to the DL, the temporal membrane is usually porous and into types A, B, and C. In type II only the medial and lateral ML trabeculated, and is occasionally sheet‐like with small openings. are present, with a course similar to that described above and When this membrane is present, the posterior communicating with no separation between the interpeduncular cistern and the artery always courses above it (Zhang et al. 2012). chiasmatic cistern (Zhang et al. 2012). The ML was divided by Zhang et al. (2012) into three parts, Regarding the oculomotor membrane, Zhang et al. (2012) one medial ML and two lateral ML. The medial ML extends distinguished it from the temporal membrane and described between the oculomotor nerves and was referred to as the ML three coronal configurations based on its relationship to in previous studies, separating the interpeduncular and prepon- the carotid membrane: inverted Y‐shaped (most common); tine cisterns (Zhang et al. 2012). A similar division was used by inverted V‐shaped; and inverted U‐shaped (least common). In Qi et al. (2011a), who also used the name “anterior perimesen- the inverted Y‐shaped configuration, the lateral carotid mem- cephalic membrane” to describe the ML. brane constitutes the upper arm of the inverted Y and attaches The relationships between the DL and the medial ML are the superiorly on the mesial temporal uncus near the attachment of types described earlier as A, B, or C (the classical classification the temporal membrane. In the inverted V‐shaped configura- of the LM). However, Zhang et al. (2012) found type B to be tion, the lateral carotid membrane is absent and the apex of the the most common, followed by type A then C. When the DL inverted V attaches directly to the mesial temporal uncus near is absent, the medial mesencephalic membrane is defined as the attachment of the temporal membrane. In the inverted U‐ the combination of an anteriorly located crescent‐shaped dense shaped configuration, the dome of the oculomotor membrane non‐porous part, which attaches to the basal arachnoid mem- adheres to the dorsal surface of the oculomotor nerve and can brane (exactly the same as that of the DL) and courses between be connected to the mesial temporal uncus by scattered arach- the oculomotor nerves (to which it attaches laterally), and a noid trabeculae, which represents a less well‐developed lateral posteriorly located porous trabeculated part that extends to the carotid membrane. According to the authors, the LM can attach caudal end of the medial ML (Zhang et al. 2012) (Fig. 80.10). to the mesial temporal uncus either directly by its temporal According to Zhang et al. (2012), regardless of the type of membrane or indirectly by the oculomotor membrane (Zhang medial ML, its caudal end can be above, at, or below the level et al. 2012). of the terminal basilar bifurcation. The lateral ML is equiva- lent to the lateral pontomesencehalic membrane. It separates Triple membranes the ambient and cerebellopontine cisterns and communicates Diencephalic‐mesencephalic membrane (DML) medially with the DL and medial ML below the oculomotor The LM was first described as comprising three leaves by nerve (the part of the LM that forms part of the ventral sheath Lu and Zhu (2003). These leaves were the DL, ML, and the of the oculomotor), and attaches to the anterior tentorial edge diencephalic‐mesencephalic leaf (DML). These authors laterally. Anteriorly it attaches to the basal arachnoid mater described the ML (but not the DL) differently from others. In covering the posterior border of the oculomotor trigone, and their study of eight cadavers, Lu and Zhu stated that the ML posteriorly it sends out variable arachnoid trabeculae to attach represents an intact, thick, dense, and unperforated membrane to the anterolateral pontomesencephalic junction. The size that forms the anterioinferior wall of the interpeduncular cis- of the non‐porous sheet‐like portion of this membrane var- tern. According to them, the ML intersects with the DL at the ies, and is inversely proportional to the non‐porous sheet‐like dorsum sellae and posterior clinoid processes rather than orig- portion of the DL (or ML when the DL is absent). When the inating from this point. Rostrally, it spreads along the surface non‐porous sheet‐like part of the DL or ML is prominent the of the diaphragma sellae and attaches to the posterior surface counterpart of the lateral ML is smaller, and vice versa (Zhang of the infundibulum, 1.48–3.98 mm above its inferior bottom, et al. 2012). and fuses with the basal chiasmatic membrane (the arachnoid On the basis of these findings, Zhang et al. (2012) proposed covering the floor of the chiasmatic cistern). In most cases another classification of the LM according to presence (type I) (seven out of eight specimens) the ML was totally above the or absence (type II) of the DL. In type I, most common, the LM diaphragma sellae and did not enter the intrasellar region. In

Figure 80.10 Schematic drawing of (a, b) type I and (c) type II of Liliequist’s membrane.

Source: Zhang et al. (2012). 970 Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation the remaining specimen it turned downward around the infun- located at the medial part of the pontomedullary sulcus and dibulum through the opening of the diaphragma sellae along separates the prepontine and premedullary cisterns, and the with the chiasmatic membrane to encircle the pituitary gland. lateral pontomedullary membrane is located at the lateral pon- Caudally, the ML ends at the junction of the superior one‐third tomedullary sulcus and separates the cerebellopontine and cer- and the inferior two‐thirds of the basilar artery or the midpoint ebellomedullary cisterns. of the basilar artery and the ventral surface of the pons at this The DML is a pair of parallel leaflets connecting the DL to the level; in contrast to the classical description, it does not attach ML. It represents a triangular or quadrilateral membrane that is to the pons directly or form a cuff around the basilar artery, but dense and intact in most cases (seven out of eight specimens) only parallels the anterior wall of the basilar artery and the ven- but can also be composed of sparse networks (Lu and Zhu 2003). tral surface of the pons. The authors added that it is not the ML In the study of Anik et al. (2011) the DML was not consistently but the medial pontomesencephalic membrane that separates present but was seen in 17 out of 24 specimens (70.8%). The the interpeduncular and prepontine cisterns and is penetrated DML is located ventral to the cerebral peduncles and medial by the basilar artery. This medial pontomesencephalic mem- to the oculomotor nerves, separating the interpeduncular and brane was also found to join the ML to the pons in most cases oculomotor cisterns; along with the other LM leaves it partici- (seven out of eight specimens), but the ML had a free posterior pates in the formation of the oculomotor sheath. It attaches to border in the remaining specimen, similar to that described by the DL anterosuperiorly, the lateral margin of the mamillary Froelich et al. Laterally, the ML attaches to the mesial surface of bodies superiorly, the ML anteroinferiorly, the medial or lateral the temporal lobe but also encircles the oculomotor nerve for pontomesencephalic membranes inferiorly (representing the variable distance (2.72–4.98 mm) through the cavernous sinus direct continuation of the ML), and has a free posterior border (Lu and Zhu 2003). (between the attachment to the lateral margin of the mamillary Anik et al. (2011), who regarded the LM as a single, double, body and the attachment to the ML). The space between the or triple membrane, gave an almost similar description but con- posterior margin of the DML and the cerebral peduncles allow sidered that the posterior end of the ML to the basilar bifur- the interpeduncular cistern to communicate with the crural and cation could also course toward the vertebrobasilar junction ambient cisterns. The authors stated that absence of the DML in through the prepontine cistern. They also reported one spec- previous studies is probably due to this leaf being fragile, thin, imen in which two ML were identified, one splitting from the and easily destroyed. They stated that it is often overlooked or anterior portion and attached to the basilar artery at the level of described as arachnoid trabeculae joining the LM to the oculo- the vertebral artery bifurcation, and the other splitting from the motor nerves (Lu and Zhu 2003). posterior portion of the LM and attached to the basilar artery bifurcation. However, they did not comment on the anterior Hypothalamic membrane extension of ML described by Lu and Zhu, but considered the In their study of 15 cadavers, Wang et al. (2011b) divided the ML to be in direct continuation anteriorly with the basal arach- LM into three parts (or leaflets): the DL, ML, and hypothalamic noid membrane (Anik et al. 2011). In contrast, Fushimi et al. leaflets. Beside the previously described superior attachment of (2003) recognized the anterior extension as a distinct part of the the DL, Wang et al. added that it can be attached to the ante- LM, named the sellar part. This part could be identified in most rior, middle, or posterior edge of the tuber cinereum. Laterally, cases, but sometimes could not be visualized. it attaches to the oculomotor nerve and is continued with the In the study by Anik et al. (2011), the ML continues cau- inferior oculomotor sheath. Between the superior attachment dally as the medial and lateral pontomesencephalic mem- and the oculomotor nerve, a free border forms a cuff around the brane. The medial pontomesencephalic membrane (MPMM) posterior cerebral artery. The authors also found that the poste- courses anterolaterally, medial to the trigeminal and abducens rior communicating artery only rarely penetrates the DL, as a nerves. The lateral pontomesencephalic membrane (LPMM) small branch of the basilar artery can also do. Many arachnoid courses posterolaterally, lateral to the trigeminal and abducens trabeculae were also found extending from the DL to the pos- nerves. Both membranes are connected between these two terior communicating and posterior cerebral arteries and from nerves. The LPMM joins the formation of a ring that covers the superior end of the DL to the surrounding structures (Wang the third nerve, attaching to the DL on the distal posterior sur- et al. 2011b). face of the nerve and to the mesial temporal surface coursing Similar to the findings of Matsuno et al. (1988), the ML in lateral to the uncus. Both the MPMM and LMPMM continue the study of Wang et al. (2011b) extended to the pontomesen- inferiorly as the medial and lateral pontomedullary membranes cephalic junction but could also reach up to 5.0 mm (mean 2.5 respectively. They continue as a single membrane through the mm) above the junction. Beside the classical A and B types of prepontine and premedullary areas as the prepontine and pre- ML origin, the authors reported the ML arising from the hypo- medullary membranes, respectively. They attach to the dura thalamic leaflet (HL) in 3 out of 15 specimens (20%) and having covering the superior aspects of the cranial nerves laterally a free anterior edge in one (6.7%). The lateral attachment of the (Anik et al. 2011). According to Matsuno et al. (1988) and ML was mostly to the oculomotor sheath, but was also occa- Lu and Zhu (2007), the medial pontomedullary membrane is sionally seen with the posterior cerebral arteries or the superior Chapter 80: Subarachnoid space 971 cerebellar arteries. Free lateral borders were also observed in Arachnoid membranes over the pineal some specimens. Many arachnoid trabeculae were also found region extending from the ML to the surrounding neurovascular structures (Wang et al. 2011b). In contrast to Lu and Zhu (2005b), who described the arach- Between the sellar segment of the DL, the anterior part of the noid envelope over the pineal region (AEPG) as being formed ML, and the posterior part of the superior clivus, a space could by the cerebellar precentral membrane (CPM), Qi et al. (2011b) be found anteroinferior to the interpeduncular cistern; Wang believed that this membranous covering of the vein of Galen et al. (2011b) called this the post‐dorsum cistern. There is no and surrounding structures (forming a closed, non‐commu- arachnoid mater separating the post‐dorsum from the prepon- nicating compartment) is formed by the confluence of the tine cistern; when the DL is absent, all the space beneath the supratentorial and infratentorial outer arachnoid membranes at ML becomes the prepontine cistern and the ML constitutes its the tentorial apex. They added that the CPM, which is a trabec- superior wall (Wang et al. 2011b). ular arachnoid membrane separating the quadrigeminal from The HL described by Wang et al. (2011b) were pairs of trian- the supracerebellar cistern, has part of its superior attachments gular or quadrangle membranes that extend upwards from the on the ventral surface of the posterior AEPG but does not enve- oculomotor nerve and/or the lateral part of the DL (or ML) to lope the vein of Galen. The other difference from the description attach to the lateral edge of the hypothalamus. In most cases, of Lu and Zhu (2005b) was that the AEPG does not end at the these membranes were thin and trabeculated, with many scat- origin of the vein of Galen but extends anteriorly to enclose the tered holes. Only rarely did they develop into complete net‐like suprapineal recess, and can also enclose the pineal gland and shapes. In two specimens with absent DL, the HL was devel- distal segment of the internal cerebral veins (Qi et al. 2011b). oped so well that it seemed to replace the DL. Inferiorly, each The AEPG is divided into two parts by a perpendicular plane HL is mostly attached to the superomedial or inferomedial edge crossing the origin of the vein of Galen: a tuciform posterior of the oculomotor nerve. They can also be attached to superior part envelopes the vein of Galen and the terminal segments of wall of the oculomotor nerve sheath, the lateral part of the DL, its tributaries, and the trumpet‐ or funnel‐shaped anterior part or the lateral part of the ML (when the DL is absent). The HL envelopes the suprapineal recess, the pineal gland, and the distal can extend laterally above the oculomotor nerve attaching to segments of the internal cerebral veins. Occasionally, a signif- the temporal lobe, with an attaching line ranging from 1.5 to icant prominent suprapineal recess extends into the posterior 8 mm. Inferoanteriorly, it is attached to the arachnoid mem- AEPG over the vein of Galen. In these cases, the arachnoid cuff brane covering the diaphragma sellae, the dorsum sellae, or the may be enlarged, and through it the tip of the suprapineal recess superior wall of the cavernous sinus by some fibrous trabec- can protrude out of the posterior AEPG and reach the tentorial ulae. Superiorly, it attaches mostly to the inferolateral surface apex (Qi et al. 2011b). or the lateral edge of the tuber cinereum. It can also attach to the lateral edge of the median eminence area or the side of the The posterior AEPG infundibulum, the paramedian area below the optic chiasm/ As viewed laterally, the posterior end of the posterior AEPG, tract, or extend to the inferolateral surface of the mamillary also called the arachnoid cuff, is divided into two types accord- bodies. The length of the superior edge falls within the range ing to its relationship with the tentorial dura mater overlying the 6–20 mm (mean 10 mm), and the distance between the upper posterior end of the vein of Galen, to which it attaches. In type attaching edges is 2–8 mm. The anterior edge of the HL is I, the arachnoid cuff is totally covered by the tentorium, and the mostly attached to the dorsum sellae or the posterior clinoid posterior segment of the vein of Galen cannot be seen because process. It can also be continuous with the carotid–chiasmatic of the overlapping of the arachnoid envelope and dural cover- walls (which indicates that they represent distinct structures), age. In type II, more common, a crescent‐shaped segment of the connected to the fibrous trabecular network in the chiasmatic vein of Galen can be seen between the tentorial edge and the cistern, attached to the anterior edge of the DL or ML, or com- arachnoid cuff as a result of the forward convexity of the lateral pletely free. Mostly, the posterior edge adheres in multiple edges of the arachnoid cuff (Qi et al. 2011b). places to the posterior communicating artery or its branches, Below the junction of the vein of Galen and the straight sinus, which course through the HL to supply the tuber cinereum the arachnoid membrane at the ventral edge of the arachnoid and the mamillary bodies. It can also be completely free, sur- cuff becomes thickened with marked variations, forming intrasi- rounding the posterior cerebral artery in a cuff‐like shape and nus arachnoid structures. In most cases, oval or round nodular connected via arachnoid trabeculae to the tuber cinereum, the arachnoid clusters (or granulations) bulge into the inferior wall mamillary bodies, or the cerebral peduncle. Like the DL and of the vein of Galen, narrowing its lumen. In other cases, similar ML, the HL can also send many arachnoid trabeculae to the structures can be incorporated into the venous wall at the junc- surrounding structures, including the posterior cerebral artery tion of the vein of Galen, rather than protruding into the lumen. or its branches. It was also found to separate the superolaterally Least commonly, the thickened membrane causes gentle eleva- located posterior communicating cistern from the interpedun- tion without compressing the vein of Galen, and no changes in cular cistern (Wang et al. 2011b). the vein of Galen and its junction can be seen (Qi et al. 2011b). 972 Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation

The anterior AEPG the ML of the LM, turned downward around the infundibulum The anterior end of the anterior AEPG is attached to the dor- through the opening of the diaphragma sellae to encircle the sal surface of the suprapineal recess superiorly and the lateral pituitary gland (Lu and Zhu 2003). surfaces of the suprapineal recess laterally; inferiorly, it can be attached on either the inferior or the superior surface of the pineal gland. When the whole pineal gland is enclosed in the ante- Subarachnoid space within the Fallopian rior AEPG, the inner surface of its inferior wall can either be canal smooth or (more commonly) have a crescent‐shaped arachnoid ridge between the inferior wall of the suprapineal recess and the Gacek (1998) described variations in the subarachnoid space posterosuperior surface of the pineal gland (Qi et al. 2011b). within the Fallopian canal (FC). On the basis of the lateral limits of the arachnoid membrane within the FC, the subarachnoid Others space is divided into three categories. In type I, most common, it The fibrous pedicle that connects the tip of the suprapineal terminates at or proximal to the lateral end of the petrosal FC and recess and the outer surface of the vein of Galen near its ori- its junction with the tympanic FC. In type II, it extends beyond gin can be either thick and long in cases of a small suprapineal the medial aspect of the geniculate ganglion and penetrates into recess (and longer distance), or short and thin in cases of a large the substance of the geniculate ganglion and surrounding facial suprapineal recess (and shorter distance) (Qi et al. 2011b). nerve fascicles. The subarachnoid space displaces fascicles of The relationship between the AEPG and the internal cer- the facial nerve and portions of the geniculate ganglion by dis- ebral veins (ICV) can be classified into two types based on secting between the perineural membrane covering these neu- the site of entrance of the ICV. In type I (more common), the ral structures. In type III, least common, it extends beyond the ICV enter through the lateral wall of the anterior AEPG at any tympanic facial nerve. This configuration is separated from the point from the anterior to the posterior portion. In type II, the middle ear space by the fibrous tissue sheath of the nerve and ICV enter at the junction of the anterior and posterior AEPG; the bony FC wall. The subarachnoid space reaches this lateral the compartments of the anterior and posterior AEPG (which position in the FC by extending the dorsal cul‐de‐sac over the are otherwise connected) are separated by the arachnoid sep- geniculate ganglion. In types II and III, the laterally extended tum located between the posterior ends of the ICV (Qi et al. subarachnoid space can present clinically as an asymptomatic 2011b). enlargement of the canal by computed tomography or as cerebrospinal fluid otorrhea (Gacek 1998).

Other arachnoid membranes References According to Lu and Zhu (2005b), arachnoid membranes that can be either unilaterally or bilaterally absent include the basilar Adeeb N, Deep A, Griessenauer CJ, Mortazavi MM, Watanabe K, artery bifurcation membrane, lateral carotid membrane, poste- Loukas M, Tubbs RS, Cohen‐Gadol AA. 2013. The intracranial rior communicating membrane, anterior choroidal membrane, arachnoid mater : a comprehensive review of its history, anatomy, basilar artery bifurcation membrane, posterior perforated imaging, and pathology. Childs Nerv Syst 29(1): 17–33. Anik I, Ceylan S, Koc K, Tugasaygi M, Sirin G, Gazioglu N, Sam B. membrane, medial pontomesencephalic membrane, basilar 2011. Microsurgical and endoscopic anatomy of Liliequist’s mem- membrane, medial pontomedullary membrane, superior cere- brane and the prepontine membranes: cadaveric study and clinical bellar membrane, posteroinferior cerebellar artery membrane, implications. Acta Neurochir (Wien) 153(8): 1701–1711. and dorsal vermian membrane (Lu and Zhu 2005b). Liliequist’s Brasil AV, Schneider FL. 1993. Anatomy of Liliequist’s membrane. membrane was not reported absent by Lu and Zhu (2005b) but Neurosurgery 32(6): 956–960. other authors have reported it either wholly or partly absent. Buxton N, Vloeberghs M, Punt J. 1998. Liliequist’s membrane in min- The lateral lamina terminalis membrane and the intracrural imally invasive endoscopic neurosurgery. Clin Anat 11(3): 187–190. membrane were also reported occasionally absent by Inoue et al. Di Ieva A, Tschabitscher M, Matula C, Komatsu F, Komatsu M, Colombo (2009). G, Sherif C, Galzio RJ. 2012. The subdiaphragmatic cistern: historic The superior margin of the posterior communicating mem- and radioanatomic findings. Acta Neurochir (Wien) 154(4): 667–674. brane (PCM) can be free or joined to the anterior choroidal Epstein BS. 1965. The role of a transverse arachnoidal membrane within the interpeduncular cistern in the passage of pantopaque into the membrane or the inferior aspect of the diencephalon by arach- cranial cavity. Radiology 85(5): 914–920. noid trabeculae. The PCM can also be absent; in such cases the Fox JL. 1989. Atlas of Neurosurgical Anatomy: The Pterional Perspective. carotid cistern and the posterior communicating cistern merge New York: Springer‐Verlag. into one (Lu and Zhu 2007). Frankel DA, Fessell DP, Wolfson WP. 1998. High resolution sono- The chiasmatic membrane almost always lies above the dia- graphic determination of the normal dimensions of the intracranial phragma sellae, but in one specimen reported by Lu and Zhu extraaxial compartment in the newborn infant. J Ultrasound Med (2003), this membrane, along with the anterior extension of 17(7): 411–418. Chapter 80: Subarachnoid space 973

Froelich SC, Abdel Aziz KM, Cohen PD, van Loveren HR, Keller JT. Qi ST, Fan J, Zhang XA, Pan J. 2011a. Reinvestigation of the ambient 2008. Microsurgical and endoscopic anatomy of Liliequist’s mem- cistern and its related arachnoid membranes: an anatomical study. brane: a complex and variable structure of the basal cisterns. J Neurosurg 115(1): 171–178. Neurosurgery 63(1 Suppl 1): ONS1–9. Qi ST, Zhang XA, Fan J, Huang GL, Pan J, Qiu BH. 2011b. Anatomical Fushimi Y, Miki Y, Ueba T, Kanagaki M, Takahashi T, Yamamoto A, study of the arachnoid envelope over the pineal region. Neurosurgery Haque TL, Konishi J, Takahashi JA, Hashimoto N. 2003. Liliequist 68(1 Suppl Operative): 7–15. membrane: three‐dimensional constructive interference in steady Sabouri S, Khatami A, Shahnazi M, Tonekaboni SH, Momeni A, Meh- state MR imaging. Radiology 229(2): 360–365. rafarin M. 2011. Ultrasonographic measurement of subarachnoid Gacek RR. 1998. Anatomy and significance of the subarachnoid space space and frontal horn width in healthy Iranian infants. Iranian J in the Fallopian canal. Am J Otol 19(3): 358–365. Child Neurol 5(1). Gulsen S, Dinc AH, Unal M, Canturk N, Altinors N. 2010. Characteri- Vinas FC, Panigrahi M. 2001. Microsurgical anatomy of the Liliequist’s zation of the anatomic location of the pituitary stalk and its relation- membrane and surrounding neurovascular territories. Minim Inva- ship to the dorsum sellae, tuberculum sellae and chiasmatic cistern. sive Neurosurg 44(2): 104–109. J Korean Neurosurg Soc 47(3): 169–173. Vinas FC, Dujovny M, Fandino R, Chavez V. 1994. Microsurgical anat- Hodges FJ. 1970. Anatomy of the ventricles and subarachnoid spaces. omy of the supratentorial arachnoidal trabecular membranes and Seminars in Roentgenology 5(2): 101–121. cisterns. Neurol Res 16(6): 417–424. Inoue K, Seker A, Osawa S, Alencastro LF, Matsushima T, Rhoton AL Vinas FC, Dujovny M, Fandino R, Chavez V. 1996a. Microsurgical Jr. 2009. Microsurgical and endoscopic anatomy of the supratentorial anatomy of the arachnoidal trabecular membranes and cisterns at the arachnoidal membranes and cisterns. Neurosurgery 65(4): 644–665. level of the tentorium. Neurol Res 18(4): 305–312. Key A, Retzius M. 1875. Studien in der Anatomie des Nervensystems und Vinas FC, Dujovny M, Fandino R, Chavez V. 1996b. Microsurgical anat- des Bindegewebes. Stockholm: Samson & Wallin. omy of the infratentorial trabecular membranes and subarachnoid Lam WW, Ai VH, Wong V, Leong LL. 2001. Ultrasonographic meas- cisterns. Neurol Res 18(2): 117–125. urement of subarachnoid space in normal infants and children. Wang SS, Zheng HP, Zhang X, Zhang FH, Jing JJ, Wang RM. 2008. Pediatr Neurol 25(5): 380–384. Microanatomy and surgical relevance of the olfactory cistern. Micro- Libicher M, Troger J. 1992. US measurement of the subarachnoid space surgery 28(1): 65–70. in infants: normal values. Radiology 184(3): 749–751. Wang SS, Zheng HP, Zhang FH, Wang RM. 2011a. The microanatom- Liliequist B. 1956. The anatomy of the subarachnoid cisterns. ical structure of the cistern of the lamina terminalis. J Clin Neurosci Acta Radiol 46(1–2): 61–71. 18(2): 253–259. Liliequist B. 1959. The subarachnoid cisterns. An anatomic and roent- Wang SS, Zheng HP, Zhang FH, Wang RM. 2011b. Microsurgical anat- genologic study. Acta Radiol Suppl 185: 1–108. omy of Liliequist’s membrane demonstrating three‐dimensional con- Lu J, Zhu XL. 2003. Microsurgical anatomy of Liliequist’s membrane. figuration. Acta Neurochir (Wien) 153(1): 191–200. Minim Invasive Neurosurg 46(3): 149–154. Yaşargil MG. 1984. Microsurgical Anatomy of the Basal Cisterns and Ves- Lu J, Zhu XL. 2005a. Microsurgical anatomy of the interpeduncu- sels of the Brain: Diagnostic Studies, General Operative Techniques and lar cistern and related arachnoid membranes. J Neurosurg 103(2): Pathological Considerations of the Intracranial Aneurysms. New York: 337–341. Thieme. Lu J, Zhu XL. 2005b. Characteristics of distribution and configuration of Yaşargil MG, Kasdaglis K, Jain KK, Weber HP. 1976. Anatomical obser- intracranial arachnoid membranes. Surg Radiol Anat 27(6): 472–481. vations of the subarachnoid cisterns of the brain during surgery. Lu J, Zhu XL. 2007. Cranial arachnoid membranes: some aspects of J Neurosurg 44(3): 298–302. microsurgical anatomy. Clin Anat 20(5): 502–511. Zaaroor M, Kosa G, Peri‐Eran A, Maharil I, Shoham M, Goldsher D. Matsuno H, Rhoton AL Jr, Peace D. 1988. Microsurgical anatomy of the 2006. Morphological study of the spinal canal content for subarach- posterior fossa cisterns. Neurosurgery 23(1): 58–80. noid endoscopy. Minim Invasive Neurosurg 49(4): 220–226. Narli N, Soyupak S, Yildizdas HY, Tutak E, Ozcan K, Sertdemir Y, Zhang M, An PC. 2000. Liliequist’s membrane is a fold of the arachnoid Satar M. 2006. Ultrasonographic measurement of subarachnoid mater: study using sheet plastination and scanning electron micros- space in normal term newborns. Eur J Radiol 58(1): 110–112. copy. Neurosurgery 47(4): 902–909. Okur A, Küçük O, Karaçavuş S, Yıldırım A, Erdoğan Y, Serin H. 2013. Zhang XA, Qi ST, Huang GL, Long H, Fan J, Peng JX. 2012. Anatomical A novel index in healthy infants and children – subarachnoid space: and histological study of Liliequist’s membrane: with emphasis on its ventricle ratio. Folia Morphol (Warsz) 72(2): 142–146. nature and lateral attachments. Childs Nerv Syst 28(1): 65–72.