Endoscopic Anatomical Study of the Arachnoid Architecture on the Base of the Skull

Home , Arachnoid trabeculae, Chiasmatic cistern, Diaphragma sellae

DOI 10.1515/ins-2012-0005 Innovative Neurosurgery 2013; 1(1): 55–66

Original Research Article

Peter Kurucz* , Gabor Baksa , Lajos Patonay and Nikolai J. Hopf Endoscopic anatomical study of the arachnoid architecture on the base of the skull. Part I: The anterior and middle cranial fossa

Abstract: Minimally invasive neurosurgery requires a Introduction detailed knowledge of microstructures, such as the arachnoid membranes. In spite of many articles addressing The arachnoid was discovered and named by Gerardus arachnoid membranes, its detailed organization is still not Blasius in 1664 [22 ]. Key and Retzius were the first who well described. The aim of this study is to investigate the studied its detailed anatomy in 1875 [ 11 ]. This description was topography of the arachnoid in the anterior cranial fossa an anatomical one, without mentioning clinical aspects. The and the middle cranial fossa. Rigid endoscopes were intro- first clinically relevant study was provided by Liliequist in duced through defined keyhole craniotomies, to explore 1959 [ 13 ]. He described the radiological anatomy of the sub- the arachnoid structures in 110 fresh human cadavers. We arachnoid cisterns and mentioned a curtain-like membrane describe the topography and relationship to neurovascu- between the supra- and infratentorial cranial space bearing lar structures and suggest an intuitive terminology of the his name still today. Lang gave a similar description of the arachnoid. We demonstrate an “ arachnoid membrane sys- subarachnoid cisterns in 1973 [12 ]. With the introduction of tem ” , which consists of the outer arachnoid and 23 inner microtechniques in neurosurgery, the detailed knowledge arachnoid membranes in the anterior fossa and the middle of the surgical anatomy of the cisterns became more impor- fossa. The inner membranes are arranged in two “ arach- tant. The first microneurosurgically relevant description of noid membrane groups” in the examined regions. The first the subarachnoid space was provided by Yasargil et al. in is the carotid membrane group, located in the suprasellar 1976 [30 ]. He published the most complete study about the region, consisting of seven paired and three unpaired extensions and contents of the subarachnoid cisterns and inner membranes and the outer arachnoid on its base. The illustrated it with intraoperative photographs [ 29 ]. Although second is the Sylvian membrane group, composed of three numerous membranes can be identified on his photographs, inner membranes of the Sylvian fissure and completed by he named only the membrane of Liliequist. Matsuno et al. in the outer arachnoid. Our findings should be very helpful 1988 [19 ] and later in the 1990s– 2000s, Vinas et al. [25 – 27 ], in understanding the complex organization of the cranial Lu and Zhu [14 – 17 ] and Inoue et al. [10 ] were the founders of arachnoid, which is mandatory for the safe and effective a new concept concentrating on the microsurgical anatomy use of minimally invasive endoscopic techniques. of the arachnoid membranes separating the suba rachnoid cisterns. They provided full descriptions of the intracranial Keywords: Arachnoid membranes; arachnoid membrane arachnoid. These works were followed by a series of articles system; endoscopic anatomy; skull base; subarachnoid about the microscopic [ 3 , 4 , 6 , 7 , 18 , 20 , 23 , 24 , 28 , 31 ] and in cisterns. the last time the endoscopic anatomy [ 1 , 2 , 32 ] of the cisterns and membranes. In most articles, the description of the arachnoid *Corresponding author: Peter Kurucz, Dr. Med., Laboratory for Applied and Clinical Anatomy, Institute of Anatomy, Histology membranes has been restricted only to their individual and Embryology, Semmelweis University, T ü zolt ó utca 58, 1094 location. However, nobody has recognized a systematic Budapest, Hungary, Tel.: +36 30 527 4722, composition of these structures yet. In addition, photo- E-mail: [email protected] graphic depiction of the arachnoid membranes is also Gabor Baksa and Lajos Patonay: Laboratory for Applied and limited and endoscopic studies are pending, to support Clinical Anatomy, Institute of Anatomy, Histology and Embryology, Semmelweis University, Budapest, Hungary endoscopic microsurgery. Furthermore, the terminology Nikolai J. Hopf: Department of Neurosurgery, Katharinenhospital, used by previous authors is non-uniform and sometimes Klinikum Stuttgart, Stuttgart, Germany not appropriate. 56 P. Kurucz et al., Anatomy of the arachnoid membranes, Part I

According to the aforementioned aspects, the aim Outer arachnoid of this study is to provide sufficient information on the topography of the arachnoid membranes at the skull At the frontal base, the outer arachnoid covers the basal base, suggesting a revised and intuitive terminology, and surface of both frontal lobes ( Figure 1 A and B). It encases to provide an extensive photo documentation. basally both olfactory nerves and forms an out-bulging sleeve around the olfactory bulbs. It bridges basally the posterior part of the interhemispheric fissure between Materials and methods the frontal lobes and covers the falx cerebri ( Figure 1 C). Posteromedially, it covers the central part of the middle skull base and posterolaterally, after closing the Sylvian The study was performed on a total of 110 fresh human cadavers (75 male, 35 female); postmortem not more than 72 h. The cadavers fissure, extends to the temporal pole (Figure 1A and B). were between the ages of 30 and 80 years and without signifi cant in- Anteriorly and laterally it continues to the cerebral tracranial pathology. In each cadaver, the intracranial arterial system convexity. was injected with red gelatin solution. The dissections were carried The outer arachnoid on the basal surface of the tempo- out on the entire skull base in each cadaver, even though in this part, ral lobe continues posteriorly to the direction of the occi- only the results concerning the anterior cranial fossa and the middle cranial fossa are provided. Brains were removed completely from pital lobes. Medially, it covers the lower part of the medial the cranial cavity, with intact outer arachnoid in 14/110 cadavers for surface of the temporal lobe, until it reaches the level of the dissections only under the operating microscope. In 96/110 cadavers, anterior petroclinoid ligament and continues as the outer the dissections were performed through defi ned keyhole approaches, arachnoid of the suprasellar region between the two unci including the supraorbital [ 21 ] and the pterional craniotomy, using ( Figure 1 D). endoscope-assisted (n = 27) or endoscope-controlled microsurgical The outer arachnoid of the central part of the middle (n = 69) technique [9 ]. We used a 0- and 30-degree rigid, rod-lens endoscopes (B. skull base forms the floor of the carotid and chiasmatic Braun/Aesculap AG, Tuttlingen, Germany) with a diameter of 4 mm cisterns. Anteriorly, it is continuous with the arachnoid for endoscope-controlled microsurgery (ECM). For endoscope-assist- cover of the basal surface of the frontal lobes. At the ed microsurgery (EAM), an operating microscope (Opmi, Carl Zeiss, transition between the anterior fossa and the middle Oberkochen, Germany) was used in addition to the endoscope. fossa, it follows the optic nerves to the optic canals ( Figure 1 B). The supraclinoid segments of the internal carotid artery are covered by the inward protrusion of the outer arachnoid ( Figure 1 E). Posteriorly from the Results carotid arteries, the outer arachnoid covers the surface of the diaphragma sellae. If the superior surface of the Endoscopic dissections, either using EAM or ECM, were pituitary gland is displaced inferiorly to the diaphragm found to be superior to dissections only under the micro- and the diameter of the ostium is large enough, the scope, because the deep seated structures of the skull outer arachnoid extends into the intrasellar region and base were better illuminated, could also be seen around covers the superior surface of the pituitary gland, result- the corner when using 30-degree optics and produced less ing in a subdiaphragmatic extension of the chiasmatic destruction of the normal anatomy. cistern (Figure 1F). In case of a small ostium or upward We found two main types of arachnoid structures: an herniated pituitary dome, we could not find a subdia- outer and an inner arachnoid construct. The outer arach- phragmatic extension of the outer arachnoid (Figure noid construct consists of a strong, clear membrane which 1 G). The pituitary stalk is encased by an inward protru- forms a closed cover around the brain. The inner arachnoid sion of the outer arachnoid from the superior surface of construct is located between the outer arachnoid mem- the pituitary gland. Posteriorly from the diaphragm, the brane and the pia mater. The inner arachnoid construct outer arachnoid extends to the dorsum sellae. Here, the is best developed on the base of the skull. The network of arachnoid is detached from the inner surface of the dura single arachnoid trabeculae, located in the subarachnoid mater, resulting in a real subdural space (Figure 1H). space, forms a stabilizing system around the neurovas- The Liliequist’ s membrane complex is attached to this cular structures. The cumulation of trabeculae can form part of the outer arachnoid. Laterally, the outer arach- either complete or incomplete sheet-like structures, which noid extends at both sides, to adhere to the anterior pet- we called “ inner arachnoid membranes ” . These mem- roclinoid ligaments and continues to cover the temporal branes build the natural walls of the basal cisterns. lobe ( Figure 1 D). P. Kurucz et al., Anatomy of the arachnoid membranes, Part I 57

Figure 1 The outer arachnoid. (A) Basal view of the outer arachnoid on the cerebral surface of the anterior fossa and the middle fossa on en bloc removed brain. Red – outer arachnoid of the anterior fossa. Yellow – outer arachnoid cover of the temporal lobe. Green – outer arachnoid closing the Sylvian fissure. Blue – outer arachnoid cover of the suprasellar region. (B) The outer arachnoid on the anterior fossa and the middle fossa from the subfrontal direction. The outer arachnoid follows the optic nerves to the optic canals. (C) Endoscopic view of the anterior fossa through the left anterior interhemispheric approach. Note the out-bulging of the outer arachnoid around the olfactory bulb (blue arrow-head). The outer arachnoid bridges the two cerebral hemispheres, just behind the falx cerebri (red arrow-head). (D) Endoscopic view of the outer arachnoid cover above the anterior petroclinoid ligament through the left subtemporal approach. The temporal lobe is slightly elevated. (E) Endoscopic view of the internal carotid artery through the left supraorbital approach. The inward protrusion of the outer arachnoid forms an envelope around the artery (blue arrow-head). (F) The chiasmatic cistern through the median subfrontal approach. The intrasellar protrusion of the outer arachnoid is well recognizable from its reflection of light on the superior surface of the pituitary gland located deep in the sella turcica. (G) Endoscopic left supraorbital approach in a cadaver, with upward herniated dome of the pituitary gland. In this case, the outer arachnoid does not have an intrasellar protrusion. (H) Endoscopic view of the region of the dorsum sellae through the left supraorbital approach. The outer arachnoid is detached here from the inner surface of the dura (blue arrow-head), resulting in a real subdural space. ant. petrocl. lig. = anterior petroclinoid ligament, CNI = olfactory nerve, CNII = optic nerve, CNIII = oculomotor nerve, diaphr. sellae = diaphragma sellae, DL = diencephalic leaf of the Liliequist ’ s membrane complex, falx = falx cerebri, front. base = frontal base, front. lobe = frontal lobe, ICA = internal carotid artery, left olf. bulb = left olfactory bulb, out. arachn. = outer arachnoid, P.Co.A. = posterior communicating artery, pit. gland = pituitary gland, pit.stalk = pituitary stalk, temp. base = temporal base, temp. lobe = temporal lobe.

Inner arachnoid membranes of these membranes were found to be paired, summing up to a total of 23 distinct inner arachnoid membranes. In the anterior cranial fossa and the middle cranial fossa, The inner arachnoid membranes are described in we could distinguish 13 inner arachnoid membranes. Ten order as they appear from a subfrontal direction. 58 P. Kurucz et al., Anatomy of the arachnoid membranes, Part I

Olfactory membrane membrane at the level of the medial edge of the olfactory nerve; inferior – upper surface of the lateral edge of This is a paired membrane which is always present and the optic chiasm and nerve where it is connected to the without perforations. In a closed skull, it stretches over the anterosuperior edge of the medial carotid membrane. basal surface of the olfactory trigone (Figures 2C, 3A and B). Here, at the lateral side of the optic nerve, an additional There is no perforating artery through this membrane. It membrane on the superior surface of the optic nerve separates the carotid cistern from the olfactory cistern. attaches to the inferior edge of the lateral lamina termi- Connections: superior – posterior edge of the olfac- nalis membrane. tory trigone; inferior – outer arachnoid cover of the basal surface of the frontal lobe; medial – superior edge of the lateral lamina terminalis membrane; and lateral – ante- Medial lamina terminalis membrane rior and superior edge of the proximal Sylvian membrane. This is a semi-oval shaped, unpaired membrane located in the midline (Figure 3D). Sometimes it is not membrane- Lateral lamina terminalis membrane like, but more a dense network of arachnoid trabeculae filling the anterior portion of the chiasmatic cistern. This is a paired, constant and intact membrane which is The membrane is located in the same plane as the optic located above and parallel to the optic chiasm and optic nerves. Its superior surface is attached through numerous nerves ( Figures 2 C, 3C ). The posterior part of the mem- trabeculae to the posterior ends of the gyri recti. The membrane is perforated by the A1 segment of the anterior brane incorporates numerous medial perforator branches cerebral artery and the recurrent artery of Heubner. The of the internal carotid artery and separates the chiasmatic membrane separates the lamina terminalis cistern from from the lamina terminalis cistern. the carotid cistern. Connections: anterior – outer arachnoid cover of Connections: anterior – outer arachnoid cover tuberculum sellae; posterior – anterior edge of the optic of the basal surface of the frontal lobe; posterior – chiasm; lateral – medial edges of the optic nerves. The optic chiasm; superior – lateral edge of the olfactory lateral edge of the membrane is attached to the inner

Figure 2 Overview of the inner arachnoid structures around the internal carotid artery on en bloc removed brains. (A) Topography of the inner membranes around the posterior part of the carotid cistern after partly removing the outer arachnoid. (B) After dissection of the inferior edge of the medial carotid membrane, the diencephalic leaf of the Liliequist membrane complex became visible. (C) Connection of the olfactory and lateral lamina terminalis membranes and their relations to the surrounding structures. ACA = anterior cerebral artery, A.Ch.A. = anterior choroidal artery, CNI = olfactory nerve, CNII = optic nerve, CNIII = oculomotor nerve, DL = diencephalic leaf of the Liliequist ’ s membrane complex, ICA = internal carotid artery, LCM = lateral carotid membrane, LLTM = lateral lamina terminalis membrane, MCA = middle cerebral artery, MCM = medial carotid membrane, olf. trig. = olfactory trigone, OM = olfactory membrane, P.Co.A. = posterior communicating artery, PCA = posterior cerebral artery, pit.stalk = pituitary stalk, TM = temporal membrane. P. Kurucz et al., Anatomy of the arachnoid membranes, Part I 59 arachnoid sheaths on the superior and inferior surfaces but covers partly the arachnoid sheath of the oculomotor of the optic nerves, which connect the anteroinferior edge nerve from above. It acts as the lateral wall of the carotid of the lateral lamina terminalis membrane (Figure 3C) cistern. and the anterosuperior edge of the medial carotid mem- Connections: anterior – posterior edge of the proxi- brane. This results in inner arachnoid sheaths around the mal Sylvian membrane; posterior – lateral edge of the optic nerves. temporal membrane; superior – inferolateral edge of the optic tract; inferior – the outer arachnoid along the anterior petroclinoid ligament. Proximal Sylvian membrane

This is a constant and paired membrane, which is the Temporal membrane continuation of the lateral carotid membrane to the anterior direction ( Figure 3 E). It is strong and similar to the This is a paired membrane, which is the lateral continu- outer arachnoid. The membrane is perforated by the M1 ation of the diencephalic leaf of the Liliequist ’s mem- segment of the middle cerebral artery and separates the brane complex (Figures 2A, 3H ). It is a constant structure, carotid cistern from the Sylvian cistern. sometimes with a trabeculated appearance, sometimes Connections: anterior – lateral edge of the olfactory with a clear outer membrane-like structure. The poste- membrane and the medial edge of the lateral and inter- rior communicating artery perforates the membrane at mediate Sylvian membranes; posterior – anterior edge of its medial edge. The P2 segment of the posterior cere- the lateral carotid membrane; superior – lateral edge of bral artery is located directly behind the membrane and the olfactory membrane; inferior – outer arachnoid cover sometimes attached to its posterior surface. The anterior of the anterior clinoid process and the anterior part of the choroidal artery courses superolaterally above the mem- anterior petroclinoid ligament. brane passing from the carotid to the ambient cistern. The oculomotor nerves are located inferolaterally under the membrane. It separates the carotid cistern from the inter- Internal carotid membrane peduncular cistern. Connections: medial – junction between the lateral This is a paired membrane, sometimes existing only edge of the diencephalic leaf and the posterior edge of the as a dens network of numerous stabilizing trabeculae medial carotid membrane; lateral – posterior edge of the between the internal carotid artery and the medial surface lateral carotid membrane; superior – posteromedial edge of the temporal lobe (Figure 3F). If the medial carotid of the optic tract; inferior – if the Liliequist’ s membrane membrane (see below) is absent, the internal carotid complex has a common leaf, then the temporal membrane membrane becomes thicker. It is located in the caro tid is connected to its posterior edge. If the common leaf is cistern and partly divides it to an anterior and a posterior missing, it is connected to the outer arachnoid cover of the compartment. dorsum sellae and the oculomotor triangle. Connections: lateral – the middle of the lateral carotid membrane on the medial surface of the uncus, above the oculomotor nerve; medial – lateral edge of the arach- Common leaf of the Liliequist ’ s membrane noid sheath of the internal carotid artery; superior and inferior – these edges of the membrane are free. The Liliequist’ s membrane complex is composed by the diencephalic, mesencephalic and a variable common leaf. Only the diencephalic and the common leaves are Lateral carotid membrane located in the examined area. The common leaf is a variant, unpaired membrane. It was present only in 23% This is a constant, intact and paired membrane with a of the cases. It is an intact membrane without perforat- similar structure to the outer arachnoid. It stretches over ing vessels and serves as the common origin of the dien- the superomedial surface of the uncus, playing a similar cephalic and mesencephalic leaves ( Figure 3 H and I). role to the outer arachnoid attached to the pia mater This leaf separates the chiasmatic from the prepontine ( Figure 3 G). The posterior end of the membrane bridges cistern. the space between the posterior surface of the uncus and Connections: anterior – outer arachnoid cover of the the crus cerebri (Figure 2A). It has no perforating vessel, dorsum sellae and the oculomotor triangle; posterior 60 P. Kurucz et al., Anatomy of the arachnoid membranes, Part I

– the junction between the diencephalic and mesence- Medial carotid membrane phalic leaves; lateral – it is connected to the lateral mesencephalic membrane below the oculomotor nerves, This is a paired membrane which is parallel to the lateral which is the lateral continuation of the mesencephalic carotid membrane and perpendicular to the diencephalic leaf of the Liliequist ’ s membrane complex around the leaf of the Liliequist ’ s membrane complex ( Figure 2 A mesencephalon. and B). It is highly trabeculated and composed by the P. Kurucz et al., Anatomy of the arachnoid membranes, Part I 61

Figure 3 Endoscopic observation of the inner arachnoid membranes from left subfrontal direction. (A) The olfactory membrane after retraction of the frontal lobe. (B) Medial and lateral border of the olfactory membrane after retraction of the frontal lobe. (C) The lateral lamina terminalis membrane after removing the olfactory membrane. The blue arrow-head indicates the arachnoid sheath around the optic nerve. (D) The medial lamina terminalis membrane after its separation from the basal surface of the frontal lobe. (E) The proximal Sylvian membrane viewed through a small incision on the outer arachnoid. The M1 segment of the middle cerebral artery perforates the membrane. (F) The internal carotid membrane. (G) After resection of the internal carotid membrane, the lateral carotid membrane became visible. (H) At the posterior pole of the carotid cistern, the temporal membrane and its neurovascular relation can be seen. In this specimen, the common leaf of the Liliequist ’ s membrane complex is also present. (I) The perforation of the common leaf gives a direct view to the basilar artery trunk located in the prepontine cistern (blue arrow-head). In this specimen we also perforated the temporal membrane, therefore, the intracisternal part of the oculomotor nerve and the upper surface of the mesencephalic leaf of the Liliequist ’ s membrane complex became visible in the interpeduncular cistern. (J) Between the optic nerve and the internal carotid artery, the medial carotid membrane is visible along the entire length of the carotid cistern. (K) At the middle part of the medial carotid membrane, numerous medial perforator branches are visible, originating from the internal carotid and posterior communicating artery. (L) After resection of the posterior part of the medial carotid membrane, the anterior surface of the diencephalic leaf of the Liliequist ’ s membrane complex in the chiasmatic cistern became visible from the carotid cistern. In this specimen the temporal membrane is also perforated, therefore the interpeduncular segment of the basilar artery is visible. This cadaver also has a common leaf. (M) The lateral Sylvian membrane is visible just under the opened outer arachnoid membrane. In the space between the lateral Sylvian membrane and the outer arachnoid, some superficial veins of the Sylvian fissure were located (blue arrow-head). (N) After resection of the lateral Sylvian membrane, the intermediate Sylvian membrane became visible. The branches of the middle cerebral artery are located under the membrane (blue arrow-head). (O) The medial Sylvian membrane is the deepest layer of arachnoid in the Sylvian fissure, which is located between the branches of the middle cerebral artery. ACA = anterior cerebral artery, BA = basilar artery, chiasm = optic chiasm, CL = common leaf of the Liliequist ’ s membrane complex, CNI = olfactory nerve, CNII = optic nerve, CNIII = oculomotor nerve, DL = diencephalic leaf of the Liliequist ’ s membrane complex, front. lobe = frontal lobe, front. operc. = frontal operculum, ICA = internal carotid artery, ICM = internal carotid membrane, ISM = intermediate Sylvian membrane, LCM = lateral carotid membrane, LSM = lateral Sylvian membrane, MCA = middle cerebral artery, MCM = medial carotid membrane, ML = mesencephalic leaf of the Liliequist ’ s membrane complex, MLTM = medial lamina terminalis membrane, MSM = medial Sylvian membrane, OM = olfactory membrane, out. arachn. = outer arachnoid, PCA = posterior cerebral artery, P.Co.A. = posterior communicating artery, PSM = proximal Sylvian membrane, temp. lobe = temporal lobe, TM = temporal membrane. adhesions of the arachnoid trabeculae surrounding the membrane complex is present, the posterior part of the medial perforator arteries originating from the internal medial carotid membrane is attached inferiorly to it and carotid and the posterior communicating arteries. As a the rest merges inferiorly to the outer arachnoid (Figure result of this, the mentioned arteries run in the wall of the 3 L). If the common leaf is missing, the whole membrane is medial carotid membrane ( Figure 3 K). The superior hypo- attached inferiorly to the outer arachnoid. physeal artery also runs in the wall of the membrane and then penetrates it to reach the pituitary stalk. The posterior part of the membrane is sometimes not a membrane-like Diencephalic leaf of the Liliequist ’ s membrane complex structure, but a dense trabecular network. The membrane separates the carotid cistern from the chiasmatic cistern. The diencephalic leaf is an unpaired midline membrane. Connections: anterior – it merges into the medial We define this membrane as a structure between the pos- edge of the outer arachnoid envelope around the terior edges of the medial carotid membranes, or between internal carotid artery; posterior – junction between the penetration points of the posterior communicating the lateral edge of the diencephalic leaf of the Liliequist’ s arteries, which are the same in most of the cases ( Figure membrane complex and the medial edge of the temporal 2 B). The appearance of the membrane varies from a tra- membrane ( Figure 3 L). In most of the cases, this junction beculated one, with small perforations to an outer mem- is the same as the penetration points of the posterior com- brane-like clear sheet without any openings. The height municating arteries ( Figure 2 B); superior – the anterior of the membrane also varies greatly, sometimes it can be portion of the membrane is attached superiorly to the extremely small. The angle between the outer arachnoid posteroinferior edge of the lateral lamina terminalis mem- of the suprasellar region and the diencephalic leaf ranges brane, at the inferolateral side of the optic chiasm and between 90 and 160 degrees. In the case of a 90° position, optic nerve ( Figure 3 J). Here, an additional membrane the anterior surface of the diencephalic leaf is sometimes on the inferior surface of the optic nerve connects to the attached to the posterior surface of the arachnoid envelope medial carotid membrane. The posterior part of the mem- around the pituitary stalk. There is no perforating vessel brane is attached superiorly along the medial edge of the passing through the diencephalic leaf. The membrane optic tract; inferior – if the common leaf of the Liliequist ’ s separates the chiasmatic from the interpeduncular cistern. 62 P. Kurucz et al., Anatomy of the arachnoid membranes, Part I

Connections: lateral – it is continuous with the medial structure than a sheet-like arachnoid form. The proximal edge of the temporal membrane. The lateral edge of the part of the membrane situated between the insula and the diencephalic leaf is connected to the posterior edge of the M1 and M2 segments of the middle cerebral artery. In the medial carotid membrane; inferior – if the common leaf is lateral portion of the Sylvian fissure, the distal part of the present, the inferior border of the membrane is connected membrane courses between the M3 branches ( Figure 30 ). to the junction between the common leaf and the mesencephalic leaf (Figure 3L). If the common leaf is missing, it is connected to the junction between the mesencephalic leaf and the outer arachnoid covering the dorsum sellae Discussion ( Figure 1 H); superior – attaches premammillary (75%), or retromammillary (25%). The anatomy of the arachnoid membranes in the anterior cranial fossa and the middle cranial fossa was first published by Vinas et al. [25 , 26 ], Vinas and Panigrahi Lateral Sylvian membrane [27 ], Lu and Zhu [14 – 17 ] and most recently by Inoue et al. [10 ]. These studies described the existence of the mem- This membrane is located just under the outer arach- branes, but only few anatomical details were provided noid cover of the Sylvian fissure ( Figure 3 M). It originates and arachnoid membranes were thought to be variable. medially from the anterolateral surface of the proximal The present study was performed on a high number of Sylvian membrane and runs nearly parallel and attached fresh human cadavers (n = 110) in order to recognize a to the inner surface of the outer arachnoid. The membrane possible system in its organization or common varia- extends along the entire length of the Sylvian fissure. The tions. In addition, we aimed to update and rationalize superficial Sylvian veins are located in the narrow space the existing different nomenclatures used in the previ- between the lateral Sylvian membrane and the outer ous publications. arachnoid. The M3 segment of the middle cerebral artery Another unique feature of this study is that endo- perforates the membrane. scopes were used as the main optical tool for our dissections. This technique enables examination of the natural positions and relations of the deep-seated arachnoid Intermediate Sylvian membrane structures to the neurovascular structures, with minimal approach-related distortion of the surrounding struc- The intermediate Sylvian membrane is the third level of tures. Furthermore, this surgically oriented endoscopic arachnoid layers of the Sylvian fissure located under the anatomical knowledge about the presently not well rec- lateral Sylvian membrane. This is the most well-devel- ognized details of the arachnoid membranes, seems to oped inner membrane of the Sylvian fissure, with its clear, be important to safely apply and further push forward sheet-like structure ( Figure 3 N). It originates medially the rapidly developing, minimally invasive techniques in from the lateral surface of the proximal Sylvian membrane neurosurgery [ 9 , 21 ]. and runs nearly parallel to the lateral Sylvian membrane Based on our study, the inner arachnoid trabecular along the entire length of the Sylvian fissure. The space membranes seem to vary to a great extent among indi- between the lateral and intermediate Sylvian membrane viduals. However, a higher systematic organization was is wider than that between the outer arachnoid and the found to be present, although not complete, in all of lateral Sylvian membrane. This compartment is filled the examined cadavers. The inner membranes are con- with numerous single trabeculae. The distal part of the M1 centrated around the neurovascular structures of well- and the entire M2 segment of the middle cerebral artery defined skull base areas in a regular pattern. Therefore, courses under the membrane. The branches of the M3 we suggest using the term “ arachnoid membrane system ” . segment perforate the membrane to continue as the M4 The arachnoid membrane system of the anterior cranial segment on the cortical surface. fossa and the middle cranial fossa consists of 13 distinct inner arachnoid membranes, 10 of them are paired, giving a total of 23 inner arachnoid membranes. This system acts Medial Sylvian membrane as the frame of the subarachnoid space and defines the three-dimensional shape of the basal cisterns. For a better This is the deepest inner arachnoid membrane of the Syl- understanding, we described the ideal “ all-in-one ” case vian fissure. It has a rather more densely trabeculated and common individual variations. P. Kurucz et al., Anatomy of the arachnoid membranes, Part I 63

Within the arachnoid membrane system of the ante- cistern. These two membranes form the central part of the rior cranial fossa and the middle cranial fossa, we could carotid membrane group. further distinguish two distinct membrane groups. The The base of the carotid membrane group is the outer “ carotid membrane group ” located in the suprasellar arachnoid of the central part of the middle skull base. The region and the “ Sylvian membrane group ” located in the latter finding is supported by the literature [ 16 ]. In con- Sylvian fissures on both sides (Figure 4A). The Sylvian trast to the previous publications [6 , 23 ], we think that the membrane group is connected to the carotid membrane arachnoid formations of the intrasellar area are the exten- group by the proximal Sylvian membrane. sions of the outer arachnoid of the suprasellar region. As a result of our examinations, we could confirm the existence of a real subdural space at the dorsum sellae, The carotid membrane group as stated by others [ 3 ]. If the common leaf of the Lilie- quist ’ s membrane complex is present, it acts as the base The carotid membrane group is composed of 17 inner of the posterior part of the carotid membrane system. The membranes. It has a lateral part on both sides and a description of the common leaf is controversial in the liter- central part ( Figure 4 B). The lateral part is organized ature. Several authors mentioned a structure which could along two circles around the internal carotid artery and be the common leaf described by us [7 , 8 , 17 , 19 , 24 , 32 ]. encloses the carotid cisterns. The two arachnoid circles Our endoscopic examinations confirmed the existence of are connected to each other at both the anterior and pos- a common leaf of the Liliequist’ s membrane complex in terior poles forming the chiasmatic and lamina terminalis 23% of cases.

Figure 4 Schematic drawings of the inner arachnoid membrane system on the anterior and middle cranial fossa. (A) Basal projections of the carotid and Sylvian membrane groups. Yellow – Sylvian cistern. Green – carotid cistern. Red – chiasmatic cistern. Blue – lamina terminalis cistern. (B) Three-dimensional representation of the carotid membrane group. ACA = anterior cerebral artery, BA = basilar artery, CL = common leaf of the Liliequist ’ s membrane complex, CNI = olfactory nerve, CNII = optic nerve, CNIII = oculomotor nerve, DL = diencephalic leaf of the Liliequist ’ s membrane complex, ICA = internal carotid artery, ICM = internal carotid membrane, ISM = intermediate Sylvian membrane, LCM = lateral carotid membrane, LLTM = lateral lamina terminalis membrane, LSM = lateral Sylvian membrane, MCA = middle cerebral artery, MCM = medial carotid membrane, ML = mesencephalic leaf of the Liliequist ’ s membrane complex, MLTM = medial lamina terminalis membrane, MSM = medial Sylvian membrane, OM = olfactory membrane, PCA = posterior cerebral artery, PSM = proximal Sylvian membrane, TM = temporal membrane. 64 P. Kurucz et al., Anatomy of the arachnoid membranes, Part I

Lateral parts describes that the membranous structure located laterally to the diencephalic leaf is called the temporal membrane, The lateral parts of the carotid membrane group consist and is a part of the Liliequist ’ s membrane. In our concept, of the olfactory membrane, which forms the anterior wall the diencephalic leaf is only that part of this curtain-like of the arachnoid circle around the internal carotid artery. structure which is located between the penetration area Previously, it was described as a membrane encasing the of the posterior communicating arteries, or between the olfactory nerve and the olfactory bulb [26 ]. Other authors posterior edges of the medial carotid membranes, which have also mentioned its connections [ 17 ]. Inoue et al. [ 10 ] was found to be the same in most of the examined cases. described only the posterior part of it, which is located The lateral continuation of the diencephalic leaf, until the on the basal surface of the olfactory trigone. Our results medial surface of the uncus, should be called the tempo- confirm this finding and completed the description as the ral membrane. Sometimes, the temporal membrane has inferior edge of the membrane is attached to the outer a completely different optical appearance compared to arachnoid of the frontal base. We could not find any inner the diencephalic leaf. Therefore, the temporal membrane membrane cover of the olfactory bulb. In our concept, the should be recognized as a separate membrane. floor of the olfactory cistern is formed by the outer arach- The medial wall of the arachnoid circle around the noid of the frontal lobes and closed anteriorly around the internal carotid artery is composed of the medial carotid olfactory bulb by its outer arachnoid sleeve and posteri- membrane. In the literature, this membrane is known orly by the olfactory membrane. as the “ carotid membrane ” [ 26 ], the “ carotid-chiasmatic The anterolateral segment of the lateral part of the wall” [4 , 28 , 31 ] or as the “ medial carotid membrane” carotid membrane group is composed of the proximal [ 2 , 10 , 17 – 19 , 23 , 31 , 32 ]. The name “ medial carotid mem- Sylvian membrane. It serves as the junction-point between brane” is commonly accepted. Therefore, we suggest the carotid and the Sylvian membrane group. Yasargil was using this term. The suprachiasmatic continuation of the the first who described this membrane as a group of strong medial carotid membrane at the anteromedial border of membranous fibers at the proximal part of the Sylvian the arachnoid circle around the internal carotid artery, fissure between the fronto-orbital and temporal gyrus but is the lateral lamina terminalis membrane. It is called, without naming it [29 ]. This membrane, also known as by several authors, the “ anterior cerebral membrane ” the “ anterior cerebral membrane” , was described previ- [ 17 , 26 ] or the “ lateral lamina terminalis membrane ” [ 10 ]. ously as a structure serving also as a border of the Sylvian However, because the cistern next to this membrane is fissure [26 ]. The most detailed study refers to it as the called the lamina terminalis cistern, we suggest using the “ proximal Sylvian membrane” [10 ]. Our results confirmed term “ lateral lamina terminalis membrane” . and completed this description, therefore we also suggest If the internal carotid membrane is present, it is the term “ proximal Sylvian membrane” . located inside of the arachnoid circle around the internal The lateral wall of the arachnoid circle around the carotid artery. It was mentioned by other authors as a part internal carotid artery is composed of the lateral carotid of different membranes. Inoue described it as a membrane membrane. This membrane was already mentioned in the extending downward from the inferolateral surface of the literature [ 17 , 19 ]. It has been also named as the “ anterior optic tract, attached to the anterior segment of the uncus choroidal membrane” [26 ]. The existence of a “ crural ” [ 10 ]. Others mentioned a membrane between the posterior or “ intracrural ” membrane, described by other authors branches of the internal carotid artery and the surround- extending between the posterior part of the uncus and the ing structures [17 , 26 ]. In our dissections, the internal crus cerebri, is controversial [10 , 19 , 20 ]. In our concept, carotid membrane was a rare finding, but certainly a dis- such a membrane would be identical to the posterior part tinct and separated membrane. of the lateral carotid membrane, which is attached to the lateral edge of the temporal membrane. Therefore, we do not handle it as a separate membrane. Central part The posterior wall of the lateral part of the carotid membrane group is composed of the temporal membrane. The central part of the carotid membrane group consists The existence of the temporal membrane is based on the of the medial lamina terminalis membrane and the dien- definition of the lateral edge of the Liliequist ’ s membrane cephalic leaf of the Liliequist’ s membrane complex. The complex, which was previously stated to be the tempo- former connects the anterior poles of the circles around ral lobe [4 , 27 , 29 ], the oculomotor nerve [8 , 10 , 13 , 19 , 20 , the internal carotid artery, between the lateral lamina 26 ] or the tentorial edge [7 , 20 , 28 , 31 ]. Zhang et al. [32 ] terminalis membrane superiorly and the medial carotid P. Kurucz et al., Anatomy of the arachnoid membranes, Part I 65 membranes inferiorly. This connection is made through membranous structure is more similar to a cerebral fissure the inner arachnoid sheaths of the optic nerves, which than to a basal cistern. The membranes of this group are are formed by arachnoid trabeculae on the superior and originating from the lateral surface of the proximal Sylvian inferior surfaces of the optic nerves. The medial lamina membrane and run almost parallel to each other in various terminalis membrane as an inner arachnoid structure depths, dividing the Sylvian cistern into four compart- was mentioned already in the literature [10 ], but we could ments. The anatomy of these membranes was described in not confirm its bilateral extension to the gyrus rectus detail previously by others using the same nomenclature and a free posterior edge. The “ suprachiasmatic leaf” of [ 10 ]. Our dissections could confirm these previous find- the basal chiasmatic membrane described by others [ 17 ] ings and supplement them with the demonstration and seems to be the same structure as the medial lamina termi- description of an endoscopic anatomical appearance. nalis membrane. The diencephalic leaf of the Liliequist ’s membrane complex connects the posterior poles of the arachnoid circles around the internal carotid artery. The Conclusion diencephalic leaf was mentioned as a structure extending between the dorsum sellae and the anterior [ 2 , 4, 5 , 7 , 8 , 13 , The systemic knowledge of the arachnoid architecture and 29 , 32 ] or posterior edge [ 10 , 19 , 26 , 27 ] of the mammillary its relation to neurovascular structures is mandatory for bodies. In our study, we could verify both variations. The the use of minimally invasive neurosurgical techniques, lateral edge of the membrane is controversial as discussed including endoscopic neurosurgery. This anatomical above. Its lateral continuation at both sides is thought to information is essential for the intraoperative orientation be the temporal membrane, as shown in this study. with the endoscope and for safe and effective manipula- tions, as well as for supporting the gravity related brain retraction or using surgical instruments parallel to the The Sylvian membrane group endoscope.

The Sylvian membrane group is composed of three Received August 24, 2012. Accepted November 11, 2012. Previously inner membranes in the Sylvian fissure at both sides. Its published online December 18, 2012

References

[1] Abuzayed B, Tanriover N, Akar Z, Eraslan BS, Gazioglu N. [8] Fushimi Y, Miki Y, Ueba T, Kanagaki M, Takahashi T, Yamamoto Extended endoscopic endonasal approach to the suprasellar A, et al. Liliequist membrane: three-dimensional constructive parachiasmatic cisterns: anatomic study. Childs Nerv Syst. interference in steady state MR imaging. Radiology. 2010;26:1161 – 70. 2003;229:360– 5; discussion 5. [2] Anik I, Ceylan S, Koc K, Tugasaygi M, Sirin G, Gazioglu N, [9] Hopf NJ, Perneczky A. Endoscopic neurosurgery and et al. Microsurgical and endoscopic anatomy of Liliequist ’ s endoscope-assisted microneurosurgery for the treatment of membrane and the prepontine membranes: cadaveric study and intracranial cysts. Neurosurgery. 1998;43:1330 – 6; discussion clinical implications. Acta Neurochir (Wien). 2011;153:1701 – 11. 6 – 7. [3] Ayberk G, Ozveren MF, Aslan S, Yaman ME, Yaman O, Kayaci S, [10] Inoue K, Seker A, Osawa S, Alencastro LF, Matsushima T, et al. Subarachnoid, subdural and interdural spaces at the clival Rhoton AL Jr. Microsurgical and endoscopic anatomy of region: an anatomical study. Turk Neurosurg. 2011;21:372 – 7. the supratentorial arachnoidal membranes and cisterns. [4] Brasil AV, Schneider FL. Anatomy of Liliequist ’ s membrane. Neurosurgery. 2009;65:644 – 64; discussion 65. Neurosurgery. 1993;32:956– 60; discussion 60– 1. [11] Key A, Retzius G. Studien in der Anatomie des Nervensystems [5] Buxton N, Vloeberghs M, Punt J. Liliequist ’ s membrane in und des Bindegewebes. Stockholm: P. A. Norstedt and Sö ner; minimally invasive endoscopic neurosurgery. Clin Anat. 1875. 1998;11:187 – 90. [12] Lang J. The subarachnoid space. Acta Anat (Basel). [6] Di Ieva A, Tschabitscher M, Matula C, Komatsu F, Komatsu M, 1973;86:267 – 99. Colombo G, et al. The subdiaphragmatic cistern: historic and [13] Liliequist B. The subarachnoid cisterns. An anatomic and radioanatomic findings. Acta Neurochir (Wien). 2012;154:667– 74. roentgenologic study. Acta Radiol Suppl. 1959;185:1 – 108. [7] Froelich SC, Abdel Aziz KM, Cohen PD, van Loveren HR, Keller [14] Lu J, Zhu X. Microsurgical anatomy of the interpeduncular JT. Microsurgical and endoscopic anatomy of Liliequist ’ s cistern and related arachnoid membranes. J Neurosurg. membrane: a complex and variable structure of the basal 2005;103:337 – 41. cisterns. Neurosurgery. 2008;63(1 Suppl 1):ONS1 – 8; discussion [15] Lu J, Zhu XI. Microsurgical anatomy of Liliequist ’ s membrane. ONS-9. Minim Invasive Neurosurg. 2003;46:149 – 54. 66 P. Kurucz et al., Anatomy of the arachnoid membranes, Part I

[16] Lu J, Zhu XL. Characteristics of distribution and configuration and cisterns at the level of the tentorium. Neurol Res. of intracranial arachnoid membranes. Surg Radiol Anat. 1996;18:305 – 12. 2005;27:472 – 81. [26] Vinas FC, Fandino R, Dujovny M, Chavez V. Microsurgical [17] Lu J, Zhu XL. Cranial arachnoid membranes: some aspects of anatomy of the supratentorial arachnoidal trabecular microsurgical anatomy. Clin Anat. 2007;20:502 – 11. membranes and cisterns. Neurol Res. 1994;16:417 – 24. [18] Martins C, Yasuda A, Campero A, Rhoton AL Jr. Microsurgical [27] Vinas FC, Panigrahi M. Microsurgical anatomy of the anatomy of the oculomotor cistern. Neurosurgery. 2006;58(4 Liliequist ’ s membrane and surrounding neurovascular Suppl 2):ONS-220 – 7; discussion ONS-7 – 8. territories. Minim Invasive Neurosurg. 2001;44:104 – 9. [19] Matsuno H, Rhoton AL Jr, Peace D. Microsurgical anatomy [28] Wang SS, Zheng HP, Zhang FH, Wang RM. Microsurgical of the posterior fossa cisterns. Neurosurgery. 1988;23: anatomy of Liliequist ’ s membrane demonstrating three- 58 – 80. dimensional configuration. Acta Neurochir (Wien). [20] Qi ST, Fan J, Zhang XA, Pan J. Reinvestigation of the ambient 2011;153:191 – 200. cistern and its related arachnoid membranes: an anatomical [29] Yasargil MG. Microneurosurgery. Stuttgart: Thieme; 1984. study. J Neurosurg. 2011;115:171 – 8. [30] Yasargil MG, Kasdaglis K, Jain KK, Weber HP. Anatomical [21] Reisch R, Stadie A, Kockro RA, Hopf N. The keyhole concept in observations of the subarachnoid cisterns of the brain during neurosurgery. World Neurosurg. 2012 Feb 10. Epub ahead of surgery. J Neurosurg. 1976;44:298 – 302. print]. [31] Zhang M, An PC. Liliequist ’ s membrane is a fold of the [22] Sanan A, van Loveren HR. The arachnoid and the myth of arachnoid mater: study using sheet plastination and scanning Arachne. Neurosurgery. 1999;45:152– 5; discussion 5– 7. electron microscopy. Neurosurgery. 2000;47:902 – 8; [23] Song-tao Q, Xi-an Z, Hao L, Jun F, Jun P, Yun-tao L. The discussion 8– 9. arachnoid sleeve enveloping the pituitary stalk: anatomical [32] Zhang XA, Qi ST, Huang GL, Long H, Fan J, Peng JX. Anatomical and histologic study. Neurosurgery. 2010;66:585 – 9. and histological study of Liliequist ’ s membrane: with [24] Sufianov AA, Sufianova GZ, Iakimov IA. Microsurgical emphasis on its nature and lateral attachments. Childs Nerv study of the interpeduncular cistern and its communication Syst. 2012;28:65 – 72. with adjoining cisterns. Childs Nerv Syst. 2009;25:301 – 8. [25] Vinas FC, Dujovny M, Fandino R, Chavez V. Microsurgical The authors stated that there are no conflicts of interest regarding anatomy of the arachnoidal trabecular membranes the publication of this article.