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Endoscopic anatomical study of the arachnoid architecture on the base of the skull. Part II: Level of the tentorium, posterior fossa and the craniovertebral junction

Peter Kurucz
  • Corresponding author
  • Laboratory for Applied and Clinical Anatomy, Institute of Anatomy, Histology and Embryology, Semmelweis University, Faculty of Medicine, Budapest, Hungary
  • Department of Neurosurgery, Katharinenhospital, Klinikum Stuttgart, Stuttgart, Germany
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  • De Gruyter OnlineGoogle Scholar
/ Gábor Baksa
  • Laboratory for Applied and Clinical Anatomy, Institute of Anatomy, Histology and Embryology, Semmelweis University, Faculty of Medicine, Budapest, Hungary
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Lajos Patonay
  • Laboratory for Applied and Clinical Anatomy, Institute of Anatomy, Histology and Embryology, Semmelweis University, Faculty of Medicine, Budapest, Hungary
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/ Nikolai J. Hopf
Published Online: 2013-05-31 | DOI: https://doi.org/10.1515/ins-2013-0008

Abstract

Interest in surgical anatomy of arachnoid membranes is relatively new and became more important with the development of endoscopic techniques in neurosurgery. In the first part we introduced the term “arachnoid membrane system” and “arachnoid membrane groups” and described them in the anterior and middle cranial fossa. The objective of this second part is to discuss the arachnoid membranes of the tentorial level, posterior fossa and the craniovertebral junction. Rigid endoscopes were introduced through defined keyhole craniotomies to explore the arachnoid in 127 fresh human cadavers. We defined 12 inner membranes that are arranged in three membrane groups. The “tentorial membrane group” consists of five paired membranes forming an almost complete barrier between the supra- and infratentorial spaces. The “clival membrane group” consists of three membranes and completes the separation created by the tentorial group. The superior part of the “perimedullary group” located around the medulla oblongata and consists of three inner membranes. The inferior part located in the craniovertebral junction consisting of four membranes. Intracranial arachnoid membranes are constant and defined structures that are well arranged in distinct groups. These new findings are essential in understanding the three-dimensional architecture of the arachnoid and its importance in endoscopic neurosurgery.

Keywords: Arachnoid membranes; arachnoid membrane system; endoscopic anatomy: skull base; subarachnoid cisterns

Introduction

The microsurgical anatomy of the arachnoid at the level of the tentorium and the posterior fossa were published by Matsuno et al. [21], Vinas et al. [32–34], and Lu and Zhu [16–19]. Most of the descriptions about the microsurgical anatomy of the craniovertebral junction concentrate on the relations of the neurovascular structures but only a few publications deal with its meningeal architecture [5, 13, 14, 22, 30, 31]. The endoscopically applied anatomical aspects of these areas are even more rarely studied topics [1, 7, 38].

In most of the publications, the description of the arachnoid membranes have been restricted only to their individual location. However, nobody has recognized a systematic composition of these structures yet. In addition, photographic documentation of the arachnoid membranes is limited and endoscopic studies are pending to support endoscopic microsurgery. Furthermore, the terminology used by previous authors is heterogene, and sometimes not appropriate.

In the first part of this study we described the endoscopic anatomy of the anterior and middle cranial fossa arachnoid [12] and introduced the terms “arachnoid membrane groups” and “arachnoid membrane system”.

According to the aforementioned aspects, the objective of the present study is to provide sufficient information on the topography of the arachnoid membranes at the level of the tentorium, posterior fossa, and the craniovertebral junction, suggesting a revised and intuitive terminology, to provide an extensive photographic documentation, and thus complete the description of the arachnoid architecture of the entire skull base.

Materials and methods

The complete study was performed on a total of 127 fresh human specimens (85 male, 42 female); postmortem not more than 72 h. The specimens were between the ages of 30 and 80 years and without significant intracranial pathology. In each specimen, the intracranial arterial system was injected with red gelatin solution. The dissections were carried out on the entire skull base in each cadaver, even though in this part only the results concerning the level of the tentorium, posterior cranial fossa, and the craniovertebral junction are provided. Brains were removed completely from the cranial cavity, with intact outer arachnoid in 14/127 cadavers for dissections only under the operating microscope. In 113/127 cadavers, the dissections were performed through defined keyhole approaches, including the supraorbital [26], subtemporal, retrosigmoid, supracerebellar-infratentorial and median suboccipital craniotomy [23], and in one case the transnasal-transclival approach using endoscope-assisted (n=27) or endoscope-controlled microsurgical (n=86) technique [9].

We used 0- and 30-degree rigid, rod-lens endoscopes (B. Braun/Aesculap AG, Tuttlingen, Germany) with a diameter of 4 mm for endoscope-controlled microsurgery (ECM). For endoscope-assisted microsurgery (EAM), an operating microscope (Opmi, Carl Zeiss, Oberkochen, Germany) was used in addition to the endoscope.

Results

The natural position of the arachnoid membranes could be observed much better using endoscopic dissections than using dissections only under the microscope. With endoscopes the deep seated structures on the base of the skull could be better illuminated and it was possible to see around the corner with the aid of angled optics. Endoscopes did produce significant less destruction of the normal anatomy, this is essential for the observation of such fine structures.

In the intracranial space we could distinguish two main types of arachnoid: an outer and an inner construct. The outer arachnoid is a strong, clear membrane that forms a closed cover around the whole brain. The inner arachnoid construct is located between the outer arachnoid and the pia mater. The inner arachnoid construct is best developed on the base of the skull. The network of single trabeculae, located in the subarachnoid space, forms a stabilizing system around the neurovascular structures. The accumulation of trabeculae can form either complete or incomplete sheet-like structures, referred to as “inner arachnoid membranes”. These membranes build the natural walls of the basal cisterns.

Outer arachnoid

The oculomotor trigone is the area between the anterior and posterior petroclinoid folds and the interclinoid fold. The outer arachnoid covers this area from above as a continuation of the outer arachnoid on the suprasellar area (Figure 1A and 2B). At the lateral edge of the oculomotor trigone under and medially to the anterior petroclinoid fold, the outer arachnoid is penetrated by the oculomotor nerve and follows it with an outward protrusion into the cavernous sinus (Figure 1A). Between the two oculomotor trigones the outer arachnoid stretches on the surface of the dorsum sellae and acts as a place for basal attachment of the Liliequist’s membrane complex (Figure 2A and B).

Endoscopic anatomy of the outer arachnoid. (A) Outer arachnoid cover of the left oculomotor trigone through left supraorbital approach. Note the outward protrusion of the outer arachnoid along the oculomotor nerve into the cavernous sinus (blue arrow-head). (B) Transition of the outer arachnoid from the tentorial surface of the cerebellum to the basal surface of the temporal lobe along the tentorial edge. Endoscopic view through left subtemporal approach. The blue arrow-head points to the trochlear nerve between its uncovered intracisternal segment and the beginning of the fixed part in the wall of the outer arachnoid. (C) Outer arachnoid relations of the tentorial apex viewed through a left supracerebellar-infratentorial approach. The arachnoid of the occipital lobe, cerebellum, and the splenium of the corpus callosum converges around the junction between the great vein of Galen and the straight sinus and follows the vein with an inward protrusion to the direction of the third ventricle. (D) Endoscopic view of the suprapineal arachnoid body through the same approach. (E) The outer arachnoid cover around the great vein of Galen follows its tributaries to the direction of the velum interpositum. The blue arrow-head points to this strong outer arachnoid cover around the left internal cerebral vein. Left supracerebellar-infratentorial approach. (F) Membranous sleeves around the deep veins in continuation with the meningeal structures of the velum interpositum in the top of the third ventricle. The approach is the same as on the previous picture. (G) Dural entrance of the right vertebral artery viewed through a right retrosigmoid approach. The blue arrow-head points to the inward protrusion of the outer arachnoid from the inner surface of the dura to the vertebral artery. The endoscope was introduced between the cranial and spinal roots of the accessory nerve. (H) Transition of the outer arachnoid between the intracranial and the intraspinal spaces. Through the small opening, the right posterior inferior cerebellar artery is visible (blue arrow-head). Median suboccipital approach. (I) After the introduction of the angled-endoscope through this small opening (blue arrow-head) the most caudal part of the cerebellomedullary cistern and the upper portion of the ventral spinal subarachnoidal space is visible. a.=artery, ant.=anterior, arachn.=arachnoid, cer.=cerebral, cerebell.=cerebellum, chor.=choroid, CNIII=oculomotor nerve, CNXI=accessory nerve, ICS=intermediat cervical septum, int.=internal, med.=medial, occ.=occipital, petrocl.=petroclinoid, PICA=posterior inferior cerebellar artery, plex.=plexus, post.=posterior, SPAB=suprapineal arachnoidal body, str.=straight, subd.=subdural, tent.=tentorial, tons.=tonsil, trig.=trigone, v.=vein, VA=vertebral artery.
Figure 1

Endoscopic anatomy of the outer arachnoid. (A) Outer arachnoid cover of the left oculomotor trigone through left supraorbital approach. Note the outward protrusion of the outer arachnoid along the oculomotor nerve into the cavernous sinus (blue arrow-head). (B) Transition of the outer arachnoid from the tentorial surface of the cerebellum to the basal surface of the temporal lobe along the tentorial edge. Endoscopic view through left subtemporal approach. The blue arrow-head points to the trochlear nerve between its uncovered intracisternal segment and the beginning of the fixed part in the wall of the outer arachnoid. (C) Outer arachnoid relations of the tentorial apex viewed through a left supracerebellar-infratentorial approach. The arachnoid of the occipital lobe, cerebellum, and the splenium of the corpus callosum converges around the junction between the great vein of Galen and the straight sinus and follows the vein with an inward protrusion to the direction of the third ventricle. (D) Endoscopic view of the suprapineal arachnoid body through the same approach. (E) The outer arachnoid cover around the great vein of Galen follows its tributaries to the direction of the velum interpositum. The blue arrow-head points to this strong outer arachnoid cover around the left internal cerebral vein. Left supracerebellar-infratentorial approach. (F) Membranous sleeves around the deep veins in continuation with the meningeal structures of the velum interpositum in the top of the third ventricle. The approach is the same as on the previous picture. (G) Dural entrance of the right vertebral artery viewed through a right retrosigmoid approach. The blue arrow-head points to the inward protrusion of the outer arachnoid from the inner surface of the dura to the vertebral artery. The endoscope was introduced between the cranial and spinal roots of the accessory nerve. (H) Transition of the outer arachnoid between the intracranial and the intraspinal spaces. Through the small opening, the right posterior inferior cerebellar artery is visible (blue arrow-head). Median suboccipital approach. (I) After the introduction of the angled-endoscope through this small opening (blue arrow-head) the most caudal part of the cerebellomedullary cistern and the upper portion of the ventral spinal subarachnoidal space is visible.

a.=artery, ant.=anterior, arachn.=arachnoid, cer.=cerebral, cerebell.=cerebellum, chor.=choroid, CNIII=oculomotor nerve, CNXI=accessory nerve, ICS=intermediat cervical septum, int.=internal, med.=medial, occ.=occipital, petrocl.=petroclinoid, PICA=posterior inferior cerebellar artery, plex.=plexus, post.=posterior, SPAB=suprapineal arachnoidal body, str.=straight, subd.=subdural, tent.=tentorial, tons.=tonsil, trig.=trigone, v.=vein, VA=vertebral artery.

Outer and inner arachnoid relations of the tentorial level and the posterior fossa in en-bloc removed brains. (A) The clival line (white arrow-heads). (B) Outer arachnoid relations of the tentorial edge on the left side. Note the arachnoid and dural exit-points of the oculomotor and trochlear nerves. In this case the left temporal lobe was only retracted from the skull base. (C) Overview of the mesencephalic leaf of the Liliequist’s membrane complex. The outer arachnoid of right oculomotor trigone is opened. On the left side the base of the ambient cistern is opened to visualize some trabeculae of the posterior cerebral membrane. Note the transversally oriented arachnoid trabeculae of the mesencephalic leaf under both oculomotor nerves. (D) Overview of the median medullary membrane. a.=artery, AICA=anterior inferior cerebellar artery, arachn.=arachnoid, ASA=anterior spinal artery, BA=basilar artery, cerebell.=cerebellum, CNIII=oculomotor nerve, CNIV=trochlear nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, Co.=communicating, ICA=internal carotid artery, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, MMM=median medullary membrane, p.=posterior, PCM=posterior cerebral membrane, PICA=posterior inferior cerebellar artery, SCA=superior cerebellar artery, temp.=temporal, trig.=trigone, VA=vertebral artery.
Figure 2

Outer and inner arachnoid relations of the tentorial level and the posterior fossa in en-bloc removed brains. (A) The clival line (white arrow-heads). (B) Outer arachnoid relations of the tentorial edge on the left side. Note the arachnoid and dural exit-points of the oculomotor and trochlear nerves. In this case the left temporal lobe was only retracted from the skull base. (C) Overview of the mesencephalic leaf of the Liliequist’s membrane complex. The outer arachnoid of right oculomotor trigone is opened. On the left side the base of the ambient cistern is opened to visualize some trabeculae of the posterior cerebral membrane. Note the transversally oriented arachnoid trabeculae of the mesencephalic leaf under both oculomotor nerves. (D) Overview of the median medullary membrane.

a.=artery, AICA=anterior inferior cerebellar artery, arachn.=arachnoid, ASA=anterior spinal artery, BA=basilar artery, cerebell.=cerebellum, CNIII=oculomotor nerve, CNIV=trochlear nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, Co.=communicating, ICA=internal carotid artery, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, MMM=median medullary membrane, p.=posterior, PCM=posterior cerebral membrane, PICA=posterior inferior cerebellar artery, SCA=superior cerebellar artery, temp.=temporal, trig.=trigone, VA=vertebral artery.

Caudal to the dorsum sellae, the outer arachnoid covers the inner surface of the clivus. (Figure 2A). The abducent nerves penetrate the dura of the clivus and are covered by an arachnoid sheath within Dorello’s canal. In the midline, from the level of the dorsum sellae to the middle of the clivus, the outer arachnoid has a white-gray, inverted U-shaped thickening that we named the “clival line” (Figure 2A). The top of the line (base of the inverted U-shape) is built by the basal attachment of the Liliequist’s membrane complex between the oculomotor nerves, at the level of the dorsum sellae in the midline. Laterally from its top, the line turns first medially and then caudally to the oculomotor nerves, and is shaped by the basal attachments of the caudally oriented lateral edges of the mesencephalic leaf of the Liliequist’s membrane complex (Figure 3E). Caudally from this membrane the line is formed by the basal attachments of the anterior pontine membranes at both sides (Figure 3F).

Endoscopic anatomy of the clival and perimedullary membrane groups. (A) The mesencephalic leaf of the Liliequist’s membrane complex viewed through left supraorbital approach. Note the transition between the intact middle portion of the membrane and the trabecular part around the basilar artery trunk (blue arrow-head). (B) The lateral edge of the mesencephalic leaf on the left side. The endoscope was introduced through a contralateral supraorbital approach. The blue arrow-head points to the trabecular portion of the mesencephalic leaf. Through the holes on this portion the left posterior cerebral artery is also visible. (C) Junction of the lateral edge of the mesencephalic leaf and the anterior pontine membrane at the left side (blue arrow-head). The approach is the same as Figure 3B. (D) The anterior pontine membrane on the left side viewed from the same approach as Figure 3C. (E) Membranous relations of the left superior cerebellar artery. The artery passes through (blue arrow-head) at the three-point junction between the superior edge of the anterior pontine membrane, the lateral edge of the mesencephalic leaf and the medial edge of the superior cerebellar membrane (not visible, because the lateral edge of the mesencephalic leaf is intact). The same approach as Figure 3B. (F) View of the lateral surface of the right anterior pontine membrane through a right retrosigmoid approach. Note the extra connection between the trigeminal membrane and the anterior pontine membrane (blue arrow-head). (G) The pontomedullary membrane on the right side through right retrosigmoid approach. Note the dorsal attachment of the membrane along the pontomedullary sulcus (blue arrow-head). (H) The superior surface of the left pontomedullary membrane viewed through a left supraorbital approach. Note the junction between the medial edge of the pontomedullary membrane and the inferior edge of the anterior pontine membrane (blue arrow-head). In this case the abducent nerve is located below the level of the membrane in contrast to Figure 3G. (I) View of the lateral portion of the left pontomedullary membrane along the inferior limb of the cerebellopontine fissure below the flocculus. Note the connection between the glossopharyngeal nerve and the inferior surface of the membrane. The endoscope was introduced in the same manner as Figure 3H but the medial part of the membrane was removed. (J) The median medullary membrane from below visualized through a right retrosigmoid approach. Note the anterior spinal arteries running in the wall of the membrane. (K) The upper portion of the rhomboid membrane in the corner between the lateral surface of the medulla oblongata, right vertebral artery and the superior edge of the right denticulate ligament. Right retrosigmoid approach. (L) View of the right apex of the rhomboid membrane through a transnasal-transclival approach. The C1 spinal nerve perforates the membrane but the ventral root of the C2 spinal nerve runs below it (blue arrow-head). Directly under the rhomboid membrane is the denticulate ligament locted. Its second insertion is in the same level as the connection of the lateral apex of the rhomboid membrane to the outer arachnoid. The spinal roots of the accessory nerve are located below the denticulate ligament. The dorsal root of the C2 spinal nerve is the deepest structure. (M) The first insertion of the right denticulate ligament, located between the vertebral artery (ventral) and the spinal roots of the accessory nerve (dorsal). Medially, the ligament is attached to the lateral surface of the medulla oblongata. The rhomboid membrane was removed, therefore, the upper edge of the ligament is disconnected (blue arrow-head). Right retrosigmoid approach. Same approach as Figure 3K. (N) Second insertion of the right denticulate ligament. Same approach as Figure 3L. View after removal of the rhomboid membrane. Note the two macroscopically different tissue-types of the ligament: medially an arachnoid membrane-like transparent structure, laterally a white band-like strong construct. (O) View of the intermediate cervical septum from the right side. The approach is the same as Figure 3M. Above the level of the foramen magnum the membrane is only a dense network of arachnoid trabeculae. a.=artery, AICA=anterior inferior cerebellar artery, APM=anterior pontine membrane, arachn.=arachnoid, ASA=anterior spinal artery, BA=basilar artery, Boch.=Bochdalek flower basket, C1=C1 spinal nerve, C2=C2 spinal nerve, cliv.=clival, CNIII=oculomotor nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, CNIX-X-XI=caudal cranial nerves, co.=communicating, dors.=dorsal, flocc.=flocculus, ICS=intermediate cervical septum, ins.=insertion, l. VA=left vertebral artery, LD=denticulate ligament, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, MMM=median medullary membrane, p.=posterior, PCA=posterior cerebral membrane, PICA=posterior inferior cerebellar artery, PM=pontomedullary membrane, r. VA=right vertebral artery, RM=rhomboid membrane, SCA=superior cerebellar artery, SCM=superior cerebellar membrane, ventr.=ventral.
Figure 3

Endoscopic anatomy of the clival and perimedullary membrane groups. (A) The mesencephalic leaf of the Liliequist’s membrane complex viewed through left supraorbital approach. Note the transition between the intact middle portion of the membrane and the trabecular part around the basilar artery trunk (blue arrow-head). (B) The lateral edge of the mesencephalic leaf on the left side. The endoscope was introduced through a contralateral supraorbital approach. The blue arrow-head points to the trabecular portion of the mesencephalic leaf. Through the holes on this portion the left posterior cerebral artery is also visible. (C) Junction of the lateral edge of the mesencephalic leaf and the anterior pontine membrane at the left side (blue arrow-head). The approach is the same as Figure 3B. (D) The anterior pontine membrane on the left side viewed from the same approach as Figure 3C. (E) Membranous relations of the left superior cerebellar artery. The artery passes through (blue arrow-head) at the three-point junction between the superior edge of the anterior pontine membrane, the lateral edge of the mesencephalic leaf and the medial edge of the superior cerebellar membrane (not visible, because the lateral edge of the mesencephalic leaf is intact). The same approach as Figure 3B. (F) View of the lateral surface of the right anterior pontine membrane through a right retrosigmoid approach. Note the extra connection between the trigeminal membrane and the anterior pontine membrane (blue arrow-head). (G) The pontomedullary membrane on the right side through right retrosigmoid approach. Note the dorsal attachment of the membrane along the pontomedullary sulcus (blue arrow-head). (H) The superior surface of the left pontomedullary membrane viewed through a left supraorbital approach. Note the junction between the medial edge of the pontomedullary membrane and the inferior edge of the anterior pontine membrane (blue arrow-head). In this case the abducent nerve is located below the level of the membrane in contrast to Figure 3G. (I) View of the lateral portion of the left pontomedullary membrane along the inferior limb of the cerebellopontine fissure below the flocculus. Note the connection between the glossopharyngeal nerve and the inferior surface of the membrane. The endoscope was introduced in the same manner as Figure 3H but the medial part of the membrane was removed. (J) The median medullary membrane from below visualized through a right retrosigmoid approach. Note the anterior spinal arteries running in the wall of the membrane. (K) The upper portion of the rhomboid membrane in the corner between the lateral surface of the medulla oblongata, right vertebral artery and the superior edge of the right denticulate ligament. Right retrosigmoid approach. (L) View of the right apex of the rhomboid membrane through a transnasal-transclival approach. The C1 spinal nerve perforates the membrane but the ventral root of the C2 spinal nerve runs below it (blue arrow-head). Directly under the rhomboid membrane is the denticulate ligament locted. Its second insertion is in the same level as the connection of the lateral apex of the rhomboid membrane to the outer arachnoid. The spinal roots of the accessory nerve are located below the denticulate ligament. The dorsal root of the C2 spinal nerve is the deepest structure. (M) The first insertion of the right denticulate ligament, located between the vertebral artery (ventral) and the spinal roots of the accessory nerve (dorsal). Medially, the ligament is attached to the lateral surface of the medulla oblongata. The rhomboid membrane was removed, therefore, the upper edge of the ligament is disconnected (blue arrow-head). Right retrosigmoid approach. Same approach as Figure 3K. (N) Second insertion of the right denticulate ligament. Same approach as Figure 3L. View after removal of the rhomboid membrane. Note the two macroscopically different tissue-types of the ligament: medially an arachnoid membrane-like transparent structure, laterally a white band-like strong construct. (O) View of the intermediate cervical septum from the right side. The approach is the same as Figure 3M. Above the level of the foramen magnum the membrane is only a dense network of arachnoid trabeculae.

a.=artery, AICA=anterior inferior cerebellar artery, APM=anterior pontine membrane, arachn.=arachnoid, ASA=anterior spinal artery, BA=basilar artery, Boch.=Bochdalek flower basket, C1=C1 spinal nerve, C2=C2 spinal nerve, cliv.=clival, CNIII=oculomotor nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, CNIX-X-XI=caudal cranial nerves, co.=communicating, dors.=dorsal, flocc.=flocculus, ICS=intermediate cervical septum, ins.=insertion, l. VA=left vertebral artery, LD=denticulate ligament, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, MMM=median medullary membrane, p.=posterior, PCA=posterior cerebral membrane, PICA=posterior inferior cerebellar artery, PM=pontomedullary membrane, r. VA=right vertebral artery, RM=rhomboid membrane, SCA=superior cerebellar artery, SCM=superior cerebellar membrane, ventr.=ventral.

Lateral to the clivus, the outer arachnoid covers the posterior surface of the petrous bone. In this area seven cranial nerves penetrate the outer arachnoid at both sides. The trigeminal nerves are followed by an outward extension from their entrance to Meckel’s cave. The vestibulocochlear, facial and caudal cranial nerves also have outwardly protruded arachnoid sheaths. The petrosal vein located in this area and drains the venous blood from the brainstem into the superior petrosal sinus. Similarly to other vessels penetrating the outer arachnoid, it is also encased by an inward envelop of the outer arachnoid.

Caudal to the posterior surface of the petrous bone, at the level of the foramen magnum, the outer arachnoid follows the medulla oblongata to the spinal canal and continuous with the outer arachnoid of the spinal canal (Figure 1H and I). The vertebral arteries penetrate the dura at this level and covered by the outer arachnoid with inwardly protruded sheaths in the same manner as the internal carotid arteries (Figure 1G). On the dorsal surface of the posterior fossa the outer arachnoid covers the medulla, the cerebellar hemispheres and superiorly the tentorial surface of the cerebellum.

From the tentorial surface of the cerebellum, the outer arachnoid turns superiorly and continues on the basal surface of the temporal lobe forming a medially closed cover along the free edge of the tentorium (Figure 1B). The trochlear nerve runs after a short free segment in the dorsal part of the quadrigeminal cistern (Figure 4L), strongly attached to the inner surface of the outer arachnoid by numerous inner trabeculae, just parallel to and below the level of the tentorial edge. The dural exit point of the nerve located at the posterolateral edge of the oculomotor trigone, below the level of the anterior free edge of the tentorium where it joins the petrous apex (Figure 2B). After its dural exit, the nerve is covered by an outer arachnoid sheath intracavernously similar to the oculomotor nerve.

Endoscopic anatomy of the tentorial membrane group. (A) The left posterior cerebral membrane through a left retrosigmoid approach. (B) The connection of the medial edge of the left posterior cerebral membrane in the interpeduncular fossa viewed through a left supraorbital approach. (C) The left lateral mesencephalic membrane viewed through a left supraorbital approach. The blue arrow-head points to the basal attachment of the membrane along the outer arachnoid over the posterior petroclinoid fold. (D) Relation of the left posterior cerebral artery to the lateral mesencephalic membrane viewed through the same approach. (E) Endoscopic view of the left lateral mesencephalic membrane from below, in the lateral part of the quadrigeminal cistern viewed through a right supraorbital appoach. Note the left trochlear nerve in the wall of the outer arachnoid. (F) The horizontal part of the left posterior mesencephalic membrane viewed through a left subtemporal approach. (G) The vertical part of the left posterior mesencephalic membrane viewed through the same approach. Note the penetration-point of the left posterior cerebral artery through the membrane (blue arrow-head). (H) The dorsal attachment of the vertical part of the right posterior mesencephalic membrane along the lateral side of the great vein of Galen and the basal vein of Rosenthal viewed from below, from the middle part of the quadrigeminal cistern. Right supracerebellar-infratentorial approach. (I) The ventral part of the left superior cerebellar membrane viewed from above, after preforation of the lateral mesencephalic membrane (blue arrow-head). Endoscopic view through left supraorbital approach. (J) Relation of the left superior cerebellar membrane to the superior cerebellar artery (above the membrane) and the trigeminal nerve (below the membrane, blue arrow-head). Its dorsal attachment to the pons is also visible. Left supraorbital approach. (K) The three-point junction (blue arrow-head) between the left anterior pontine and superior cerebellar membrane and the lateral edge of the Liliequist membrane complex (partly removed) on the left side. As the mesencephalic leaf was removed, it is possible to view into the lateral part of the quadrigeminal cistern. Right supraorbital approach. (L) The dorsal attachment of the left superior cerebellar membrane (blue arrow-head) in the cerebellomesencephalic fissure. Left sided subtemporal approach with angled-optic. (M) Junction between the left anterior pontine and superior cerebellar membrane viewed from below (from the direction of the left cerebellopontine cistern). Note the clival line (blue arrow-head) as the basal attachment of the anterior pontine membrane on the outer arachnoid. Left retrosigmoid approach. (N) The lateral portion of the trigeminal membrane on the left side, viewed from the direction of the left cerebellopontine cistern. In this case the lateral edge of the membrane is extremely far from the superior cerebellar membrane and forms an extraordinary big trigeminal cistern. Left retrosigmoid approach. (O) Medial portion of the right trigeminal membrane (blue arrow-head) viewed from left supraorbital approach. AICA=anterior inferior cerebellar artery, APM=anterior pontine membrane, bas.=basal, cerebell.=cerebellum, cerebellomes.=cerebellomesencephalic, CNIII=oculomotor nerve, CNIV=trochlear nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, LMM=lateral mesencephalic membrane, mesenc.=mesencephalon, occ.=occipital, PCM=posterior cerebral membrane, PMM=posterior mesencephalic membrane, quadr.=quadrigeminal, Ros.=Rosenthal, SCA=superior cerebellar artery, SCM=superior cerebellar membrane, tent.=tentorium, v.=vein.
Figure 4

Endoscopic anatomy of the tentorial membrane group. (A) The left posterior cerebral membrane through a left retrosigmoid approach. (B) The connection of the medial edge of the left posterior cerebral membrane in the interpeduncular fossa viewed through a left supraorbital approach. (C) The left lateral mesencephalic membrane viewed through a left supraorbital approach. The blue arrow-head points to the basal attachment of the membrane along the outer arachnoid over the posterior petroclinoid fold. (D) Relation of the left posterior cerebral artery to the lateral mesencephalic membrane viewed through the same approach. (E) Endoscopic view of the left lateral mesencephalic membrane from below, in the lateral part of the quadrigeminal cistern viewed through a right supraorbital appoach. Note the left trochlear nerve in the wall of the outer arachnoid. (F) The horizontal part of the left posterior mesencephalic membrane viewed through a left subtemporal approach. (G) The vertical part of the left posterior mesencephalic membrane viewed through the same approach. Note the penetration-point of the left posterior cerebral artery through the membrane (blue arrow-head). (H) The dorsal attachment of the vertical part of the right posterior mesencephalic membrane along the lateral side of the great vein of Galen and the basal vein of Rosenthal viewed from below, from the middle part of the quadrigeminal cistern. Right supracerebellar-infratentorial approach. (I) The ventral part of the left superior cerebellar membrane viewed from above, after preforation of the lateral mesencephalic membrane (blue arrow-head). Endoscopic view through left supraorbital approach. (J) Relation of the left superior cerebellar membrane to the superior cerebellar artery (above the membrane) and the trigeminal nerve (below the membrane, blue arrow-head). Its dorsal attachment to the pons is also visible. Left supraorbital approach. (K) The three-point junction (blue arrow-head) between the left anterior pontine and superior cerebellar membrane and the lateral edge of the Liliequist membrane complex (partly removed) on the left side. As the mesencephalic leaf was removed, it is possible to view into the lateral part of the quadrigeminal cistern. Right supraorbital approach. (L) The dorsal attachment of the left superior cerebellar membrane (blue arrow-head) in the cerebellomesencephalic fissure. Left sided subtemporal approach with angled-optic. (M) Junction between the left anterior pontine and superior cerebellar membrane viewed from below (from the direction of the left cerebellopontine cistern). Note the clival line (blue arrow-head) as the basal attachment of the anterior pontine membrane on the outer arachnoid. Left retrosigmoid approach. (N) The lateral portion of the trigeminal membrane on the left side, viewed from the direction of the left cerebellopontine cistern. In this case the lateral edge of the membrane is extremely far from the superior cerebellar membrane and forms an extraordinary big trigeminal cistern. Left retrosigmoid approach. (O) Medial portion of the right trigeminal membrane (blue arrow-head) viewed from left supraorbital approach.

AICA=anterior inferior cerebellar artery, APM=anterior pontine membrane, bas.=basal, cerebell.=cerebellum, cerebellomes.=cerebellomesencephalic, CNIII=oculomotor nerve, CNIV=trochlear nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, LMM=lateral mesencephalic membrane, mesenc.=mesencephalon, occ.=occipital, PCM=posterior cerebral membrane, PMM=posterior mesencephalic membrane, quadr.=quadrigeminal, Ros.=Rosenthal, SCA=superior cerebellar artery, SCM=superior cerebellar membrane, tent.=tentorium, v.=vein.

At the tentorial apex, the outer arachnoid of the splenium of the corpus callosum, the medial surface of the occipital lobes and the tentorial surface of the cerebellum converges around the junction between the straight sinus and the great vein of Galen (Figure 1C). At the inferior angle of this junction the outer arachnoid has a granulation-like thickening and compresses the junction form below (Figure 1D). The outer arachnoid converging at the tentorial apex, extends inwardly to the direction of the third ventricle and forms an arachnoid envelop around the great vein of Galen, its tributaries and the pineal gland in the quadrigeminal (Figure 1E), and anteriorly in the velum interpositum cistern (Figure 1F).

Inner arachnoid

We could distinguish 11 inner arachnoid membranes and the denticulate ligaments from the level of the tentorium, through the posterior cranial fossa to the craniovertebral junction. Eight of these structures were found to be paired, summing up to a total of 20 distinct membranes.

The inner arachnoid membranes are described from cranial to caudal direction, in order as they appear during endoscopic observation from a subfrontal approach.

Posterior cerebral membrane

This is a paired membrane located parallel to, but above the anterior free edge of the tentorium. It has about a bow-like shape and fills the space between the P1 and P2 segments of the posterior cerebral artery and the crus cerebri (Figure 4A). In the majority, there is no connection between the two posterior cerebral membranes, therefore, they are separated by the interpeduncular fossa. In some cases the medial edges of the posterior cerebral membranes are connected by a dense network of arachnoid trabeculae, located within the depth of the interpeduncular fossa, around the thalamoperforating arteries (Figure 4B). The macrosopic appearance of the membrane varies from a clear, sheet-like membrane to a dense network of arachnoid trabeculae. Except its connection with the mentioned vessels the membrane has no perforating structure. It partly divides the ambient cistern to a superior and an inferior part.

Connections: anterior: cerebral surface of the P1 and P2 segments of the posterior cerebral artery. Posterior: crus cerebri. Medial: it could be connected or not to the trabecular network of the interpeduncular fossa. Lateral: it terminates at the area of the branching of the lateral posterior choroidal artery.

Mesencephalic leaf of the Liliequist’s membrane complex

This midline membrane is the most constant and characteristic part of the Liliequist’s membrane complex. It looks like a “half parachute” located between the supra- and infratentorial cranial spaces, where the outer surface faces dorsally to the brainstem. The highest point of the membrane is located in the midline, between the oculomotor nerves (Figure 2C). The two lateral edges are the lowest (most caudal) parts and situated perpendicularly to the middle portion of the membrane (Figure 3B and C), just under the third cranial nerves. These parts of the membrane are always without perforations (the “canopy” of the “parachute”). Directly around the basilar artery, the sheet-like intact membrane turns to a dense network of arachnoid trabeculae and joins to the vessel in most of the cases between the origin of the superior cerebellar and posterior cerebral arteries (the “suspension lines” of the “parachute”; Figure 3B). The posterior cerebral artery always runs above the membrane, however, the posterior communicating artery is sometimes located in its wall (Figure 3A), just medially to the oculomotor nerves. The superior cerebellar artery passes through directly under the caudal termination of the membrane (Figure 3B and E), at the three-point junction of the superior cerebellar, anterior pontine membrane, and the mesencephalic leaf, between the dorsal edges of the membranes and the ventral surface of the pons. The mesencephalic leaf separates the interpeduncular cistern and the lateral portions of the quadrigeminal cistern (see below) from the prepontine cistern.

Connections: basal: if the common leaf of the Liliequist’s membrane complex is present, the middle part of the membrane is connected to the junction between the diencephalic and the common leaf. If the common leaf is missing it is connected to the junction between the diencephalic leaf and the outer arachnoid. The lateral portion of the mesencephalic leaf is curved caudally to the anterior pontine membrane under the oculomotor nerves and attached basally to the outer arachnoid. Dorsal: the basilar artery trunk, between the origin of the superior cerebellar arteries and the posterior cerebral arteries. Lateral: it is attached to the inferomedial surface of the oculomotor nerve and connected to the medial edge of the lateral mesencephalic membrane below and also above the nerve. Caudally it joins to the junction between the anterior pontine and the superior cerebellar membrane.

Lateral mesencephalic membrane

This is a paired membrane that has a similar structure to the outer arachnoid. It is located at the level of the tentorium between its anterior free edge, the posterior petroclinoid fold, the crus cerebri, and the mesencephalic leaf of the Liliequist’s membrane complex (Figure 4C). It is a constant and intact membrane without perforating structures. The posterior cerebral artery and the oculomotor nerve runs above the membrane (Figure 4D) but the superior cerebellar artery is located below it (Figure 4E). Some additional arachnoid trabeculae extend from the medial edge of the lateral mesencephalic membrane to the superior surface of the oculomotor nerve and join to the mesencephalic leaf forming a complete inner arachnoid sheath around the intracisternal segment of the oculomotor nerve. The membrane separates the inferior portion of the ambient cistern from the lateral portion of the quadrigeminal cistern.

Connections: anterior: it is connected to the transition of the outer arachnoid from the clivus to the oculomotor trigone at the level of the posterior petroclinoid fold just below the subarachnoid exit point of the oculomotor nerve. The inferior edge of the temporal membrane spreads also to this junction from above. Medial: it is connected to the caudally curved lateral surface of the mesencephalic leaf around the oculomotor nerve. Lateral: outer arachnoid cover of the anterior free edge of the tentorium. The trochlear nerve runs under the level of the lateral mesencephalic membrane closely attached to the inner surface of the outer arachnoid with numerous arachnoid trabeculae. Posteromedial: crus cerebri. Posterior: if the tentorial incisura is wide (no connection between the lateral surface of the mesencephalon and the tentorial edge), the lateral mesencephalic membrane continues dorsally as posterior mesencephalic membrane. If the tentorial incisura is narrow (the lateral surface of the mesencephalon is attached to the tentorial edge), it forms an interruption between the lateral and posterior mesencephalic membrane.

Posterior mesencephalic membrane

The posterior mesencephalic membrane is a paired, constant and always intact membrane. It is located at the same level as the lateral mesencephalic membrane but dorsal to it, between the free edge of the tentorium and the posterolateral and dorsal surface of the mesencephalon (Figure 4F). The membrane has a horizontal and an ascending part. The horizontal part is parallel to the lateral mesencephalic membrane. After it reaches the quadrigeminal plate, it turns upward with the tentorial apex (Figure 4G) and joins the outer arachnoid envelop of the vein of Galen (Figure 4H). This is the ascending part of the membrane. In the wall of the membrane there are numerous preforating branches from the posterior cerebral artery. The ascending part is perforated by the medial posterior choroidal artery entering into the quadrigeminal cistern. The trochlear nerve originates below the level of the membrane. It separates the inferior portion of the ambient cistern from the lateral portion of the quadrigeminal cistern and in the midline the posterior end of the pericallosal cistern from the dorsal portion of the quadrigeminal cistern.

Connections: medial: midbrain tegmentum and the arachnoid envelop around the vein of Galen. Anterior: in case of wide tentorial incisura it is connected to the posterior edge of the lateral mesencephalic membrane. If the tentorial incisura is narrow it is connected to the crus cerebri. Lateral: outer arachnoid along the free edge of the tentorium.

Superior cerebellar membrane

It is a paired, constant but very thin membrane located at the ventrolateral surface of the pons and curves dorsally to the cerebellomesencephalic fissure along the inferior edge of the superior cerebellar artery and terminates on the dorsal surface of the superior cerebellar peduncle just under the origin of the trochlear nerves. It stretches parallel to and below the posterior and lateral mesencephalic membranes (Figure 4I). The trigeminal nerve and the petrosal vein are located under the membrane (Figure 4J). The trigeminal membrane (see below) joins the inferior surface of the membrane (Figure 4N and O). The trochlear nerve with its entire length (Figure 4E and L) and the superior cerebellar artery (Figure 4E and L) after its penetration through the caudally curved lateral edge of the mesencephalic leaf (Figure 3E) are located above the level of the membrane. Some smaller branches of the superior cerebellar artery and some rami ad pontem run in the wall of it (Figure 4I and K). The membrane separates the lateral portion of the quadrigeminal cistern from the cerebellopontine and the trigeminal cistern.

Connections: basal: outer arachnoid on the clivus (Figure 4M). Dorsal: ventral surface of the pons just under and along the superior cerebellar artery (Figure 4J) and the cerebellomesencephalic fissure. Medial: junction between the lateral edge of the mesencephalic leaf and the superior edge of the anterior pontine membrane. Lateral: outer arachnoid along the inferior surface of the tentorium to the tentorial apex.

Trigeminal membrane

This is a U-shaped intact and paired membrane. Almost its entire surface is attached to the trigeminal nerve and acts like an inner arachnoid sheath. As its lateral edge, in most of the cases, is detached from the lateral surface of the nerve, and joins superiorly the inferior surface of the superior cerebellar membrane or the outer arachnoid on the inferior surface of the tentorium forming a separated cistern around the trigeminal nerve (Figure 4N) it is described as a separate membrane. There is no structure perforating the membrane. It separates the trigeminal cistern from the cerebellopontine cistern.

Connections: basal: outer arachnoid around the entrance of Meckel’s cave. Dorsal: origin of the trigeminal nerve. Lateral: this edge is curved superiorly to the outer arachnoid on the inferior surface of the tentorium or to the inferior surface of the superior cerebellar membrane. Medial: its medial edge turns superiorly and spreads into the inferior surface of the superior cerebellar membrane (Figure 4O).

Anterior pontine membrane

This is a paired, always constant and intact membrane located on the ventral surface of the pons at both sides of the basilar artery. Its superior edge is located under the oculomotor nerve (Figure 3E), which is the widest part of the membrane, and then it converges caudally to the direction of the vertebrobasilar junction (Figure 3H). The superior cerebellar artery is located above the superior edge of the membrane (Figure 3E) directly at the junction of the here converging membranes (described above, Figure 3D). The anterior inferior cerebellar artery passes through the caudal edge of the membrane. There is no vessel in the wall of the membrane. It separates the prepontine cistern from the cerebellopontine cistern.

Connections: basal: outer arachnoid on the clivus. Dorsal: ventral surface of the pons (Figure 3F). Superior: junction between the medial edge of the superior cerebellar and the lateral edge of the mesencephalic leaf of the Liliequist’s membrane complex. Inferior: junction between medial edges of the bilateral pontomedullary membranes and the superior edge of the median medullary membrane.

Pontomedullary membrane

This is a paired but very variable membrane located at the level of the pontomedullary junction (Figure 3G). Occasionally, it is completely missing or only a sparse trabecular network can be detected. During its course it follows inferiorly the anterior inferior cerebellar artery from its origin (Figure 3G and H) to the glossopharyngeal nerve (Figure 3I), where its inferior surface is connected to the common inner arachnoid sheath around the caudal cranial nerves and then runs laterally to spread into the outer arachnoid on the posterior surface of the petrous bone along the inferior limb of the cerebellopontine fissure, just under the flocculus. It separates the cerebellopontine cistern from the premedullary cistern.

Connections: basal: outer arachnoid on the clivus and the posterior surface of the petrous bone. Dorsal: along the pontomedullary sulcus and the inferior limb of the cerebellopontine fissure. Lateral: the height of the membrane reduces from medial to lateral direction and the lateral apex is merged to the angle between the petrosal surface of the cerebellum and the posterior surface of the petrous bone. Medial: junction between the inferior edge of the anterior pontine membrane and the superior edge of the median medullary membrane.

Median medullary membrane

This is an unpaired midline membrane located at the level of the vertebrobasilar junction and follows the anterior spinal arteries to the foramen magnum (Figures 2D and 3J). The structure of the membrane varies greatly from an intact membrane to only a trabecular network. Except its contact with the mentioned arteries the membrane is without perforating vessels. It separates partly the bilateral premedullary cisterns.

Connections: basal: dorsal surface of the rhomboid membrane. Dorsal: the anterior median fissure on the ventral surface of the medulla oblongata. Superior: junction between the medial edges of the pontomedullary membranes and the inferior edges of the anterior pontine membranes. Inferior: it is free and terminates in the level of the foramen magnum.

Rhomboid membrane

It is a rhomboid-shaped unpaired midline membrane, located in the craniovertebral junction, ventral to the medulla oblongata and the spinal cord. Its macroscopic appearance is very similar to the denticulate ligaments. The upper apex of the rhomboid is located in the midline around in the level of the origin of the anterior spinal arteries. The lower apex extends to the level of the C3-C4 segments of the spinal cord. The lateral apex at both sides are located between the C1 roots and the ventral roots of the C2 spinal nerves (Figure 3L) ventral to the second insertion of the denticulate ligament. The two upper edges of the membrane are straight and strongly adhered to the underlying structures. The supreolateral portion of the membrane at both sides fills the triangular space between the vertebral artery, lateral surface of the medulla and the superior edge of the first insertion of the denticulate ligament (Figure 3K). Here, the dorsal surface of the rhomboid membrane is attached to the ventral surface of the denticulate ligaments. The two inferior edges of the membrane have an inverted J-shape and float freely just lateral to the medulla oblongata. The roots of the C1 spinal nerve perforate the membrane at their origin (Figure 3L). The ventral roots of the C2 spinal nerve is located dorsal to the membrane (Figure 3L). A small part of the membrane above the superior edge of the first insertion of the denticulate ligaments at both sides separates the premedullary cistern from the cerebellomedullary cistern. The rest of the membrane divides the premedullary cisterns and caudally the ventral spinal subarachnoid space to a further dorsal and ventral portion.

Connections: superior: vertebrobasilar junction. Superolateral: outer arachnoid envelop around the vertrebral arteries. Lateral: inner surface of the outer arachnoid between the C1 and venral roots of the C2 spinal nerves, ventral to the dural attachment of the second insertion of the denticulate ligament. Inferolateral: these edges of the membrane are free and spreading to the direction of the caudal apex. Inferior: located in the midline about at the C3-C4 level of the spinal cord.

The denticulate ligament (first and second insertions)

The denticulate ligaments are not arachnoid formations, the uppermost parts of these structures belong to the meningeal construct of the craniovertebral junction. The denticulate ligaments are paired structures and located at the lateral side of the medulla oblongata between the ventral and dorsal roots of the spinal nerves, from the level of the dural entrance of the vertebral arteries along the whole spinal cord and attaches to the inner surface of the dura at both sides in 19–23 insertions. The first two insertions are located at the craniovertebral junction. Two macroscopicaly different tissues could be distinguished in their structures (Figure 3N). A strong, white band-like construct which is parallel to the medulla and joins the inner surface of the dura mater. These junctions are the insertions of the denticulate ligaments. The second type of tissue is a clear, arachnoid membrane-like construct filling the space between the band-like structures and the medulla as a transverse plate. The first insertion of the denticulate ligaments is located at the level of the dural entrance of the vertebral artery but dorsal to it (Figure 3M). The second insertion is located caudally (Figure 3N), between the dural exits of the C1 and C2 spinal nerves. The space above the superior edge of the first insertion of the denticulate ligament is filled by the rhomboid membrane and attaches to the ventral surface of the ligament with its dorsal surface (Figure 3K). The space above the second insertion is free and acting as a connection between the dorsal and ventral spinal subarachnoid spaces (Figure 3N). The vertebral arteries, the rhomboid membrane and the ventral roots of the spinal nerves are located ventral to the denticulate ligaments. The dorsal roots of the spinal nerves, the posterior inferior cerebellar artery and the spinal roots of the accessory nerve are situated dorsal to the ligaments. There is no perforating structure through the denticulate ligaments. At the craniovertebral junction the denticulate ligaments separate the cerebellomedullary cistern from the premedullary cisterns and caudally the ventral and dorsal spinal subarachnoid spaces.

Connections: medial: lateral surface of the medulla oblongata and the spinal cord. Lateral: inner surface of the dura mater. Superior: its superior edge merges into the dorsal surface of the rhomboid membrane. Inferior: the ligaments spread into the spinal canal and terminate at the level of lumbal spine.

Intermediate cervical septum (septum posticum)

This is a midline structure located dorsal to the level of the foramen Magendi along the entire spinal cord (Figures 1I and 3O). The upper portion of the membrane, located at the craniovertebral junction, is always a dense network of arachnoid trabeculae and not an intact, sheeth-like membrane. During its course caudally, it converts to a clear plate around the C3-C4 level. The posterior inferior cerebellar arteries are located at both side of the membrane but never perforate it. Therefore, there is no preforating structure through the membrane. It divides the cerebellomedullary and the dorsal spinal subarachnoid space partly into two parts.

Connections: dorsal: inner side of the outer arachnoid at the dorsal surface of the foramen magnum and the spinal canal. Ventral: dorsal surface of the medulla oblongata and the spinal cord.

Discussion

There are numerous anatomical studies about the arachnoid organization at the level of the tentorium, the posterior fossa, and the craniovertebral junction in the literature [16–19, 21, 32–34]. They described the existence of these membranes, but just like in the anterior and middle cranial fossa, only few anatomical details were provided, and the membranes were thought to be very variable. The present study was performed on 127 fresh human cadavers in order to be able to recognize a systematic organization or common variations and propose an updated and intuitive terminology.

Another unique feature of this study is that endoscopes were used as the main optical tool for our dissections. This technique enables the examination of the natural position and relations of the deep-seated arachnoid structures to the neurovascular structures, with minimal approach-related distortion of the surrounding structures. Furthermore, this surgically oriented endoscopic anatomical knowledge about the presently not well recognized details of the arachnoid membranes seems to be important to safely apply, and further push forward, the rapidly developing, minimally invasive techniques in neurosurgery [9, 26].

Based on our study, the inner arachnoid trabecular membranes seem to vary to a great extent among individuals. However, a higher systematic organization was found to be present, although not complete, and not in all of the examined cadavers. The inner membranes are concentrated around the neurovascular structures of well-defined skull base areas in a regular pattern. Therefore, we suggested in the first part of this study to use the term “arachnoid membrane system” [12]. As a part of this arachnoid membrane system, we described in details for the first time, the carotid and the Sylvian membrane groups at the anterior and middle fossa. As a continuation of it, we propose to distinguish further three membrane groups at the level of the tentorium, posterior fossa, and the craniovertebral junction, completing our studies on to the arachnoid architecture of the entire skull base and accomplish the description of the complete arachnoid membrane system.

The three distinct membrane groups (Figure 5A–C) are the “tentorial membrane group” located in the level of the tentorium, the “clival membrane group” located in the midline at the ventral surface of the mesencephalon, and the pons and the “perimedullary membrane group” located around the medulla oblongata in the level of the craniovertebral junction. They consist of 11 distinct inner arachnoid membranes, seven of them are paired, summing up to a total of 18 inner arachnoid membranes and the two denticulate ligaments. This system acts as the frame of the subarachnoid space and defines the three-dimensional shape of the here located basal cisterns. For a better understanding, we described the ideal “all-in-one” case and common individual variations.

Schematic drawings of the inner arachnoid membrane groups at the (A) level of the tentorium: tentorial membrane group (B) posterior fossa: clival membrane group, (C) craniovertebral junction: superior and inferior part of the perimedullary membrane group. APM=anterior pontine membrane, ICS=intermediate cervical septum, ins.=insertion, LD=denticulate ligament, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, LMM=lateral mesencephalic membrane, MMM=median medullary membrane, PCM=posterior cerebral membrane, PM=pontomedullary membrane, PMM=posterior mesencephalic membrane, RM=rhomboid membrane, SCM=superior cerebellar membrane, TrM=trigeminal membrane.
Figure 5

Schematic drawings of the inner arachnoid membrane groups at the (A) level of the tentorium: tentorial membrane group (B) posterior fossa: clival membrane group, (C) craniovertebral junction: superior and inferior part of the perimedullary membrane group.

APM=anterior pontine membrane, ICS=intermediate cervical septum, ins.=insertion, LD=denticulate ligament, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, LMM=lateral mesencephalic membrane, MMM=median medullary membrane, PCM=posterior cerebral membrane, PM=pontomedullary membrane, PMM=posterior mesencephalic membrane, RM=rhomboid membrane, SCM=superior cerebellar membrane, TrM=trigeminal membrane.

Tentorial membrane group

The tentorial membrane group is composed of ten inner arachnoid membranes and located at the level of the tentorial edge. It is a C-shaped four-level barrier between the supra- and infratentorial cranial spaces at both sides of the mesencephalon connected to each other dorsally by the outer arachnoid envelop around the great vein of Galen and ventrally by the clival membrane group (Figures 5A, 6, 7A and B).

Schematic drawing of the tentorial and the clival membrane group from lateral (right side). Note the relations of the quadrigeminal cistern: the middle portion located between the outer arachnoid envelop around the great vein of Galen and the quadrigeminal plate. The lateral portion is located between the posterior and lateral mesencephalic membrane and the superior cerebellar membrane. The superior cerebellar artery is located within the cistern and the trochlear nerve also, but strongly attached with numerous inner arachnoid trabeculaes to the inner surface of the outer arachnoid just below the tentorial edge. AE=arachnoidal envelop around the great vein of Galen, APM=anterior pontine membrane, LM-LM=mesencephalic leaf of the Liliequist’s membrane complex, LMM=lateral mesencephalic membrane, PCM=posterior cerebral membrane, PMM=posterior mesencephalic membrane, SCM=superior cerebellar membrane, TrM=trigeminal membrane.
Figure 6

Schematic drawing of the tentorial and the clival membrane group from lateral (right side). Note the relations of the quadrigeminal cistern: the middle portion located between the outer arachnoid envelop around the great vein of Galen and the quadrigeminal plate. The lateral portion is located between the posterior and lateral mesencephalic membrane and the superior cerebellar membrane. The superior cerebellar artery is located within the cistern and the trochlear nerve also, but strongly attached with numerous inner arachnoid trabeculaes to the inner surface of the outer arachnoid just below the tentorial edge.

AE=arachnoidal envelop around the great vein of Galen, APM=anterior pontine membrane, LM-LM=mesencephalic leaf of the Liliequist’s membrane complex, LMM=lateral mesencephalic membrane, PCM=posterior cerebral membrane, PMM=posterior mesencephalic membrane, SCM=superior cerebellar membrane, TrM=trigeminal membrane.

(A) Overview of the complete organization of the arachnoid membrane groups at the level of the tentorium, posterior fossa and the craniovertebral junction (AP view). (B) The complex relations of the tentorial and clival membrane group at the level of the tentorial edge. (C) Axial view of the relations of the neurovascular structures to the inner membranes at the level of the craniovertebral junction. Left side of the drawing: the level of the C1 spinal nerve. Rigth side: level of the C2 spinal nerve. AICA=anterior inferior cerebellar artery, APM=anterior pontine membrane, ASA=anterior spinal artery, C1 root=C1 spinal nerve, C2 root=C2 spinal nerve, CNIII=oculomotor nerve, CNIV=trochlear nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, CNIX=glossopharyngeal nerve, CNX=vagal nerve, CNXI=accessory nerve, CNXII=hypoglossal nerve, ex.=exit, ins.=insertion, LD=denticulate ligament, LMM=lateral mesencephalic membrane, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, OA=outer arachnoid, PCA=posterior cerebral artery, PCM=posterior cerebral membrane, PICA=posterior inferior cerebellar artery, PM=pontomedullary membrane, RM=rhomboid membrane, SCM=superior cerebellar membrane, tent.=tentorium, TrM=trigeminal membrane, VA=vertebral artery.
Figure 7

(A) Overview of the complete organization of the arachnoid membrane groups at the level of the tentorium, posterior fossa and the craniovertebral junction (AP view). (B) The complex relations of the tentorial and clival membrane group at the level of the tentorial edge. (C) Axial view of the relations of the neurovascular structures to the inner membranes at the level of the craniovertebral junction. Left side of the drawing: the level of the C1 spinal nerve. Rigth side: level of the C2 spinal nerve.

AICA=anterior inferior cerebellar artery, APM=anterior pontine membrane, ASA=anterior spinal artery, C1 root=C1 spinal nerve, C2 root=C2 spinal nerve, CNIII=oculomotor nerve, CNIV=trochlear nerve, CNV=trigeminal nerve, CNVI=abducent nerve, CNVII-VIII=vestibulocochlear and facial nerves, CNIX=glossopharyngeal nerve, CNX=vagal nerve, CNXI=accessory nerve, CNXII=hypoglossal nerve, ex.=exit, ins.=insertion, LD=denticulate ligament, LMM=lateral mesencephalic membrane, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, OA=outer arachnoid, PCA=posterior cerebral artery, PCM=posterior cerebral membrane, PICA=posterior inferior cerebellar artery, PM=pontomedullary membrane, RM=rhomboid membrane, SCM=superior cerebellar membrane, tent.=tentorium, TrM=trigeminal membrane, VA=vertebral artery.

The arachnoid base of the tentorial membrane group is the outer arachnoid formation around the tentorial edge and the tentorial apex. The microsurgical anatomical aspects of the outer arachnoid relations around the tentorial edge have already been extensively studied [1, 19, 20, 25, 32, 33]. The special arachnoid relations around the great vein of Galen, its tributaries [24, 25], and in the velum interpositum [37] were also described. Our observations confirm these results and add important endoscopic anatomical aspects. We could also verify, and for the first time, endoscopically show the existence of the suprapineal arachnoid body, which is the granulation-like thickening between the junction of the great vein of Galen and the straight sinus, described first by Clark [6, 25].

The most superior of the four levels is the posterior cerebral membrane. This membrane was never mentioned in the literature. A membrane described by others as “basilar bifurcation” [16, 17, 19, 29] or “top basilar membrane” [33, 34] could be the interconnected medial edges of the posterior cerebral membrane in the depth of the interpeduncular fossa. As the closest structure around the membrane is the posterior cerebral artery we named it “posterior cerebral membrane”. This membrane does not provide a complete closure around the mesencephalon as dorsally, and in most of the cases also ventrally, it terminates free.

Just below the posterior cerebral membrane, along the tentorial edge, the second level of the tentorial membrane group is located, which separates the supra- and infratentorial cranial space completely. This level is formed by the lateral and posterior mesencephalic membranes at both sides. Both of the membranes have already been mentioned in the literature [1, 19, 21, 27, 33, 38]. Qi et al. also described that these membranes belong to an arachnoid closure around the mesencephalon, together with the Liliequist membrane [24]. It was also known that the posterior mesencephalic membrane is attached to the outer arachnoid envelop around the great vein of Galen and its tributaries [25]. Our findings confirm these results and provide additional endoscopic anatomical informations. In contrast to the mentioned studies, we categorize the mesencephalic leaf of Liliequist membrane as a part of another membrane group, the clival membrane group because of its clear macroscopic continuation into the anterior pontine membranes.

The third level of membranes around the mesencephalon are formed by the two superior cerebellar membranes just below the tentorium. They provide only a partial separation of the middle and posterior cranial fossa. This membrane has not been mentioned or shown before. We call it “superior cerebellar membrane” because of its close relation to the superior cerebellar artery along its entire length. A membrane described by Lu et al. [19] as “cerebellar precentral membrane” may be the dorsal ending of the superior cerebellar membrane.

The fourth level of membranes of the tentorial group is the trigeminal membrane. This membrane was also never mentioned before as separate structure. We named it “trigeminal membrane” regarding its close relation to the trigeminal nerve.

As a consequence of this four-level organization, some anatomical information must be reconsidered and discussed with presently well-accepted, but also controversial, facts. The ambient cistern is a completely supratentorial cistern, located above the lateral and posterior mesencephalic membranes (second level of membranes) and divided partially by the posterior cerebral membrane (first level of membranes) into a superior and inferior portion. As a result of the presence of the superior cerebellar membrane, there is an additional cistern between the supratentorially located ambient cistern and the infratentorially located cerebellopontine cistern. This space is in continuation with the subarachnoid space above the quadrigeminal plate and turns ventrally along the cerebellomesencephalic fissure to the ventrolateral surface of the pons (Figure 6). Therefore, we suggest to divide the quadrigeminal cistern into a dorsal and two lateral portions. The third cistern around the pontomesencephalic junction is the trigeminal cistern produced by the trigeminal membrane detaching from the lateral surface of the trigeminal nerve.

Clival membrane group

The clival membrane group is composed of the three biggest intracranial inner arachnoid membranes and has an inverted U-shape (Figures 5B and 7A). It is located superiorly in the ventral opening of the tentorial membrane group, completing the separation between the supra- and infratentorial cranial space and extends caudally with its two legs to the pontomedullary junction. The membranes of the group separate the subarachnoid space ventral to the pons into a midline prepontine and two laterally located cerebellopontine cisterns.

The base of the membrane group is formed by the outer arachnoid on the dorsum sellae and the clivus [2, 19, 21, 27]. The basal attachments of the inner arachnoid membranes of the group are visible as an inverted U-shaped white-grey thickening on the outer arachnoid. Regarding its location and relation to the clival membrane group we named it the “clival line”. This structure has not been described and named before this study. However, it can be recognized on the pictures of numerous previous publications [29, 33, 34].

The uppermost structure of this membrane group (the base of the inverted U-shape) is the mesencephalic leaf of the Liliequist’s membrane complex. The Liliequist’s membrane complex is one of the most controversial structures in the literature about arachnoid membranes as an exact, well-accepted definition does not exist [1, 3, 4, 7, 8, 10, 15–18, 21, 24, 28, 34–36]. Based on our extended cadaveric work, we found a diencephalic leaf and a variable common leaf [12] and categorized both as parts of the carotid membrane group of the middle cranial fossa. In the present study, we describe a third structure, the mesencephalic leaf as a part of the clival membrane group. These three leafs together form the “Liliequist’s membrane complex”. In the proposed terminology “Liliequist’s membrane complex” is not a separate membrane group but an extra category as we would like to keep the name of “Liliequist” because of its historical importance.

The anterior pontine membranes are the caudal continuations of the lateral edges of the mesencephalic leaf. They form the “legs” of the inverted U-shaped clival line with their basal attachments. This membrane has been mentioned in every anatomical study that describes the arachnoid relations of the posterior fossa. Some authors called it the “basilar membrane” [19, 32]. The most accepted name is the “anterior pontine membrane” [20, 21, 27], therefore, we suggest to use the latter. Its anatomical description is relatively uniform in the literature. Our endoscopic observations are identical with these microsurgical findings.

Perimedullary membrane group

The perimedullary membrane group is composed of five inner arachnoid membranes and the first two insertions of the denticulate ligaments are at both sides (Figures 5C, 7A and C). The group is divided to a superior and an inferior part. The base of the whole membrane group is the tube-shaped outer arachnoid around the medulla oblongata and the uppermost part of the spinal cord, attached to the inner surface of the dura mater [19, 32].

Superior part

The superior part is composed of three inner membranes and shaped like a T (Figure 5C). It is located at the level of the pontomedullary junction and the uppermost part of the medulla oblongata. It divides the subarachnoid space ventrally to the medulla into two premedullary cisterns at both sides and separates them superiorly from the cerebellopontine cisterns and the prepontine cistern. Inferiorly the two premedullary cisterns are in continuation with the ventral spinal subarachnoid space. The horizontal line of the T-shape is formed by the two pontomedullary membranes. These structures were first described by Matsuno et al. [21] as lateral pontomedullary membranes and later by others with the same name [1, 19, 20, 27]. Vinas referred to the membrane as “anterior inferior cerebellar membrane” [32]. As we could not confirm the existence of a medial pontomedullary membrane we favored the term “pontomedullary membrane” to these structures. The vertical line of the T-shape is the median medullary membrane. Previously, only the most superior part of the membrane was described as “medial pontomedullary membrane” [1, 21, 27] that connects the medial edges of the pontomedullary membranes at both sides. We propose the name “median medullary membrane” because it is located in the midline and spreads caudally until the level of the pyramid decussation.

Inferior part

The inferior part of the membrane group is composed of two inner membranes and the first two insertions of the denticulate ligaments at both sides. It has also quite a T-shape but in the axial plane (Figure 5C). Between the horizontal and vertical line is located the lower part of the medulla oblongata and caudally the most upper part of the spinal cord. The meningeal organization of the craniovertebral junction is structurally independent, it differs from the cranially located arachnoid membranes and the caudally located spinal membranes.

The vertical line of the virtual T-shape is formed by the intermediate cervical septum or septum posticum. This structure was firstly and in the most detailed manner described by Key and Retzius [11]. Lang also mentioned this structure in two articles [13, 14]. Lu describes a “ventral pontine membrane” [19] that is probably the cranial part of this membrane. We verified these results and added important endoscopic anatomical information. The horizontal line of the virtual T-shape is duplicated. It is composed by the bilaterally located denticulate ligaments and in the midline located rhomboid membrane. The detailed anatomy of the denticulate ligaments was published first by Key and Retzius. Later Lang et al. and others [5, 13, 14, 22, 30, 31] also mentioned this structure. As a result of our examinations, we confirmed the findings of the previous authors. As far as we know, this is the first study that provides detailed endocopic anatomical description of the first two denticulate ligament insertions. The rhomboid membrane is a rarely mentioned structure in the literature. It was also first described by Key and Retzius [11]. They named it “sail-shaped structure” and discussed its possible function as a valve between the basal cisterns and the ventral spinal subarachnoid space. Later, Lang et al. mentioned this structure as “Rhomboid halfter” but did not provide new anatomical details [13, 14]. In our description we named it “rhomboid membrane” referring to its functionally similar role like the other inner arachnoid membranes (Figure 7C). During our examinations we could verify the findings of the previous authors and for the first time in the literature also showed every anatomical property of this structure in high-quality endoscopic images.

Connections of the arachnoid membrane groups

The membrane groups described here and in the first part of this study [12] are strongly adhered to each other at defined locations. Therefore, they are acting as an interconnected membrane system of the skull base.

The tentorial membrane group is connected superiorly to the lateral part of the carotid membrane group by the junction between the inferior edge of the temporal membrane and the anterior edge of the lateral mesencephalic membrane (Figure 8). Medially, the tentorial membrane group is connected to the clival membrane group by the junction between the medial edge of the lateral mesencephalic membrane and the mesencephalic leaf of the Liliequist’s membrane complex. The clival membrane group is connected superiorly to the central part of the carotid membrane group through the junction between the inferior edge of the diencephalic leaf and the basal attachment of the mesencephalic leaf of the Liliequist’s membrane complex (Figure 8). Inferiorly the clival membrane group is connected to the superior part of the perimedullary membrane group through the junction between the inferior edge of the anterior pontine membrane, the medial edges of the pontomedullary membranes and the superior edge of the median medullary membrane. The inferior part of the perimedullary membrane group is connected to the superior part by the adhesions between the basal edge of the median medullary membrane and the dorsal surface of the rhomboid membrane.

Schematic drawing of the connections between the carotid membrane group and the attached parts of the tentorial and clival membrane groups. LCM=lateral carotid membrane, LLTM=lateral lamina terminalis membrane, LM-DL=diencephalic leaf of the Liliequist’s membrane complex, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, LMM=lateral mesencephalic membrane, MCM=medial carotid membrane, OM=olfactory membrane, PSM=proximal Sylvian membrane, TM=temporal membrane.
Figure 8

Schematic drawing of the connections between the carotid membrane group and the attached parts of the tentorial and clival membrane groups.

LCM=lateral carotid membrane, LLTM=lateral lamina terminalis membrane, LM-DL=diencephalic leaf of the Liliequist’s membrane complex, LM-ML=mesencephalic leaf of the Liliequist’s membrane complex, LMM=lateral mesencephalic membrane, MCM=medial carotid membrane, OM=olfactory membrane, PSM=proximal Sylvian membrane, TM=temporal membrane.

Summary of parts I and II

This, and our previous study, clearly show that the arachnoid membrane system is a complex three-dimensional and interconnected construct of the entire skull base. For better understanding of the spatial relations of this uniform and continuous system, it may be divided into five arachnoid membrane groups based on their specific anatomical locations. These are the carotid, Sylvian, tentorial, clival, and perimedullary membrane groups. The carotid membrane group is located in the anterior fossa and consists of a central and two lateral parts. The inner arachnoid membranes of the Sylvian membrane group are connected to the lateral parts of the carotid membrane group. Posteriorly, the carotid membrane group is connected to a further unique membrane construct at the level of the tentorium. Here, the located membranes form the tentorial membrane group around the mesencephalon and the membranes ventral to the pons, the clival membrane group. More caudally, the membranes are cumulated around the medulla oblongata and the upper part of the spinal cord forming the perimedullary membrane group which consists of a superior and an inferior part. The entire arachnoid membrane system consists of 24 distinct inner arachnoid membranes plus the denticulate ligaments. Eighteen of these structures are paired summing up to a total of 43 individual membranes.

Conclusion

The systemic knowledge of the arachnoid architecture and its relation to neurovascular structures is mandatory for the use of minimally invasive neurosurgical techniques, including endoscopic neurosurgery. This anatomical information is essential for the intraoperative orientation with the endoscope and for safe and effective manipulations, as well as for supporting the gravity related brain retraction or using surgical instruments parallel to the endoscope.

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The authors stated that there are no conflicts of interest regarding the publication of this article.

About the article

Corresponding author: Dr. med. Peter Kurucz, Department of Neurosurgery, Katharinenhospital, Klinikum Stuttgart, Kriegsbergstrasse 60, 70174 Stuttgart, Germany, Tel.: +49 1522 699 1301


Received: 2013-04-30

Accepted: 2013-05-06

Published Online: 2013-05-31

Published in Print: 2013-06-01


Citation Information: Innovative Neurosurgery, Volume 1, Issue 2, Pages 91–108, ISSN (Online) 2193-5238, ISSN (Print) 2193-522X, DOI: https://doi.org/10.1515/ins-2013-0008.

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