Microsurgical Anatomy Of The Arachnoid Membranes And Cisterns In The Perimesencephalic Region

Background and ObjectiveThe perimesencephalic region refers to the area surrounding the midbrain. Specifically, it can be divided into anterior (interpeduncular), lateral and posterior (pineal) mesencephalic region. The subarachnoid space of the perimesencephalic region is surrounded by the temporal lobe, occipital lobe, tentorial incisura, midbrain and inner arachnoid membrane, forming cisterns, in which the arachnoid membranes are closely related to adjacent neurovascular structures. The perimesencephalic region is one of the most complex areas lying deep within the brain and containing arteries, deep veins, cranial nerves and brainstem. Many lesions like germinomas, meningiomas, trigeminal neurinomas and aneurysms frequently arise from the region, presenting unique challenges to the neurosurgeon about the knowledge of the anatomy and management. For this reason, a complete understanding of the microsurgical anatomic features in this region play an important role inVarious descriptions of the ambient cistern can be found in the literature, and the anatomy of neurovascular structures or surgical approaches in this region has been well illustrated. However, only few microscopic studies of the arachnoid membranes related to the region have been published, which is limited to such structures as Liliequist's membrane. Lu, Rothon and Vinas have described some aspects of the arachnoid membranes in the perimesencephalic region. However, they had not make a detailed and complete description, and there still exist some conflict among their illustration about the arachnoid membranes and cisterns. For example, Rhoton identified, lateral to the oculomotor nerve, a "lateral pontomesencephalic membrane" that was "attached to the pontomesencephalic junction and to the outer arachnoidal membrane near the free edge of the tentorium." They demonstrated that this membrane separated the cerebellopontine from the ambient cistern. But Vinas identified a membrane, the "superior cerebellar membrane" that originates "from the cerebellar precentral membrane and runs around the midbrain towards the oculomotor cistern." Rhoton and Vinas also mentioned that the vein of Galen and its tributaries are surrounded by a broad membranous envelope, while they failed to provide further description about it. In addition, most authors have considered the ambient cistern to be a subarachnoid space extending across the tentorial incisura. Some authors even divided the cistern into supra- and infratentorial compartments.Focused on the above-mentioned issues, we reinvestigated the anatomy of the arachnoid membranes and cisterns in the perimesencephalic region in an attempt to gain a thorough understanding about it. Hopefully, it will be helpful to explore some factors possibly related to the growth of lesions in this region and more precisely manage lesions in this region.Materials and MethodsMaterials:Twenty adult cadaveric brains fixed in formaldehyde solution were carefully prepared for microsurgical dissection. On macroscopic examination, none of the brains showed signs of cerebral diseases. Some microsurgical instruments, a Leica surgical microscope and a digital video recorder were also used in this study.Methods:10 specimens were selected randomly and injected by color silicon through internal carotid artery and vein. The cranium of all 20 specimens was first removed at the level of line between the superciliary arch and the inion after the dura mater has been dissected from the skull. The dura mater was then opened along the line about lcm to the superior sagittal sinus and turned over downwards to expose bilateral hemispheres. The supratentorial cerebral lobes were subpially removed under a surgical microscope, step by step, until it reached the wall of ventricle, corpus callosum and brainstem. The leptomeninges near the falx and the skull base was totally reserved. After the brain parenchyma was removed, the pia mater was then carefully dissected away from the surfaces of the arachnoid membranes surrounding the midbrain, with special attention to observe the relationship between the arachnoid membrane and the pia mater. It is important to handle tenderly in some region where the arachnoid membrane was adhered tightly to the pia matter, in case of the destruction of the membrane. Some timely irrigation also prevents the membrane from shrinking which may lead to an incorrect result. Finally, the arachnoid membranes with their adjacent neurovascular structures in the perimesencephalic region were carefully dissected. During the whole course of the study, the microscope was connected to the digital video recorder for photographic documentation. The cisterns and their arachnoid membranes, configurations, borders, contents, and communications with adjacent cisterns were examined in detail in this study.ResultsThe inner arachnoid membranes in the perimesencephalic region include the perimesencephalic membrane, Liliequist's membrane, the arachnoid envelope surrounding the vein of Galen (AEPG) and the precentral cerebellar membrane.Perimesencephalic membrane. The perimesencephalic membrane is a set of inner arachnoid membranes surrounding the midbrain at the level of the tentorial incisura. It originates from the outer arachnoidal membrane covering the tentorial edge and the dorsum sellae. This membrane usually changes in structure from an intact and thick membrane to a thinner trabeculated membrane with many perforations near its attachment. The membrane is composed of 2 distinct membranes—anterior and posterior. The anterior membrane is actually the mesencephalic leaf of Liliequist membrane. It extends between the dorsum sellae and bilateral tentorial edges. The oculomotor nerve divides it into medial and lateral parts. The medial part extends posteriorly with a free edge attaching to the basilar bifurcation and the junction of the midbrain and pons by trabeculae. This part usually presents as a structure of trabecular network with large perforations. The lateral part is frequently intact without perforations. As it extends backward, the lateral part becomes narrow, gradually, until it disappears. The anterior and posterior membranes are mostly connected by some sparse trabeculae. The posterior membrane is surrounding the midbrain tegmentum and can be divided into horizontal and ascending parts. The horizontal part was attached anteriorly to the midbrain tegmentum or the basal vein. It separates the posterior ambient cistern from the cerebellomesencephalic cistern. The ascending part is attached anteriorly to the pulvinar and superiorly to the AEPG. The posterior membrane is mostly thinner and incomplete with multiple perforations near its attachment, which causes a wide communication between the ambient and quadrigeminal cistern.Liliequist's membrane. Liliequist's membrane arises from the arachnoid covering the dorsum sellae and posterior clinoid processes, and can be divided into two distinct leaves near its origination. The diencephalic leaf originates from Liliequist's membrane, extends posterosuperiorly and attaches to the pia of the diencephalon between the infundibulum and mamillary bodies. The leaf is usually intact and complete without openings. The mesencephalic leaf refers to the anterior perimesencephalic membrane in this study.AEPG. The supratentorial outer arachnoid membrane covering the edial surface of bilateral parietooccipital lobes and the posterior urface of splenium and the infratentorial outer arachnoid embrane covering the superior surface of the cerebellum converged near the site where the vein of Galen emptied into the straight sinus. The thickened outer arachnoid membrane then embraced and ran forward along the vein of Galen to form the AEPG. The AEPG could be arbitrarily divided into 2 parts:anterior and posterior. Anterior AEPG (aAEPG) is relatively thick and encloses the great cerebral vein and its proximal tributaries. The posterior edge of pAEPG forms an arachnoid cuff near the site where the great cerebral vein joins the straight sinus. Based on the distance between the cuff and the tentorial apex, it can be divided into typeⅠand typeⅡ. Posterior AEPG (pAEPG) is relatively thin and contains the proximal inner cerebral vein, the pineal vein, the suprapineal recess and the pineal body. It enters the posterior compartment of the third ventricle together with the inner cerebral vein and the suprapineal recess.Precentral cerebellar membrane. The membrane originates from the lower surface of pAEPG near the cuff, extends anteroinferiorly, attaches to the quadrigeminal plate anteriorly and to the ascending part of the posterior perimesencephalic membrane laterally. This membrane is usually intact an complete with few perforations, separating the quadrigeminal cistern from the superior cerebellar cistern. The superior vermian vein runs upwards along the posterior edge of the membrane and perforates the lower surface of pAEPG to join the great cerebral vein.The cisterns in the perimesencephalic region include the interpeduncular cistern, the oculomotor cistern, the ambient cistern, the cerebellomesencephalic cistern, the quadrigeminal cistern and the superior cerebellar cistern.Interpeduncular cistern. The interpeduncular cistern is a pyramid-shaped compartment enclosed by the peduncle, the posterior perforated substance, the posterior diencephalon and both leaves of Liliequist's membrane. It is located between the peduncle and the posterior perforated substance. Its anterior wall is formed by the anteroinferior part of the diencephalic leaf. The roof consists of diencephalic and mesencephalic parts:the diencephalic part refers to the posterior-superior part of the diencephalic leaf and the mamillary bodies, and the mesencephalic part refers to the upper surface of the interpeduncular fossa. The posterior wall is formed by the peduncle, the interpeduncular fossa and upper surface of the pons. The inferior will is formed by mesencephalic leaf. Its lateral wall usually presents as some trabeculae ro incomplete arachnoid septum attached to the oculomotor nerve. The content of the interpeduncular cistern includes the bifurcation of the basilar artery, the P1, the posterior thalamoperforating arteries, the posterior communicating artery with its branches, the peduncular vein and the posterior communicating vein. The interpeduncular cistern borders the chiasmatic cistern by the diencephalic leaf anteriorly and the prepontine cistern by the mesencephalic leaf inferiorly. Laterally, it communicates with the oculomotor cistern and the anterior ambient cistern via some sparse trabeculae.Oculomotor cistern. The diencephalic, mesencephalic, medial carotid, lateral pontomesencephalic, and anterior pontine membranes attach to form a sleeve, mostly thin and incomplete, around the nerve, constructing the oculomotor cistern. The cistern spans the interval of the interpeduncular and the ambient cistern. The oculomotor nerve is the only content of the cistern. It arises from the medial side of the peduncle, passes between the posterior cerebral and superior cerebellar arteries and courses anterolaterally at the junction of the carotid, interpeduncular, prepontine, and cerebellopontine cisterns to reach the dural roof of the cavernous sinus.Ambient cistern. The ambient cistern is a paired ring-shaped cistern situated above the level of the tentorial incisura and the perimesencephalic membrane. It is surrounded by the upper midbrain laterally in a semiring shape and is limited by the medial temporal lobe, the inferior occipital lobe, the midbrain, and the perimesencephalic membrane. The cistern can be divided into anterior and posterior compartments. The superior wall of the anterior compartment is formed by the pial layers covering the lateral surface of the upper peduncle, the optic tract, and the uncus. The inferior wall is formed by the lateral part of the anterior perimesencephalic membrane, the medial wall by the lateral peduncle, and the lateral wall by the medial temporal lobe. The anterior ambient cistern communicates with the carotid cistern anteriorly, the interpeduncular cistern medially, the cerebellopontine cistern inferiorly, and the oculomotor cistern inferomedially. The superior wall of the posterior compartment is is formed by the pial layers covering the midbrain tegmentum, the lateral geniculate body, and the medial occipital lobe. The inferior wall is formed by the horizontal part of the posterior perimesencephalic membrane, the medial wall by the midbrain tegmentum, the lateral wall by the medial occipital lobe, and the posteromedial wall by the ascending part of the posterior perimesencephalic membrane. The posterior ambient cistern communicates with the cerebellomesencephalic cistern inferiorly and the quadrigeminal cistern posteromedially. The ambient cistern contains the AChA, the P2 and P3 segments with their branches, the basal vein of Rosenthal, and, infrequently, a segment of the superior cerebellar artery.Cerebellomesencephalic cistern. The cistern is a wing-shaped infratenrorial compartment and enclosed by the cerebellar peduncle, the central lobule, the ala cerebella and dorsal midbrain. It can be divided into central and lateral compartments. The central compartment is located anteroinferiorly to the central lobule. Its anterior wall is formed by the lingual lobe and the posterior wall by the central lobule. It contains the trochlear nerve and some vessel branches, and communicates with the superior cerebellar cistern. The lateral compartment is positioned anteriorly to the ala cerebella. Its anterior wall is formed by the lower dorsal midbrain, the posterior wall by the ala cerebella, the superior wall by the horizontal part of the posterior perimesencephalic membrane, and the inferior wall by the superior cerebellar peduncle. It contains the superior cerebellar artery and the trochlear nerve. The compartment communicates with the posterior ambient cistern superiorly and the cerebellopontine cistern anteriorly.Quadrigeminal cistern. The quadrigeminal cistern is located inferior to the AEPG and contains five walls. Its superior wall is formed by AEPG, the anterior wall by the quadrigeminal plate medially and the medial pulvinar laterally, the posterior wall by the precentral cerebellar membrane, and the lateral wall by the ascending part of the posterior perimesencephalic membrane. The cistern contains medial posterior choroidal artery (MPChA) and some branches nourishing the dorsal midbrain. The MPChA perforates the ascending membrane, courses in the quadrigeminal cistern, and then passes through the gap between the medial pulvinar and the AEPG to enter the velum interpositum. The quadrigeminal cistern communicates with the posterior ambient cistern laterally, the superior cerebellar cistern posteriorly and the pericallosal cistern superiorly.Superior cerebellar cistern. The superior cerebellar cistern is positioned superior to the vermis and includes anterior and posterior parts. The anterior compartment is situated anterior to the central lobule. Its anterior wall is formed by the precentral cerebellar membrane and the inferior colliculus, the posterior wall by the central lobule, and the lateral wall by the posterior perimesencephalic membrane. It contains the superior vermian vein and some branches of the superior cerebellar artery. The anterior compartment communicates with the cerebellomesencephalic cistern inferiorly and the quadrigeminal cistern anteriorly. The posterior part is located above the culmen and clivas of cerebellum. Its superior wall is formed by the outer arachnoid membrane covering the cerebellum, and the inferior wall by the culmen and clivas. It contains the branches of the superior cerebellar artery. This compartment communicates with the cistern covering the upper the cerebellar hemisphere laterally and the cisterna magna posteriorly.ConclusionThe anatomy of the cisterns and its related arachnoid membranes in the perimesencephalic region has been reinvestigated in this study. Compared with previously reported studies, some new information was updated:1) The perimesencephalic membrane was identified as a set of inner arachnoid membranes surrounding the midbrain at the level of the tentorial incisura, it was an important membranous barrier between the supra- and infra-tentrial cisterns. Its formation and distribution were also been described in detail.2) The anterior tentorial edge was verified to be the lateral border of the mesencephalic membrane.3) The AEPG, including its formation, construction, content and relationship with adjacent arachniod membranes and structures, was illustrated systematically, which cannot been found in previous studies.4) The precentral cerebellar membrane has been identified and described in detail.5) The ambient cistern was verified, anatomically, to be a supratentorial cistern located above the level of the tentorial edge and perimesencephalic membrane.6) The borders and contents of the cisterns in the perimesencephalic region, as well as its relationship with adjacent cisterns have also been redefined.7) The arachnoid membranes may be one of the most important factors related to the growing pattern of the perimesencephalic tumors.8) A better understanding of the cisterns and membranes may be helpful to explore the morphologic features, design optimal surgical approaches and more precisely manage lesions in the perimesencephalic region.