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Abstract

The subarachnoid space is commonly regarded as the highway for neurosurgeons. The cisterns which are considered expansions of subarachnoid space consists of compartmentalized trabeculae filled with CSF, situated between the arachnoid and pia. They serve as runways for major intracranial nerves and vessels, as well as a cushion for the suspended brain.
In this work, we will go over the major cisterns with particular correlation with its surgical anatomy, as they provide a harmless pathway for accessing numerous pathologies such as tumors, aneurisms, relieving hydrocephalus, etc.

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Introduction

The term arachnoid, derived from the Greek “arachnea” (Arachne=spider, eidos=web), was first introduced in 1699 by Frederick Ruysch, who described it as having a spider-like morphology by which the brain was covered in its totality 1. Other terminology used included meninx media, meninx mucosa, and meninx serosa, but never gained much acceptance by the scientific community 2. The study of the subarachnoid cisterns has been of primary concern for neuroscientists, mainly neurosurgeons, who use these defined pathways as navigation corridors in order to access, evaluate, and treat neurological pathologies.
Early day anatomic description of the cisterns was based on macroscopic observations, mostly attributed to Key and Retzius thanks to their work in 1875 in which they described the subarachnoid space with its major compartments and its relationship to cerebral vessels and structures 3. In the early 1900s thanks to the development of ventriculography and pneumoencephalography by Dandy, it exposed intercommunication and segmentation of the subarachnoid space, accompanied by new observations made by Locke confirming similar architectural arrangements as described earlier by Retzius 4, 5.
Modern day microneurosurgery has been dictated by the introduction of the microscope into the surgical field as early as 1970s. This novel instrument led the way into a new era of neurosurgery, in which a greater understanding of the subarachnoid space and its relationships to vascular and nerve structures was attained. The most complete description of the subarachnoid space was first made by Yasargil in the mid 1970s underlying the limits, relationships, and content of the basal cisterns 6. Under this initial paper is where we base our review.

Materials and methods

A PubMed search was made under “basal cisterns anatomy” which gave a total of 335 matches. These where further analyzed resulting in the presented paper. Anatomical description, approaches and techniques were the main points analyzed by the authors.

Results (embryology, anatomy, physiology, histology)

Embryology

Full understanding of embryonic development of the human nervous system is yet to be accomplished, ethical and moral values restrain for detailed study with human embryos. Most of the data available on nervous system embryology is based on animal models, most of which attributed to McLone 7.
Meninges formation varies among species, in mammals, the somatic mesoderm gives rise to spinal meninges, brainstem meninges from the cephalic mesoderm and the neural crest giving the telencephalic meninges. Meninge differentiation contributes to the formation of the subarachnoid space play while also playing a key role in regulating the growth of underlying nervous structures, such as inducing the formation of the superficial glial limiting layer and stimulating the growth of precursors located in the superficial blastemas of the cerebellum and hippocampus 8.

The first step in forming the subarachnoid space begins with the closure of the neural tube. As early as in a 10-day fetus, the subarachnoid space covering the telencephalon can be seen, it is yet to be filled with CSF so it appears as a typically large extracellular space of mesenchyme. This Primitive Pia Arachnoid Space (PPASS) is composed by widely separated stellate mesenchymal cells interconnected to each other through pseudopodia with glycosaminoglycan (GAG) gel filling the extracellular space 9.
By day 13 of fetal development, CSF begins to flow into the PPASS replacing the mesenchyme, reducing it in a peripheral manner resulting in a compacted pia-arachnoidal tissue which limits the peripheral extent of the subarachnoid space. The typical adult mammal subarachnoid space can be seen fully formed only after birth, during the neonatal period, around the 21st postnatal day 10.

Anatomy

From the 3 different meningeal layers that protect the brain, being the dura mater (also known as pachymeninx) the more rigid and external layer while the arachnoid and pia mater (in this order respectively from external to internal) form what is known as the leptomeninges. Our particular interest in this paper is focused in the middle layer of the above-mentioned meninges, the arachnoid mater.
The arachnoid which lies in direct contact with the dura, but can be easily dissected forming a virtual space known as the subdural space, is a thin delicate avascular membrane that revisit the entire brain. As part of the leptomeninges, the arachnoid follows the pia mater, covering the entire brain surface but does not follow deep into the sulci and fissures like the pia, instead it bridges across the circumvolutions 11. It is thicker at the basal surface of the brain at the level of the temporal lobes, and at the anterior surface of the pons, and is divided in both cerebral hemispheres at the level of the great longitudinal fissure. It also serves as a coating membrane over intracranial nerves and vessels mainly ICA and vertebrobasilar complex 12.

Physiology

The subarachnoid space, is the main compartment (excluding ventricles) in which cerebrospinal fluid (CSF) flows. The arachnoid also plays a fundamental role in production and reabsorption of CSF.
Normal CSF production in the encephalon is constant, facilitating flow, which starts at the level of the lateral ventricles passing through both foramen of Monro into the 3rd ventricle, it then reaches the 4th ventricle via the cerebral aqueduct of Sylvius, where it flows into the subarachnoid space and basal cisterns via foramen of Luschka (bilaterally), at the level of the cerebropontine angle. Finally, it reaches the cisterna magna after passing through foramen of Magendie (midline) 13.
At the level of the encephalon, CSF production is done by choroid plexus, accounting for 80% of total CSF production, while the rest of intracranial production occurs in the interstitial space. A small amount is also produced by the ependymal lining of the ventricles, while in the spine it is produced primarily in the dura of the nerve root sleeves 14. In the adult CSF production rate occurs at about 0,3ml/min which approximates 450ml per day meaning CSF is reabsorb and reconstituted 3 times a day, where the mean CSF volume is 150 ml, with 25 ml in the ventricles and 125 ml in subarachnoid spaces. CSF works as a dynamic pressure system, it contributes to intracranial pressure with physiological values ranging between 3 and 4 mmHg in infants (up to 1 year), and between 10 and 15 mmHg in adults 15. Other factors that contribute to CSF flow are: cardiac cycle, specifically during early systole, where blood flow within the brain tissue compresses the ventricles leading to choroid plexus expansion and contraction, propelling CSF caudally; inspiration and expiration (changes in CO2 levels and pressure variations), and intracranial pressure variation and resistance to outflow by the arachnoid villi 16, 17.
Reabsorption of CSF occurs through arachnoid villi and Pacchionian bodies (arachnoid granulations) 18. These granulations are better visible when a subject obtains an upright position, creating a negative pressure at the dural sinuses, causing the Pacchionian bodies to enlarge and bulge into the lumen. The main factor that contributes to CSF filtration is given by the differences in hydrostatic pressure, although some authors attribute it also to the colloid osmotic pressure between the CSF in the subarachnoid space and the blood at the level of the sinuses 16, 19, 20. Finally, the CSF may take 2 main pathways, the first occurs when it is transported via the adventitia of cerebral blood vessels, terminating at the cervical lymph nodes; the other pathway described is when CSF travel along the prolongation of the subarachnoid space through cranial nerves principally by olfactory (cranial nerve I) reaching the cribriform plate and nasal submucosa to then be absorbed by extracranial lymphatic vessels 21, 22.

The subarachnoid trabeculae (SAT), also referred as subarachnoid space trabeculae, or leptomeningeal trabeculae, are collagen type I reinforced columns serving as mechanical stabilization and support for the brain and neural structures 23, 24. They stretch between the arachnoid and pia membranes, can be visualized with light microscope (sharp dissection is preferred over blunt when working in these areas), whereas radiological imaging can only be obtained using high resolution MRI 25. Spinal SAT knowledge is sparse, Parkinson in 1991 gave a detailed description, in which he states that anteriorly there were no trabeculae between the spinal cord and arachnoid membrane, whereas posteriorly there was found to be a series of connecting fibers that extend from the lower cervical region dwindling all the way to the filum terminale 26. These SAT also found at the spinal nerve rootlets, serving as movement restriction, holding each root in its position within the dural sac and in relation to other nerve roots 27.

Basal Cisterns

The cisterns consist CSF filled pockets, limited by subarachnoid trabeculae and neural structures; nerves and vessels travel through them as they provide a safe and protected pathway.
They can be classified by its location: supratentorial, at the level of the tentorium, and infratentorial. These three can be further subclassified based on their partnership, as paired (found bilaterally) and unpaired (unilateral) cisterns 28-30, a summary is given in table 1.

Table 1.
Supratentorial at the level of the Tentorium Infratentorial
Paired Olfactory cistern Ambiens cistern Ponto cerebellar cistern
Carotid cistern
Sylvius cistern Cerebello medullar cistern
Crural cistern
Posterior communicating cistern Ambiens cistern
Oculomotor cistern
Unpaired Chiastmatic cistern Interpeduncular cistern Basilar cistern

Lamina terminalis cistern Quadrigeminal cistern Cisterna magna
Superior cerebellar cistern
Callosal cistern Velum interpositum cistern Supracerebellar cistern

Supratentorial paired

• Olfactory cistern: it has a triangular shape as seen from a coronal plane, extending anteriorly from the anterior olfactory tentorium, to the olfactory trigone posteriorly. Medially is limited by the pia covering the gyrus rectus, while the pia covering the orbital gyrus is found laterally. The roof is formed by the medial and lateral surfaces of the rectus and orbital gyrus respectively. The roof is formed by the arachnoid matter bridging from the before mentioned gyri 31, 32. It houses olfactory bulb and tract, olfactory artery, fronto-orbital artery, olfactory and orbital veins.

• Sylvius cistern: a transitional space between the basal cisterns and the hemispheric subarachnoid space that contains the MCA and vein, fronto-orbital veins, and collaterals to Rosenthal. Its limits given by the optic tract medially, anterior cerebral membrane anteriorly, anterior choroidal membrane, and the insular and opercular cortex provide a “T” shape appearance 6, 27.

• Carotid cistern: located surrounding the ICA, hence its name, it contains the ICA and the origins of both anterior choroidal and posterior communicating arteries. The optic chiasm is responsible for its anterior medial and posterior limits, laterally the uncus and anterior clinoid process are found. The roof is shared by two structures, the anterior perforated substance and the floor of the dura of the cavernous sinus 32, 33.

• Posterior communicating cistern: this cistern lies over the cavernous sinus, contiguous to the carotid cistern, limited by the carotid membrane, Liliequist membrane, and posterior communicating membrane, this cistern contains the posterior communicating artery (PComA) and perforating branches of ICA 32.

• Oculomotor cistern: this cistern resembles a sleeve covering the oculomotor nerve. It encases the nerve as it enters the cavernous sinus roof until terminating at the tip of the anterior clinoid process. It does not enter the orbital apex though the superior orbital fissure as the nerve does 32, 34, 35.

• Crural cistern: it is a subarachnoid pocket communicating anterior and posterior structures. This cistern can be found just between the optic tract and the uncus at the level of the cerebral peduncles. Anteriorly we find the oculomotor and posterior communicating cisterns, dorsally it communicates with the Sylvius cistern (over the superior edge of the optic tract), and with the ambiens cistern (posterior cerebral division). Its contents include the basal vein of Rosenthal, the anterior choroidal artery, and the medial posterior choroidal artery 6, 30.

Supratentorial unpaired

? Lamina terminalis cistern: located at the midline level of the telencephalon. This tent-shaped subarachnoid space is limited laterally by the septal area and the medial surface of the posterior gyrus rectus. The anterior limit is composed by the union of the pia mater of the lateral walls in front of the anterior communicating arteries whereas the lamina terminals forms its posterior and posterior inferior wall. The inferior wall is formed by the optic chiasm. CSF passage is permitted towards the callosal cistern above via a narrow passage surrounding the A2 segment of the Anterior Cerebral Artery near the rostrum of the Corpus Callosum. The Lamina Terminalis cistern envelops most of the components of the anterior circulating system, which includes the A1 segment and the proximal part of the A2 segment of the anterior cerebral arteries (ACA), the anterior communicating artery (ACoA), Heubner’s artery, other vessels such as the hypothalamic arteries, the origin of the fronto-orbital arteries, and the venous system of the LT are also found within the contents of this cistern. It is an important site for aneurism formation 6, 36, 37.

? Chiasmatic cistern: this cistern has the particularity that communicates with three other cisterns, the LT cistern superiorly (midline level), anterior-laterally with the Sylvian fissure (Sylvius cistern), and the interpeduncular cistern posteriorly, from which is partially separated by Liliequist’s membrane. It houses neural and vascular structures such as the hypophyseal stalk, the anterior aspect of the optic chiasm and optic nerves, the origin of the anterior cerebral arteries, and the anterior communicating vein 32, 38, 39.

? Callosal cistern: this subarachnoid pocket extends under the falx cerebri between the cerebral hemispheres above the CC. It contours the CC, thus receiving a convex shape when observed in a sagittal plane. Anteriorly it goes from the level of the rostrum all the way posteriorly over the splenium. Some authors prefer to further subdivide this cistern according to the level of which the pericallosal and callosomarginal arteries branch, into anterior (pericallosal artery, the origins of the frontopolar and callosomarginal arteries, and small anterior cerebral veins) and posterior divisions (pericallosal arteries and posterior pericallosal veins) 30, 32.

Tentorial paired

? Ambiens cistern: located in the lateral aspect of the brainstem, this cistern has a particular surgical importance that it has both supra and infratentorial extension. Divided by the superior cerebellar membrane, the superior compartment or posterior cerebral ambiens cistern, houses posterior cerebral artery, both medial and lateral posterior choroidal arteries, numerous perforating branches to the brainstem, and the basal vein of Rosenthal, whereas the inferior compartment or superior cerebellar ambiens cistern contains superior cerebellar artery and the fourth cranial nerve 6, 40, 41.

Tentorial unpaired

? Interpeduncular cistern: also known as intercrural cistern, formed by the confluence of supratentorial and infratentorial subarachnoid space; it is located between the cerebral peduncles and the posterior perforated substance, occupying the interpeduncular fossa, hence its name. it is conic shaped, containing the bifurcation of the basilar artery, peduncular segments of the posterior cerebral artery (PCA) and superior cerebellar artery (SCA) medial and lateral posterior choroidal arteries, basal vein of Rosenthal and the oculomotor nerve which travels between the superior cerebellar artery and the posterior cerebral artery 13, 32, 42.

? Quadrigeminal cistern: also considered the medial extension of the ambiens cistern; it is a site of venous confluence, characteristic that has earned it the name of “cisterna venae magnae cerebri” 43. It contains 13 vessels (different extent and portions) and the 4th cranial nerve (trochlear). The veins include the vein of Galen, internal cerebral veins, basal vein of Rosenthal, posterior pericallosal veins, atrial veins, vein of the cerebellomesencephalic fissure. Arteries include the posterior pericallosal arteries, the 3rd portion of the superior cerebellar and posterior cerebral arteries with its perforators, medial posterior choroidal artery and the lateral posterior choroidal artery 6, 28.

? Superior cerebellar cistern: containing branches of the superior cerebellar artery and the superior vermian veins, this small cistern is located just dorsally to the ambiens cistern at the level of the superior surface of the vermis 28, 32.

? Vellum interpositum cistern: This cistern can be found between the boundaries formed by the corpus callosum dorsally and the roof of the third ventricle ventrally. It extends from the splenium of CC to the foramen of Monro, between both pulvinar. It contains branches of the pericallosal artery, medial posterior choroidal arteries, and internal cerebral veins. It possesses no communication with the cerebral ventricles. 32, 44, 45.

Infratentorial paired

• Pontocerebellar cistern: with a rhomboid shape and 6 six walls, located at the pontocerebellar angle we find the pontocerebellar cistern also known as the prepontine cistern. It is an important landmark and surgical corridor for lateral and posterior approaches to infratentorial pathologies. The abducens nerve reaches the pontocerebellar cistern after perforating the AICA membrane, it courses parallel to the basilar artery. We also find the trigeminal nerve with the superior cerebellar artery running behind it. The facial and vestibulocochlear nerves can be seen at the cerebellopontine angle as they exit the brainstem from the posterolateral aspect to enter the internal acoustic meatus. Other structures found at this cistern are the venous basilar plexus, superior petrosal vein and AICA. The posterior petrous bone forms its anterior wall, the surface of the pons and cerebellum give out the posterior wall. The AICA membrane containing AICA and its perforating branches, separates the prepontine from the cerebellomedullary cistern, serving as it inferior medial wall, while the inferolateral is given by the cerebellopontine fissure. Superiorly it is limited by the superior cerebellar membrane which separates the prepontine from the ambiens cistern 29, 46.

• Cerebellomedullar cistern: considered by some authors as part of the Cisterna Magna, it actually lies above it, communicating via the cerebellomedullary fissure. Located behind the lower Clivus, it is an important structure that houses the PICA as it courses from the basilar cistern towards the cisterna magna; it also contains the glossopharyngeal, pneumogastricus, and accessory nerves as well as lateral-medullary, ponto-medullary, and transverse medullary veins. Superiorly it is limited by the AICA membrane separating it from the pontocerebellar cistern 29, 32.

• Ambiens cistern: also considered as a tentorial cistern, see description above.

Infratentorial unpaired

? Cisterna Magna: located at the midline, extending from the superior surface of the atlas to the cerebellar vermis just at the level of the pyramids. Communicates superiorly with the supracerebellar cistern, inferiorly it is connected with the 4th ventricle via the foramen of Magendie, and is continuous with the subarachnoid at the atlas through the valecullar cistern which is a compartment inside the cisterna magna formed by the PICA membrane. This membrane splits the cisterna magna into medial (valecullar cistern) and lateral (PICA cistern) compartments. The lateral compartment contains the 3rd and 4th segments of PICA, whereas its 5th segment lies inside the valecullar cistern. veins found in the cisterna magna include inferior vermian, medial posterior medullary and the vein of the cerebellomedulary fissure 6, 29, 32.

? Basilar cistern: located medially behind the clivus. Of particular importance, we find at this level, the basilar and AICA membranes, whose fusion at the supratentorial level with the oculomotor membrane gives rise to Liliequist’s membrane. Neural structures such as the hypoglossal nerve (originating at the preolivar sulcus at the anterior surface of the medulla), arteries include the origins of AICA, PICA and SCA, whereas venous circulation is given by the median anterior medullary and medial anterior mesencephalic veins coursing parallel to the basilar artery inside the cistern 29, 47.

? Supracerebellar cistern: containing terminal branches of the superior cerebellar artery and vein, and the superior vermian vein. It covers the superior vermis, communicating laterally with the ambiens cistern, ventrally with the quadrigeminal cistern and tentorium, posteriorly with the cisterna magna.

Histology

Arachnoid mater of the adult brain is composed by 2 main layers (outer and inner). The inner layer is mainly composed by loose arrangement of reticular cells with a denser cytoplasm in comparison to the outer or mesothelial layer. Small packed mitochondria and intermediate filaments are also found at this level. The extracellular space of this layer we can find small lacunae containing collagen fibers intermingled with microfibrils; it is connected to the mesothelial layer by gap junctions and desmosomes, while its inner face (in contact with the pia) is lined by elongated cells with dense nuclei, lysosomes, fewer mitochondria than its counterpart and long cytoplasmic extensions 48.
The outer or mesothelial layer is considered to be the arachnoid barrier, property given by tightly packed cells interconnected by tight junctions, although desmosomes and gap junctions can also be found. This outer layer consists of two to three layers of closely packed flattened cells. In the cytoplasm, we can find prominent Golgi apparatus, numerous mitochondria, vesicles and lysosomes (protection and barrier). The inner surface of this layer (in contact with the previously described inner layer), we find hemidesmosomes linking cells together 49-51.

Discussion (surgical anatomy approaches, treatment)

Many techniques and approaches have been described for accessing deep intracranial structures, but it is mostly through the surgical corridor given by the subarachnoid space hence the basal cisterns into which neurosurgeons navigate, mainly cerebrovascular and skullbase oriented pathologies.

Nowadays neurosurgery is focusing on new minimally invasive techniques, but without excluding classical transcranial approaches.
The approaches for the sellar area, central core, and brainstem can well be divided into 6; orbito-zygomatic and pterional, temporal and extended subtemporal, retrosigmoid and far lateral, whereas the olfactory groove, prechiasmiatic cistern, optic chiasm, entire suprasellar, para sellar, pre-and perimesencephalic cisterns, lateral, third and fourth ventricle have been gaining much appeal for an endoscopic approach 52.

For instance, the preferred approach for accessing the 3rd ventricle is now via endoscopy. Selected approaches include Precoronal Transcortical, and Transcallosal; whereas if access to the pineal region is required, a posterior fossa approach can be implemented. This could be a suboccipital transtentorial or infratentorial supracerebellar depending on the anatomic and pathologic condition of the patient 53, 54. It is important to understand the anatomy of the approach since there are important neuro-vascular structures and hypothalamic nuclei surrounding the 3rd ventricle. As described by Vinas in 1996 the best location to perforate the floor of the 3rd ventricle, a double layer arachnoid spanning from Liliequist’s membrane, is at the midline of the floor, behind the infundibular recess and in front of the mammillary bodies; communicating the 3rd ventricle with the anterior compartment of the interpeduncular cistern 37, 55.

For tuberculum sellae lesions and around the sellar and parasellar area; the endoscopic approach is often preferred by skull base neurosugeons as it provides a greater field of view and direct access to the aforementioned areas. Multiple scores can be utilized to aid in decision making between transcranial or transphenoidal approaches, for instance the one presented by Magill with grading characteristics that include tumor size, optic canal invasion and ICA involvement 56.
Characteristics of the sphenoid sinus, and clival involvement should also be taken into consideration when selecting an approach in order to prevent vascular complications mainly 57, 58.

Endoscopic access to the posterior fossa in order to treat 4th ventricle, and cerebropontine angle (CPA) lesions is gaining much ground. Keyhole retrosigmoid or burr hole over the inferior edge of foramen magnum for a telovelar approach are well described techniques in the literature, with minor morbidity, accompanied with high visibility and resection rate of lesions. Using the natural cleft of the cerebellomedullary fissure for the passage of the endoscope allowing for direct visualization of the ventricular cavity; whereas decompression of neurovascular structures and exposure of ambiens, quadrigeminal and interpeduncular cisterns can be achieved through a retroauricular incision no more than 4cm long 59-61.

Current neurosurgery is aiming towards minimalism. New endoscopic techniques are being developed and combined with classical transcranial approaches which give the neurosurgeon a better understanding of the anatomy and how to treat the pathology. Three fields of intracranial neuroendoscopy have been gaining field: endonasal transphenoidal, transventricular neuroendoscopy and endoscope assisted neurosurgery which may or may not include biportal approaches 52, 62, 63.

Conclusion

The subarachnoid space and basal cisterns offer a harmless pathway for neurosugeons, thereby good understanding of the anatomy is imperative. New neurosurgical techniques are being developed in hand with technology but this must never superimpose over the knowledge and understanding of classical approaches. A good analysis of this review will soak the neurosurgical resident and the young neurosurgeon with key concepts, anatomical landmarks, and techniques that will positively impact on the patients.

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