CHAPTER 2 Meningeal Anatomy
THE MENINGEAL COVERINGS
The brain and spinal cord are covered by layers of connective tissue called meninges, from the Greek word meninx, which means membrane. In fishes, only a single layer, the primitive meninx, is present. Amphibians and reptiles have two meningeal layers, the outer dura mater (meaning “hard mother”) and an inner, thin layer the secondary meninx. In mammals and birds, three meningeal layers are present. The pia mater (meaning “tender mother”) is thin, vascular, and closest to the brain. The arachnoid membrane, which has a spider web–like appearance, is the middle, avascular layer. The space between the pia mater and arachnoid is the subarachnoid space. The outermost layer is the dura mater, composed of two layers. Therefore, the meningeal coverings consist of three membranous layers, composed primarily of fibroblasts, varying amounts of extracellular connective tissue and one well-organized fluid-containing space. The membranes are the dura mater (pachymeninx) and the leptomeninges (arachnoid and pia mater). The use of the word mater (“mother”) to describe these membranes comes from the ancient notion that they were the origin, or mother, of all membranes in the body.1
THE LEPTOMENINGES
Leptomeninx is the term used when the pia mater and arachnoid are considered together as a functional unit and contraposed to pachymeninx (from the Greek packys, meaning thick), designates the finer meningeal coverings.2
The arachnoid is attached to the overlying dura mater. It consists of several layers of translucent cells that follow with the dura and a contingent of cells that form spindly trabeculae that bridge the subjacent space and attach to the pia mater on the surface of the brain. The subarachnoid space is bordered outside by the layer of arachnoid cells attached to the dura and on the inside by pial cells on the surface of the neural tissue. These structural relationships form the basis for the occurrence of the subarachnoid cisterns, which are dilations of the subarachnoid space containing arteries, veins, and neural structures (see Table 2-1 later).
GENERAL STRUCTURE OF THE DURA MATER: ENDOSTEAL AND MENINGEAL LAYERS
The dura is composed of an endosteal layer that faces the bone and a meningeal layer that faces the brain.3 These layers are distinguished as separate sheaths at the venous sinuses, foramen magnum, and optic canal. The meningeal layer is continuous with the dural covering of the spinal cord and optic nerves, providing tubular sheaths for the cranial nerves as they pass through the cranial foramina. These sheaths fuse with the epineurium as the cranial nerves emerge from the skull, except at the optic nerve, where the dural sheath blends into the sclera. At the vascular foramina, the meningeal layer fuses with the adventitia of the vessel. The meningeal layer folds inwards to form the falx cerebri, the tentorium cerebelli, the falx cerebelli, and the diaphragm sellae, which partially divide the cranial cavity into freely communicating spaces. The endosteal layer of dura is continuous through the cranial sutures and foramina with the pericranium and through the superior orbital fissure and optic canal with the periorbita.3
The walls of the cavernous sinus are formed by the dura lining the internal surface of the calvaria. In the lateral portion of the middle cranial fossa, the meningeal and endosteal layers are tightly adherent, but at the lateral aspect of the trigeminal nerve they are separated into two layers. At the upper border of the maxillary nerve, which is the most inferior limit of the cavernous sinus, the meningeal layer extends upward to form the outer part of the lateral wall of the cavernous sinus, and it wraps around the anterior petroclinoid fold, extending medially to form the roof of the cavernous sinus and the upper layer of the diaphragm sellae. The endosteal layer, at the upper border of the maxillary nerve and the lower margin of the carotid sulcus, divides into two layers. One layer adheres to the sphenoid bone, covering the carotid sulcus and the floor of the sella, and the other layer extends upward to constitute the internal layer of the lateral wall and roof of the cavernous sinus and diaphragm sellae. The endosteal layer invests the cranial nerves coursing in the lateral wall of the cavernous sinus. The thin layer in the sellar part of the medial wall of the cavernous sinus is thought to represent a continuation of the meningeal dural layer that faces the brain. Thus, two layers line the sellar floor and the lower surface of the pituitary gland, one that is adherent to the sphenoid bone and the other that comes from the diaphragm and wraps around the pituitary gland. Therefore, with the exception of the paired lateral aspects of the sella and pituitary gland that are covered by one layer, two layers cover the other sellar surfaces. The meningeal and endosteal layers of the lateral wall and cavernous sinus roof and diaphragm sellae continue anteriorly to line the anterior cranial fossa and posteriorly as the covering of the dorsum sellae and clivus. The meningeal layer also continues anteriorly to form the upper (distal) dural ring around the carotid artery and the optic sheath, whereas the endosteal layer continues anteriorly and medially to form the lower (proximal) dural ring around the carotid artery.4
VASCULAR ORGANIZATION OF DURA
The origin of the membranes of the skull starts when the embryo has a crown-to-rump length of 12 to 20 mm, at which time differentiation of the skull, dura mater, arachnoid, and pial membranes begins. The gradual cleavage of the vascular system into external, dural, and cerebral layers also takes place at this stage, which has been referred to as the third stage of cerebrovascular development.5 As the membranes covering the brain differentiate, the anastomosing channels that connect the deep capillary plexus with the superficial vessels close, thus separating the vessels surrounding the brain from those belonging to the skull and its coverings.5,6 The major meningeal arteries originating from this cleavage give rise to a rich anastomotic network that may enlarge after various insults7 and play a role in the genesis of dural arteriovenous malformations. This anastomotic network divides progressively into primary, secondary, and penetrating vessels.
The primary anastomotic vessels change little in diameter as they course over the dural surface and anastomose frequently with each other. They cross the superior sagittal sinus, connecting the dura over the paired cerebral hemispheres into a single vascular unit. Crossing vessels are particularly large when one middle meningeal artery is hypoplastic. The primary anastomotic arteries have a straight course and measure 100 to 300 μm in diameter, whereas the main meningeal feeders have a diameter of 400 to 800 μm. The primary anastomotic arteries give rise to arteries to the skull, secondary anastomotic arteries, penetrating dural vessels, and arteriovenous shunts.8
Secondary anastomotic arteries also lie on the outer dural surface. They measure 20 to 40 microns in diameter, are short, and their anastomotic pattern form a regular polygonal network.8 Penetrating vessels arise from primary and secondary anastomotic arteries, leave the dural surface and extend to within 5 to 15 μm of inner and juxta-arachnoid surface of dura, to end in the capillary network. Capillaries, 8 to 12 μm in diameter, are present throughout dura, including the falx and tentorium, and are especially rich parasagittally, where they may form several layers. The capillary bed is located on the inner or cerebral surface of dura and is separated from arachnoid by only a few microns.8
Overview of Dural Supply
The dural arteries arise from the internal and external carotid, vertebral, and basilar arteries (Table 2-1) and may be the site of formation of saccular aneurysms, pseudoaneurysms, and arteriovenous fistulas and the source of traumatic and spontaneous hemorrhage into the epidural, subdural, and intraparenchymal area, in addition to the well known role in the vascularization of meningiomas, other tumors, and parenchymal arteriovenous malformations (AVMs).
The dura covering the anterior fossa floor draws its supply from the anterior and posterior ethmoidal arteries, the superficial recurrent ophthalmic artery, and the middle meningeal artery (Fig. 2-1). The middle meningeal artery will not contribute to the supply of the dura lining the floor of anterior fossa if the artery or its anterior branch arises from the ophthalmic arterial system. The territory of the anterior convexity and parasagittal area is supplied by both the anterior branch of the middle meningeal artery and the anterior meningeal branch from the ophthalmic artery (Fig. 2-2).
The supply to middle fossa and paracavernous dura derives laterally from the middle meningeal, accessory meningeal, and ascending pharyngeal arteries. In an anterior to posterior direction, it receives contributions from the recurrent branches of the ophthalmic and lacrimal arteries, as well as from the medial tentorial artery (Figs. 2-1 and 2-3). Medially those arteries anastomose with the cavernous branches of the internal carotid artery. In this system, dominance of a particular vessel can lead to unusual anatomic variants. The sellar dura has a bilateral supply from the paired capsular, inferior hypophyseal, medial clival, and dorsal meningeal arteries that anastomose across the midline in front and behind the dorsum sellae9,10 (Figs. 2-1, 2-3, and 2-4). The inferior hypophyseal artery can supply pituitary adenomas and tumors of the sphenoid sinus.11–13
The convexity dura is supplied predominantly by branches of the middle meningeal arteries. These branches course toward the superior sagittal sinus, where they are distributed to the sinus walls and give off descending branches to the adjacent falx cerebri. The scalp arteries, through the emissary foramina, also send branches to the convexity dura. The dura over the frontal convexity is supplied by the anterior meningeal branch of the anterior ethmoidal artery and branches of the anterior division of the middle meningeal artery that also distributes to the dura in the anterior parietal region. The dura over the posterior convexity is supplied by the parieto-occipital an petrosquamosal branches of the posterior division of the middle meningeal artery.9,10 This area also receives a contribution from the posterior meningeal branch of the vertebral artery, when this vessel extends above the torcular14 (see Fig. 2-2).
The falx cerebri, falx cerebelli, and tentorium are supplied by basal and convexity branches of the meningeal arteries and receive a contribution from the cerebral arteries, making these structures an anastomotic pathway between dural and parenchymal arteries. Most of the vascular supply of the falx cerebri comes through its insertion on the vault, with the anterior basal insertion, the falcotentorial angle, and the free margin receiving independent contributions15 (Figs. 2-3 and 2-5). The dural walls of the superior sagittal sinus, the site of insertion of the falx on the dura of the convexity, are supplied by the middle meningeal arteries, which form two paramedial arcades, and are reinforced anteriorly, at the level of the insertion of the falx on the crista galli, by the anterior falcine arteries (see Fig. 2-5).
Posteriorly, at the falcotentorial junction, the paramedial arcades are reinforced from three sources: the posterior meningeal artery from the vertebral artery, medial tentorial artery from the cavernous carotid, and an occasional branch of the posterior cerebral artery. The posterior meningeal artery, the major contributor, extends along the insertion of the falx cerebri after coursing into the insertion of the falx cerebelli. The medial tentorial artery, which supplies the medial third of the tentorium, reaches the straight sinus and torcular and may ascend in the posterior portion of the falx cerebri9,10 (see Fig. 2-5). The pericallosal branches of the anterior cerebral artery may also pierce the falx at or near its free edge to reinforce the arterial network along the deep edge of the falx.
The tentorium receives supratentorial and infratentorial contributions (Figs. 2-3, 2-5, 2-6). The supratentorial sources are the marginal and lateral tentorial branches of the cavernous carotid medially and the branches of the middle meningeal artery anterolaterally. The infratentorial components are the superior extensions of the jugular branch of the ascending pharyngeal artery and the tentorial branch of the posterior cerebral artery medially, the occipital artery laterally, and the posterior meningeal artery posteriorly (see Fig. 2-3). The lateral two thirds of the tentorium and its edge along the transverse sinus derive their supply mainly from two arterial arcades, petrosal and occipital. The petrosal arcade follows the superior petrosal sinus and is composed of the lateral tentorial artery, branches from the petrous and petrosquamosal trunk of the middle meningeal artery, and the lateral branch of the dorsal meningeal artery. The occipital arcade is composed above the tentorium by the petrosquamosal trunk and occipital branchs of the middle meningeal artery, and the occipital and posterior meningeal arteries form its infratentorial limb9,10 (see Fig. 2-6). The medial third of the tentorium is supplied by the medial tentorial artery from the internal carotid artery. This artery may receive a contribution from the posterior cerebral artery through the artery of Davidoff and Schechter (see Figs. 2-3 and 2-6).
The clival area derives its supply from the medial clival and dorsal meningeal, branches of the internal carotid artery, the anterior meningeal branch of the vertebral artery, and branches of the ascending pharyngeal artery. The dura over the posterior surface of the petrous bone is supplied by the dorsal meningeal and subarcuate arteries and branches of the middle meningeal, occipital, and ascending pharyngeal arteries (see Figs. 2-1 and 2-6). The dura of the lateral portion of the cerebellar fossa receives its supply from the ascending pharyngeal, occipital, and vertebral arteries. The posterior meningeal artery is the major supplier of the paramedial and medial portions of the cerebellar dura, but this area also receives contributions from the middle meningeal and occipital branches to the region of the torcular (Fig. 2-7).
In this discussion, the dura of the posterior fossa has been subdivided into several areas. The clival dura extends from the dorsum sellae to the anterior border of foramen magnum and is limited laterally by the petroclival fissure. The posterior petrous dura extends from the petroclival fissure to the sigmoid and superior petrosal sinuses. The cerebellar fossa dura is limited laterally by the sigmoid sinuses and extends over the cerebellar surface from the transverse sinus to the foramen magnum. The dura on each side of the midline has been further subdivided into a medial region, adjacent to the falx cerebelli; a lateral region, adjacent to the sigmoid sinus; and a paramedial region between the two. At the level of the foramen magnum, the dural supply arises predominantly from the external carotid and vertebral arteries16 (see Fig. 2-6). The anterior and posterior meningeal arteries, branches of the vertebral artery, anastomose with the jugular and hypoglossal branches of the ascending pharyngeal artery and the mastoid branch of the occipital artery. The cavernous carotid may also contribute through the clival branches of the dorsal meningeal arteries.12 The dural branches of the vertebral artery are usually small but may enlarge to supply dura-based lesions. Enlargement of the anterior meningeal artery is seen with meningiomas, glomus jugulare tumors, recurrent hemangioblastomas, and metastatic tumors.17
Dural territories often have overlapping supply from several sources. A reciprocal relationship between the territories of adjacent arteries is common so that when the area supplied from one source is small another artery enlarges to supply the area. This reinforces the need to see all possible sources of supply to a lesion before any surgical or endovascular treatment. Areas supplied from several overlapping sources are the tentorium and adjacent falx, the walls of the cavernous sinus, and the dura around the gasserian ganglion.18
Dural Arteries
External carotid artery branches
Ascending pharyngeal artery
The ascending pharyngeal artery, the smallest branch of the external carotid artery, usually arises from the proximal portion of the external carotid artery. It has an ascending vertical course, along the posterolateral wall of pharynx, anterior to the longus capitis muscle, and medial to the styloglossus and stylopharyngeus muscles (Fig. 2-8A, B). This initial segment of the artery can be seen, in the lateral angiogram, in front of the vertebral column, and medial to the main external carotid trunk on the anteroposterior view.
The meningeal contribution of the ascending pharyngeal artery is via three branches: hypoglossal, jugular, and carotid (see Fig. 2-8A). The hypoglossal and jugular branches, the more constant, originate from the posterior division,10 and the carotid branch from the anterior division (Fig. 2-8C–G). The hypoglossal branch accompanies the hypoglossal nerve and enters the skull through the hypoglossal (anterior condylar) canal, to be distributed to the dura surrounding the foramen magnum and clivus, where it anastomoses with the branches arising from the ipsilateral cavernous carotid and vertebral arteries, and its mate from the opposite side. The hypoglossal artery may also arise from the vertebral artery (see Fig. 2-8G). The area of supply of the hypoglossal branch (see Figs. 2-1, 2-6, and 2-7) may extend to the dura of the lateral portion of the cerebellar fossae, where it borders and has a reciprocal relationship with the territory supplied by the mastoid branch of the occipital artery and the posterior meningeal artery of the vertebral artery. In the clival area it may anastomose superiorly with the medial clival branch of the inferior hypophyseal artery and the dorsal meningeal artery and inferiorly with the anterior meningeal artery of the vertebral artery.9,10
The jugular branch enters the jugular foramen with cranial nerves IX, X, and XI, where it divides into medial and lateral branches. The lateral branch courses along the dural wall of the sigmoid sinus (see Fig. 2-8D), where it anastomoses with the jugular branch of the occipital artery (Fig. 2-9). The medial branch courses along and supplies the dura bordering the inferior petrosal sinus. Its territory (see Figs. 2-1, 2-6, and 2-7) borders the area supplied by the dorsal meningeal artery and medial clival artery from the cavernous carotid. Superiorly, it anastomoses with the subarcuate artery and the petrosquamosal branch of the middle meningeal artery and laterally with the mastoid branches of the occipital artery. The jugular branch distal to the jugular foramen supplies the dura facing the inferior part of the cerebellopontine angle9,10 (see Fig. 2-6). The hypoglossal and jugular branches also supply of the adjacent segments of cranial nerves IX through XII.10,19,20 On lateral angiograms, the posterior division of the ascending pharyngeal artery ascends besides and overlaps the foramen magnum. On anteroposterior views, the hypoglossal is the most medial of the terminal branches of the posterior division.
The carotid ramus originates from the anterior branch of the ascending pharyngeal artery. It courses in the periosteal lining of the carotid canal and anastomoses, at the level of the foramen lacerum, with branches arising from the carotid siphon9,10 to form the recurrent artery of the foramen lacerum. This recurrent artery also anastomoses at the lower edge of the trigeminal ganglion with the posterior branch of the inferolateral trunk and the cavernous branch of the middle meningeal artery. The carotid branch usually does not extend to the dura of clivus and cerebellopontine angle as do the other dural branches of the ascending pharyngeal artery.9,10 The recurrent artery of foramen lacerum may be involved in the supply of angiomas, lymphoid tumors, angiofibromas of the nasopharynx, and tumors of the cavernous sinus and caroticocavernous fistulas.9,10
Occipital artery
The occipital artery originates from the posterior surface of the external carotid artery, at the level of the angle of the mandible, and courses posteriorly and upward, being crossed superficially by the hypoglossal nerve. It passes deep to the posterior belly of the digastric muscle and lateral to the internal jugular vein, vagus nerve, internal carotid artery, and accessory nerve (see Fig. 2-9A). At the level of a vertical plane crossing the posterior border of the external auditory canal, the occipital artery can be found in a tunnel formed above by the occipital groove of the temporal bone—a prominent sulcus on the undersurface of the temporal bone, medial to the digastric groove—medially by the attachment of the superior oblique muscle on the transverse process of atlas, and laterally by the cranial insertion of the posterior belly of the digastric muscle in the digastric groove (see Fig. 2-9B–F). The presence of the occipital groove is dependent on whether the artery courses superficial or deep the longissimus capitis muscle. The groove is present if the artery courses deep to the longissimus capitis muscle along the lower surface of the skull base and is absent if the artery courses inferior to the skull base or lateral to the longissimus capitis muscle (see Fig. 2-9E–G).12
The occipital artery at the level of the posterior border of the upper insertion of the longissimus capitis muscle courses in the upper part of the space between the occipital bone and C1 and lateral to the rectus capitis posterior major and semispinalis capitis muscle. It is covered by a deeper layer formed by the splenius capitis muscle and a more superficial layer formed, from lateral to medial, by the sternocleidomastoid and trapezius. The occipital artery pierces the fascia between the trapezius and sternocleidomastoid, near the superior nuchal line and ascends in the superficial fascia of the scalp, where it is accompanied by the greater occipital nerve (see Fig. 2-9H).
The occipital artery gives rise to the auricular branch, which anastomoses with the posterior auricular artery behind the ear; the stylomastoid artery, muscular branches to the sternocleidomastoid, digastric, stylohyoid, splenius, and longissimus capitis muscles; and meningeal branches to the posterior fossa that enter the skull through the jugular foramen and condylar canal and to inconstant branches that runs through the mastoid foramen (see Fig. 2-9B, D, G).
The occipital artery is divided into three portions: (1) ascending cervical, (2) cervico-occipital or horizontal, and (3) ascending occipital21 (see Fig. 2-9A). The meningeal branches most frequently originate from the second and third arterial segments.
The mastoid branch, present in about one half of specimens21 (see Fig. 2-9B, D, G), also called the transmastoid branch or the artery of the mastoid foramen,3,9,10 originates from the second segment of occipital artery, at the level of the insertion of the semispinalis capitis muscle, midway between the inferior and superior nuchal lines. From its origin, the mastoid branch courses between the splenius capitis muscle and the junction of the mastoid and occipital bones. It enters the cranial cavity at the level of the superior nuchal line, by passing through the mastoid foramen. Intracranially, the superior nuchal line corresponds to the level of the transverse sinus. The mastoid branch emerges intracranially at the posterior border of the upper end of the sigmoid sinus and divides into three groups of branches: descending, ascending, and posteromedial.21 The descending branches are directed toward the jugular foramen and border the dural territory supplied by the jugular branch of the ascending pharyngeal artery (see Fig. 2-8D). The posteromedial branches anastomose with the petrosquamous branch of the middle meningeal artery and constitute the main supply to the lateral part of the cerebellar fossae that borders the territory of the hypoglossal branch of the ascending pharyngeal artery or the posterior meningeal branch of the vertebral artery, or both. The ascending branches, which are directed to the dura covering the superior part of the posterior surface of the temporal bone that faces the cerebellopontine angle, anastomoses with the subarcuate branch of the anterior inferior cerebellar artery (see Figs. 2-1 and 2-6), and can supply acoustic neurinomas, meningiomas, and arteriovenous fistulas. The mastoid branches also supply the endolymphatic duct and sac.22
The third or ascending occipital portion gives rise to the terminal branches of the occipital artery, which supply the musculocutaneous structures of the posterior portion of the cranial vault, and anastomoses with the branches of the superficial temporal artery (see Fig. 2-9H). The parietal foramen (see Fig. 2-9J), which is an inconstant opening located near the sagittal suture, about 3 to 5 cm in front of the lambda,3 transmits a meningeal branch of the ascending occipital segment and a small emissary vein.21