Cranial Meninges

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Chapter 4 Cranial Meninges

The brain and spinal cord are entirely enveloped by three concentric membranes, the meninges, which provide support and protection. The outermost meningeal layer is the dura mater (pachymeninx). Beneath this lies the arachnoid mater. The innermost layer is the pia mater. The dura is an opaque, tough, fibrous coat. It incompletely divides the cranial cavity into compartments and accommodates the dural venous sinuses. It is separated from the arachnoid by a narrow subdural space. The arachnoid mater and pia mater are sometimes referred to collectively as the leptomeninges, and they share many similarities. The arachnoid is much thinner than the dura and is mostly translucent. It surrounds the brain loosely, spanning depressions and concavities. Beneath the arachnoid lies the subarachnoid space, which contains cerebrospinal fluid (CSF), secreted by the choroid plexuses of the cerebroventricular system. The pia mater is a transparent, microscopically thin membrane that follows the contours of the brain and is closely adherent to its surface. The subarachnoid space varies greatly in depth, and the larger expanses are termed subarachnoid cisterns. CSF circulates within the subarachnoid space and is reabsorbed into the venous system through arachnoid villi and granulations associated with the dural venous sinuses. Cranial and spinal meninges are continuous through the foramen magnum. Only the cranial meninges are described in this chapter.

Dura Mater

The dura mater is a thick, dense, fibrous membrane composed of densely packed fascicles of collagen fibres arranged in laminae. The fascicles run in different directions in adjacent laminae, producing a lattice-like appearance. This is particularly obvious in the tentorium cerebelli and around the defects or perforations that sometimes occur in the anterior portion of the falx cerebri. There is little histological difference between the endosteal and meningeal layers of the dura. The dura is largely acellular, but it contains fibroblasts, which are distributed throughout, and osteoblasts, which are confined to the endosteal layer. Focal calcification may occur in the falx cerebri.

The cranial dura differs from the spinal dura mainly in its relationship to the surrounding bones. The cranial dura lines the cranial cavity. It is composed of two layers: an inner, or meningeal, layer and an outer, or endosteal, layer. They are united except where they separate to enclose the venous sinuses that drain blood from the brain. The dura mater adheres to the internal surfaces of the cranial bones, and fibrous bands pass from it into the bones. Adhesion of the dura to the bones is firmest at the sutures, at the cranial base and around the foramen magnum. In children it is difficult to remove the dura from the suture lines, but in adults the dura becomes separated from the suture lines as they fuse. With increasing age the dura becomes thicker, less pliable and more firmly adherent to the inner surface of the skull, particularly that of the calvaria. The endosteal layer of the dura is continuous with the pericranium through the cranial sutures and foramina and with the orbital periosteum through the superior orbital fissure. The meningeal layer provides tubular sheaths for the cranial nerves as they pass out through the cranial foramina, and these sheaths fuse with the epineurium as the nerves emerge from the skull. The dural sheath of the optic nerve is continuous with the ocular sclera. At sites where major vessels, such as the internal carotid and vertebral arteries, pierce the dura to enter the cranial cavity, the dura is firmly fused with the adventitia of the vessels.

The inner aspect of the dura mater is closely applied to the arachnoid mater over the surface of the brain. They are easily separated, however, and are physically joined only at sites where veins pass from the brain into venous sinuses (e.g. superior sagittal sinus) or where they connect the brain to the dura (e.g. anterior pole of the temporal lobe).

The anatomical organization of the dura and its relationships to the major venous sinuses, sutures and blood vessels have significant pathological implications. In the case of head trauma, separation of the dura from the underlying periosteum requires significant force; consequently, this occurs only when high-pressure arterial bleeding occurs into the virtual space. This can result from damage to any arterial vessel, commonly following skull fracture. The classic site for such injury is along the course of the middle meningeal artery, where a direct blow causing a bone fracture can rupture the artery and cause rapid collection of an extradural haematoma. The haematoma is under considerable pressure due to the arterial blood pressure feeding it and the resistance of the strong adhesion between the dura and the periosteum. As a result of these factors, an extradural haematoma acts as a rapidly expanding intracranial mass lesion and poses a classic medical emergency requiring immediate diagnosis and surgery.

CASE 1 EPIDURAL HAEMATOMA

An 18-year-old boy is involved in a high-speed motor vehicle accident. He is an unrestrained passenger in the front seat. When the paramedics arrive he is awake and conversant but mildly disoriented. He is transported to the local hospital for evaluation. In the emergency department (ED) he becomes progressively lethargic, cannot follow commands and develops a right hemiparesis. He is sent for a computed tomography (CT) scan of the head. On his return to the ED he is unconscious, requiring intubation and mechanical ventilation. The CT scan demonstrates a large epidural haematoma (EDH) on the left, with mass effect on the cerebral hemisphere. He is taken to the operating room for emergent evacuation of the haematoma.

Discussion: EDH occurs most often in adolescents and young adults. The most common cause is closed head injury sustained in a traffic accident, fall or assault. A skull fracture may be present in 75% to 95% of cases. The majority of EDHs are caused by arterial injury, usually the middle meningeal artery; however, they may also be caused by injury to the anterior meningeal artery, dural venous sinuses or vascular malformation.

The presentation of EDH may be variable, depending on the severity of the initial injury. It can range from transient loss of consciousness in mild cases to coma associated with severe head trauma. A commonly observed pattern is the so-called lucid interval: the patient is conscious after the initial injury but deteriorates over the course of a few hours due to increasing intracranial pressure from continued haematoma growth. Associated symptoms may include headache, nausea, vomiting, lethargy, confusion, aphasia, hemiparesis and seizures.

An EDH can readily be seen on an unenhanced head CT scan and typically has a lens-shaped appearance, as it lies in the potential space between the dura and the calvaria (Fig. 4.1). It does not cross the cranial suture lines because at those locations the dura is tightly adherent to the skull. Emergency surgery is required in most cases to relieve the pressure caused by the haematoma and, if possible, identify the source of bleeding.

Dural Partitions

The meningeal layer of the dura is reflected inward to form four septa that partially divide the cranial cavity into compartments in which subdivisions of the brain are lodged.

Falx Cerebri

The falx cerebri is a strong, crescent-shaped sheet of dura mater lying in the sagittal plane and occupying the great longitudinal fissure between the two cerebral hemispheres (Figs. 4.2, 4.3). The crescent is narrow in front, where the falx is fixed to the crista galli, and broad behind, where it blends into the midline with the tentorium cerebelli. The anterior part of the falx is thin and may have a number of irregular perforations (see Fig. 4.2). Its convex upper margin is attached to the internal cranial surface on each side of the midline, as far back as the internal occipital protuberance. The superior sagittal sinus runs within the dura along this margin, in a cranial groove, and the falx is attached to the lips of this groove. At its lower edge, the falx is free and concave and contains the inferior sagittal sinus. The straight sinus runs along the line of attachment of the falx to the tentorium cerebelli (see Fig. 4.2).

Tentorium Cerebelli

The tentorium cerebelli (Figs. 4.24.4) is a sheet of dura mater with a peaked configuration reminiscent of a single-poled tent, from which its name is derived. It covers the cerebellum and passes under the occipital lobes of the cerebral hemispheres. Its concave anterior edge is free; between it and the dorsum sellae of the sphenoid bone is a large curved hiatus (the tentorial incisure or notch), which is occupied by the midbrain and the anterior part of the superior aspect of the cerebellar vermis. The tentorium divides the cranial cavity into supratentorial and infratentorial compartments that contain the forebrain and hindbrain, respectively. The convex outer limit of the tentorium is attached posteriorly to the lips of the transverse sulci of the occipital bone and the posteroinferior angles of the parietal bones, where it encloses the transverse sinuses. Laterally, the tentorium is attached to the superior borders of the petrous temporal bones, where it contains the superior petrosal sinuses (see Fig. 4.3). Near the apex of the petrous temporal bone, the lower layer of the tentorium is evaginated anterolaterally under the superior petrosal sinus to form a recess between the endosteal and meningeal layers in the middle cranial fossa. This recess is the trigeminal cave (Meckel’s cave) and contains the roots and ganglion of the trigeminal nerve. The evaginated meningeal layer fuses in front with the anterior part of the trigeminal ganglion. At the apex of the petrous temporal bone, the free border and attached periphery of the tentorium cross each other (see Fig. 4.4). The anterior ends of the free border are fixed to the anterior clinoid processes, and the attached periphery is fixed to the posterior clinoid processes. The oculomotor nerve lies in the groove between them on each side.

Diaphragma Sellae

The diaphragma sellae (see Fig. 4.2) is a small, circular, horizontal sheet of dura mater that forms a roof to the sella turcica and, in many cases, almost completely covers the pituitary gland (hypophysis). The central opening in the diaphragma allows the infundibulum and pituitary stalk to pass into the pituitary fossa. There is wide individual variation in the size of the central opening. The diaphragma sellae was an important landmark in pituitary surgery in the past—extension of a pituitary tumour above it was an indication for a subfrontal approach through a craniotomy. A transsphenoidal approach is currently preferred, irrespective of whether there is suprasellar extension.

The arrangement of the dura mater in the central part of the middle cranial fossa is complex (see Fig. 4.4). The tentorium cerebelli forms a large part of the floor of the middle cranial fossa and fills much of the gap between the ridges of the petrous temporal bones. On both sides, the rim of the tentorial incisure is attached to the apex of the petrous temporal bone and continues forward as a ridge of dura mater to attach to the anterior clinoid process. This ridge marks the junction of the roof and the lateral part of the cavernous sinus (Figs. 4.5, 4.6). The periphery of the tentorium cerebelli is attached to the superior border of the petrous temporal bone, crosses under the free border of the tentorial incisure and continues forward to the posterior clinoid processes as a rounded, indefinite ridge of the dura mater. Thus, an angular depression exists between the anterior parts of the peripheral attachment of the tentorium and the free border of the tentorial incisure (see Figs. 4.2, 4.4). This depression in the dura mater is part of the roof of the cavernous sinus and is pierced in front by the oculomotor nerve and behind by the trochlear nerve, which proceed anteroinferiorly into the lateral wall of the cavernous sinus (Fig. 4.7). In the anteromedial part of the middle cranial fossa, the dura mater ascends as the lateral wall of the cavernous sinus. It reaches the ridge produced by the anterior continuation of the free border of the tentorium and runs medially as the roof of the cavernous sinus, where it is pierced by the internal carotid artery (see Figs. 4.2, 4.4). Medially, the roof of the sinus is continuous with the upper layer of the diaphragma sellae. At or just below the opening in the diaphragma for the infundibulum and pituitary stalk, the dura, arachnoid and pia mater blend with one another and with the capsule of the pituitary gland. It is not possible to distinguish the layers of the meninges within the sella turcica, and the subarachnoid space is obliterated.

Through its projections as the falx cerebri and tentorium cerebelli, the dura may act to stabilize the brain within the cranial cavity. However, this arrangement causes problems when there is focal brain swelling or a focal space-occupying lesion within the brain or cranial cavity. Consequently, herniation of the brain may occur under the falx cerebri or, more significantly, through the tentorial incisure, which compresses the oculomotor nerve, midbrain and arteries on the inferomedial surface of the temporal lobe. This process of transtentorial coning is particularly dangerous because of the risk of secondary vascular compression, and it often represents the terminal event in patients with evolving supratentorial space-occupying lesions. Similarly, space-occupying lesions in the small infratentorial compartment may cause upward herniation through the tentorial hiatus or downward herniation through the foramen magnum.

Dural Venous Sinuses

Dural venous sinuses (see Fig. 6.16) are a complex of venous channels that lie between the two layers of dura mater, draining blood from the brain and cranial bones. They are lined by endothelium and have no valves; their walls are devoid of muscular tissue. Developmentally, the venous sinuses emerge as venous plexuses, and most sinuses preserve a plexiform arrangement to a variable degree rather than being simple vessels with a single lumen. Browder and Kaplan (1976) examined human venous sinuses in hundreds of corrosion casts and observed vascular plexuses adjoining the superior and inferior sagittal and straight sinuses and, with a lower incidence, the transverse sinuses. There was much individual variation, and departures from ‘average’ patterns were frequent in early life; for example, in infancy, the falx cerebelli may contain large plexiform channels and venous lacunae, augmenting the occipital sinus. These variations cannot be detailed in a general text. They must be established on an individual basis by angiography when the clinical necessity arises. However, it is important to emphasize the wide variation possible in the structure of cranial venous sinuses, together with their plexiform nature and wide connections with cerebral and cerebellar veins. Another kind of connection has been shown experimentally. Parts of sinuses (and even diploic veins) can be filled by forcible internal carotid injection, suggesting the existence of arteriovenous shunts (Browder and Kaplan 1976). A connection between the middle meningeal arteries and the superior sagittal sinus has been demonstrated in this way, although the sites of communication are unknown.

Superior Sagittal Sinus

The superior sagittal sinus runs in the attached, convex margin of the falx cerebri; it grooves the internal surface of the frontal bone, the adjacent margins of the two parietal bones and the squamous part of the occipital bone (Fig. 4.8; see also Figs. 4.2, 6.16). It begins near the crista galli, a few millimetres posterior to the foramen caecum, and receives primary tributaries from cortical veins of the frontal lobes, the ascending frontal veins. Narrow anteriorly, the sinus runs backward, gradually widening to approximately 1 cm. Near the internal occipital protuberance it deviates, usually to the right, and continues as a transverse sinus. Triangular in cross-section, the interior of the superior sagittal sinus possesses the openings of superior cerebral veins and projecting arachnoid granulations. It is traversed by many fibrous bands. It also communicates by small orifices with irregular venous lacunae, situated in the dura mater near the sinus. There are usually two or three of these on each side—a small frontal, a large parietal and an intermediate-sized occipital. In the elderly, the lacunae tend to become confluent, so there is one elongated lacuna on each side. Fine fibrous bands cross them, and numerous arachnoid granulations project into them. The superior sagittal sinus receives the superior cerebral veins and, near the posterior end of the sagittal suture, veins from the pericranium, which pass through the parietal foramina. The lacunae also drain the diploic veins and meningeal veins.

Lateral lacunae are often so complex that they are almost plexiform; they are rarely simple venous spaces. Plexiform arrays of small veins adjoin the sagittal, transverse and straight sinuses, and ridges of such ‘spongy’ venous tissue often project into the lumina of the superior sagittal and transverse sinuses. The superior sagittal sinus is also invaded, in its intermediate third, by variable bands and projections from its dural walls, which extend as horizontal shelves that divide its lumen into superior and inferior channels. Such variable features make it impossible to give a simple description of this or other venous sinuses, and individual variations can be shown only by radiological investigations.

The dilated posterior end of the superior sagittal sinus is referred to as the confluence of the sinuses (see Fig. 4.4). This is situated to one side (usually the right) of the internal occipital protuberance, where the superior sagittal sinus turns to become a transverse sinus. It also connects with the occipital and contralateral transverse sinus. The size and degree of communication of the channels meeting at the confluence are highly variable. In more than half of subjects, all venous channels that converge toward the occiput interconnect, including the straight and occipital sinuses. In many instances, however, communication is absent or tenuous. Any sinus involved may be duplicated, narrowed or widened near the confluence.

CASE 2 SUPERIOR SAGITTAL SINUS THROMBOSIS

A 41-year-old woman, previously well, has purulent frontal sinusitis. She complains of increasingly severe headache and has evidence of increased intracranial pressure, with papilledema but no focal neurological signs. After several days she becomes lethargic and abruptly develops a right hemiparesis with aphasia, with repeated focal seizures involving the left side. She is septic at that juncture. Her spinal fluid contains a moderate pleocytosis and several thousand erythocytes per cubic millimetre, with a normal sugar content.

CT scan of the head demonstrates bilateral venous infarctions involving most prominently the left cerebral hemisphere. Magnetic resonance imaging (MRI) documents obstruction of the superior sagittal sinus (Fig. 4.9).

Discussion: This woman has thrombosis of the superior sagittal sinus secondary to spread of infection from her frontal sinus. (Such infection may also spread from a focus of osteomyelitis.) Non-septic thrombosis may result from invasion of the superior sagittal sinus by tumour, but it has also been associated with a host of systemic and neurological disorders. In some cases, no recognizable cause can be identified. Initially, as in this patient, there may be no focal neurological signs. However, many patients develop occlusion of the draining cerebral veins, with resultant venous infarction (and haemorrhagic spinal fluid) and recurrent focal seizures, along with appropriate neurological signs.

Inferior Sagittal Sinus

The inferior sagittal sinus is located in the posterior half or two-thirds of the free margin of the falx cerebri (see Fig. 4.2). It increases in size posteriorly and ends in the straight sinus. It receives veins from the falx and sometimes from the medial surfaces of the cerebral hemispheres.

Straight Sinus

The straight sinus lies in the junction of the falx cerebri and tentorium cerebelli (see Figs. 4.2, 4.4). It runs posteroinferiorly as a continuation of the inferior sagittal sinus into the transverse sinus. It is not continuous (or only tenuously so) with the superior sagittal sinus. Its tributaries include the great cerebral vein (see Figs. 4.2, 6.16) and some superior cerebellar veins. Internally, the straight sinus is triangular in cross-section.

Transverse Sinus

The transverse sinuses begin at the internal occipital protuberance (see Figs. 4.4, 4.5). One of them, usually the right, is directly continuous with the superior sagittal sinus; the other is continuous with the straight sinus. On both sides the sinuses run in the attached margin of the tentorium cerebelli, first on the squama of the occipital bone, then on the mastoid angle of the parietal bone. Each follows a gentle anterolateral curve, increasing in size as it does so, to the posterolateral part of the petrous temporal bone. There it turns down as a sigmoid sinus, which ultimately becomes continuous with the internal jugular vein. Transverse sinuses are triangular in section and usually unequal in size; the one draining the superior sagittal sinus is larger. They receive the inferior cerebral, inferior cerebellar, diploic and inferior anastomotic veins and are joined by the superior petrosal sinuses, where they continue as sigmoid sinuses.

Sigmoid Sinus

The sigmoid sinuses are continuations of the transverse sinuses, beginning where these leave the tentorium cerebelli (Figs. 4.5, 4.10). Each sigmoid sinus curves inferomedially in a groove on the mastoid process of the temporal bone, crosses the jugular process of the occipital bone and turns forward to the superior jugular bulb, lying posterior in the jugular foramen. Anteriorly, a thin plate of bone separates its upper part from the mastoid antrum and air cells. It connects with pericranial veins via mastoid and condylar emissary veins.

Occipital Sinus

The occipital sinus is the smallest of the sinuses. It lies in the attached margin of the falx cerebelli (see Fig. 4.5) and is occasionally paired. It commences near the foramen magnum in several small channels, one joining the end of the sigmoid sinus, and connects with the internal vertebral plexuses. It ends in the confluence of the sinuses.

Cavernous Sinus

The cavernous sinus is a large venous plexus that lies on both sides of the body of the sphenoid bone (see Figs. 4.54.7). The sinus extends from the superior orbital fissure to the apex of the petrous temporal bone, with an average length of 2 cm and a width of 1 cm. The sphenoidal air sinus and pituitary gland are medial to the cavernous sinus. The trigeminal cave is near the inferoposterior part of its lateral wall and extends posteriorly beyond it to enclose the trigeminal ganglion. The uncus of the temporal lobe is also lateral to the sinus.

The internal carotid artery, and its associated sympathetic plexus, passes forward through the sinus together with the abducens nerve, which lies lateral to the artery. The oculomotor and trochlear nerves and the ophthalmic and maxillary divisions of the trigeminal nerve all lie in the lateral wall of the sinus (see Fig. 4.7). Their diameters are such that they project into the lumen and are usually covered medially by little more than endothelium. Propulsion of blood in the cavernous sinus is partly due to pulsation of the internal carotid artery, but it is also influenced by gravity and hence by the position of the head.

Tributaries of the cavernous sinus are the superior ophthalmic vein, a branch from the inferior ophthalmic vein (or sometimes the whole vessel), the superficial middle cerebral vein, inferior cerebral veins and sphenoparietal sinus. The central retinal vein and frontal tributary of the middle meningeal vein sometimes drain into it. The sinus drains to the transverse sinus via the superior petrosal sinus; to the internal jugular vein via the inferior petrosal sinus and a plexus of veins on the internal carotid artery; to the pterygoid plexus by veins traversing the emissary sphenoidal foramen, foramen ovale and foramen lacerum; and to the facial vein via the superior ophthalmic vein.

Carotid cavernous fistula and cavernous sinus thrombosis

The unique location of the internal carotid artery within a venous structure occasionally gives rise to direct communication between the two structures by means of a carotid cavernous fistula (CCF), which is established as a result of either severe head trauma or degenerative or aneurysmal vessel disease (see Chapter 6, Case 3). A CCF causes proptosis, which may be pulsatile, together with vascular dilatation in the tissues of the orbit and globe and combinations of third, fourth and sixth cranial nerve palsies. These changes can cause permanent blindness. CCFs are most commonly treated by passing a catheter up the carotid into the fistula and then occluding it with dilatable balloons or flexible metal coils. Any spreading infection involving the upper nasal cavities, paranasal sinuses, cheek (especially near the medial canthus), upper lip, anterior nares or even upper incisor or canine tooth may rarely lead to septic thrombosis of the cavernous sinuses as infected thrombi pass from the facial vein or pterygoid venous complex into the sinus (via either ophthalmic veins or emissary veins that enter the cranial cavity through the foramen ovale). This is a critical medical emergency with a high risk of disseminated cerebritis and cerebral venous thrombosis (see Case 2).

Intercavernous Sinus

The two cavernous sinuses are connected by anterior and posterior intercavernous sinuses (see Fig. 4.5) and the basilar plexus (see Fig. 4.6). The intercavernous sinuses lie in the anterior and posterior attached borders of the diaphragma sellae, thus forming a complete circular venous sinus (see Fig. 4.6). All connections are valveless, and the direction of flow is reversible. Small irregular sinuses inferior to the pituitary gland drain into the intercavernous sinuses. These inferior intercavernous sinuses are plexiform in nature and are important in a transnasal surgical approach to the pituitary.

Superior Petrosal Sinus

This small, narrow sinus drains the cavernous sinus into the transverse sinus on either side (see Figs. 4.44.6). It leaves the posterosuperior part of the cavernous sinus, runs posterolaterally in the attached margin of the tentorium cerebelli and crosses above the trigeminal nerve to lie in a groove on the superior border of the petrous part of the temporal bone. It ends by joining a transverse sinus where this curves down to become the sigmoid. It receives cerebellar, inferior cerebral and tympanic veins and connects with the inferior petrosal sinus and the basilar plexus.

Sphenoparietal Sinus

The sphenoparietal sinus is located below the periosteum of the lesser wing of the sphenoid bone, near its posterior edge (see Fig. 4.5). It curves medially to open into the anterior part of the cavernous sinus. It receives small veins from the adjacent dura mater and sometimes the frontal ramus of the middle meningeal vein. It may also receive connecting rami, in its middle course, from the superficial middle cerebral vein and veins from the temporal lobe and the anterior temporal diploic vein. When these connections are well developed, the sphenoparietal sinus is a large channel.

Basilar Sinus and Plexus

The basilar sinus and plexus consist of interconnecting channels between layers of dura mater on the clivus (see Fig. 4.6). The basilar venous plexus interconnects the inferior petrosal sinuses and joins with the internal vertebral venous plexus. It also usually connects with the cavernous and superior petrosal sinuses at its anterior end. When veins around the foramen magnum (so-called marginal sinuses) are large, they communicate anteriorly with the plexus, and this produces an almost complete circular venous channel around the foramen magnum, connecting the basilar plexus intracranially to the inferior petrosal, sigmoid and occipital sinuses and extracranially to variable vertebral plexuses in the suboccipital region.

Emissary Veins

Emissary veins traverse cranial apertures and make connections between intracranial venous sinuses and extracranial veins. Some emissary veins are relatively constant; others are sometimes absent. These connections are of clinical significance in the spread of infection from extracranial foci to venous sinuses. The success of ligature of the internal jugular vein to limit the spread of some oral and pharyngeal pathologies depends on the adequacy of the collateral drainage. The following emissary veins are recognized: a mastoid emissary vein in the mastoid foramen, which unites the sigmoid sinus with the posterior auricular or occipital veins; a parietal emissary vein that traverses the parietal foramen to connect the superior sagittal sinus with the veins of the scalp; the venous plexus of the hypoglossal canal, which is occasionally a single vein and runs between the sigmoid sinus and the internal jugular vein; a (posterior) condylar emissary vein that runs between the sigmoid sinus and veins in the suboccipital triangle via the (posterior) condylar canal; a plexus of emissary veins (venous plexus of the foramen ovale) that links the cavernous sinus to the pterygoid plexus via the foramen ovale; two or three small veins that traverse the foramen lacerum and run between the cavernous sinus and the pharyngeal veins and pterygoid plexus; a vein in the emissary sphenoidal foramen (of Vesalius) that connects the cavernous sinus with the pharyngeal veins and pterygoid plexus; the internal carotid venous plexus, which passes through the carotid canal and connects the cavernous sinus to the internal jugular vein; and the petrosquamous sinus, which connects the transverse sinus with the external jugular vein. A vein may traverse the foramen caecum (which is patent in approximately 1% of adult skulls) and connect nasal veins with the superior sagittal sinus. An occipital emissary vein usually connects the confluence of sinuses with the occipital vein through the occipital protuberance and also receives the occipital diploic vein. The occipital sinus connects with variably developed veins around the foramen magnum (so-called marginal sinuses) and thus with the vertebral venous plexuses. This is an alternative venous drainage when the jugular vein is blocked or tied. The ophthalmic veins are potentially emissary, because they connect intracranial to extracranial veins. However, parietal emissary veins, included here, are usually minute and do not appear to connect with veins of the scalp in corrosion casts.

Arterial Supply and Venous Drainage of the Cranial Dura Mater

The arterial supply of the dura mater is derived from numerous vessels. In the anterior cranial fossa, the dura is supplied by the anterior meningeal branches of the anterior and posterior ethmoidal and internal carotid arteries and a branch of the middle meningeal artery. In the middle cranial fossa, it is supplied by the middle and accessory meningeal branches of the maxillary artery, a branch of the ascending pharyngeal artery (entering via the foramen lacerum), branches of the internal carotid artery and a recurrent branch of the lacrimal artery. Dura mater in the posterior fossa is supplied by the meningeal branches of the occipital artery (one enters the skull by the jugular foramen and another by the mastoid foramen), the posterior meningeal branches of the vertebral artery and occasional small branches of the ascending pharyngeal artery, which enter by the jugular foramen and hypoglossal canal. The cranial meningeal arteries are chiefly distributed to bone. In contrast to the arterial supply of the spinal dura mater, only very fine arterial branches are distributed to the cranial dura mater per se. The smaller branches of the meningeal vessels are, therefore, mainly in the endosteal layer of dura.

The middle meningeal is the largest of the meningeal arteries. It passes between the roots of the auriculotemporal nerve and may lie lateral to the tensor veli palatini before entering the cranial cavity through the foramen spinosum. It then runs in an anterolateral groove on the squamous part of the temporal bone, dividing into frontal and parietal branches. The larger frontal (anterior) branch crosses the greater wing of the sphenoid, reaches a groove or canal in the sphenoidal angle of the parietal bone and divides into branches between the dura mater and cranium, with some ascending to the vertex and others to the occipital region. One ascending branch grooves the parietal bone approximately 15 mm behind the coronal suture, corresponding approximately to the precentral sulcus (see Fig. 4.10). The parietal (posterior) branch curves back on the squamous temporal bone, reaching the lower border of the parietal bone anterior to its mastoid angle and dividing to supply the posterior parts of the dura mater and cranium. These branches anastomose with their fellows and with the anterior and posterior meningeal arteries.

In the cranial cavity the artery has several branches. Numerous ganglionic branches supply the trigeminal ganglion and roots. A petrosal branch enters the hiatus for the greater petrosal nerve and supplies the facial nerve, geniculate ganglion and tympanic cavity, anastomosing with the stylomastoid artery. A superior tympanic artery runs in the canal for the tensor tympani, supplying both the muscle and the mucosa lining the canal.

Temporal branches traverse minute foramina in the greater wing of the sphenoid and anastomose with deep temporal arteries. An anastomotic branch enters the orbit laterally in the superior orbital fissure and anastomoses with a recurrent branch of the lacrimal artery. Enlargement of this anastomosis explains the occasional origin of the lacrimal from the middle meningeal artery.

Apart from these branches and a supply to the dura mater, the middle meningeal artery is predominantly periosteal and supplies bone and red bone marrow.

The accessory meningeal artery may arise from the maxillary or the middle meningeal artery. It enters the cranial cavity through the foramen ovale and supplies the trigeminal ganglion, dura mater and bone. However, its main distribution is extracranial, principally to the medial pterygoid, lateral pterygoid (upper head), tensor veli palatini, greater wing and pterygoid processes of the sphenoid bone, mandibular nerve and otic ganglion. It is sometimes replaced by separate small arteries.

Meningeal veins begin from plexiform vessels in the dura mater and drain into efferent vessels in the outer dural layer. The latter connect with the lacunae of the superior sagittal sinus and with other cranial sinuses, including those accompanying the middle meningeal arteries, and with diploic veins.

Innervation of the Cranial Dura Mater

The innervation of the cranial dura mater is derived mainly from the three divisions of the trigeminal nerve, the first three cervical spinal nerves and the cervical sympathetic trunk. Less well-established meningeal branches have been described arising from the vagus and hypoglossal nerves and possibly from the facial and glossopharyngeal nerves.

In the anterior cranial fossa, the dura is innervated by meningeal branches of the anterior and posterior ethmoidal nerves and anterior filaments of the meningeal rami of the maxillary (nervus meningeus medius) and mandibular (nervus spinosus) trigeminal divisions. Nervi meningeus medius and spinosus are, however, largely distributed to the dura of the middle cranial fossa, which also receives filaments from the trigeminal ganglion. The nervus spinosus reenters the cranium through the foramen spinosum with the middle meningeal artery and divides into anterior and posterior branches, which accompany the main divisions of the artery and supply the dura mater in the middle cranial fossa and, to a lesser extent, the anterior fossa and calvaria. The anterior branch communicates with the meningeal branch of the maxillary nerve; the posterior branch also supplies the mucous lining of the mastoid air cells. The nervus spinosus contains sympathetic postganglionic fibres from the middle meningeal plexus. A recurrent tentorial nerve (a branch of the ophthalmic division of the trigeminal) supplies the tentorium cerebelli. The dura in the posterior cranial fossa is innervated by ascending meningeal branches of the upper cervical nerves, which enter through the anterior part of the foramen magnum (second and third cervical nerves) and through the hypoglossal canal and jugular foramen (first and second cervical nerves). Meningeal branches of both the vagus and hypoglossal nerves have been described. Those from the vagus apparently start from the superior vagal ganglion and are distributed to the dura mater in the posterior cranial fossa. Those from the hypoglossal leave the nerve in its canal to supply the diploë of the occipital bone, the dural walls of the occipital and inferior petrosal sinuses and much of the floor and anterior wall of the posterior cranial fossa. These meningeal rami may not contain vagal or hypoglossal fibres but ascending, mixed sensory and sympathetic fibres from the upper cervical nerves and superior cervical sympathetic ganglion. All meningeal nerves contain a postganglionic sympathetic component, either from the superior cervical sympathetic ganglion or by communication with its perivascular intracranial extensions.

The brain itself, the arachnoid mater and the pia mater do not contain sensory nerve endings. These are restricted to the dura mater and cerebral blood vessels. Stimulation of such nerve endings causes pain. The role of the autonomic nerve supply of the cranial dura mater is uncertain.

Arachnoid Mater

The arachnoid mater and the pia mater together are referred to as the leptomeninges. They share many similarities, including their cellular structure. The arachnoid and pia are composed of the same basic cell type embedded in bundles of collagen. The cells share a common embryological origin from mesenchyme surrounding the developing nervous system. They are flattened or cuboidal and have oval nuclei, usually with a single small but prominent nucleolus. Joined together by desmosomes, gap junctions and, in the outer layer of the arachnoid, tight junctions, these cells are not surrounded by basement membrane, except where they are in contact with collagen in the inner layers of the arachnoid and on the deep aspects of the pia mater.

The outer layer of the arachnoid, the dura–arachnoid interface, is formed from five or six layers of cells joined by numerous desmosomes and tight junctions. This layer forms a barrier that normally prevents the permeation of CSF through the arachnoid into the subdural space. The central portion of the arachnoid is closely apposed to the outer layer and is formed from tightly packed polygonal cells, which are joined by desmosomes and gap junctions. The cells are more loosely packed in the inner layer of the arachnoid, where they intermingle with bundles of collagen continuous with the trabeculae that cross the subarachnoid space.

The arachnoid and pia are separated by the subarachnoid space and joined by trabeculae (Fig. 4.11). The anatomical relationships of the arachnoid and pia differ to some extent in the cerebral and spinal regions.

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Fig. 4.11 Relationships of the pia and arachnoid mater to the dura, brain and vessels.

(Modified from Alcolado et al, 1988, according to Zhang, E.T., Inman, C.B.E., Weller, R.O. 1990. Interrelationships of the pia mater and the perivascular (Virchow–Robin) spaces in the human cerebrum. J. Anat. 170, 111–123, by permission from Blackwell Science.)

The cerebral part of the arachnoid mater invests the brain loosely but does not enter the sulci or fissures, except for the great longitudinal fissure between the cerebral hemispheres. The arachnoid also coats the superior surface of the pituitary fossa. In young individuals the arachnoid on the upper surface of the brain is transparent, but in older people it may become white and opaque, particularly near the midline. The arachnoid is thicker on the basal aspect of the brain and is also slightly opaque where it extends between the temporal lobes and the front of the pons, producing a large space between arachnoid and pia mater that is one of the subarachnoid cisterns. The arachnoid is easily separated from the dura over the surface of the brain. However, at sites where the internal carotid and vertebral arteries enter the subarachnoid space, the arachnoid mater is adherent to the adventitia of the vessels. It is then reflected onto the surface of blood vessels in the subarachnoid space and is eventually continuous with the pia mater.

Separation of the arachnoid and dura mater is easily achieved and requires little physical force. Damage to small bridging veins in the space can give rise to a subdural haematoma following even relatively mild head trauma. The characteristics of a subdural haematoma differ from those of the epidural haematoma described earlier. Clinically, the accumulation is often of relatively low pressure and seldom presents as a medical emergency. In many cases there is some predisposing factor, such as cerebral atrophy or increased size of the underlying subarachnoid space, and even sizable accumulations may be tolerated on a chronic basis with mild or no symptoms. The distinction between subdural and extradural haematomas on a neuroimaging scan relies on the anatomical features of the space. Extradural collections tend to be lentiform in shape due to the pressure required to separate the dura and periosteum. They pass deep to any major dural sinuses and cannot extend along the falx cerebri or tentorium cerebelli. Subdural haematomas tend to be biconcave in shape and more extensive, often following the line of the dura along the falx or tentorium and always lying superficial to the deep venous sinuses.

CASE 3 SUBDURAL HAEMATOMA

A 62-year-old woman with chronic renal disease who is on Coumadin for atrial fibrillation stumbles and falls on the sidewalk. She does not hit her head, and other than being bruised, she is not injured. In the ED, a precautionary head CT scan is obtained, which is normal except for age-appropriate cerebral atrophy. Several days later, while bending over, she develops a severe right-sided headache. She returns to the ED, where she is noted to have left facial palsy and mild left-sided weakness. The head CT scan is repeated, this time showing a large subacute right subdural haematoma (SDH). After the effect of Coumadin is reversed, she undergoes surgical evacuation of the haematoma.

Discussion: SDHs arise in the space between the dura and the arachnoid membranes. They are most commonly caused by tearing of the bridging veins that traverse the subdural space. SDH can also be caused by bleeding from small cortical arteries. Symptoms may include headache, nausea, vomiting, lethargy, confusion, aphasia, hemiparesis and seizures. An SDH may present acutely or in a subacute or chronic fashion. Chronic SDH may cause insidious cognitive impairment.

There is a history of antecedent head trauma in most cases of SDH, but they may also arise spontaneously. Falls or “whiplash” injuries without overt head injury can tear bridging veins, leading to SDH. Predisposing factors include cerebral atrophy, as occurs with age or alcohol abuse, and coagulopathy from medications (Coumadin, antiplatelet agents) or medical illness (renal failure, haematological conditions).

SDH can be seen on head CT or MRI; the latter is more sensitive for small SDHs (Fig. 4.12). The accumulated subdural blood typically has a crescent shape, as it can flow freely in the subdural space. Larger SDHs, or those causing neurological dysfunction, require surgical drainage; smaller, asymptomatic SDHs can sometimes be followed expectantly.

Subarachnoid Space

The subarachnoid space lies between the arachnoid and the pia mater. It contains CSF and the larger arteries and veins that traverse the surface of the brain. Arachnoid and pia mater are in close apposition over the convexities of the brain, such as the cortical gyri, whereas concavities are followed by the pia but spanned by the arachnoid. This arrangement produces a subarachnoid space of greatly variable depth that is location dependent. The more expansive spaces are identified as subarachnoid cisterns (Fig. 4.13). Cisterns are continuous with each other through the general subarachnoid space, of which there are dilatations.

The largest cistern, the cisterna magna or cerebellomedullary cistern, is formed where the arachnoid bridges the interval between the medulla oblongata and the inferior surface of the cerebellum. The cistern is continuous above with the lumen of the fourth ventricle through its median aperture—the foramen of Magendie—and below with the subarachnoid space of the spinal cord. The pontine cistern is an extensive space ventral to the pons, continuous below with the spinal subarachnoid space, behind with the cisterna magna and, rostral to the pons, with the interpeduncular cistern. The basilar artery runs through the pontine cistern into the interpeduncular cistern. As the arachnoid mater spans between the two temporal lobes, it is separated from the cerebral peduncles and structures within the interpeduncular fossa by the interpeduncular cistern, which contains the circulus arteriosus (circle of Willis). Anteriorly, the interpeduncular cistern extends to the optic chiasma. The cistern of the lateral fossa is formed by the arachnoid as it bridges the lateral sulcus between the frontal, parietal and temporal opercula, and it contains the middle cerebral artery. The cistern of the great cerebral vein (cisterna ambiens or superior cistern) lies posterior to the brain stem and third ventricle and occupies the interval between the splenium of the corpus callosum and the superior cerebellar surface. The great cerebral vein traverses this cistern, and the pineal gland protrudes into it.

Several smaller cisterns have been described, including the prechiasmatic and postchiasmatic cisterns related to the optic chiasma, the cistern of the lamina terminalis and the supracallosal cistern, all of which are extensions of the interpeduncular cistern and contain the anterior cerebral arteries. The subarachnoid space also extends along the optic nerves to the back of the globe, where the dura fuses with the sclera of the eye. There is a connection between the subarachnoid space and the inner ear through the cochlear duct.

The cerebral subarachnoid space is connected with the fourth ventricle of the brain by three openings, through which CSF flows. The median aperture, or foramen of Magendie, lies in the median plane in the inferior part of the roof of the fourth ventricle and provides communication with the cisterna magna. The paired lateral apertures, or foramina of Luschka, are located at the ends of the lateral recesses of the fourth ventricle and open into the subarachnoid space at the cerebellopontine angle, behind the upper roots of the glossopharyngeal nerves (see Fig. 5.10). Occlusion of these foramina in cases of chronic meningitis, such as tuberculous meningitis, may lead to interruption of CSF outflow from the ventricular system, resulting in hydrocephalus.

Trabeculae, in the form of sheets or fine filiform structures, traverse the subarachnoid space from the deep layers of the arachnoid mater to the pia mater and are also attached to large blood vessels within the subarachnoid space (Figs. 4.11, 4.14). Each trabecula has a core of collagen and is coated by leptomeningeal cells. Subarachnoid trabeculae are long and filamentous and cross the subarachnoid cisterns. The topography of trabeculae that cross the subarachnoid space may, in effect, form compartments, particularly in the perivascular regions, enabling directional flow of CSF through the subarachnoid space.

Arteries and veins in the subarachnoid space are coated by a thin layer of leptomeninges, often only one cell thick. The pia mater, the blood vessels and the arachnoid mater are connected by collagenous trabeculae and sheets, which are also coated by leptomeningeal cells (see Fig. 4.11). Cranial and spinal nerves that traverse the subarachnoid space to pass out of cranial or intervertebral foramina are coated by a thin layer of leptomeninges, which fuses with the arachnoid at the exit foramina.

Arachnoid Villi and Granulations

Arachnoid villi and the larger arachnoid granulations represent extensions of the arachnoid mater and subarachnoid space through the wall of the dural venous sinuses. As such, they present an exchange surface to the sinus endothelium (Fig. 4.16), which constitutes the major pathway for the passage of CSF from the subarachnoid space into the blood. They are, therefore, an essential step in the normal circulation and reabsorption of CSF.

These structures are most prominent along the margins of the great longitudinal fissure, where they project into the superior sagittal sinus (see Fig. 4.8). Arachnoid villi are also found in association with other cerebral venous sinuses, such as the transverse sinus. Microscopic villi are present in the superior sagittal sinus of the fetus and newborn infant. These hypertrophy to form granulations that are visible by age 18 months in the parieto-occipital region of the superior sagittal sinus and by 3 years in the laterally located sinuses of the posterior fossa. The arachnoid granulations become more lobulated and complex with increasing age. They may become calcified, when they are known as Pacchionian bodies.

At the base of each arachnoid granulation, a thin neck of arachnoid mater projects through an aperture in the dural lining of the venous sinus and expands to form a core of collagenous trabeculae and interwoven channels (Fig. 4.17). The core is surmounted by an apical cap of arachnoid cells, some 150 µm thick. Channels extend through the cap to reach the subendothelial regions of the granulation. The cap region of each granulation is attached to the endothelium of the sinus over an area some 300 µm in diameter, whereas the rest of the granulation core is separated from the endothelium by a fibrous dural cupola.

Pia Mater

The pia mater is a delicate membrane that closely invests the surface of the brain, from which it is separated by a microscopic subpial space (see Fig. 4.11). It follows the contours of the brain into concavities and into the depths of fissures and sulci. During development, it becomes apposed to the ependyma in the roof of the telencephalon and fourth ventricle to form the stroma of the choroid plexus.

The pia mater shares a common embryological origin and structural similarity with the arachnoid mater. Their common features were previously described under arachnoid mater.

Pia mater is formed from a layer of leptomeningeal cells that is often only one to two cells thick. The cells are joined by desmosomes and gap junctions but few if any tight junctions, and they are continuous with the coating of the subarachnoid trabeculae. They are separated from the basal lamina of the glia limitans by collagen bundles, fibroblast-like cells and arteries and veins lying in the subpial space (see Fig. 4.14).

Despite its delicate and thin nature, the pia mater appears to form a regulatory interface between the subarachnoid space and the brain. In addition to separating the subarachnoid space from the subpial and perivascular spaces, cells of the pia mater exhibit pinocytotic activity and ingest particles up to 1 µm in diameter. They contain enzymes such as catechol-O-methyltransferase and glutamine synthetase, which degrade neurotransmitters. Further evidence of the pia’s effectiveness as a barrier is seen in subarachnoid haemorrhages and in subpial haemorrhages in infants—in neither of these situations do red blood cells penetrate the pia mater.

It was long thought that the subarachnoid space connected directly with the perivascular spaces (Virchow–Robin spaces) surrounding blood vessels in the brain. However, it is now recognized that the pia mater is reflected from the surface of the brain onto the surface of blood vessels in the subarachnoid space. Thus, the subarachnoid space is separated by a layer of pia from the subpial and perivascular spaces of the brain (see Figs. 4.11, 4.14).