In addition to the protection provided by the skull and the vertebral column and its ligaments, the soft, gelatinous central nervous system (CNS) receives physical support from the meninges. These are the thick dura mater externally, the delicate arachnoid lining the dura, and the thin pia mater adhering to the brain and spinal cord. The latter two layers bound the subarachnoid space, which is filled with cerebrospinal fluid (CSF). The main support and protection provided by the meninges come from the dura mater and the cushion of CSF in the subarachnoid space.
Dura Mater and Associated Structures
The internal surfaces of the cranial bones are clothed by periosteum, which is continuous with the periosteum on the external surface at the margins of the foramen magnum and of smaller foramina for nerves and blood vessels. The cranial dura mater is intimately attached to the periosteum, which is sometimes incorrectly called the “external layer” of the dura mater.
PERIOSTEUM AND MENINGEAL BLOOD VESSELS
The periosteum consists of collagenous connective tissue and contains arteries, somewhat inappropriately called meningeal arteries, which mainly supply the adjoining bone. Of these, the largest is the middle meningeal artery, a branch of the maxillary artery that enters the cranial cavity through the foramen spinosum in the floor of the middle cranial fossa. Its branches extend over the lateral interior surface of the cranium, producing grooves on the bones. Smaller meningeal arteries are branches of the ophthalmic, occipital, and vertebral arteries.
The meningeal arteries are accompanied by meningeal veins, which are also subject to tearing in fractures of the skull. The largest meningeal veins accompany the middle meningeal artery, leave the cranial cavity through the foramen spinosum or the foramen ovale, and drain into the pterygoid venous plexus. Diploic veins, within the cancellous bone of the vault of the skull, drain into the veins of the scalp and into the dural venous sinuses described below.
The dura mater, or pachymeninx, is a dense, firm layer of collagenous connective tissue. The spinal dura mater takes the form of a tube, pierced by the roots of spinal nerves, that extends from the foramen magnum to the second segment of the sacrum. The spinal dura mater is separated from the wall of the spinal canal by an epidural (extradural) space that contains adipose tissue and a venous plexus. The cranial dura mater is firmly attached to the periosteum, as previously described, from which it receives small blood vessels. The outer layer of the dura consists largely of collagen and elastic fibers, and the smooth inner surface of the dura is a simple squamous epithelium. A microscopically narrow film of fluid occupies the subdural space between the dura and outer layer of cells of the arachnoid. The cranial dura mater has several features of importance, notably the dural reflections and dural venous sinuses.
A fracture in the temporal region of the skull may tear a branch of the middle meningeal artery. The extravasated blood accumulates between the bone and the periosteum. As in the case of any space-occupying lesion in the nonexpansile cranial cavity, intracranial pressure increases, and prompt surgical intervention is necessary. The effects of the expanding lesion are similar to those of a subdural hemorrhage (see Chapter 25) and are discussed in this chapter under the heading “Transtentorial and Other Herniations.” With arterial blood escaping at high pressure, the deterioration is typically faster than with venous bleeding into the subdural space.
The dura is reflected along certain lines to form the dural reflections or septa. The intervals between the periosteum and dura along the lines of attachment of the septa accommodate dural venous sinuses (Fig. 26-1). The largest septa, the falx cerebri, and the tentorium cerebelli form incomplete partitions that divide the cranial cavity into three compartments (Fig. 26-2).
The falx cerebri is a vertical partition in the longitudinal fissure between the cerebral hemispheres. This dural reflection is attached to the crista galli of the ethmoid bone in front, to the midline of the vault as far back as the internal occipital protuberance, and to the tentorium cerebelli. The anterior end of the falx cerebri is often fenestrated.
The tentorium cerebelli intervenes between the occipital lobes and the cerebellum. The attachment of the falx cerebri along the midline draws the tentorium upward, giving it a shallow, tent-like shape. The peripheral border of the tentorium is attached to the upper edges of the petrous parts of both temporal bones and to the occipital bone at the margins of the sulci for the transverse sinuses. The free anterior border bounds the incisura of the tentorium (tentorial notch), which accommodates the midbrain.
FIGURE 26-1 Coronal section at the vertex of the skull, including the superior sagittal sinus (venous blood is blue) and the attachment of the falx cerebri. The dura mater is yellow, and the pia-arachnoid is green.
The falx cerebelli is a small dural fold in the posterior cranial fossa, extending vertically for a short distance between the cerebellar hemispheres. The diaphragma sellae roofs over the pituitary fossa or sella turcica of the sphenoid bone and has a hole in its middle for passage of the pituitary stalk.
NERVE SUPPLY OF THE DURA MATER
The dura mater is innervated by nerves that travel alongside the arteries and veins. The cranial dura has a plentiful sensory supply, mainly from branches of all three divisions of the trigeminal nerve. The sensory fibers terminate as unencapsulated endings in the outer, fibroelastic layer of the dura, and they are of significance in certain types of headache. Sympathetic axons also accompany the dural blood vessels.
The dura lining the anterior and middle cranial fossae is supplied by branches from all three divisions of the trigerminal nerve. The dura lining the floor of the posterior cranial fossa is supplied by a meningeal branch from the superior ganglion of the vagus nerve and also by sensory twigs from spinal nerves C1 to C3, which enter the posterior fossa through the hypoglossal canal. (Nerve C1 lacks a sensory component in about half of individuals.)
Recurrent branches of all spinal nerves enter the vertebral canal through the intervertebral
foramina and give off meningeal branches to the spinal dura mater.
FIGURE 26-2 Dural reflections (yellow) and dural venous sinuses (blue) after removal of the brain. The sigmoid sinus of the right side is seen through the tentorial incisura.
DURAL VENOUS SINUSES
As described in Chapter 25, the veins draining the brain empty into the venous sinuses of the dura mater, from which blood flows into the internal jugular veins. The walls of the sinuses consist of dura mater (and periosteum) lined by endothelium. The locations of most of the dural venous sinuses are shown in Figure 26-2.
The superior sagittal sinus lies along the attached border of the falx cerebri. It begins in front of the crista galli of the ethmoid bone, where there may be a narrow communication with nasal veins. Venous lacunae, which are shallow, blood-filled spaces within the dura, lie alongside the superior sagittal sinus and open into it. The superior cerebral veins drain into the sinus or into the lacunae. The superior sagittal sinus is usually continuous with the right transverse sinus.
The small inferior sagittal sinus runs along the free border of the falx cerebri, receiving veins from the medial aspects of the cerebral hemispheres. The inferior sagittal sinus opens into the straight sinus, which lies in the attachment of the falx cerebri to the tentorium cerebelli. The straight sinus also receives the great cerebral vein (see Fig. 25-4). The straight sinus is usually continuous with the left transverse sinus. Venous channels connect the transverse sinuses at the internal occipital protuberance; the configuration of venous channels in this location is called the confluence of the sinuses or torcular Herophili. It also receives the small occipital sinus, which is in the attached margin of the falx cerebelli.
Each transverse sinus lies in a groove on the occipital bone along the attached margin of the tentorium cerebelli. On reaching the petrous part of the temporal bone, the transverse sinus continues as the sigmoid sinus. The latter follows a curved course in the posterior fossa and becomes continuous with the internal jugular vein at the jugular foramen.
Transtentorial and Other Herniations
The narrow interval between the midbrain and the boundary of the tentorial incisura is the only communication between the subtentorial and supratentorial compartments of the cranial cavity. An expanding lesion in the supratentorial compartment, such as a subdural hematoma or a tumor in a cerebral hemisphere, may push the medial part of the temporal lobe (the uncus) down into the incisura of the tentorium. An uncal herniation presses on the ipsilateral oculomotor nerve. The first clinical sign of this event is impairment of the pupillary light reflex (seeChapter 8) because the preganglionic parasympathetic fibers for constriction of the pupil are superficially located in the nerve.
Further herniation can damage descending motor fibers in one or both cerebral peduncles, causing weakness, spasticity, and exaggerated tendon reflexes on either side or bilaterally. When the midbrain is displaced toward the opposite side, the pressure of the rigid edge of the tentorium on the basis pedunculi may result in the unusual finding of upper motor neuron paresis on the same side of the body as the cerebral lesion. Sometimes the downward displacement of the brain occludes one or both posterior cerebral arteries by stretching these vessels over the free edge of the tentorium, with consequences that are explained in Chapter 25. In the later stages of transtentorial herniation, the contralateral oculomotor nerve may be affected. The pupil that dilates first is the most reliable lateralizing sign for the causative lesion.
There are other abnormal movements of parts of the brain from one dural compartment to another. A subfalcial herniation occurs when a space-occupying lesion pushes the cingulate gyrus of one hemisphere across the midline beneath the anterior part of the free edge of the falx cerebri. In an upward transtentorial herniation, the brain stem and cerebellum are displaced into the supratentorial compartment by a mass in the posterior fossa. Such a mass may also cause medullary coning, when the brain stem and part of the cerebellum descend through the foramen magnum into the spinal canal. Medullary coning can occur after withdrawal of CSF from the lumbar subarachnoid space in a patient with raised intracranial pressure. The tonsils of the cerebellum compress the medulla, and the condition can be quickly fatal.
The cavernous sinus is an extradural compartment filled with very thin-walled veins and traversed by the internal carotid artery and various nerves, present on each side of the body of the sphenoid bone and connected by venous channels in the anterior and posterior margins of the diaphragma sellae. A more correct but seldom-used name is lateral sellar (orparasellar) compartment. Each cavernous sinus receives the ophthalmic vein and the superficial middle cerebral vein
and drains into the transverse sinus through the superior petrosal sinus, which runs along the attachment of the tentorium cerebelli to the petrous part of the temporal bone. Theinferior petrosal sinus lies in the groove between the petrous part of the temporal bone and the basilar part of the occipital bone, providing a communication between the cavernous sinus and the internal jugular vein. The sinuses at the base of the cranium receive veins from adjacent parts of the brain.
Thrombosis in Venous Sinuses
Thrombosis in the superior sagittal sinus can occur after a fracture that damages the dura. If the posterior part of the sinus is obstructed, blood cannot escape from much of the cerebral cortex, and areas of infarction form in the frontal and parietal lobes.
Sometimes, infective particles can become dislodged from a facial lesion (e.g., a carbuncle of the upper lip) and pass through the veins of the orbit and the ophthalmic vein into the cavernous sinus. The effects of septic thrombosis of the cavernous sinus include compression of the oculomotor, trochlear, abducens, and maxillary nerves, which are located in the walls of the sinus (see Chapter 8), together with swelling and protrusion of the conjunctiva and systemic signs of a serious infection. A congenital weakness in the wall of the internal carotid artery may cause a split that leaks into the cavernous sinus. Similar to a septic thrombosis, this arteriovenous fistula compresses the nerves that pass through the sinus and causes considerable venous congestion of the eye. The eyeball protrudes and pulsates, and a loud pulsating sound is heard by the patient and by anyone applying a stethoscope to the head.
Within the orbit, the ophthalmic vein has anastomotic communications with the superficial veins of the middle part of the face. Some blood from the facial skin can therefore enter the cavernous sinus and pass into the internal jugular vein. Emissary veins connect dural venous sinuses with veins outside the cranial cavity. Blood may flow in either direction, depending on venous pressures. The parietal and mastoid emissary veins are the largest of these connecting channels. The parietal emissary vein joins the superior sagittal sinus with tributaries of the occipital veins. The mastoid emissary vein joins the sigmoid sinus with the occipital and posterior auricular veins.
FIGURE 26-3 Perivascular spaces in the brain. The subarachnoid space (SAS) separates the arachnoid (A) from the pia mater. The pia splits to ensheath the artery but not the vein. The periarterial space (PAS) has subpial and intrapial compartments, which become continuous as the pial periarterial sheath becomes perforated (PF). Capillaries (CAPS) have no pial ensheathment. (With permission from Zhang ET, Inman CBE, Weller RO. Interrelationships of the pia mater and the perivascular [Virchow-Robin] spaces of the human cerebrum. J Anat 1990;170:111-123.)
The pia mater and the arachnoid together constitute the leptomeninges (thin membranes). They develop initially as a single layer from the mesoderm surrounding the embryonic brain and spinal cord. Fluid-filled spaces form within the layer and coalesce to become the subarachnoid space. The origin from a single membrane is reflected in the numerous trabeculae passing between the two layers (Fig. 26-3). The arachnoid
is closely applied to the inside of the dura mater, so the subdural space normally contains only a film of extracellular fluid. The pia mater adheres to the external glial-limiting membrane of the CNS (see Chapter 2).
The arachnoid is thick enough to be manipulated with fingers or forceps. In contrast, the pia mater is barely visible to the unaided eye, although it imparts a shiny appearance to the surface of the brain. Both surfaces of the arachnoid and the external surface of the pia are covered by simple squamous epithelium. The trabeculae crossing the subarachnoid space are delicate strands of connective tissue with squamous epithelial cells on their surfaces. Tight junctions (zonulae occludentes) connect adjacent arachnoid epithelial cells, preventing exchange of large molecules between the blood in the dural vasculature and the CSF. No tight junctions exist between the pial cells, so there can be free exchange of macromolecules between the CSF and the CNS tissue.
The avascular arachnoid is separated from the dura mater by a film of fluid. The pia mater, which contains a network of fine blood vessels, adheres to the surface of the brain and spinal cord, following all their contours. The collagen fibers in the spinal pia-arachnoid run mostly in a longitudinal direction. This is accentuated along the ventromedian line of the spinal cord, where a thickened strand of fibers, the linea splendens, lies superficial to the anterior spinal artery. The denticulate ligament, described in Chapter 5, is also derived from the pia-arachnoid.
It was formerly thought that the subarachnoid space continued around arteries and veins entering and leaving the CNS tissue. Electron microscopy of surgically removed human cerebral cortex, however, reveals that where an artery enters the substance of the brain, the pia mater splits, and one leaflet forms a cellular sheath that constitutes the adventitia of the vessel. A periarterial subpial space separates the piaadventitia from the external glial-limiting membrane of the brain. An intrapial periarterial space is also present between the smooth muscle of the artery and the pia. The latter space is a continuation of the space that separates an artery from its leptomeningeal covering as it crosses the subarachnoid space (see Fig. 26-3). Veins do not have pial extensions, so the perivenular spaces within the brain are equivalent to the intrapial periarterial spaces. The subarachnoid space is continuous, through fenestrations in the pia, with all three types of perivascular space.
The old term Virchow-Robin spaces applies to all perivascular spaces seen in sections prepared for light microscopy. Capillary blood vessels in the CNS are surrounded by single basal laminae, against which abut the foot processes of astrocytes (see Chapter 2). Spaces are often seen around capillaries in material conventionally prepared for light microscopy, but these are artifacts caused by differential shrinkage, as are the spaces commonly seen around the cell bodies of neurons.
The width of the subarachnoid space varies because whereas the arachnoid rests on the dura mater, the pia mater adheres to the irregular contours of the brain. The space is narrow over the summits of gyri, wider in the regions of major sulci, and wider yet at the base of the brain and in the lumbosacral region of the spinal canal. Regions of the subarachnoid space that contain more substantial amounts of CSF are called subarachnoid cisterns (Fig. 26-4).
The cerebellomedullary cistern (cisterna magna) occupies the interval between the cerebellum and medulla and receives CSF through the median aperture of the fourth ventricle. The basal cisterns beneath the brain stem and diencephalon include the pontine and interpeduncular cisterns and the cistern of the optic chiasma. The cistern of the optic chiasma is continuous with the cistern of the lamina terminalis, which, in turn, continues into the cistern of the corpus callosum above this commissure. The subarachnoid space dorsal to the midbrain is called the superior cistern or, alternatively, the cistern of the great cerebral vein. This cistern and subarachnoid space on the sides of the midbrain constitute thecisterna ambiens or perimesencephalic cistern (not seen in Fig. 26-4). The cistern of the lateral sulcus corresponds with that sulcus. The lumbar cistern of the spinal subarachnoid space
is especially large, extending from the second lumbar vertebra to the second segment of the sacrum. It contains the cauda equina, formed by lumbosacral spinal nerve roots.
FIGURE 26-4 Subarachnoid cisterns of the head, in and near the median plane. Red arrows show the flow of cerebrospinal fluid from the lateral to the third ventricle through the right interventricular foramen and from the fourth ventricle, through the median aperture, into the cerebellomedullary cistern. Regions occupied by cerebrospinal fluid are light blue, and the dura is green. The cisterna ambiens (extending laterally from the superior and interpeduncular cisterns) and the cistern of the lateral sulcus (see text) are not shown because they are outside the median plane.
The meningeal layers and subarachnoid space extend around cranial nerves and spinal nerve roots for a distance approximately to the level of sensory ganglia when these are present. For example, the trigeminal cave (Meckel's cave) is an extension of the subarachnoid space, enclosed by dura mater, around the proximal part of the trigeminal
ganglion at the tip of the petrous part of the temporal bone.
The meningeal extension of greatest clinical importance surrounds the optic nerve to its attachment to the eyeball. The central artery and central vein of the retina run within the anterior part of the optic nerve and cross the extension of the subarachnoid space to join the ophthalmic artery and ophthalmic vein. An increase of CSF pressure slows the return of venous blood, causing edema of the retina. This is most apparent on ophthalmoscopic examination as swelling of the optic papilla or disc (papilledema). Dilatation of the axons of the optic nerve, caused by impairment of the slow component of anterograde axoplasmic transport, also contributes to the swelling. Inspection of the ocular fundi is an important part of every physical examination of a patient.
The CSF is produced mainly by the choroid plexuses of the lateral, third, and fourth ventricles, with those in the lateral ventricles being the largest and most important.
The choroid plexus of each lateral ventricle is formed by an invagination of vascular pia mater (the tela choroidea) on the medial surface of the cerebral hemisphere. The vascular connective tissue picks up a covering layer of epithelium from the ependymal lining of the ventricle. The choroid plexuses of the third and fourth ventricles are similarly formed by invaginations of the tela choroidea attached to the roofs of these ventricles. Each choroid plexus, which has a minutely folded surface, consists of a core of connective tissue containing many wide capillaries and a surface layer of cuboidal or low columnar epithelium (the choroid epithelium; Fig. 26-5). The surface area of the choroid plexuses of the two lateral ventricles combined is about 40 cm2.
Several features of the choroid epithelium as seen in electron micrographs are of functional interest (Fig. 26-6). The large nucleus, abundant cytoplasm, and many mitochondria indicate that production of CSF is an active process that requires expenditure of energy on the part of these cells. The plasma membrane at the free surface is greatly increased in area by irregular microvilli. A basement membrane separates the epithelium from the subjacent stroma with its rich vascular network. The capillaries, unlike those generally supplying nervous tissue, have endothelial fenestrations and are permeable to large molecules. The blood-CSF barrier to macromolecules is formed by the cells of the choroid epithelium and the tight junctions (zonulae occludentes) between adjacent cells.
Production of CSF is a complex process. Some components of the blood plasma, notably water, enter and leave the CSF by diffusion. Others reach the fluid with the assistance of metabolic activity on the part of the choroid epithelial cells. An important factor is active transport of certain ions (notably sodium) through the epithelial cells, followed by passive movement of water to maintain osmotic equilibrium. Transporter proteins in the choroid epithelial cells allow controlled movement of glucose and amino acids into the CSF.
FIGURE 26-5 Fragment of choroid plexus, showing large capillaries (C) and the choroid epithelium (E). Stained with hemalum and eosin.
CSF flows from the lateral ventricles into the third ventricle through the interventricular foramina and then into the fourth ventricle by way of the cerebral aqueduct. CSF leaves the ventricular system through the median and lateral apertures of the fourth ventricle, with the former opening into the cerebellomedullary cistern and the latter into the pontine cistern (see Figs. 6-4 and 6-5). From these sites, fluid moves sluggishly through the spinal subarachnoid space, determined partly by movements of the vertebral column. More importantly, the CSF flows slowly forward through the basal cisterns and then upward over the medial and lateral surfaces of the cerebral hemispheres. Movement of CSF is assisted by the pulsation
of arteries, especially in the subarachnoid space around the spinal cord.
FIGURE 26-6 Electron micrograph of a choroid epithelial cell. ER, endoplasmic reticulum; M, mitochondria; MV, microvilli; N, nucleus; PM, folds of plasma membrane; TJ, tight junction (zonula occludens) (X8,000; courtesy of Dr. D. H. Dickson).
The main site of absorption of the CSF into venous blood is through the arachnoid villi projecting into dural venous sinuses, especially the superior sagittal sinus and its adjacent lacunae (see Fig. 26-1). Each arachnoid villus consists of a thin cellular layer, derived from the endothelium of the sinus, which encloses an extension of the subarachnoid space containing arachnoid cells and collagenous trabeculae (Fig. 26-7). The absorptive mechanism depends on the hydrostatic pressure of the CSF being higher than that of the venous blood in the dural sinuses. An increase in venous pressure collapses the extracellular channels of the villus, preventing the reflux of blood into the subarachnoid space. The final stage of absorption is the movement of fluid in large vesicles that form in the cytoplasm of the endothelial cells. Arachnoid villi become hypertrophied with age, becoming visible to the unaided eye. They are then called arachnoid granulations or pacchionian bodies; some are sufficiently large to produce erosion or pitting of the parietal bones.
Some CSF is absorbed into arachnoid villi that protrude into veins that pass alongside the spinal and cranial nerve roots before emptying into the epidural venous plexus.
FIGURE 26-7 Structure of an arachnoid granulation. The venous blood in the sinus is blue. Pia-arachnoid tissue is green, the endothelium of the sinus is red, the dura is yellow, and the cerebral cortex (stippled) is gray. Cerebrospinal fluid occupies the white areas in the subarachnoid space, between collagenous trabeculae within the granulation and between the cap of arachnoid epithelial cells and the endothelium.
PRESSURE AND PROPERTIES
The volume of the CSF varies from 80 to 150 mL; these figures include the fluid in the ventricles and the subarachnoid space. The ventricular system alone contains from 15 to 40 mL of fluid. The rate of production is sufficient to effect a total replacement several times daily. The pressure of CSF is from 80 to 180 cm H2O when a subject is recumbent; the pressure in the lumbar cistern is about twice as high when measured in a sitting position. Venous congestion in the closed space of the cranial cavity and the spinal canal, as produced by straining or coughing, is reflected in a prompt increase of CSF pressure.
CSF is clear and colorless, with a density of 1.003 to 1.008 g/cm3. The few cells present are mainly lymphocytes. These vary in number from one to eight in each cubic millimeter; a count of more than 10 cells indicates disease. The glucose level is about one-half that of blood, and the protein content is very low (15 to 45 mg/dL).
When there is an excess of CSF, the condition is known as hydrocephalus, of which there are several types. External hydrocephalus, in which the excess fluid is mainly located in the subarachnoid space, is found in senile atrophy of the brain. Internal hydrocephalus refers to dilatation of the ventricles. All the ventricles are enlarged if the apertures of the fourth ventricle are occluded. The third and lateral ventricles enlarge if the obstruction is located in the cerebral aqueduct. In the rare occurrence of occlusion of an interventricular foramen, the hydrocephalus is confined to the ipsilateral lateral ventricle.
The term communicating hydrocephalus refers to a combination of internal and external hydrocephalus. The most common cause is obstruction of the arachnoid villi by blood after a subarachnoid hemorrhage. Communicating hydrocephalus can also occur in bacterial meningitis, with pus as the obstructing material. If the flow of CSF through the incisura of the tentorium around the midbrain is obstructed, the excess fluid accumulates in the ventricles and in the part of the subarachnoid space below the tentorium.
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