Anatomical Basis of Surgical Approaches to the Region of the Foramen Magnum
Lesions in the region of the foramen magnum present special problems in operative management because many structures are involved. The structures that must be considered in planning an operative approach to the region include the brainstem and spinal cord, the lower cranial and upper spinal nerves, the vertebral artery and its branches, and the ligaments uniting the atlas, axis, and occipital bone.1,2
Osseous Relationships
The osseous structures in the region of the foramen magnum are the occipital bone, the atlas, and the axis. The occipital bone surrounds the foramen magnum ( Fig. 2.1 ). The foraminal opening is oval and wider posteriorly than anteriorly. The wider posterior part transmits the medulla, and the narrower anterior part sits above the odontoid process. The occipital bone is divided into a squamosal part located above and behind the foramen magnum, a basal part situated in front of the foramen magnum, and paired condylar parts located lateral to the foramen magnum. The squamous part is an internally concave plate located above and behind the foramen magnum. The internal surface has a prominent ridge, the internal occipital crest, which descends in the midline and serves as the attachment for the falx cerebelli. This crest bifurcates to form paired lower limbs that extend along each side of the posterior margin of the foramen magnum.
The basilar part, which is also referred to as the clivus, is a thick plate of bone that extends forward and upward at an angle of ~45 degrees from the foramen magnum to join the sphenoid bone. The superior surface of the clivus is concave from side to side and is separated on each side from the petrous part of the temporal bone by the petro-occipital fissure. The inferior surface has a small elevation, the pharyngeal tubercle, which gives attachment to the raphe of the pharynx.
The paired condylar parts are situated at the sides of the foramen magnum. The occipital condyles, which articulate with the atlas, are located lateral to the anterior half of the foramen magnum. A tubercle, which gives attachment to the alar ligament of the odontoid process, is situated on the medial side of each condyle. The hypoglossal canal, which transmits the hypoglossal nerve, is situated above and forward of the condyle. The condylar fossa, a depression located on the external surface behind the condyle, is often perforated to form a canal through which an emissary vein passes.
The atlas, the first cervical vertebra, differs from the other cervical vertebrae by being ring shaped and by lacking a vertebral body and a spinous process ( Fig. 2.2 ). It consists of two thick lateral masses connected in front by a short anterior arch and behind by a longer curved posterior arch. The position of the usual vertebral body is occupied by the odontoid process (dens). The posterior arch has a groove on the lateral part of its upper outer surface in which the vertebral artery courses. The groove may be partly or fully converted into a foramen by a bridge of bone that arches backward from the superior articular facet to the posterior arch. The upper and lower surfaces of each lateral mass have oval facets that articulate with the occipital condyles and the superior articular facets of the axis. The medial aspect of each lateral mass has a small tubercle for the attachment of the transverse ligament of the atlas. The transverse processes are unusually long and can be felt through the overlying tissues. Each transverse foramen, which transmits a vertebral artery, is situated between the lateral mass and the transverse process.
The axis, the second cervical vertebra, more closely resembles typical vertebrae than the atlas but is distinguished by the odontoid process, which projects upward from the body ( Fig. 2.2 ). On the front of the dens is an articular facet, which forms a joint with the back of the anterior arch of the atlas. The dens has a pointed apex that is joined by the apical ligament, a flattened side where the alar ligaments are attached, and a groove at the base of its posterior surface where the transverse ligament of the atlas passes. The dens and body are flanked by a pair of large oval facets that extend laterally from the body onto the adjoining parts of the pedicles and articulate with the inferior facets of the atlas. The superior facets do not form an articular pillar with the inferior facets but are anterior to the latter. The transverse processes are small. Each transverse foramen faces superolaterally, thus permitting the lateral deviation of the vertebral artery as it passes up to the more widely separated foramina in the atlas.
Ligamentous and Articular Relationships
The ligaments and articulations important in planning operative approaches are those joining the atlas, axis, and occipital bone ( Fig. 2.3 ). The articulation of the atlas and axis comprises four synovial joints: two median ones on the front and back of the dens and paired lateral ones between the opposing articular facets on the lateral masses of the atlas and axis. Each joint on the front and back of the dens has its own capsule and synovial cavity. The anterior one is situated between the anterior surface of the dens and the posterior aspect of the anterior arch of the atlas. The posterior one lies between the cartilage-covered anterior surface of the transverse ligament of the atlas and the posterior surface of the dens.
The atlas and axis are united by the cruciform and the anterior and posterior longitudinal ligaments and the articular capsules surrounding the joints between the opposing articular facets on the lateral masses. The cruciform ligament has transverse and vertical parts that form a cross behind the dens. The transverse part, called the transverse ligament, arches across the ring of the atlas behind the dens and is broader behind the dens than where it is attached to a tubercle on the medial side of the lateral masses of the atlas. As it crosses the dens, small longitudinal bands are directed upward and downward. The cranial extension is attached to the upper surface of the clivus between the apical ligament of the dens and the tectorial membrane. The lower band is attached to the posterior surface of the body of the axis.
In front, the atlas and axis are connected by the anterior longitudinal ligament, a wide band fixed to the anterior arch of the atlas and the front body of the axis. The posterior longitudinal ligament is attached above to the transverse part of the cruciform ligament and the clivus. Posterior to the spinal canal, the atlas and axis are joined by a broad, thin membrane that extends from the posterior arch of the atlas to the laminae of the axis (ligamentum flavum).
The atlas and the occipital bone are united by the articular capsules surrounding the atlanto-occipital joints and by the anterior and posterior atlanto-occipital membranes ( Fig. 2.3 ). The anterior atlanto-occipital membrane extends from the anterior edge of the foramen magnum to the anterior arch of the atlas. The posterior atlanto-occipital membrane extends from the posterior margin of the foramen magnum to the posterior arch of the atlas. The lateral border of this membrane arches behind the vertebral artery and the first cervical nerve root and may be ossified in the area where it arches behind the vertebral artery.
Four fibrous bands—the tectorial membrane, the paired alar ligaments, and the apical ligament—connect the axis and the occipital bone ( Fig. 2.3 ). The tectorial membrane is a cephalic extension of the posterior longitudinal ligament that covers the dens and cruciform ligament. It is attached below to the posterior surface of the body of the axis and above to the upper surface of the occipital bone in front of the foramen magnum. The alar ligaments arise on each side of the upper part of the dens and attach to the medial surfaces of the occipital condyles. The apical ligament extends from the tip of the dens to the anterior margin of the foramen magnum and is situated between the anterior atlanto-occipital membrane and the cruciform ligament.
Neural Relationships
The neural structures situated in the region of the foramen magnum are the caudal part of the brainstem, cerebellum, and fourth ventricle; the rostral part of the spinal cord; and the lower cranial and upper cervical nerves ( Figs. 2.4 and 2.5 ). The spinal cord blends indistinguishably into the medulla at a level arbitrarily set at the upper limit of the dorsal and ventral rootlets forming the first cervical nerve. It is easier to differentiate this level on the ventral than on the dorsal surface because the ventral rootlets of the first cervical nerve are always present, and the dorsal rootlets are absent in many cases. The fact that the junction of the spinal cord and medulla is situated at the rostral margin of the first cervical root means that the medulla, and not the spinal cord, occupies the foramen magnum. In the upper cervical region the rootlets, which unite to form the spinal part of the accessory nerve, emerge through the lateral funiculus in front of the dorsal roots.
The dentate ligament is a white fibrous sheet that is attached to the spinal cord medially and to the dura laterally ( Fig. 2.4 ). Its medial border has a continuous linear attachment to the spinal cord midway between the dorsal and ventral roots. Its lateral border is attached to the dura at intervals by fibrous triangular processes. The most rostral triangular process is attached to the dura at the level of the foramen magnum, and the second one is attached posterior and inferior to the initial intradural segment of the vertebral artery. The lateral border of the dentate ligament between the two most rostral triangular processes is attached to the vertebral and posterior spinal arteries and to the C1 root, making separation of these structures difficult.
The upper spinal cord blends indistinguishably into the lower medulla ( Figs. 2.4 and 2.5 ). The anterior surface of the medulla is formed by the medullary pyramids, which face the clivus, the anterior edge of the foramen magnum, and the rostral part of the odontoid process. The anterior median sulcus divides the upper medulla in the anterior midline between the pyramids, disappears on the lower medulla at the level of the decussation of the pyramids (but reappears below the decussation), and is continuous caudally with the anterior median fissure of the spinal cord. The lateral surface of the medulla is formed predominantly by the inferior olives. The posterior surface of the medulla is formed by the inferior cerebellar peduncles, medially by the gracile fasciculus and tubercle, and laterally by the cuneate fasciculus and tubercle. The belly of the pons, which sits on the clivus, is convex from side to side as well as from top to bottom.
The cerebellum rests above the posterior and lateral edges of the foramen magnum. Only the lower part of the hemispheres (formed by the tonsils and the biventral lobules) and the lower part of the vermis (formed by the nodule, uvula, and pyramid) are related to the foramen magnum. The biventral lobule sits above the lateral part of the foramen magnum, and the tonsils rest above the level of the posterior edge.
The cerebellar surface above the posterior part of the foramen magnum has a deep vertical depression, the posterior cerebellar incisura, which contains the falx cerebelli and extends inferiorly toward the foramen magnum. The vermis is folded into and forms the cortical surface within this incisura. The vermian surface within the incisura has a diamond shape. The upper half of the diamond-shaped formation has a pyramidal shape; thus, it is called the pyramid. The lower half of the diamond-shaped formation, the uvula, projects downward between the tonsils, thus mimicking the situation in the oropharynx. Inferiorly, the posterior cerebellar incisura is continuous with the vallecula cerebelli, an opening between the tonsils that extends upward through the foramen of Magendie into the fourth ventricle.
The tonsils, which sit above the posterior edge of the foramen magnum, are commonly involved in herniations through the foramen magnum. Each tonsil is an ovoid structure that is attached along its superolateral border to the remainder of the cerebellum. The inferior pole and posterior surface of the tonsils face the cisterna magna and are visible from the suboccipital operative exposure. The lateral surface of each tonsil is covered by the biventral lobule. The medial and anterior surfaces and the superior pole of each tonsil all face, but are separated from, other neural structures by narrow clefts. The anterior surface of each tonsil faces and is separated from the posterior surface of the medulla by the cerebellomedullary fissure. The medial surfaces of the tonsils face each other across the vallecula. The ventral aspect of the superior pole faces the inferior half of the roof of the fourth ventricle.
The cerebellomedullary fissure, which extends superiorly between the cerebellum and the medulla, is situated rostral to the dorsal margin of the foramen magnum. This fissure extends superiorly to the level of the roof of the fourth ventricle and the lateral recesses of the fourth ventricle. The dorsal wall of the fissure is formed by the uvula in the midline and the tonsils and biventral lobules laterally. The ventral wall, formed by the inferior medullary velum and tela choroidea, is exposed by removing the tonsils. The inferior medullary velum is a thin, bilateral, semitranslucent butterfly-shaped sheet of neural tissue that blends into the ventricular surface of the nodule medially and stretches laterally across the superior pole of the tonsil. The tela choroidea, from which the choroid plexus projects, forms the lowest part of the roof of the fourth ventricle.
Cranial Nerves
The lower four cranial nerves are sufficiently close to the foramen magnum that they may be involved in lesions arising there. The rootlets forming the hypoglossal nerve arise from the medulla along a line that is continuous inferiorly with the line along which the ventral spinal roots arise ( Figs. 2.4 and 2.5 ). These rootlets exit the medulla along the anterior margin of the olive and pass behind the vertebral artery to reach the hypoglossal canal. The vertebral artery may stretch the hypoglossal rootlets posteriorly over its dorsal surface. The hypoglossal canal may be divided by a bony septum that separates the nerve into two bundles as it exits the skull.
The glossopharyngeal, vagus, and accessory nerves are considered together because they are formed by a series of rootlets that arise in a continuous line along the medulla and spinal cord and exit the skull through the jugular foramen ( Figs. 2.4 and 2.5 ). The glossopharyngeal and vagus nerves arise from the medulla along the posterior margin of the olive. The only location where the glossopharyngeal nerve may consistently be distinguished from the vagus nerve is just proximal to a dural septum, which separates these nerves as they penetrate the dura to enter the jugular foramen.2,3
The accessory nerve is the only cranial nerve that passes through the foramen magnum ( Figs. 2.4 and 2.5 ). It has a cranial part composed of the rootlets that arise from the medulla and join the vagus nerve, and a spinal portion formed by the union of a series of rootlets that arise from the lower medulla and upper spinal cord. In the posterior fossa, the accessory nerve is composed of one main trunk from the spinal cord and three to six small rootlets that emerge from the medulla. The most rostral medullary rootlets are functionally inferior vagal rootlets, as they arise from the vagal nuclei. The lower medullary rootlets join the spinal portion of the nerve. The spinal contribution arises as a series of rootlets situated midway between the ventral and dorsal rootlets. The rootlets contributing to the accessory nerves may arise as low as the C7 root level.2 These rootlets unite to form a trunk having a diameter of ~1.0 mm, which ascends through the foramen magnum between the dentate ligament and the dorsal roots.
All of the 50 accessory nerves examined in our study had connections with the dorsal roots of the upper cervical nerves.2 The most common and largest anastomosis was with the dorsal root of the first cervical nerve. The C1 dorsal roots frequently arose solely from the accessory nerve without a contribution from the C1 level of the spinal cord. About one third of C1 dorsal roots received rootlets that arose from the spinal cord at the C1 level, but these also had anastomotic fibers from the accessory nerve. The accessory nerves may also have an anastomotic connection with the C2 to C5 dorsal roots.2,4
Spinal Nerve Roots
The spinal rootlets in the region of the foramen magnum pass directly lateral to reach their dural foramina ( Figs. 2.3, 2.4, and 2.5 ). The first cervical nerve is located just below the foramen magnum and differs from the other cervical nerves in the consistency and origin of the dorsal rootlets forming the nerve. The C1 ventral root is composed of four to eight rootlets that join and course laterally. Before entering the dural foramen, the C1 ventral root and the corresponding dorsal root, if present, attach to the posterior inferior surface of the initial intradural part of the vertebral artery. They then pass through the funnel-shaped dural foramen around the vertebral artery. The ventral root joins the dorsal root in or external to the dural foramen.
The dorsal root of the first cervical nerve is more complicated than the ventral root because of the variations in its composition and its connections with the accessory nerve. In our study of the 25 spinal cords in which one would expect to find 50 C1 dorsal roots arising from the cord, only 15 were found.2 The accessory nerve contributed a root to the first cervical nerve in 28 cases of the 35 roots lacking a dorsal root that arose from the spinal cord. In the remaining 7 cases, the C1 dorsal root was absent. Each of the 15 dorsal roots that arose from the spinal cord also had a contribution from the accessory nerve.2
Arterial Relationships
The major arteries related to the foramen magnum are the vertebral and posterior inferior cerebellar arteries, as well as the meningeal branches of the vertebral and external and internal carotid arteries ( Figs. 2.4, 2.5, and 2.6 ).2,5–7 The paired vertebral arteries ascend through the transverse processes of the upper six cervical vertebrae, enter the dura behind the occipital condyles, and ascend through the foramen magnum to reach the front of the medulla. The segment most intimately related to the foramen magnum passes medially behind the lateral mass of the atlas and across the groove on the upper surface of the lateral part of the posterior arch of the atlas. This bony groove is frequently transformed into a bony canal that completely surrounds a short segment of the artery ( Fig. 2.4 ).
The intradural segment begins at the dural foramen just inferior to the lateral edge of the foramen magnum. The dura in this region forms a funnel-shaped foramen around a 4 to 6 mm length of the artery. The first cervical nerve exits the spinal canal, and the posterior spinal artery enters the spinal canal through this dural foramen with the vertebral artery. These three structures are bound together at the foramen by fibrous dural bands ( Fig. 2.4 ). The initial intradural segment of the vertebral artery passes just superior to the dorsal and ventral roots of the first cervical nerve and just anterior to the posterior spinal artery, the dentate ligament, and the spinal portion of the accessory nerve.
The branches arising from the vertebral artery in the region of the foramen magnum are the posterior spinal, anterior spinal, posterior inferior cerebellar, and the anterior and posterior meningeal arteries. The paired posterior spinal arteries usually arise from the vertebral arteries, just outside the dura, but they may also arise inside the dura or from the posteroinferior cerebellar arteries ( Figs. 2.4, 2.5, and 2.6 ). In the subarachnoid space, they course medially behind the rostral-most attachments of the dentate ligament and divide into a branch ascending to the medulla and a branch descending to the spinal cord.
The posteroinferior cerebellar artery usually originates within the dura, but it may infrequently originate from the terminal extradural part of the vertebral artery.5,8 It may arise at, above, or below the level of the foramen magnum; of the 42 arteries found in 50 cerebella in our study, 35 arose above and 7 arose below the foramen.2,5 In its course around the anterolateral surface of the medulla, it passes rostral or caudal to or between the rootlets of the hypoglossal nerve, and in its course around the posterolateral medulla it passes above, below, or between the rootlets of the glossopharyngeal, vagus, and accessory nerves. As it passes between the latter nerves, it may be ascending, descending, or passing laterally or medially, or it may be involved in a complex loop that stretches and distorts these nerves. Of the 42 arteries, 16 passed between the rootlets of the accessory nerve, 10 passed between the rootlets of the vagus nerve, 13 passed between the vagus and accessory nerves, 2 passed above the glossopharyngeal nerve between the latter nerve and the vestibulocochlear nerve, and 1 passed between the glossopharyngeal and vagus nerves.2,5 After reaching the area dorsal to the glossopharyngeal, vagus, and accessory nerves, it passes around the cerebellar tonsil near the roof of the fourth ventricle and bifurcates into a medial and a lateral trunk. The medial trunk supplies the vermis and the adjacent part of the hemisphere, and the lateral trunk supplies the tonsil and the hemispheres.
The anterior spinal artery is formed by the union of the paired anteroventral spinal arteries, which originate from the vertebral arteries ( Fig. 2.5 ). One of the anteroventral spinal arteries may continue inferiorly as the anterior spinal artery, and the other may terminate on the medulla. The anterior spinal artery descends through the foramen magnum on the anterior surface of the medulla and the spinal cord in or near the anterior median fissure.
The dura around the foramen magnum is supplied by the meningeal branches of the ascending pharyngeal and occipital arteries, the anterior and posterior meningeal branches of the vertebral artery, and the dorsal meningeal branch of the meningohypophyseal trunk of the intracavernous segment of the internal carotid artery ( Figs. 2.4, 2.5, and 2.6 ). Infrequently, the posterior inferior cerebellar and posterior spinal arteries and the intradural part of the vertebral artery give rise to meningeal branches. The anterior meningeal branch of the vertebral artery enters the spinal canal through the C2 to C3 intervertebral foramen and ascends between the posterior longitudinal ligament (tectorial membrane) and the dura ( Fig. 2.3A–C ). At the level of the apex of the dens, these paired arteries join to form an arch over the apex of the dens. The posterior meningeal artery arises from the vertebral artery as it courses around the lateral mass of the atlas and ascends in the dura near the falx cerebelli. The ascending pharyngeal branch of the external carotid artery sends branches through the hypoglossal canal and jugular foramen to the dura above the foramen magnum ( Fig. 2.5 ). The meningeal branch of the occipital artery is inconstant. It penetrates the cranium through a mastoid emissary foramen.