Innervation of the Extraocular Muscles
MICHAEL X. REPKA and MARSHALL M. PARKS
Table Of Contents
|The third, fourth, and sixth cranial nerves innervate six extraocular muscles. These
muscles are responsible for controlling the ocular rotations
in horizontal, vertical, and torsional directions. The third cranial
nerve also provides parasympathetic motor innervation to the intrinsic
eye muscles, the ciliary muscle, and the iris sphincter muscle. Although
these nerves originate at separate locations in the brain stem, they
converge in the subarachnoid space and become closely associated
in the cavernous sinus, superior orbital fissure, and posterior orbit (Fig. 1). From the cavernous sinus to the eye, they may be involved simultaneously
in pathologic processes.|
The oculomotor nerve is the largest of the ocular motor nerves. It contains some 15,000 axons, including motor fibers and parasympathetic motor fibers. The nucleus of the third cranial nerve is located in the inferior periaqueductal gray matter of the mesencephalon. It is a complex of both paired and midline motor cells. These cells are found from the posterior commissure superiorly to the pontomesencephalic junction caudally (Fig. 2) in the dorsal midbrain. Classically, this complex has been described with four paired subnuclei supplying innervation to the inferior, medial, and superior rectus muscles and to the inferior oblique muscle. There is a single caudal, dorsal midline nucleus providing innervation to the levator muscle. Innervation of the extraocular muscle from the paired nuclei is ipsilateral for the inferior and medial rectus muscles and the inferior oblique muscle. However, innervation of the superior rectus is contralateral. The motor fibers to the superiorrectus decussate within the third nerve nucleus and join the fascicle of the contralateral oculomotor nerve.
The organizational scheme of the oculomotor nucleus was proposed by Warwick.1 This hypothesis was substantiated by using retrograde degeneration techniques in monkeys. Substantiation of Warwick's hypothesis in humans relies on autopsy findings and neuroimaging results.2–4 Recent research in monkeys has suggested that the medial rectus muscle may not have only one subnucleus, as suggested by Warwick, but may receive innervation from three separate regions within the oculomotor nerve complex, which have been labeled A, B, and C.5
In addition to the extraocular muscle motor fibers, the Edinger-Westphal nuclei supply the parasympathetic preganglionic neurons that project to the ciliary ganglion. These nuclei are positioned dorsal and medial to the muscle motor nuclei. They are composed of two cell groups, a medial unpaired column and a lateral paired column. All evidence suggests that these fibers project ipsilaterally. There is a second source of parasympathetic fibers projecting to the ciliary ganglion in monkeys. Burde and Loewy6 have shown the source of these fibers to be Perlia's nucleus. This nucleus is found in the middle third of the oculomotor complex, positioned dorsally. The role of this structure in humans is unknown.
The fascicular portion of the oculomotor nerve descends as its moves ventrally and laterally through the mesencephalon (Fig. 3A). The fascicles pass through the medial longitudinal fasciculus, the red nucleus, and the medial portion of the cerebral peduncle. During the passage through the ventral midbrain, there appears to be topographic organization of the fascicles so that a divisional paresis is possible even with intrinsic lesions.4 The oculomotor nerve exits the brain stem into the interpeduncular fossa as a horizontal arrangement of multiple fiber bundles that rapidly coalesce to form the subarachnoid portion of the third cranial nerve.
After exiting the brain stem, the oculomotor nerve continues to course downward and laterally, reaching the top of the clivus at a point just lateral to the posterior clinoid process. During the passage through the subarachnoid space, the nerve passes just below the posterior cerebral artery and above the superior cerebellar artery (Fig. 4). After passing between these two arteries, the nerve travels adjacent to the posterior communicating artery. The close apposition of third nerve to these vascular structures accounts for the frequent involvement of this nerve by vascular anomalies, such as an aneurysm of the posterior communicating artery.
Once the oculomotor nerve penetrates the dura, it continues forward in the lateral wall of the cavernous sinus. It is positioned just above the fourth cranial nerve. In the anterior cavernous sinus, the oculomotor nerve divides anatomically into two distinct divisions, superior and inferior. The superior division innervates the levator and superior rectus muscles, whereas the inferior division innervates the inferior rectus, the medial rectus, and the inferior oblique muscles. The inferior division also contains the parasympathetic fibers for the ciliary muscle, the ciliary body, and the iris sphincter. Although a distinct anatomic separation into two divisions is not evident until the nerve reaches the anterior cavernous sinus, multiple clinical cases suggest that a discrete topographic arrangement of fibers exists as far proximally as the fasciculus.2–5,7–9
The superior and inferior divisions of the third cranial nerve enter the orbit through the superior ophthalmic fissure, subsequently passing through the annulus of Zinn. The superior division passes lateral to the optic nerve, where it divides into a number of branches, some entering the superior rectus muscle. Additional branches pass beyond the lateral aspect of the superior rectus muscle to reach the levator muscle. The inferior division splits into multiple branches that innervate the medial and inferior rectus muscles. The branch to the inferior oblique muscle passes laterally around the inferior rectus muscle and enters the inferior oblique muscle along its posterior and lateral border. This site has become an important anatomic landmark for surgery on the inferior oblique muscle.10
The nuclei of the trochlear nerve are a paired group of motor cells located in the floor of the cerebral aqueduct. They are positioned just caudal to the oculomotor nerve complex in the midbrain.
About 2100 axons emerge from each nucleus, passing first laterally and then dorsally to converge and decussate over the roof of the cerebral aqueduct just caudal to the inferior colliculi where they exit the brain stem (see Fig. 3B). The short fascicular course makes it difficult clinically to separate nuclear from fascicular involvement.
The trochlear nerve passes around the brain stem and courses forward between the posterior cerebral and superior cerebellar arteries (see Fig. 4). It passes around the cerebral peduncles, penetrating the dura to reach the cavernous sinus. The trochlear nerve has the longest subarachnoid course of the ocular motor nerves. Within the cavernous sinus, the nerve is positioned in the lateral wall just below the third cranial nerve and above the ophthalmic division of the trigeminal nerve. The nerve continues forward, passing through the superior orbital fissure above and medial to the annulus of Zinn to reach the superior oblique muscle. It is the only ocular motor nerve that does not pass through the annulus of Zinn (see Fig. 1).
The nucleus of the abducens nerve is located immediately beneath the floor of the fourth ventricle at the junction of the pons and medulla. Several important brain stem structures are closely associated. The genu of the facial nerve fasciculus curves dorsally and laterally over the nucleus. The medial longitudinal fasciculus is just medial to the sixth nerve nucleus, and the vestibular nuclei are positioned just laterally (see Fig. 3C).
There are two cell populations within the sixth nerve nucleus. One group of cell bodies contains motor neurons that innervate the ipsilateral lateral rectus. The other group of cell bodies produces axons, which decussate and enter the contralateral medial longitudinal fasciculus. There they ascend via the medial longitudinal fasciculus to the oculomotor nerve complex, forming synapses in the region of the medial rectus subnucleus. This latter group of fibers participates in horizontal conjugate gaze.
The abducens fascicle courses ventrally, laterally, and caudally to emerge at the junction of the pons and medulla. During its course, the fascicle is in close proximity to the facial nerve nucleus, the facial nerve fascicle, motor and sensory nuclei of the trigeminal nerve, and the pyramidal tract.
The nerve exits the brain stem just lateral to the pyramid. It ascends in the subarachnoid space along the clivus, passing near the inferior petrosal venous sinus and then passing beneath the petrosphenoid ligament (see Fig. 4). This space is called Dorello's canal. The abducens nerve penetrates the dura to enter the cavernous sinus, where it is located just lateral to the carotid artery within the substance of the sinus. This location, rather than in the wall of the sinus, seems to make it the most vulnerable of the ocular motor nerves to pathology within the cavernous sinus. In the cavernous sinus, the abducens nerve combines briefly with the ocular sympathetics before exiting through the superior ophthalmic fissure. The simultaneous occurrence of an abducens nerve paresis and an ipsilateral oculosympathetic paresis is exquisitely localizing the lesion to the cavernous sinus.
The abducens nerve enters the orbit through the superior ophthalmic fissure. It subsequently passes through the annulus of Zinn, positioned lateral to the optic nerve and medial to the lateral rectus. The nerve divides into multiple branches, innervating the lateral rectus muscle.
9. Castro O, Johnson LN, Mamourian AC: Isolated inferior oblique paresis from brain-stem infarction: perspective on oculomotor fascicular organization in the ventral midbrain tegmentum. Arch Neurol 47:235, 1990