Ocular Motor Cranial Nerves
Without neural activity, the visual axes are usually mildly to moderately divergent. The major tonic input to ocular motility is supplied by 3 pairs of ocular motor CNs—CNs III, IV, and VI—that innervate the 6 EOMs controlling ocular movement (Fig 1-29). In addition, CN III innervates the levator palpebrae superioris and the pupillary sphincter muscles.
Except for the inferior oblique muscle, the innervation to each of the EOMs occurs at approximately one-third of the distance from the apex. The inferior oblique muscle receives its innervation at approximately its midpoint from a neurovascular bundle running parallel to the lateral aspect of the inferior rectus muscle. All 6 EOMs receive their innervation on the inside surface, except for the superior oblique, where branches of CN IV terminate on the upper (outer) surface of the muscle.
See Chapter 7 for information on the clinical presentation of disorders due to infranuclear, fascicular, and peripheral ocular motor CN lesions.
Abducens nerve (sixth cranial nerve)
CN VI originates in the dorsal caudal pons just beneath the fourth ventricle. Its nucleus is surrounded by the looping fibers (genu) of CN VII and is adjacent to the PPRF and the MLF (Fig 1-30). The CN VI nucleus contains primary motoneurons and interneurons that cross to the contralateral MLF to reach the CN III nucleus. Thus, pathology affecting the CN VI nucleus produces an ipsilateral gaze palsy. The motor axons exiting the CN VI nucleus (approximately 4000–6000 axons) travel ventrally and slightly laterally, medial to the superior olivary nucleus, to exit on the ventral surface of the caudal pons. As the fascicles pass through the brainstem, they lie adjacent to the spinal tract of CN V and traverse the corticobulbar tracts. Exiting the brainstem, the nerve runs rostrally within the subarachnoid space on the surface of the clivus from the area of the cerebellopontine angle to the posterior superior portion of the posterior fossa. The nerve pierces the dura approximately 1 cm below the petrous apex and travels beneath the petroclinoid ligament (Gruber ligament, which connects the petrous pyramid to the posterior clinoid) to enter the canal of Dorello. Within the canal, CN VI travels with the inferior petrosal sinus. Once it becomes extradural, the nerve is within the cavernous sinus (the only CN within the substance of the cavernous sinus), where it runs parallel to the horizontal segment of the carotid artery and CN V1. It is also joined for a short segment by branches of the sympathetic chain lying within the wall of the intrapetrous carotid artery. Reaching the anterior portion of the cavernous sinus, CN VI traverses the superior orbital fissure (Fig 1-31) through the annulus of Zinn (see Fig 1-2C) to enter the medial surface of the lateral rectus muscle.
Figure 1-29 Lateral view of the course of CNs III, IV, and VI.
(Illustration by Dave Peace.)
Figure 1-30 Intra-axial course of the ocular motor nerves at the level of the pons (below) and midbrain (above). Note the relationship to the surrounding cerebellum and CNs V and VII.
(Illustration by Craig A. Luce.)
Figure 1-31 Anatomic relationships of the ocular motor nerves. A, Subarachnoid course of the ocular motor nerves. Note the relationship to the surrounding dural structures, particularly the tentorium and the dura of the clivus. The nerves enter dural canals at the posterior aspect of the cavernous sinus for CN III, at the tentorial edge for CN IV, and along the clivus for CN VI. B, Major blood vessels and their relationships to the ocular motor nerves. Note the passage of CN III between the superior cerebellar artery below and posterior cerebral artery above. CN VI runs by the anterior inferior cerebellar artery, which is a major branch off the basilar artery. C, Intracavernous course of the ocular motor nerves. CNs III and IV run in the lateral wall of the cavernous sinus along with CN V divisions CN V1 and CN V2. CN VI runs in close approximation to the carotid artery within the cavernous sinus itself. As the nerves course toward the anterior aspect of the cavernous sinus and the superior orbital fissure, the ophthalmic branch of CN V (CN V1) divides into 3 branches: the lacrimal, frontal, and nasociliary nerves. ACoA = anterior communicating artery; ACP = anterior clinoid process; ICA = internal carotid artery; Inf. Br. = inferior branch; Prox = proximal; Sup. Br. = superior branch. C, Intracavernous course of the ocular motor nerves. CNs III and IV run in the lateral wall of the cavernous sinus along with CN V divisions CN V1 and CN V2. CN VI runs in close approximation to the carotid artery within the cavernous sinus itself. As the nerves course toward the anterior aspect of the cavernous sinus and the superior orbital fissure, the ophthalmic branch of CN V (CN V1) divides into 3 branches: the lacrimal, frontal, and nasociliary nerves. ACoA = anterior communicating artery; ACP = anterior clinoid process; ICA = internal carotid artery; Inf. Br. = inferior branch; Prox = proximal; Sup. Br. = superior branch.
(Illustrations by Craig A. Luce.)
Trochlear nerve (fourth cranial nerve)
The CN IV nucleus lies within the gray matter in the dorsal aspect of the caudal midbrain just below the aqueduct, directly contiguous with the more rostral CN III nucleus (see Fig 1-30). The intra-axial portion (fascicle) of CN IV is very short, running dorsally around the periaqueductal gray to cross within the anterior medullary vellum just caudal to the inferior colliculi and below the pineal gland. CN IV is the only CN that exits on the dorsal surface of the brainstem and has the longest unprotected intracranial course (which is probably responsible for its frequent involvement in closed-head trauma). Within the subarachnoid space, CN IV (which contains approximately 2000 fibers) swings around the midbrain, paralleling the tentorium just under the tentorial edge (where it is easily damaged during neurosurgical procedures that involve the tentorium).
CN IV enters the posterior lateral aspect of the cavernous sinus below the anterior tentorial insertion and underneath CN III. Covered by a variable sheath, CN IV runs forward within the lateral wall of the cavernous sinus. Anteriorly, CN IV crosses over CN III to enter the superior orbital fissure outside and superior to the annulus of Zinn. CN IV crosses over the optic nerve to enter the superior oblique muscle within the superior medial orbit.
Oculomotor nerve (third cranial nerve)
The CN III nucleus is located dorsally within the midbrain beneath the aqueduct connecting the third and fourth ventricles (see Fig 1-30). The nuclear complex itself represents a collection of subnuclei that have specific identifiable functions (Fig 1-32). The fibers destined to innervate the levator palpebrae superioris, medial rectus, inferior rectus, pupil sphincter, and ciliary body muscles exit ventrally ipsilateral to the individual nuclei from which they originate. In contrast, the fibers from the superior rectus subnucleus, which lies along the midline, cross before exiting the brainstem to innervate the superior rectus muscle. Within the midbrain, CN III is topographically organized into a superior division (supplying the superior rectus and levator palpebrae superioris muscles) and an inferior division (supplying the medial and inferior rectus, inferior oblique, pupillary sphincter, and ciliary body muscles), but the true anatomical division into 2 branches occurs at the level of the anterior cavernous sinus/superior orbital fissure.
The fascicles of CN III traverse the ventral midbrain tegmentum, passing near and possibly through the red nucleus, the substantia nigra, and the corticospinal tracts within the cerebral peduncle. Numerous fascicles, totaling approximately 15,000 fibers, exit on the ventral surface of the peduncles. Although considered to be a single structure within the subarachnoid space, as is the case in the midbrain, the nerve and its various fibers are topographically organized. Within the subarachnoid space, the nerve passes between the SCA below and the PCA above. The nerve runs slightly oblique to the tentorial edge, parallel and lateral to the PCoA. The pupillary fibers are usually found on the dorsomedial surface of the nerve, where they are anatomically vulnerable to compression. The uncus, which is the most medial aspect of the temporal lobe, is located just above the tentorium and the subarachnoid portion of CN III. Unilateral supratentorial mass lesions may force the uncus through the tentorial notch (uncal herniation) to compress the ipsilateral CN III.
Figure 1-32 Oculomotor nucleus complex. Note that all extraocular muscles served by CN III are innervated by their respective ipsilateral nuclei except the superior rectus muscle. Parasympathetic fibers traveling to the pupillary sphincter muscle synapse in the ciliary ganglion in the orbit (see Fig 1-38).
(Illustration by Christine Gralapp.)
At the back edge of the dura of the clivus and cavernous sinus, the nerve enters its own dural canal just above CN IV. Running forward in the superior lateral wall of the cavernous sinus, the nerve separates into 2 divisions: (1) superior and (2) inferior. These divisions enter the orbit through the superior orbital fissure within the annulus of Zinn. The superior division runs forward intraconally to innervate first the superior rectus muscle and then the levator palpebrae superioris muscle. The inferior division sends parasympathetic fibers to the ciliary ganglion in the orbital apex approximately 10 mm anterior to the annulus of Zinn and lateral to the optic nerve. Within the ciliary ganglion, the fibers destined for the pupillary sphincter and the ciliary body synapse. The fibers subsequently accompany the branch destined for the inferior oblique muscle. There are approximately 9–10 times as many fibers associated with accommodation innervating the ciliary body as there are fibers reaching the pupillary sphincter muscle. This disparity may be one reason for the development of light–near dissociation in Adie tonic pupil (see Fig 10-6). The remaining branches of CN III within the orbit innervate the medial rectus and inferior rectus muscles.
Bhatti MT, Eisenschenk S, Roper SN, Guy JR. Superior divisional third cranial nerve paresis: clinical and anatomical observations of 2 unique cases. Arch Neurol. 2006;63(5): 771–776.
Excerpted from BCSC 2020-2021 series: Section 5 - Neuro-Ophthalmology. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.