Oculomotor Nerve (Third Cranial Nerve)
Although the oculomotor nerve (CN III) contains only 24,000 fibers, it supplies all the extraocular muscles except the superior oblique and the lateral rectus, which are innervated by the trochlear nerve and abducens nerve, respectively. It also provides parasympathetic cholinergic innervation to the pupillary sphincter and the ciliary muscle.
CN III arises from a complex group of cells in the rostral midbrain, or mesencephalon, at the level of the superior colliculus. This nuclear complex lies ventral to the periaqueductal gray matter, is immediately rostral to the CN IV nuclear complex, and is bounded inferolaterally by the medial longitudinal fasciculus.
The CN III nucleus consists of several distinct, large motor cell subnuclei, each of which subserves the extraocular muscle it innervates (Fig 3-15). The subnuclei innervate the following:
ipsilateral inferior rectus muscle
ipsilateral inferior oblique muscle
ipsilateral medial rectus muscle
contralateral superior rectus muscle
Except for a single central, caudal subnucleus that serves both levator palpebrae superioris muscles, the cell groups are paired. Notably, the shared innervation of both levator muscles is an example of Hering’s law of equal innervation.
Figure 3-16 Relationship of the lateral geniculate nucleus (LGN) to nearby structures and its blood supply. AChoA = anterior choroidal artery; BC = brachium conjunctivum; CerePed = cerebral peduncles; ICA = internal carotid artery; MCA = middle cerebral artery; MGN = medial geniculate nucleus; ON = optic nerve; PCA = posterior cerebral artery; PCoA = posterior communicating artery; PLChA = posterior lateral choroidal artery; Pulv = pulvinar; RN = red nucleus; SC = superior colliculus; SCA = superior cerebellar artery.
(Illustration by Craig A. Luce.)
Fibers from the dorsal subnucleus to the superior rectus uniquely cross, or decussate, in the caudal aspect of the nucleus and therefore supply the contralateral superior rectus muscles. The Edinger-Westphal nucleus is rostral in location. It provides the parasympathetic preganglionic efferent innervation to the ciliary muscle and pupillary sphincter. The most ventral subnuclei supply the medial rectus muscles. A subnucleus for ocular convergence has been described but is not consistently found in primates.
The fascicular portion of CN III travels ventrally from the nuclear complex, through the red nucleus, between the medial aspects of the cerebral peduncles, and through the corticospinal fibers (see Fig 3-2). It exits in the interpeduncular space. In the subarachnoid space, CN III passes below the posterior cerebral artery (PCA) and above the superior cerebellar artery, the 2 major branches of the basilar artery (Fig 3-16). The nerve travels forward in the interpeduncular cistern lateral to the posterior communicating artery (PCoA) and penetrates the arachnoid between the free and attached borders of the tentorium cerebelli. About 20% of patients with PCoA aneurysms have isolated oculomotor nerve palsy on presentation, and about 80% of aneurysms occurring with CN III palsy were located in the PCoA—usually at the junction of the PCoA and the ICA.
Figure 3-17 Anterior view of the right orbital apex showing the distribution of the nerves as they enter through the superior orbital fissure and optic canal. This view also shows the annulus of Zinn, the fibrous ring formed by the origin of the 4 rectus muscles.
(Reproduced with permission from Levin LA, Nilsson SFE, Ver Hoeve J, Wu SM. Adler’s Physiology of the Eye. 11th ed. Philadelphia: Elsevier/Saunders; 2011:187.)
The oculomotor nerve pierces the dura mater on the lateral side of the posterior clinoid process (see Fig 3-24), initially traversing the roof of the cavernous sinus (see Fig 3-25). It runs along the lateral wall of the cavernous sinus and above CN IV and enters the orbit through the superior orbital fissure (see Fig 3-1).
CN III usually separates into superior and inferior divisions after passing through the annulus of Zinn in the orbit (Fig 3-17). Alternatively, it may divide within the anterior cavernous sinus. The nerve maintains a topographic organization even in the midbrain, so lesions almost anywhere along its course may cause a divisional nerve palsy.
The superior division of CN III innervates the superior rectus and levator palpebrae superioris muscles. The larger inferior division splits into 3 branches to supply the medial rectus, inferior rectus, and inferior oblique muscles.
The parasympathetic fibers wind around the periphery of the nerve, enter the inferior division, and course through the branch that supplies the inferior oblique muscle. They join the ciliary ganglion, where they synapse with the postganglionic fibers, which emerge as many short ciliary nerves. These nerves pierce the sclera and travel through the choroid to innervate the pupillary sphincter and the ciliary muscle. The superficial location of these fibers makes them more vulnerable to compression, such as from an aneurysm, than to ischemia.
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Trobe JD. Searching for brain aneurysm in third cranial nerve palsy. J Neuro-Ophthalmol. 2009;29(3):171–173.
Pathways for the Pupil Reflexes
The light reflex (also called pupillary light reflex, pupillary reflex) consists of a simultaneous and equal constriction of the pupils in response to illumination of one eye or the other (Fig 3-18). Of note, when the preganglionic parasympathetic fibers leave each Edinger-Westphal nucleus, they run on the superficial surface of the oculomotor nerve (CN III) as it leaves the brainstem, then spiral downward to lie medially in the nerve at the level of the petroclinoid ligament and inferiorly in the inferior division of CN III as it enters the orbit. These fibers synapse in the ciliary ganglion (Fig 3-19) and give rise to postganglionic myelinated short ciliary nerves, approximately 3%–5% of which are pupillomotor. The rest are designated for the ciliary muscle and are concerned with the near reflex.
The near reflex (also called near synkinesis, near triad), is a synkinesis that occurs when attention is changed from distance to near (see Fig 3-18). This reflex includes the triad of accommodation, pupil constriction, and convergence. The convergence reflex is initiated in the occipital association cortex, from which impulses descend along corticofugal pathways to relay in pretectal and possibly tegmental areas. From these relays, fibers pass to the Edinger-Westphal nuclei and both motor nuclei of the medial rectus muscles. Fibers for the near reflex approach the pretectal nucleus from the ventral aspect; thus, compressive dorsal lesions of the optic tectum spare the near pupil reflex relative to the light reflex (light–near dissociation). Efferent fibers for accommodation follow the same general pathway as do those for the light reflex, but their final distribution (via the short ciliary nerves) is to the ciliary muscle.
Figure 3-18 Pathway of the pupillary reflexes. Light reflex (pupillary light reflex): Light from each eye passes via electrical signals through the optic nerve, and nasal fibers decussate in the optic chiasm, providing signals in both optic tracts. The pupillary fibers exit the optic tract posteriorly, reaching the pretectal nuclei at the level of the superior colliculus in the midbrain. Efferent fibers project to the ipsilateral and contralateral Edinger-Westphal nuclei. Preganglionic parasympathetic fibers leave each Edinger-Westphal nucleus and run on the superficial surface of the oculomotor nerve as it leaves the brainstem. The fibers follow the inferior division of CN III as it enters the orbit, synapsing in the ciliary ganglion. Postganglionic myelinated short ciliary nerves (3%–5% of which are pupillomotor) then innervate the iris and the ciliary muscle. Near reflex: Fibers for the near reflex follow a similar efferent course, inducing miosis, but they also act at the ciliary muscle to induce accommodation.
(Illustration by Christine Gralapp.)
Excerpted from BCSC 2020-2021 series: Section 2 - Fundamentals and Principles of Ophthalmology. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.