Cranial Nerve Innervation of Ocular Structures

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Chapter 12 Cranial Nerve Innervation of Ocular Structures

The orbital structures are innervated by cranial nerves (CNs) II, III, IV, V, VI, and VII (Table 12-1). Motor functions of the striated muscles are controlled by CN III, the oculomotor nerve; CN IV, the trochlear nerve; CN VI, the abducens nerve; and CN VII, the facial nerve. CN V, the trigeminal nerve, carries the sensory supply from the orbital structures. CN II, the optic nerve, carries visual information and is discussed in Chapter 13. This chapter discusses sensory and motor innervation of the orbit, including pathways, functions, and presenting signs of dysfunction.

Afferent Pathway: Orbital Sensory Innervation

The eye is richly supplied with sensory nerves that carry sensations of touch, pressure, warmth, cold, and pain. Sensations from the cornea, iris, conjunctiva, and sclera consist primarily of pain; even light touching of the cornea is registered as irritation or pain.1

Trigeminal Nerve

The fibers of the trigeminal nerve (CN V) serving ocular structures are sensory and originate in the innervated structures. The description of the pathways of these nerves begins at the involved structures and follows the nerves as they join to become larger nerves, come together in the ganglion of the fifth cranial nerve, and then exit the ganglion and enter the pons. It is hoped that this presentation, although unconventional, will enable the reader to keep in mind the actual direction of the action potential, and thus the information flow, in these fibers. Figure 12-1 shows the major branches and paths of the trigeminal nerve within the orbit.

Ophthalmic Division of Trigeminal Nerve

Nasociliary Nerve

Sensory fibers from the structures of the medial canthal area—caruncle, canaliculi, lacrimal sac, medial aspect of the eyelids, and skin at the side of the nose —join to form the infratrochlear nerve. This nerve penetrates the orbital septum, enters the orbit below the trochlea, and runs along the upper border of the medial rectus muscle, becoming the nasociliary nerve as other branches join it (see Figure 12-1).

Sensory fibers from the skin along the center of the nose, the nasal mucosa, and the ethmoid sinuses form the anterior ethmoid nerve; fibers from the ethmoid sinuses and the sphenoid sinus form the posterior ethmoid nerve. The ethmoid nerves enter the orbit with their companion arteries through foramina within the frontoethmoid suture.2 Both nerves join the nasociliary nerve as it runs along the medial aspect of the orbit (see Figure 12-1).

Corneal sensory innervation is dense, estimated to be 400 times as dense as other epithelial tissue innervation.3 Three networks of nerves are formed. One is located in the corneal epithelium, another (the subepithelial plexus) is in the anterior stroma, and the third, the stromal plexus, is in the middle of the stroma4 (Figure 12-2). No nerves are found in posterior stroma, Descemet’s membrane, or endothelium. The fibers from these plexus come together in peripheral stroma and radiate out into the limbus as 70 to 80 branches; they become myelinated in the last 2 mm of the cornea.57

Some of these branches join with nerves from other anterior segment structures to form two long ciliary nerves. These long ciliary nerves, one on the lateral side and one on the medial side of the globe, course between the choroid and sclera to the back of the eye, where they leave the globe at points approximately 3 mm on each side of the optic nerve (Figure 12-3). (In addition to afferent fibers, the long ciliary nerves transmit sympathetic fibers to the dilator muscle of the iris.) The two long ciliary nerves then join the nasociliary nerve.

The other branches radiating from the cornea into the limbus join other sensory nerves from the anterior segment; they enter the choroid, join with the choroidal nerves, then course to the back of the eye, where they leave as 6 to 10 short ciliary nerves (see Figure 12-3). The short ciliary nerves exit the sclera in a ring around the optic nerve in company with the short posterior ciliary arteries and enter the ciliary ganglion (see Figure 12-1). The sensory fibers do not synapse but pass through the ganglion, leaving as the sensory root of the ciliary ganglion, which then joins the nasociliary nerve. (The short ciliary nerves carry sympathetic and parasympathetic fibers in addition to sensory fibers.)

Thus, the nasociliary nerve is formed by the joining of the infratrochlear nerve, the anterior and posterior ethmoid nerves, the long ciliary nerves, and the sensory root of the ciliary ganglion (see Figure 12-1). The nasociliary nerve exits the orbit by passing through the oculomotor foramen within the common tendinous ring and the superior orbital fissure into the cranial cavity.

Clinical Comment: Herpes Zoster

HERPES ZOSTER is an acute CNS infection caused by the varicella-zoster virus. Signs and symptoms include pain and rash in the distribution area supplied by the affected sensory nerves.9 It is believed that the virus lies dormant in a sensory ganglion and, on becoming activated, migrates down the sensory pathway to the skin.10 An eruption of herpes zoster is more common in elderly persons but may occur at any age and may be related to a delayed hypersensitivity reaction.11 Approximately 10% of all cases affect the ophthalmic division of the trigeminal nerve.12 Involvement of the tip of the nose often indicates that the eye will also be involved, reflecting the distribution of the nasociliary branches. This association of ocular involvement with zoster affecting the tip of the nose is the Hutchinson sign.13

Ophthalmic Nerve Formation

After exiting the orbit, the nasociliary nerve, the lacrimal nerve, and the frontal nerve join and form the ophthalmic division of the trigeminal nerve (see Figure 12-1). The ophthalmic nerve then enters the lateral wall of the cavernous sinus, coursing between the two dural layers.14 While in the wall of the sinus the nerve receives sensory fibers from the oculomotor, trochlear, and abducens nerves. Some of these fibers probably carry proprioceptive information from the extraocular muscles.15

Maxillary Division of Trigeminal Nerve

Infraorbital Nerve

The infraorbital nerve, formed by sensory fibers from the cheek, upper lip, and lower eyelid, enters the maxillary bone through the infraorbital foramen (Figure 12-5). It runs posteriorly through the infraorbital canal and groove; while it is in the maxillary bone, branches join from the upper teeth and maxillary sinus. As the nerve leaves the infraorbital groove it exits the orbit through the inferior orbital fissure and joins other fibers in forming the maxillary nerve.

image

FIGURE 12-5 Three divisions of trigeminal nerve.

(From Mathers LH, Chase RA, Dolph J, et al: Clinical anatomy principles, St Louis, 1996, Mosby.)

Clinical Comment: Referred Pain

REFERRED PAIN is pain felt in an area remote from the actual site of involvement; however, the two areas usually are connected by a sensory nerve network. Frequently, the pathways of the trigeminal nerve are involved in referred pain. A common example is a momentary severe bilateral frontal headache sometimes experienced when an individual eats ice cream.5 An abscessed tooth can cause pain described by a patient as ocular pain and should be suspected when no orbital cause for the pain can be found. This situation likely occurs because the overload of sensation carried by the infraorbital nerve from the upper teeth is interpreted by the brain as coming from another area also served by the trigeminal nerve.

Trigeminal Nerve Formation

As the ophthalmic and maxillary divisions enter the skull, they run posteriorly within the lateral wall of the cavernous sinus (Figure 12-6).16,17 The mandibular division lies just below the cavernous sinus. The sensory fibers from the three divisions enter the trigeminal ganglion (gasserian ganglion, semilunar ganglion), where they synapse. The ganglion, flattened and semilunar in shape, is located lateral to the internal carotid artery and the posterior portion of the cavernous sinus. The motor fibers of the mandibular division, which innervate the muscles of mastication, pass along the lower edge of the ganglion.18 Only the sensory fibers synapse within the ganglion.

image

FIGURE 12-6 Detailed cross section of cavernous sinus.

(From Mathers LH, Chase RA, Dolph J, et al: Clinical anatomy principles, St Louis, 1996, Mosby.)

The fibers leave the trigeminal ganglion and enter the lateral aspect of the pons as either the sensory root or the motor root of the trigeminal nerve. The sensory root carries information from the structures of the face and head, including all orbital structures. After entering the brain stem, these fibers form an ascending and a descending tract, both terminating in sensory nuclei of the trigeminal nerve (Figure 12-7). The ascending tract terminates in the principal sensory nucleus in the pons; it registers the sensations of touch and pressure.1 The descending tract, which carries pain and temperature sensations, courses through the pons and medulla to the elongated nucleus of the spinal tract.1 The tract extends into the second cervical segment of the spinal cord.19 Information from the trigeminal nuclei is relayed to the thalamus.

Clinical Comment: Oculocardiac Reflex

THE OCULOCARDIAC REFLEX consists of bradycardia (slowed heartbeat), nausea, and faintness and can be elicited by pressure on the globe or stretch on the extraocular muscles (e.g., during ocular surgery).2022 Fibers from the trigeminal spinal nucleus project into the reticular formation near the vagus nerve nuclei and can activate vagus synapses, precipitating this reflex. The motor aspect of the reflex can be blocked by retrobulbar anesthesia or intravenous or intramuscular atropine.1,13,23,24

Efferent Pathway: Motor Nerves

The cranial nerves that supply striated muscles of the orbit and adnexa are the oculomotor nerve, the trochlear nerve, the abducens nerve, and the facial nerve.

Oculomotor Nerve: Cranial Nerve III

The oculomotor nerve innervates the superior rectus, medial rectus, inferior rectus, inferior oblique, and superior palpebral levator muscles. It also provides a route along which the autonomic fibers travel to innervate the iris sphincter muscle, the ciliary muscle, and the smooth muscles of the eyelid.

Oculomotor Nucleus

The oculomotor nucleus is located in the midbrain, at the level of the superior colliculus, ventral to the cerebral aqueduct, and dorsal to the medial longitudinal fasciculus (Figure 12-8).28 It extends in a column from the posterior edge of the floor of the third ventricle to the trochlear nucleus.2,13

A definitive area or subnucleus within the oculomotor nucleus controls each muscle. The proposed arrangement of the subnuclei are postulated primarily on the basis of animal models.23,2527 The nucleus for the medial rectus is located toward the lower border of the oculomotor nucleus; the inferior rectus nucleus lies toward the upper border, with the nucleus for the inferior oblique between. The nucleus of the superior rectus lies in the medial and caudal two thirds of the oculomotor nucleus. Each of these subnuclei are found in the right and left oculomotor nucleus. The nucleus for the levator muscle is single and is located centrally in the caudal area (Figure 12-9).

Fibers to the inferior rectus, inferior oblique, and medial rectus muscles supply the ipsilateral eye; fibers innervating the superior rectus muscle decussate and supply the contralateral eye. The decussating fibers pass through the opposite superior rectus nucleus; thus damage to the right oculomotor nucleus might have bilateral superior rectus muscle involvement.2730 The centrally placed caudal nucleus provides innervation for both levator muscles.

An autonomic nucleus, the accessory third nerve nucleus (Edinger-Westphal nucleus), supplies parasympathetic innervation to the ciliary and iris sphincter muscles. It is located in the rostral, ventral portion of the oculomotor nucleus30,31 (see Figure 12-9).

Oculomotor Nerve Pathway

Fibers from each of the individual nuclei join, forming the fascicular part of the nerve that passes through the red nucleus and the decussating fibers of the superior cerebellar peduncle.32 These fibers emerge just medial to the cerebral peduncles and within the interpeduncular fossa on the anterior aspect of the midbrain as the oculomotor nerve. The nerve passes between the superior cerebellar and posterior cerebral arteries as it runs forward, lateral to, and slightly inferior to the posterior communicating artery of the circle of Willis (Figure 12-10). The nerve pierces the roof of the cavernous sinus and runs within the two dural layers of its lateral wall above the trochlear nerve2,14,16 (see Figure 12-6). While in the cavernous sinus, the oculomotor nerve sends small sensory branches (likely proprioceptive) to the ophthalmic nerve and receives sympathetic fibers from the plexus around the internal carotid artery.2,19

The oculomotor nerve exits the sinus and enters the orbit through the superior orbital fissure, having divided into superior and inferior divisions; both divisions are located within the oculomotor foramen. The superior branch runs medially above the optic nerve and enters the superior rectus on its inferior surface; additional fibers either pierce the muscle or pass around its border to innervate the levator14,33 (Figure 12-11).

The inferior branch runs below the optic nerve and divides into three branches. One branch enters the medial rectus on its lateral surface, and one enters the inferior rectus on its upper surface (see Figure 12-11). The third branch gives off parasympathetic fibers that form the parasympathetic root extending to the ciliary ganglion; then it runs along the lateral border of the inferior rectus, crossing it to enter the inferior oblique muscle near its midpoint.5,14,34,35

Trochlear Nerve: Cranial Nerve IV

The trochlear nerve innervates the superior oblique muscle.

Trochlear Nucleus

The trochlear nucleus is located in the midbrain, at the level of the inferior colliculus, anterior to the cerebral aqueduct, dorsal to the medial longitudinal fasciculus, and below the oculomotor nucleus32 (see Figure 12-8). The fibers travel dorsally and decussate. CN IV is the only cranial nerve to cross; thus the trochlear nucleus innervates the contralateral superior oblique muscle.

Abducens Nerve: Cranial Nerve VI

The abducens nerve innervates the lateral rectus muscle.

Abducens Nucleus

The abducens nucleus is located near the inferior dorsal midline of the pons beside the floor of the fourth ventricle (see Figure 12-8). The fibers from the nucleus pass through the pons and lie adjacent to the corticospinal tract for part of their path32; they exit in the groove between the pons and the medulla oblongata. The abducens nucleus also contains internuclear neurons that communicate with the nucleus for the contralateral medial rectus muscle in the oculomotor complex via the medial longitudinal fasciculus.36 This is the pathway for conjugate horizontal eye movements. This pathway receives information from higher CNS centers, including the paramedial pontine reticular formation, the cerebellum, and the vestibular nucleus. Thus coordinated movement of the ipsilateral lateral rectus muscle and the contralateral medial rectus muscle results in conjugate horizontal eye movement.36

Abducens Nerve Pathway

In its long, tortuous, intracranial course, the abducens nerve runs along the occipital bone at the base of the skull and up along the posterior slope of the petrous portion of the temporal bone, makes a sharp bend over the petrous ridge (see Figure 12-10), and enters the cavernous sinus.5,13,37 Within the sinus it lies near the lateral wall of the internal carotid artery6,38 (see Figure 12-6). Small sympathetic branches leave the internal carotid plexus and travel with the abducens nerve. The abducens carries these autonomic fibers and sensory fibers, which are possibly proprioceptive, to the ophthalmic division of the trigeminal nerve.38 The abducens nerve enters the orbit through the superior orbital fissure within the common tendinous ring and innervates the lateral rectus muscle on the medial surface (see Figure 12-11).

Facial Nerve: Cranial Nerve VII

The facial nerve has two roots: the large motor root innervates the facial muscles, and the smaller root contains sensory and parasympathetic fibers. The sensory fibers carry taste sensations from the tongue. The parasympathetic nerves supply secretomotor fibers to various glands of the face; those supplying the lacrimal gland are discussed in Chapter 14.

Facial Nerve Pathway

The fibers leave the facial nucleus, arch around the abducens nucleus, and emerge as the facial nerve from the brain stem at the lower border of the pons. The facial nerve enters the internal acoustic foramen in the petrous portion of the temporal bone and runs through a canal in the bone. While in the temporal bone, parasympathetic fibers en route to the lacrimal gland are given off as the greater petrosal nerve.39,40 The motor fibers of the facial nerve emerge through the stylomastoid foramen, pass below the external auditory canal, travel over the mandibular ramus, and divide into several branches (Figure 12-12). The upper two — the temporal and zygomatic branches — supply the frontalis, procerus, corrugator, and orbicularis muscles.

The following Clinical Comments discuss damage to the cranial nerves, specifically the oculomotor, trochlear, and abducens nerves, caused by involvement of adjacent cranial and orbital structures and the resulting clinical presentation.

Clinical Comment: Cranial Nerve Damage

Injury to sensory cranial nerve fibers results in anesthesia, a loss of sensation in the innervated area. Injury to a cranial motor nerve causes either a partial loss (paresis) or a total loss (paralysis) of muscle function. Paresis or paralysis of an extraocular muscle can result in diplopia if the involvement is acquired; in congenital involvement, diplopia usually is not a complaint because the brain has learned to disregard the double image, resulting in suppression.

Nerve fibers can be ischemic, damaged by a compromised blood supply caused by vascular diseases (e.g., hypertension, atherosclerosis, diabetes mellitus) or by space-occupying lesions (e.g., aneurysms, hemorrhages, tumors) that exert pressure on the nerve fibers. The location of the involvement will influence the presenting signs and symptoms.

In some studies of isolated extraocular muscle nerve paralysis, the sixth cranial nerve is reported to be affected most often, and the fourth cranial nerve affected least often.4143 The tortuosity and length of the abducens nerve make it susceptible to compression and stretching injuries and may explain why it is damaged so frequently.16

A number of clinical signs and symptoms accompany damage to the motor nerves that innervate the extraocular muscles. Muscle paresis or paralysis will be evident in testing ocular motility (as described in Chapter 10). In acquired extraocular muscle impairment, a patient often attempts to minimize diplopia by carrying the head in a compensatory position. If a horizontal deviation is present, the head will be turned to the right or left. With a vertical deviation, the head is raised or lowered, and if a torsional deviation occurs the head is tilted toward the shoulder usually away from the involved side.35 With right superior oblique involvement the head may be turned to the left, positioned down, and tilted toward the left shoulder44,45 (Figure 12-13).

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FIGURE 12-13 Patient tilts head toward the left shoulder and turns head to the left and down, resulting from right superior oblique dysfunction.

(From Eskridge JB: Evaluation and diagnosis of incomitant ocular deviations, J Am Optom Assoc 60[5]:378, 1989.)

Clinical Comment: Oculomotor Damage

Midbrain Involvement

A lesion in the midbrain can affect the entire oculomotor nucleus or selectively affect only some subnuclei; however, such selective damage is unusual.28 If the lesion affects the entire oculomotor nucleus, the muscles involved are the ipsilateral medial rectus, inferior rectus, and inferior oblique, contralateral superior rectus, and both levators. The ipsilateral superior rectus might be involved as well because the decussating fibers pass through the contralateral superior rectus nucleus.28,32 Dilation of the pupil may also be present. The trochlear nucleus is near the oculomotor nucleus, and if it too is involved, the contralateral superior oblique muscle will be affected. The clinical presentation would show the ipsilateral eye positioned out in primary position and only able to move in as far as the midline. The contralateral eye would be unable to elevate in abduction and unable to depress in adduction.

Intracranial Involvement

The oculomotor nerve lies near several blood vessels in its intracranial path and frequently is affected by an aneurysm of the posterior communicating artery.46An aneurysm of the superior cerebellar artery or the posterior cerebral artery could also impinge on the nerve, damaging fibers.

Once the oculomotor nerve exits the midbrain, all its fibers supply the ipsilateral eye, and the dysfunction is unilateral. Damage to the nerve results in ptosis because of levator muscle paralysis; in primary position, the eye is positioned out because of the unopposed action of the superior oblique and lateral rectus muscles (Figure 12-14, A and B). (Because the superior oblique muscle is unaffected, the eye also should be positioned down, but clinically this is not always evident.47) The eye cannot adduct (Figure 12-14, D) and, in the abducted position, cannot move up or down (Figure 12-14, E and F).2 If injury involves the cerebral peduncles, a contralateral hemiparesis will be present.48 In paralysis of the iris sphincter and ciliary muscle, the pupil will be dilated, and accommodation will not occur.

Incomplete lesions of the oculomotor nerve are possible. In external ophthalmoplegia, the extraocular muscles are paralyzed and the intrinsic muscles (those to the iris sphincter and the ciliary muscle) are spared; in internal ophthalmoplegia the internal muscles are paralyzed and the extraocular muscles are spared. As the oculomotor nerve exits the midbrain, the parasympathetic fibers are superficial, and as the nerve nears the orbit, the parasympathetic fibers move into the center of the nerve and therefore are better protected in compressive lesions. The parasympathetic fibers are often spared in ischemic lesions, accounting for normal pupillary responses usually seen with diabetic ophthalmoplegia.28,4951 Third nerve palsies that include a dilated pupil are highly suspicious of a compressive lesion.

Aberrant Regeneration of the Oculomotor Nerve

After injury, the brain may attempt to repair a nerve, and some attempts may be misdirected, eliciting an unusual clinical presentation. Lid elevation might occur with downward gaze or adduction.32 Some cases even can involve pupil responses; fibers going to the inferior oblique may sprout branches that also innervate the sphincter, causing pupillary constriction on elevation. Fibers innervating the medial rectus may send sprouts that innervate the sphincter, causing miosis with adduction or convergence.

Clinical Comment: Trochlear Damage

When the superior oblique muscle is affected by trochlear nerve damage, the eye is elevated in primary gaze and is unable to move down in the adducted position. The head may be tilted toward the opposite shoulder to compensate for the unopposed extortion of the inferior oblique muscle5 (see Figure 12-13). Under the age of 10 years, palsies involving the trochlear nerve are usually congenital, and between 21 and 40 years of age the usual cause is trauma; otherwise the palsy may be idiopathic.5254

Clinical Comment: Abducens Damage

Damage to the abducens nerve results in paralysis of the lateral rectus muscle; because of the unopposed action by the medial rectus muscle, a convergent strabismus is evident.55 The eye will be unable to abduct (Figure 12-16). The patient might try to compensate for the diplopia by turning the face toward the paralyzed side.5

image

FIGURE 12-16 Sixth nerve palsy OS. A, Primary position, left eye positioned in. B, Unable to abduct; C, Normal adduction.

(From Kanski JJ: Clinical ophthalmology: a systematic approach, ed 5, Oxford, UK, 2003, Butterworth-Heinemann.)

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