Each eye is moved by six muscles: four rectus muscles and two oblique muscles. These muscles are controlled by three nerves: cranial nerves (CNs) 3, 4, and 6. These cranial nerves all originate from brainstem nuclei that communicate with one another through the medial longitudinal fasciculus (MLF) to coordinate movements between the left and right eyes. These nuclei are controlled by brainstem gaze centers that coordinate the eyes to move together horizontally or vertically, and these gaze centers are stimulated by cortical eye fields. From the top down, the cortical eye fields stimulate the gaze centers in the brainstem, the brainstem gaze centers communicate with the cranial nerve nuclei of CN 3, CN 4, and CN 6, and CN3, CN 4, and CN 6 activate the extraocular muscles.
The vestibular system also interacts with the eyes to coordinate eye movements with head movements. This pathway involves CN 8 and the cerebellum, and is discussed further in Chapter 12.
The six muscles that control each eye are the four rectus muscles (superior, inferior, medial, lateral) and the two oblique muscles (superior and inferior) (Fig. 11–1 and Table 11–1). CN 4 controls the superior oblique, CN 6 controls the lateral rectus, and CN 3 controls the rest (superior, inferior, and medial recti and inferior oblique). The principal eye movements performed by the rectus muscles are easy to understand:
Lateral rectus (CN 6) moves the eye laterally (abducts)
Medial rectus (CN 3) moves the eye medially (adducts)
Superior rectus (CN 3) primarily moves the eye superiorly (elevates)
Inferior rectus (CN 3) primarily moves the eye inferiorly (depresses)
FIGURE 11–1
Schematic of the extraocular muscles and eye movements. A: The attachments of the extraocular muscles on the left eye, viewed laterally from the left side. B: The actions of the superior oblique as shown from above on the right eye (see text). C: Principal functions of the extraocular muscles demonstrated for the right eye. Note that the superior oblique and inferior oblique act maximally to depress and elevate the eye in the adducted position. Reproduced with permission from Aminoff M, Greenberg D, Simon R: Clinical Neurology, 9th ed. New York: McGraw-Hill Education; 2015.
| Cranial Nerve Innervation | Principal Action | Secondary Action | Effect of Weakness | |
|---|---|---|---|---|
| Superior rectus | CN 3 | Elevation | Intorsion in adducted position | Impaired upgaze |
| Inferior rectus | CN 3 | Depression | Extorsion in adducted position | Impaired downgaze |
| Medial rectus | CN 3 | Adduction | – | Impaired medial gaze |
| Lateral rectus | CN 6 | Abduction | – | Impaired lateral gaze |
| Superior oblique | CN 4 | Intorsion | Depression in adducted position | Impaired intorsion Impaired depression in adducted position |
| Inferior oblique | CN 3 | Extorsion | Elevation in adducted position | Impaired extorsion Impaired elevation in adducted position |
The principal eye movements performed by the oblique muscles are slightly more complicated. In addition to moving up, down, left, and right, the eyes can also rotate when the head is tilted to either side. Rotation of the eye toward the nose/midline is called intorsion and rotation toward the ear is called extorsion. As the head is tilted to the left and the eyes attempt to maintain fixation straight ahead, the left eye must intort (turn toward the nose) and the right eye must extort (turn toward the ear). As the head is tilted to the right, the right eye intorts and the left eye extorts. In sum, when the head tilts to one side, the eye on the side to which the head is tilted (bottom eye) intorts and the other eye (top eye) extorts (Fig 11–2). This is important in understanding the symptoms and signs of a CN 4 palsy, which is discussed further below.
Intorsion of the eye is the main role of the superior oblique muscle. However, when the eye is fully adducted, the superior oblique depresses the eye. To understand the actions of the superior oblique, take your left hand and place it on the crown of your head with your elbow sticking out to the left. Look straight ahead. Your head now represents the right eye and your arm represents the right superior oblique muscle, bent at the elbow to represent the bend of the superior oblique muscle as it passes through the pulley (trochlea) for which CN 4 is named (i.e., trochlear nerve). If you pull with your hand, this will tilt the head inward— this is intorsion. If you turn your head all the way to the left so you are looking at your elbow crease (adducting the right eye), now pulling with your hand causes the head to look down (depressing the eye). The angle of the superior oblique allows for it to intort the eye when the eye is midline or abducted, and to depress the eye when the eye is adducted (Fig 11-1B). The inferior oblique performs an equal but opposite function: extorsion of the eye when the eye is midline or abducted, and elevation of the eye when the eye is adducted.
The primary actions of the superior rectus and inferior rectus are what would be expected based on their names: superior rectus elevates the eye, inferior depresses it. However, these two muscles also perform rotatory functions. Just as the superior oblique intorts the eye, the superior rectus also contributes to intorsion; just as the inferior oblique extorts the eye, the inferior rectus also contributes to extorsion (mnemonic to recall that inferior muscles extort and superior muscles intort: InfEXions will leave you SupINe). Just as the superior and inferior oblique perform their secondary actions (depression and elevation) in the adducted position, the superior and inferior recti also perform their secondary actions (intorsion and extorsion) in the adducted position.
All of the ocular motor nerves originate in brainstem nuclei (CN 3 and CN 4 in the midbrain; CN 6 in the pons), and travel in the subarachnoid space, through the cavernous sinus, and then into the orbit. Lesions causing dysfunction of these cranial nerves can occur at one of four locations:
Nucleus or fascicle of CNs 3, 4, or 6 in the brainstem. The term fascicle refers to the portion of a cranial nerve that is still in the brainstem. Potential pathology in the brainstem includes stroke, tumor, and demyelination.
CNs 3, 4, or 6. Trauma and nerve infarct are the most common causes of isolated 3, 4, or 6 palsy. Trauma can affect CNs 3, 4, and 6 because their length and course render them susceptible to trauma. Nerve infarct of CN 3, 4, or 6 is most commonly caused by diabetes. CNs 3, 4, and 6 can also be affected by skull base tumors, aneurysms, subarachnoid hemorrhage, meningitis, and Guillain-Barré syndrome (especially the Miller Fisher variant; see “Guillain-Barré syndrome” in Ch. 27).
Cavernous sinus. CNs 3, 4, and 6 pass through the cavernous sinus along with the V1 and V2 branches of the trigeminal nerve (Fig. 11–3). Potential pathology here includes cavernous sinus thrombosis, carotid-cavernous fistula, pituitary tumors or pituitary apoplexy, and Tolosa-Hunt syndrome (an idiopathic inflammatory condition of the cavernous sinus).
Orbit. When CNs 3, 4, and/or 6 are affected in the orbit, the optic nerve is also often affected (this is not the case with cavernous sinus pathology since the optic nerve does not pass through the cavernous sinus). Potential orbital pathology includes tumors, infections (orbital cellulitis), and orbital pseudotumor (an idiopathic inflammatory condition of the orbit).
CN 3 originates in the medial dorsal midbrain and exits the midbrain anteriorly. It travels along the medial skull base, passing adjacent to the medial temporal lobe, through the cavernous sinus, and into the orbit. CN 3 innervates:
Superior rectus, medial rectus, inferior rectus, and inferior oblique (all extraocular muscles except superior oblique [innervated by CN 4] and lateral rectus [innervated by CN 6])
Levator palpebrae, which elevates the eyelid
Parasympathetic fibers to the pupil, which constrict it (see Ch. 10)
A complete third nerve palsy (Fig. 11–4) causes:
Weakness of the four supplied muscles, leaving the eye down and out: down due to the unopposed action of the superior oblique (CN 4) and out due to the unopposed action of the lateral rectus (CN 6)
Weakness of the levator palpebrae, causing ptosis
Decreased parasympathetic input to the pupil, leading to pupillary dilation (mydriasis)
FIGURE 11–4
Right pupil-sparing third nerve palsy (due to diabetic CN 3 infarct). The patient has ptosis of the right eye with the eye “down and out” (E). There is impaired adduction (C, F, I), impaired elevation (A, B, C), and impaired depression (G, H, I) of the right eye. Abduction is spared (A, D, G). Sparing of superior oblique function is difficult to observe in the setting of impaired adduction. Reproduced with permission from Martin T, Corbett J: Practical Neuroophthalmology. New York: McGraw-Hill Education; 2013.
Due to the way the different fibers run in the third nerve, partial lesions of the third nerve can affect the pupillary fibers in isolation or the ocular motor fibers in isolation. The pupillary fibers run on the medial exterior part of the nerve, whereas the oculomotor fibers run on the inside of the nerve. A lesion compressing the third nerve affects the outermost fibers first, which can lead to impaired pupillary constriction with no extraocular muscle dysfunction (or preceding the development of extraocular muscle dysfunction). On the other hand, an ischemic insult to the nerve will affect the innermost fibers supplied by small penetrating vessels, and can cause extraocular dysfunction with sparing of pupillary reactivity. This is called a pupil-sparing third nerve palsy (Fig. 11-4).
Compressive lesions that can affect CN 3 causing isolated (or initially isolated) pupillary dilatation without eye movement abnormalities include posterior communicating artery aneurysms, skull base tumors, and uncal herniation. Pupil-sparing third nerve palsy is most commonly due to nerve infarct caused by diabetes, which usually resolves over months. Pupil-involving third nerve palsy requires urgent neuroimaging to evaluate for aneurysm or other intracranial mass lesion. When the pupil is not involved in an otherwise complete CN 3 palsy, neuroimaging can be deferred, although in practice it is often obtained in this scenario as well.
Each CN 3 nuclear complex in the dorsal midbrain has several subnuclei: one for each extraocular muscle (superior rectus, inferior rectus, medial rectus, inferior oblique). The Edinger-Westphal nuclei provide parasympathetic input for pupillary constriction. The levator palpebrae muscles (which elevate the eyelid) are supplied bilaterally by a single nucleus called the central caudal nucleus. The central caudal nucleus projects bilaterally to allow for symmetric eyelid elevation. The superior rectus subnucleus of each third nerve nucleus projects contralaterally, and the crossing fibers pass in close proximity to the contralateral CN 3 nucleus. Therefore, a very small focal lesion of the entire third nerve nuclear complex on one side will cause ipsilateral impairment of all third nerve functions and bilateral involvement of the superior rectus. Lesions of the third nerve nucleus cause bilateral superior rectus weakness because the affected superior rectus subnucleus projects contralaterally (causing contralateral impairment of upgaze), and the crossing fibers projecting from the unaffected contralateral superior rectus subnucleus pass in close proximity to the affected nucleus, causing involvement of the eye ipsilateral to the side of the nuclear lesion. If the adjacent central caudal nucleus in the dorsal midbrain is also involved, this will cause bilateral ptosis.
The fascicle of each CN 3 travels anteriorly in the midbrain in proximity to the red nucleus, substantia nigra, and descending (not-yet-crossed) corticospinal tract before exiting as the third nerve itself. Fascicular lesions cause the same ocular findings as nerve lesions (without any contralateral/bilateral findings as can occur with lesions of the nucleus), and may be associated with contralateral motor symptoms/signs (Weber’s syndrome) due to the not-yet-crossed corticospinal tract, contralateral movement disorder (Benedikt’s syndrome) due to involvement of the substantia nigra, and/or contralateral tremor and/or contralateral ataxia (Claude’s syndrome) due to involvement of the red nucleus and crossed superior cerebellar peduncle (coming from the contralateral cerebellar hemisphere; see Ch. 8).
CN 4 originates in the dorsal midbrain and is the only cranial nerve to exit posteriorly and the only cranial nerve that crosses to project contralaterally. It innervates one muscle, the superior oblique. Like CN 3 and CN 6, it is susceptible to trauma and diabetic nerve infarct (although diabetic nerve infarct occurs less commonly in CN 4 than in CN 3 or CN 6). CN 4 can also be compressed by dorsal midbrain pathology (e.g., pineal mass).
When the head is tilted to one side, the eye that intorts is the one on the side of the head to which the patient is tilting the head (for example, if the patient tilts the head to the left, the left eye must intort, rotating equal and opposite to the direction that the head is tilting). When intorsion is impaired due to a CN 4 palsy, double vision (diplopia) occurs when the head is tilted toward the affected side since that eye cannot intort to maintain fixation. Therefore, the patient’s preferred head position is to tilt the head away from the affected side to keep the eyes aligned. In a left CN 4 palsy, a patient’s double vision will worsen when tilting the head to the left, and so the patient will prefer to keep the head tilted to the right. In a right CN 4 palsy, a patient’s double vision will worsen when tilting the head to the right, and so the patient will prefer to keep the head tilted to the left.
Patients with CN 4 palsy have vertical double vision that is worst in downgaze when looking away from the side of the affected eye (e.g., looking left if the right eye affected). This is because looking away from the side of the affected eye puts the affected eye in adduction, the position in which the superior oblique functions to depress the eye. When placed in the position that most needs the superior oblique (down and in), CN 4 dysfunction will be most evident, leading to double vision that is worst in this position (Fig. 11–5).
FIGURE 11–5
Schematic of right fourth nerve palsy. The right eye appears higher at baseline due to impaired depression (A). Depression of the eye is most impaired when looking away from the side of the affected eye, placing the affected eye in the adducted position (B), with less deficit when looking toward the affected side (affected eye abducted) (C). When the head is tilted toward the side of the affected eye, the affected eye cannot intort as it normally would, leading to increased dysconjugate gaze (D). When the head tilts away from the affected side, the eyes are aligned since extorsion is preserved (E). Reproduced with permission from Aminoff M, Greenberg D, Simon R: Clinical Neurology, 9th ed. New York: McGraw-Hill Education; 2015.
In summary for superior oblique palsies, the patient tilts the head away from the side of the palsy, and the diplopia worsens with downgaze away from the side of the affected eye (i.e., affected eye in adducted position). The trochlear nerve is the only cranial nerve that crosses, and as a mnemonic, its deficits can also be thought of as “crossed”: The head tilts away from the side of the superior oblique palsy, and diplopia worsens when looking away from the side of the superior oblique palsy (i.e., adducting the affected eye).
The abducens nuclei reside in the dorsomedial pons, and the bilateral CN 6 run from their nuclei through the anterior pons, exit anteriorly, and then pass over the clivus, through the cavernous sinus, to the orbits.
An abducens palsy leads to failure to abduct the affected eye (Fig. 11–6). Abduction weakness causes horizontal diplopia that worsens when looking toward the side of the abduction deficit (e.g., a right-sided CN 6 palsy will cause diplopia when looking to the right, which requires right eye abduction). If there are no other cranial nerve or extraocular muscle deficits, looking away from the side of the deficit should lead to complete resolution of double vision, since adduction and contralateral eye abduction are spared. If a CN 6 palsy causes complete paralysis of the lateral rectus, the affected eye may be misaligned medially at rest with no lateral movement of the eye on attempted gaze toward the affected side. With partial weakness, the eye may be able to abduct only partially, allowing some of the lateral sclera to remain visible on attempted lateral gaze (called inability to “bury the sclera”).
Related posts:
Stay updated, free articles. Join our Telegram channel
Full access? Get Clinical Tree
