Chapter 4 - Extraocular movement

Eye movements are controlled by muscles innervated by cranial nerves III, IV and VI. In this chapter, the testing of these cranial nerves will be discussed. The most common symptom of damage to these nerves is double vision. The oculomotor nerve has the additional function of control of the pupil and therefore this will be discussed here as well. Eye movements are carefully controlled by other systems. Some of these will be discussed here, while others, such as the vestibular system, will primarily be discussed in other chapters.

Cranial nerves III, IV, VI. Ocular Motility

Oculomotor function can be divided into two categories: (1) extraocular muscle function and (2) intrinsic ocular muscles (controlling the lens and pupil). The extraocular muscles include: the medial, inferior, and superior recti, the inferior oblique, and levator palpebrae muscles, all innervated by the oculomotor nerve (III); the superior oblique muscle, innervated by the trochlear nerve (IV); and the lateral rectus muscle, innervated by the abducens nerve (VI). The intrinsic eye muscles are innervated by the autonomic systems and include the iris sphincter and the ciliary muscle (innervated by the parasympathetic component of cranial nerve III), and the radial pupillodilator muscles (innervated by the ascending cervical sympathetic system with its long course from spinal segments T1 through T3).

Extraocular muscle function

The muscles of the eye are designed to stabilize and move the eyes. All eye muscles have a resting muscle tone that is designed to stabilize eye position. During movements, certain muscles increase their activity while others decrease it. The movements of the eye include: adduction (the pupil directing toward the nose); abduction (the pupil directed laterally); elevation (the pupil directed up); depression (the pupil directed down); intorsion (the top of the eye moving toward the nose); and extorsion (the superior aspect of the eye moving away from the nose). Horizontal eye movements are rather simple. Increased activity of the lateral rectus will direct the pupil laterally, while increased activity of the medial rectus will direct it medially. However, movements of the eyes above or below the horizontal plane are complicated and require, at the minimum, activation of pairs of muscles. This is because the orbit is not directed straight forward in the head and, therefore, there is no one muscle positioned to direct the eye straight up or down without the simultaneous occurrence of unwanted movements. Because of this, the protocol for testing eye movements is somewhat more complicated than might be expected.

Figure 4-1 illustrates the correct eye positions for testing the extraocular muscles in relative isolation. As can be seen in Figures 4-1 and 4-2, a lateral position of the eyeball is necessary for testing the inferior and superior recti, whereas a medial position is necessary for testing the inferior and superior oblique. This is because, in the position of lateral gaze, the superior and inferior rectus muscles are in line with the axis of the globe, "straightening out the pull" of these muscles and allowing them to move the eye straight up or down. When the eye is directed nasally (medially), the oblique muscles align with the axis of the globe and are, therefore, the prime muscles for vertical gaze when the eye is adducted. Vertical gaze from the neutral position (Figure 4-1) is accomplished by simultaneous activation of the superior rectus and inferior oblique (for upgaze) and of the inferior rectus and superior oblique (for downgaze). It is not necessary to have the patient look straight up and down in order to test each of the extraocular muscles. However, this may reveal evidence of vertical nystagmus (a sign of brain stem vestibular damage) and can determine the integrity of the midbrain center for vertical gaze (which may be defective despite adequate individual muscle activity). Figure 4-3 illustrates the expected findings with isolated loss of function of cranial nerves III, IV, and VI.

Since there is resting tone in all of the eye muscles, isolated weakness in one muscle results in deviation of the eye due to the unopposed action of all of the remaining muscles. This typically results in double vision when the person tries to look straight ahead (although some patient may ignore the input from one eye). The afflicted person often adjusts their head position in an attempt to ameliorate the double vision caused by the muscle imbalance. The position that their head assumes is one that permits them to use their "good eye" to line up with the affected one. This is often successful in cases of isolated damage to cranial nerve IV or VI, with the head assuming the position shown in Figure 4-3. In this figure, the dashed vector lines show which directions of muscle pull are lost. The solid vector lines indicate the resting tonus of the remaining extraocular muscles. Note that the head is tilted in CN IV damage. This is the classic position from which the English phrase "cockeyed" is derived. When cranial nerve III is involved, there may be enough ptosis to close the eye (preventing diplopia). However, if the eye is open, there is usually too much imbalance to be overcome by head positioning and patients usually have diplopia.

The person with an extraocular muscle defect of recent onset usually complains of double vision (diplopia). This results from the inability to fuse the images on the macular regions (central vision) of both eyes. Since the weak muscle is unable to bring the eye to a position in which the object is focused on the macula, the image falls on a more peripheral part of the retina. The person sees the object in the field appropriate to the new retinal position (i.e., always farther toward the periphery in the direction of attempted gaze). Additionally, because the image falls on a retinal region with fewer cones, it is less distinct. The patient may compare it to the "ghost images" seen on maladjusted television sets.

Sometimes it is very obvious which eye is not moving sufficiently when you perform the "6 positions of gaze." Also, the direction of the diplopia can give clues about weakness. For example, horizontal diplopia (where the images are separated horizontally) is due to problems with the medial and lateral recti, while vertical diplopia is due to problems with one or more of the other muscles. When it is not obvious on observation, one can delineate which extraocular muscle or muscles are defective by determining which eye sees the abnormal image (i.e., the blurry image that is farthest toward the periphery in direction of eye movement). This can be done by placing a transparent red piece of plastic or glass in front of one eye and asking the patient (who is observing a small light source such as a penlight or white object) which image is red, the inside or outside, lower or upper, depending on whether the diplopia is maximum in the vertical or lateral field of gaze. Figure 4-4 demonstrates the findings in one patient with medial rectus dysfunction and in one with lateral rectus dysfunction. The abnormal image in both cases is laterally displaced in the field of gaze and blurred (even though different eyes are involved in each case). Alternatively, if a red glass is not available, you can use the cover test to determine which eye is involved. In this case you will need to ask the patient to identify which image disappears when you cover one eye. Again, the eye that is projecting the image most off to the periphery is the one that is affected. The red glass and cover tests are particularly useful in delineating minimal muscle dysfunction, in which it is frequently difficult to determine which muscles are involved by observation on primary muscle testing.

Central control of eye movement

It is worthwhile at this point to review the anatomy of the central pathways of the oculomotor system. Figures 4-5 and 4-6 schematically outline the major central pathways that are important to conjugate lateral gaze, conjugate vertical gaze and convergence. Additionally, the deficits caused by destructive lesions in various parts of these systems are diagrammed.

The central control of eye movement can be distilled into the principle types of functions. These include voluntary, conjugate horizontal gaze (looking side-to-side); voluntary, conjugate vertical gaze (looking up and down); smoothly tracking objects; convergence; and eye movements resulting from head movements. These latter movements are part of the vestibular reflexes for eye stabilization and will be discussed with the vestibular nerve. The vestibular chapter is also where nystagmus (a to-and-fro movement of the eye) will be discussed.

All movements of the eyes that are produce by the central nervous system are conjugate (i.e., both eyes moving in the same direction in order to keep the eyes focused on a target) except for convergence, which adducts the eyes to focus on near objects. Voluntary horizontal gaze in one direction begins with the contralateral frontal eye fields (located in the premotor cortex of the frontal lobe). This region has upper motor neurons that project to the contralateral paramedian pontine reticular formation (PPRF), which is the organizing center for lateral gaze in the brain stem. The PPRF projects to the ipsilateral abducens nucleus (causing eye abduction on that side). There are fibers extending from the abducens nucleus, which is located in the caudal pons, to the contralateral oculomotor nucleus of the midbrain. The projection pathway is the medial longitudinal fasciculus (MLF). The oculomotor nucleus then activates the medial rectus, adducting the eye in order to follow the abducting eye. This is illustrated schematically in figure 4-9 for voluntary horizontal gaze to the left.

Damage to the frontal eye-fields will initially prevent voluntary gaze away from the injured frontal lobe. However, that improves with time. Damage to the PPRF will abolish the ability to look toward the side of the lesion. Damage to the MLF produces the curious finding of “internuclear ophthalmoplegia” in which the patient will be able to abduct the eye, but the adducting eye will not follow. Additionally, there will be some nystagmus in the abducting eye.

Vertical gaze (Figure 4-10) does not have one center in the cerebral cortex. Diffuse degeneration of the cortex (such as with dementia) can diminish the ability to move the eyes vertically (particularly upward). There is a brain stem center for vertical gaze (in the midbrain – the rostral interstitial nucleus [of Cajal]). Degeneration of this nucleus (such as can occur in rare conditions like progressive supranuclear palsy) can abolish the ability to look up or down. Additionally, there are connections between the two sides that traverse the posterior commissure. Pressure on the dorsum of the midbrain, such as by a pineal tumor, can interrupt these fibers and prevent upgaze (Parinaud syndrome).

Smooth tracking eye movements are mediated through a more circuitous pathway that includes the visual association areas (necessary in order to fix interest on a visual target) and the cerebellum. Cerebellar damage often produces jerky, uncoordinated movements of the eyes.

Pupillary function

The iris receives both sympathetic and parasympathetic innervation: (1) the sympathetic nerves innervate the pupillary dilator muscles; and (2) the parasympathetic nerve fibers (from CN III) innervate the pupillary constrictor (sphincter) muscles as well as the ciliary apparatus for lens accommodation. Figures 4-7 and 4-8 show the origins and courses of these two systems.

During the normal waking state the sympathetics and parasympathetics are tonically active. They also mediate reflexes depending in part on emotionality and ambient lighting. Darkness increases sympathetic tone and produces pupillodilation. Increased light produces increased parasympathetic tone and therefore pupilloconstriction (this also accompanies accommodation for near vision). During sleep, sympathetic tone is depressed and the pupils are small. Normal waking pupil size with average ambient illumination is 2 to 6 mm. With age, the average size of the pupil decreases. Approximately 25% of individuals have asymmetric pupils (anisocoria), with a difference of usually less than 0.5 mm in diameter. This must be kept in mind when attributing asymmetry to disease, particularly if there are no other signs of neurologic dysfunction.

At the bedside, the first step in evaluating pupil dysfunction is observation of the resting size and shape. A small pupil suggests sympathetic dysfunction; a large pupil, parasympathetic dysfunction. Loss of both systems would leave one with a nonreactive, midposition pupil, 4-7 mm in diameter, with the size varying from individual to individual. This is seen most often in persons with lesions that destroy the midbrain (see Chapter 17).

Pupillary reflexes

Next, the integrity of the pupillary reflex section is evaluated. Parasympathetic function is tested by having the patient accommodate: first looking at a distant object, which tends to dilate the pupils and then quickly looking at a near object, which should cause the pupils to constrict. Additionally, the pupils constrict when the patient is asked to converge, which is most easily done by having them look at their nose. There are rare conditions damaging the pretectal region that differentially affect the constriction produced by convergence but not that produced by accommodation. More common is the loss of the light reflex with preservation of accommodation and convergence pupilloconstriction (this has been termed the Argyll-Robertson pupil). This may be caused by lesions in the peripheral autonomic nervous system or lesions in the pretectal regions of the midbrain. Variable amounts of sympathetic involvement are usually present, leaving the pupil small in the resting state. Although this was commonly associated with tertiary syphilis in the past, the Argyll-Robertson pupil is seen most often associated with the autonomic neuropathy of diabetes mellitus.

The light reflex is tested by illuminating first one eye and then the other. Both the direct reaction (constriction in the illuminated eye) and the consensual reaction (constriction in the opposite eye) should be observed. The direct and consensual responses are equal in intensity because of equal bilateral input to the pretectal region and Edinger-Westphal nuclei from each retina (see Figure 4-7).

Pupillodilation, which can be tested by darkening the room or simply shading the eye, occurs due to activation of the sympathetic nervous system, with associated parasympathetic inhibition. A sudden noxious stimulus, such as a pinch (particularly to the neck or upper thorax), causes active bilateral pupillodilation. This is called the cilio-spinal reflex and depends predominantly on the integrity of the sensory nerve fibers from the area, the upper thoracic sympathetic motor neurons (T1- T3 lateral horn) and the ascending cervical sympathetic chain (see Figure 4-8). Interruption of the descending sympathetic pathways in the brain stem frequently has no effect on the reflex. Therefore, if the patient has a constricted pupil presumably secondary to loss of sympathetic tone, absence of the ciliospinal reflex suggests peripheral sympathetic denervation or, if other neurologic signs are present, damage to the upper thoracic spinal cord. Presence of the reflex despite depressed resting sympathetic tone suggests damage to the descending central sympathetic pathways.

Horner's syndrome is a constellation of signs caused by lesions in the sympathetic system. Sweating is depressed in the face on the side of the denervation, the upper eyelid becomes slightly ptotic and the lower lid is slightly elevated due to denervation of Muller's muscles (the smooth muscles that cause a small amount of lid-opening tone during alertness). Vasodilation is transiently seen over the ipsilateral face, and the face may be flushed and warm. These abnormalities, in addition to pupilloconstriction, are seen in conjunction with peripheral cervical sympathetic system damage.

The final neuron in the cervicocranial sympathetic pathway arises in the superior cervical ganglion and sends its axons to the head as plexuses surrounding the internal and external carotid arteries. Lesions involving the internal carotid artery plexus (as in the middle-ear region) cause miosis (a small pupil) and ptosis and loss of sweating only in the forehead region - the area of the face supplied by the internal carotid system. Lesions of the superior cervical ganglion cause the same problems, except that loss of sweating occurs over the whole side of the face. Destruction of the external carotid plexus causes sweating loss over the face that spares the forehead, without pupillary or eyelid changes. Lesions of the lower portion of the cervical sympathetic chain (e.g., carcinoma of thyroid) cause a Horner's syndrome with loss of sweating in the face and neck, and if the lesion is at the thoracic outlet (such as tumors of the apex of the lung), loss of sweating extends to the upper extremity. Lesions of the brainstem and cervical spinal cord descending sympathetic pathways cause a Horner's syndrome with depression of sweating over the whole side of the body. Lesions of the spinal cord below T1- T3 cause a loss of sweating below the level of the lesion but no Horner's syndrome. Testing for sweating defects can therefore be very useful in localization of the lesion. A simple, but messy way to test sweating is to warm the patient and watch for asymmetrical loss of sweating using starch and iodine. The parts to be tested are painted with an iodine preparation (e.g., forehead, cheek, neck, hand and foot) and then when they are dry, the areas are dusted with starch. When the patient sweats after being warmed with blankets (covering the tested areas with plastic is useful), the iodine runs into the starch and blackens it. Asymmetries are relatively easy to observe.

Amblyopia

Before concluding this discussion of eye movements it would be appropriate to say a few words about "amblyopia" (literally, "dim eye"). This is a condition in which one eye obviously drifts off target (some have called it a "wandering eye"). However, the patient is unaware of this and does not see double.

This is most serious in children and occurs for one of two reasons. First of all, it may occur due to severe muscle weakness or scarring. In this case the child cannot keep the two eyes fixed on the same target. The other cause is poor vision (usually in one eye). The reason that there is no double vision is that the brain "turns off" input from the bad eye. The reason this is so bad in young children is that, up until late childhood, functionally "turned off" synapses will actually loose their connections with neurons at the level of the visual cortex. These synapses will be replaced by synapses of fibers from the intact eye and the patient will become permanently blind in that eye. "Turning off" an eye for one continuous month for each year of life (i.e., for 5 straight months in a 5-year old) is enough to cause permanent blindness. This does not happen in adolescence or adulthood because synapses have stabilized. Interestingly, the pupillary light reflex is unaffected since the projections from the retina to the pretectum are intact.

The treatment is to force the patient to use the eye at least part of the day (while providing as much visual correction as possible for the affected eye). This is often done by patching the "good eye" during school time (in a more controlled environment).

References


Questions

Define the following terms:

strabismus, abduction, adduction, elevation, depression, convergence, accommodation, diplopia, miosis, mydriasis, myopia, hyperopia, conjugate, consensual, extraocular, amblyopia, ptosis, anisocorea.
Strabismus is a position of the eyes where they are not directed at the same target (in some parts of the country this is termed a "squint").
Abduction is bringing the pupil away from the nose.
Adduction is bringing the pupil toward the nose.
Elevation is moving the pupil above the horizon.
Depression is moving the pupil below the horizon.
Convergence is directing both eyes toward the nose.
Accommodation is a combination of convergence, pupil constriction and change in lens shape to permit focus on a near object.
Diplopia is double vision. This can be horizontal, vertical or skew.
Miosis is constriction of the pupil.
Mydriasis is dilation of the pupil.
Myopia is an inability to see at distance ("nearsighted") with light focusing in front of the retina.
Hyperopia is an inability to see close up ("farsighted") with light behind the retina.
Conjugate - "together". That is, the eyes moving in parallel to keep images focused on the same part of each retina (preventing diplopia).
Consensual means "happening on both sides at the same time". A consensual reflex is one where the response is bilateral when the stimulus is unilateral (such as the papillary light reflex).
Extraocular means outside the eye and specifically is used to describe the muscles that attach to the outside of the eyeball and move it.
Amblyopia literally means "dim eye". This is a drifting or "lazy" eye that usually happens because one eye has bad vision. The brain often "turns off" control of that eye and the eye drifts. The patient usually does not have diplopia because input from that eye is turned off. In one of the most remarkable illustrations of plasticity, the eye can become permanently blind in children if this is not treated.
Ptosis is a drooping of the upper eyelid.
Anisocorea is an inequality of pupil size. This is usually not clinically significant unless it reaches one millimeter in difference.

4-1. Which muscles would be active in the right and left eye when looking up and to the right?

Answer 4-1. In the right eye the lateral rectus and the superior rectus would be the prime movers, while in the left eye, the medial rectus and the inferior oblique would be most active.

4-2. Which muscles would be active in the right and left eye when looking down and to the left?

Answer 4-2. In the right eye the medial rectus and the superior oblique would be the prime movers, while in the left eye, the lateral rectus and the inferior rectus would be most active.

4-3. What position will the patient's head assume (in order to prevent diplopia) if their right trochlear nerve is damaged?

Answer 4-3. Head tilted to the left and chin turned slightly to the right ("cockeyed").

4-4. When a patient has double vision, in which position will they have the furthest separation of the images?

Answer 4-4. The images will be furthest apart when the eyes look in the direction that the weak muscle is most active.

4-5. What is the significance of horizontal diplopia (where the images are side-by-side) as opposed to vertical diplopia?

Answer 4-5. Horizontal diplopia results from weakness of the lateral or medial rectus muscles; vertical diplopia is due to weakness of one of the other muscles.

4-6. Which eye (the one that is moving normally or the weak one) will see the image that is furthest displaced from the center of vision?

Answer 4-6. The "bad eye" sees the image that is furthest toward the periphery of vision.

4-7. Where is the cortical center that controls lateral gaze? Where is the lateral gaze center in the brain stem?

Answer 4-7. Lateral gaze centers include the frontal eye fields in the frontal lobes of the cerebral cortex and the paramedian pontine reticular formation.

4-8. Is there a vertical gaze center in the cerebral cortex? Is there a brain stem vertical gaze center?

Answer 4-8. Vertical gaze is a diffuse cerebral cortical phenomenon, while there is a vertical gaze center in the rostral midbrain (the rostral interstitial nucleus).

4-9. What are the potential causes of ptosis?

Answer 4-9. Ptosis may be due to weakness of the levator palpebrae muscle (or CNIII damage) or due to damage to the sympathetics (due to weakness of the small, superior tarsal muscle).

4-10. What are the components of Horner's syndrome?

Answer 4-10. Horner's syndrome (ptosis, miosis, anhidrosis and possibly flushing) is from damage to sympathetics anywhere along their course.

4-11. What are the functions of sympathetic and parasympathetic nerves to the orbit?

Answer 4-11. Sympathetics dilate the pupil, parasympathetics (CN III) constrict the pupil to light and accommodation; there is balance between sympathetics and parasympathetics.

4-12. Where is the brain stem center for the pupillary light reflex?

Answer 4-12. The pretectal area of the dorsolateral midbrain is the center for the pupillary light reflex.
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