Ординатура / Офтальмология / Английские материалы / The Neurology of Eye Movements_Leigh, Zee_2006

have undergone trigeminal nerve thermocoagulation for tic douloureux.656 Studies of a patient with a congenital oculomotortrigeminal nerve synkinesis, who could adduct one eye by moving her jaw, also provide evidence that extraocular proprioception could contribute to spatial localization.373 Thus, when this patient viewed with her normal eye, but adducted her covered, abnormal eye by moving her jaw, she mislocalized targets opposite to the direction of eye rotation, consistent with the effects of active contraction of the left medial rectus on palisade tendon organs. Proprioception may also play a role in maintaining correct ocular alignment.200'366 If trochlear nerve palsy is induced experimentally in m.onkeys, proprioceptive deafferentation of the paretic eye produces gradual worsening of both static alignment and saccadic conjugacy.374 Finally, there is evidence that proprioception plays a role in the normal development of binocularity.79

ANATOMY OF OCULAR MOTOR NERVES AND THEIRNUCLEI

The ocular motor nuclei are located in the brain stem, close to the midline.597 They lie adjacent to the medial longitudinal fasciculus and reticular formation, ventral to the aqueduct of Sylvius and fourth ventri-

cle. The intracranial courses of the ocular motor nerves are shown in Figure 9-7.

Anatomy of the Abducens Nerve

The abducens nucleus lies in the floor of the fourth ventricle, in the lower pons (see Fig. 6-1, Chap. 6). It is capped by the genu of the facial nerve. The abducens nucleus contains two distinct populations

Diagnosis of Diplopia and Strabismus 331

of cells: motoneurons, which innervate the lateral rectus muscle, and internuclear neurons, which innervate contralateral medial rectus motoneurons via the medial longitudinal fasciculus. Thus, the neurons of the abducens nucleus contain all the neural signals responsible for conjugate horizontal eye movements. From the medial aspect of the nucleus, fibers destined for the ipsilateral lateral rectus muscle course ventrally, laterally, and caudally, passing through the pontine tegmentum and medial lemniscus, to emerge at the caudal border of the pons. Here the abducens nerve lies close to the anterior inferior cerebellar artery. In some individuals, the nerve consists of several trunks that eventually fuse within the cavernous sinus.448 The nerve then courses nearly vertically along the clivus, through the prepontine cistern, and close to the inferior petrosal sinus. It then rises to the petrous crest, where it bends acutely forward to penetrate the dura,645'647 medial to the trigeminal nerve, and passes under the petroclinoid ligament in Dorello's canal. It courses forward in the body of the cavernous sinus, where it lies lateral to the internal carotid artery and medial to the ophthalmic division of the trigeminal nerve (Fig. 9-8). For a few millimeters, pupillosympathetic fibers run with the sixth nerve as they leave the carotid artery to reach the first division of the trigeminal nerve.386-482 The abducens nerve then enters the orbit through the superior orbital fissure449 and passes through the annulus of Zinn to innervate the lateral rectus on the inner surface of the muscle.

Anatomy of the Trochlear Nerve

The trochlear nerve is the longest and thinnest of all cranial nerves, which makes

it susceptible to trauma. Each trochlear nucleus sends axons to supply the contralateral superior oblique muscle. The trochlear nucleus lies at the ventral border of the central, periaqueductal gray matter, dorsal to the medial longitudinal fasciculus, at the level of the inferior colliculus. Its fibers pass dorsolaterally and caudally around the central gray matter and decussate completely in the anterior medullary velum (the roof of the aqueduct). The trochlear nerve emerges, as one or more rootlets,447 from the dorsal aspect of the brain stem, caudal to the inferior colliculus and close to the tentorium cerebelli. The nerve passes laterally around the upper pons, lying between the superior cere-

bellar and posterior cerebral arteries, to reach the prepontine cistern. During its

cisternal course, the trochlear nerve re-

ceives its blood supply from branches of the superior cerebellar artery.389 It then

runs forward on the free edge of the tentorium for 1 to 2 cm before penetrating the dura of the tentorial attachment and entering the cavernous sinus. Within the lateral wall of the sinus (Fig. 9-8), the fourth nerve lies below the third nerve and above the ophthalmic division of the fifth nerve, with which it shares a connective tissue coat. It then crosses over the oculomotor nerve to enter the superior orbital fissure above the annulus of Zinn,449 passing to the medial aspect of the orbit to supply the superior oblique muscle.536

Anatomy of the Oculomotor Nerve

The oculomotor nucleus is a paired structure that lies at the ventral border of the periaqueductal gray matter; it extends rostrally to the level of the posterior commissure and caudally to the trochlear nucleus (Fig. 9-9). It sends efferent fibers to the medial rectus, superior rectus, inferior rectus, and inferior oblique muscles; the levator palpebrae superioris; the pupillary

Figure 9-8. Diagram of transverse section of the cavernous sinus, showing superficial and deep layers and the relationships of the oculomotor (III), trochlear (IV), abducens (VI), and ophthalmic divi-

sion of the trigeminal nerve (Vj). (Redrawn from Umansky and Nathan.646)

constrictor muscle; and the ciliary body. Warwick's anatomic scheme678 for the oculomotor nucleus of the rhesus monkey is shown in Figure 9-9A. More recent studies have revised Warwick's scheme,81'84'85 and demonstrated that the neurons supplying the medial rectus muscle are distributed into three areas of the oculomotor nucleus, designated A, B, and C (Fig. 9-9B). Neurons from area C receive pretectal inputs,85 and their axons mainly in-

nervate the orbital layers of the medial rectus muscle; orbital fibers seem most suited to sustained contraction, such as during convergence. Neurons from all three of these locations receive inputs from the contralateral abducens nucleus via the medial longitudinal fasciculus (Fig. 9-9B). The neurons innervating each superior rectus muscle lie next to each other, and their axons decussate in the caudal portion of this nucleus.53 The caudal nucleus, supplying both levator palpebrae superioris muscles, is a single structure. All projections from the oculomotor nucleus are ipsilateral save for those to the superior rectus, which are totally crossed,

and those to the levator palpebraesuperioris, which are both crossed and uncrossed. Parasympathetic innervation for the pupil originates in the Edinger-West- phal nucleus.338

The fascicles of the oculomotor nerve originate from the entire rostral-caudal

extent of the nucleus and pass ventrally through the medial longitudinal fasciculus, the red nucleus, the substantia nigra, and the medial part of the cerebral peduncle. As they pass through the red nucleus, the fascicles fan out to converge again before exiting the midbrain. At-

tempts have been made to identify the topographic organization of the oculomotor fascicles, based on clinicoradiologic and clinicopathologic findings. One scheme proposes that from lateral to medial, the order is inferior oblique, superior rectus, medial rectus and levator palpebrae, inferior rectus, and pupil.96'198 However, selective involvement of the levator and superior rectus with some ventral midbrain lesions has suggested that, even at this stage, the organization corresponds to the superior and inferior branching of

the oculomotor nerve that occurs in the orbit.344

The third nerve emerges from the interpeduncular fossa as several rootlets which then fuse to form a single trunk.

The nerve then runs between the posterior cerebral artery and superior cerebellar artery, passing forward, downward, and laterally through the basal cistern. It passes lateral to the posterior communicating artery and below the temporal lobe uncus, where it runs over the petroclinoid ligament, medial to the trochlear nerve and just lateral to the posterior clinoid

process. During its subarachnoid course, parasympathetic pupillary fibers lie peripherally in the dorsomedial part of the nerve.314'619 Segregation of libers into those that will supply superior and inferior branches of the oculomotor nerve in the orbit may already have occurred.229As the oculomotor nerve pierces the dura, it lies close to the free edge of the tentorium cerebelli. Within the cavernous sinus, the third nerve lies initially above the trochlear nerve, and here it receives sympathetic fibers from the carotid artery

(Fig. 9-8). As it leaves the cavernous sinus, it is crossed superiorly by the trochlear and abducens nerves and divides into a superior and inferior ramus. These pass through the superior orbital fissure,449 and enter the orbit within the annulus of Zinn (Fig. 9-2). The superior oculomotor ramus or division runs lateral to the optic nerve and ophthalmic artery and supplies the superior rectus and levator palpebrae muscles. The larger inferior oculomotor ramus or division branches in the posterior orbit and supplies the medial rectus, inferior rectus, and inferior oblique mus-

336 The Diagnosis of Disorders of EyeMovements

cles, and the ciliary ganglion.536 The blood supply of the intracranial portion of the oculomotor nerve from its emergence from the brain stem until it passes the posterior cerebral artery originates from thalamoperforating branches.86 From this point until the nerve enters the cavernous sinus, it receives no nutrient arterioles from adjacent arteries. The part of the oculomotor nerve within the cavernous sinus receives branches from the inferior cavernous sinus artery and from a tentorial artery arising from the meningohypophyseal trunk.

PHYSIOLOGIC BASIS FOR CONJUGATE MOVEMENTS: YOKE MUSCLE PAIRS

Law of ReciprocalInnervation

Sherrington determined that whenever an agonist muscle (e.g., the lateral rectus) receives a neural impulse to contract, an equivalent inhibitory impulse is sent to the motoneurons supplying the antagonist muscle of the same eye (e.g., the medial rectus) so that it will relax—the law of recip-

rocal innervation.b&1 In other words, the extraocular muscles do not cocontract during conjugate eye movements, although they do so during blinks168 and vergence.197 Sherrington postulated that this reciprocal innervation was due to a stretch reflex in extraocular muscle.567 Although, as reviewed above, the extraocular muscles do possess proprioceptors, neurophysiologic evidence in monkeys argues against the existence of a classic stretch reflex. When a trained monkey fixates a target with one eye, perturbation of the other, covered eye, using a suction contact lens, produces no change in the discharge of neurons in the abducens nucleus corresponding to the perturbed eye.312 Moreover, bilateral section of the ophthalmic division of the trigeminal nerve, which conveys extraocular proprioceptive inputs,504 does not affect the ability of the brain to program saccadic eye movements accurately.226 Thus, at present, the weight of evidence suggests that the law of reciprocal innervation de-

pends upon the organization of brain stem connections. For example, the saccadic system is organized in a push-pull fashion that involves excitatory and inhibitory burst neurons (see Chap. 3).

Law of Motor Correspondence

A second physiological principle is that for the eyes to move together requires a coordination or yoking of pairs of muscles, one from each eye. For example, to produce a horizontal movement to the left requires that the left lateral rectus and right medial rectus muscles contract together. These muscles are a yoke pair, as are the left medial rectus and right lateral rectus, which relax during the same movement. Implicit in the concept of a yoke pair is that corresponding muscles of each eye (e.g., left lateral rectus and right medial rectus) receive equal innervation so that the eyes move together. This is the simplest statement of Bering's law of motor correspondence.250 Conventionally,vertically acting muscles are also conceptualized as being arranged in yoke pairs (e.g., the right superior rectus and the left inferior oblique),

a concept that has received experimental support.435 In fact, the way in which the

extraocular muscles interact is complicated and all the extraocular muscles probably contribute force during even a simple horizontal movement. Furthermore, recent studies indicate that some premotoneurons may encode monocular eye movement signals.715 Nonetheless, the concept of yoke muscle pairs is valuable in interpreting the results of clinical testing.

Deviations of the Visual Axes

Many normal subjects develop a deviation of the visual axes when sensory fusional mechanisms are temporarily interrupted by covering one eye. This is a phoria or latent deviation of the visual axes (Table 9-1). The deviation is usually constant in all directions of gaze and is called concomitant (or comitant). If, on the other hand, the amount of deviation changes according to the direction of gaze, it is called non-

CLINICAL TESTING

IN DIPLOPIA

The prerequisite for accurate diagnosis of diplopia and strabismus is a clear understanding of underlying anatomy and physiology. One should also record the results of each part of the examination, heeding Darwin's advice that "it is a fatal fault to reason while observing, though so necessary beforehand and so useful afterwards."

Figure 9-10. Disparate retinal images. The image of a distant object lies on the fovea of the left eye but, because of an esotropia in the right eye (due to a right lateral rectus weakness, for instance), the image lies medial to the fovea. Each retinal element corresponds to a specific subjective visual direction. Consequently, the subject localizes the same object in two different directions and experiences diplopia. The broken line indicates the perceived direction of the false image.

History: The symptomatology of strabismus

Misalignment of the visual axes—strabis- mus—causes the two images of a seen object to fall on noncorresponding areas of the two retinas (Fig. 9-10). This usually causes diplopia—the sensation of seeing an object at two different locations in space. In addition, the two foveae are simultaneously presented different images, so occasionally two different objects are perceived at the same point in space. This is called visual confusion.

At an early point in the evaluation, it should be determined whether the diplopia is binocular or monocular. The distinction can be made by covering one eye. Monocular diplopia is most commonly caused by astigmatism or spherical refractive errors,107-692 incipient cataract, corneal irregularity,252 lens dislocation, or eye trauma. Such patients may report that

the two images differ in brightness or that there are more than two images. Monocular diplopia caused by lens or corneal abnormality can be overcome by pinhole vision. Slitlamp examination or retinoscopy may be necessary to make the diagnosis. In some patients, monocular diplopia is a psychiatric symptom. Rarely, it is due to

retinal detachment or to cerebral disorders.404'538

Patients who complain of little or no visual disturbance despite an obvious ocular misalignment usually have had their strabismus from early in life, though this is not always the case. Thus, it is important to inquire about any history of strabismus, eye patching, or abnormal head posture; old photographs may be of help. It is also worthwhile asking about prior visits to ophthalmologists and optometrists. On occasion, patients with strabismus (especially children) present with an abnormal

338 The Diagnosis of Disorders of Eye Movements

head posture but without any visual complaints.88

Ask about the type of diplopia (horizontal, vertical, torsional), in what direction of gaze it is most marked, if it is worse for near or distant viewing, and if it is affected by head posture. For example, a lateral rectus weakness leads to horizontal diplopi that is typically worse on looking ipsilaterally and at distant objects and is less troublesome if the head is turned toward the side of the palsy.

Other symptoms caused by misalignment of the visual axes include blurred vision, vertigo, and oscillopsia; the last two complaints relate to inadequate compensatory movements of the eyes during head

rotation.165-688 Patients with diplopia tend to close one eye.676 This may be the clue to

an ocular misalignment in confused or lethargic patients who do not complain of diplopia.

The Examination in Strabismus

Certain essential preliminaries should precede ocular motor testing. These are measurement of corrected visual acuity in each eye, tests for binocularity, and a sim-

ple confrontation assessment of the central and the peripheral visual fields. In

certain patients, particularly children and some young adults, refraction isnecessary. Any abnormal head posture should also be noted. These observations completed, the examination consists of four parts: assessment of range of eye movements, subjective diplopia testing, cover testing, and, with vertical deviations, the Bielschowsky head-tilt test. Appendix A contains a summary of this testing.

RANGE OF EYEMOVEMENTS

Ask the patient to follow a small target through the full range of movement, including the nine cardinal or diagnostic positions of gaze (Table 9-1). First test one eye at a time with the other covered— ductions. Then test both eyes together— versions. Note any limitation of eye movement that persists despite vigorous encouragement. A simple, approximate method to evaluate ocular alignment dur-

ing versional movements is to ask the patient to fixate on a penlight and to note the position of the corneal reflection of the light in the nine cardinal positions. Rather than moving the penlight, move the patient's head so that the examiner's eye stays aligned with the penlight. If the images from the two corneas appear centered, then the visual axes are usually correctly aligned. This method is especially valuable when facial asymmetries, such as hypertelorism, ptosis, or epicanthic folds, give the false impression of strabismus. Epicanthic folds simulate esotropia in young children.

When the range of movement islimited, it is important to determine whether the limitation is due to muscle weakness or mechanical restriction. For this purpose, a forced duction test may be of value. After applying topical anesthesia, an attempt is made to move the eye into the direction of action of the paretic muscle. This can be done using ophthalmic forceps or by simply pressing a cotton-tipped applicator

against the limbus of the cornea. First ask the patient to attempt to look in the direction of action of the weak muscle. If it is possible for the examiner to move the eye into the paretic field, this implies weakness of that muscle. Restriction to passive movement constitutes a positive passive forced duction test and indicates mechanical restriction. Second, ask the patient to attempt to look in the direction of action of the paretic muscle while this movement is actively opposed by the examiner's forceps. Resistance to the forcepsconstitutes a positive active forced duction test and suggests that muscle strength is intact and that the loss of ocular motility is due to mechanical restriction. Modern MRI techniques often allow precise diagnosis in such patients.

In any patient with a reduced range of voluntary eye movements, it is important to exclude myasthenia gravis; usually an edrophonium (Tensilon) test is performed (see below).

SUBJECTIVE DIPLOPIA TESTING

When the patient is cooperative, subjective tests of diplopia may reliably indicate the disparity between retinal images.

When strabismus is due to extraocular muscle weakness (nonconcomitant or paralytic strabismus), the patient can view, with the fovea of the nonparetic eye, targets in all directions of gaze. The eye with the paretic muscle, however, will not be able to bring to the fovea the image of a target located in the field of weakened action; consequently, the image will be projected onto extrafoveal retina (Fig. 9-10). In other words, the patient will interpret the object to be displaced in the direction of the paralysis (or opposite to the direction of the deviation). When the image is on the nasal retina, the patient thinks the object is in the temporal field of vision. This is uncrossed diplopia and is typical of esotropia (e.g., due to lateral rectus palsy). When the image is projected onto the temporal retina, the patient thinks the object is located nasally. This is crossed diplopia and is typical of exotropia (e.g., due to medial rectus palsy).

Two further principles are important in this type of diplopia testing: (1) the two images are maximally separated when the patient looks into the direction of action of the paretic muscle, and (2) the target seen by the paretic eye is usually projected more peripherally, particularly as the patient looks into the paretic field. One can determine which image comes from the paretic eye by transiently occluding either eye and asking the patient to report to which eye the most remotely located image belongs.

The use of a red glass or Maddox rod (Fig. 9-11) usually aids examination. A Maddox rod consists of small glass rods with a red filter; it may be oriented according to the desired plane of testing— horizontal or vertical. When the Maddox rod is held before the right eye and a penlight is viewed with both eyes, the patient sees a white spot of light with the left eye and, through the Maddox rod, a red line. Since the Maddox rod can be rotated 90°, the horizontal and vertical components of diplopia can be evaluated separately. Ask the patient to follow the penlight as the eyes are taken into the nine cardinal positions. For each position, the patient reports how far the white light and red line are separated and where the white light is located in relation to the red line. The im-

Figure 9-11. The Maddox rod test. Because the Maddox rod breaks fusional vergence, it tests for both phorias and tropias. (See text forexplanation.) This patient has a left superior oblique weakness. The separation of images is greatest when the patient looks down and to the right.

age from the eye with the weakened muscle (whether it be the white light or the red line) will be projected furthest into the paretic field of gaze. Note that the Maddox rod prevents fusional vergence because the images are so dissimilar. Therefore, it primarily tests for phorias and latent palsies that may not be apparent under binocular viewing conditions. Normal individuals commonly have a phoria, so small, concomitant deviations detected during Maddox rod testing may be normal. If a phoria is nonconcomitant, however, an extraocular muscle may be weak or restricted. Two Maddox rods (one white, one red) can be used to evaluate torsional disparity between the two eyes, although careful interpretation of the results is necessary, and other methods (such as fundus photography) are sometimes indicated.665

Other subjective tests that dissociate the images seen by the two eyes include the Hess screen test and the Lancaster red-green test.^54 In the Lancaster test, the patient wears goggles with a red filter in front of the right eye and a green filter in front of the left. Thus, the patient can see the image of a red light with one eye and the image of a green light with the other.