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

ANATOMY OF THE ORBITAL FASCIA AND THE EXTRAOCULARMUSCLES

The Pulling Directions of the Extraocular Muscles and the Planes of Rotation of the Eye

STRUCTURE AND FUNCTION OF EXTRAOCULAR MUSCLE

Unique Characteristics of Extraocular Muscle Structure and Function of Extraocular

Muscle Fiber Types Extraocular Proprioception

ANATOMY OF OCULARMOTORNERVES AND THEIR NUCLEI

Anatomy of the Abducens Nerve

Anatomy of the Trochlear Nerve Anatomy of the Oculomotor Nerve PHYSIOLOGIC BASIS FORCONJUGATE

MOVEMENTS: YOKE MUSCLE PAIRS Law of Reciprocal Innervation

Law of Motor Correspondence

Deviations of the VisualAxes CLINICAL TESTING IN DIPLOPIA

History: The symptomatology of strabismus The Examination in Strabismus PATHOPHYSIOLOGY OF SOME

COMMONLY ENCOUNTERED SIGNS IN

STRABISMUS

Primary and Secondary Deviation

Past-pointing and Disturbance of Egocentric Localization

Head Tilts and Turns

Dynamic Properties of Eye Movements in Paralytic Strabismus

CLINICAL FEATURES AND DIAGNOSIS

OF CONCOMITANT STRABISMUS

CLINICAL FEATURESOF OCULAR NERVE

PALSIES

Abducens Nerve Palsy

Trochlear Nerve Palsy

Oculomotor Nerve Palsy

Multiple Ocular Motor Nerve Palsies

DISORDERS OF THE NEUROMUSCULAR

JUNCTION

Botulism

The Lambert-Eaton Myasthenic Syndrome

Myasthenia Gravis

CHRONIC PROGRESSIVE EXTERNAL

OPHTHALMOPLEGIA AND

RESTRICTIVE OPHTHALMOPATHIES

Involvement of the Extraocular Muscles in

Muscular Dystrophies

Kearns-Sayre Syndrome and Disorders of

Mitochondrial DNA

Thyroid Ophthalmopathy

Restrictive Ophthalmopathy and Congenital

Fibrosis of the Extraocular Muscles

The most common symptom caused by abnormal eye movements is double vision (diplopia). Diplopia is usually due to misalignment of the visual axes—strabismus (Table 9-1). The clinical evaluation of diplopia or strabismus may be challenging, especially in young or uncooperative

patients, and requires an organized and systematic approach. Recognizing this problem, Alfred Bielschowsky (1871-1940) commented: "In examining and treating motor anomalies (of the eyes), one never loses an uneasy feeling of incompetence until he has become thoroughly familiar with the physiologic fundamentals from which the signs and symptoms of those anomalies are to be derived."52

Those physiologic fundamentals had been established by the 19th-century masters. One pioneer worthy of special note was Ewald Hering (1834-1918), who taught Bielschowsky. When Hering published his Theory of Binocular Vision in 1868,250 it was widely held that coordinated movement of the eyes was an acquired skill. Hering challenged this view in his treatise, stating that "one and the same impulse of will drives both eyes simultaneously as we can direct a pair of horses with single reins." Although recent research has questioned the mechanisms by which equal innervation reaches each eye,715 the idea that the brain controls the globes as a single or- gan—"the Double Eye"—still forms the basis for our understanding of diplopia.

ANATOMY OF THE ORBITAL FASCIA AND THE EXTRAOCULAR MUSCLES

The eyeball is suspended in the coneshaped orbit by a fibrous sac of fascia called Tenons capsule, which is attached anteriorly to the conjunctiva behind the corneal lim-

bus and posteriorly to the orbital fat surrounding the optic nerve. Tenon's capsule has a tough peripheral part, which is penetrated by the rectus extraocular muscles, and a thin, delicate central region, which is penetrated by the optic nerve, posterior ciliary nerves, and ciliary vessels. The attachments of Tenon's capsule, between the anterior circumference of the eyeball (behind the corneal limbus) and the orbital rim, effectively suspend the eye in a "drumhead" that mechanically governs its freedom of rotation (Fig. 9-1).142 The thin, central part of Tenon's capsule allows the optic nerve and the ciliary vessels and nerves to move with the eye. One other important fascial connection is between the superior surface of the superior rectus muscle sheath and the lower surface of the levator palpebrae superioris.666

Each eye is rotated by six muscles: four rectus muscles and two oblique muscles (Fig. 9-1 and Table 9-2). The four recti and the superior oblique arise from the apex of the orbit (the annulus of Zinn, Fig. 9-2). The inferior oblique muscle arises from the inferior nasal aspect of the orbit. The four rectus muscles insert into the sclera anterior to the equator of the globe: the medial rectus muscle on the nasal side, the lateral rectus muscle on the temporal side, the superior rectus muscle on the superior side and the inferior rectus muscle on the inferior side. The superior and inferior oblique muscles approach the globe from its anterior and medial aspect and insert posterior to the equator of the globe. The superior oblique muscle first passes through the trochlea (a fibrous, cartilaginous, U-shaped ring that

lies just inside the superior medial orbital rim) before inserting on the superior side of the globe. The inferior oblique inserts on the temporal side.

An important new discovery is that the tendons of the rectus extraocular muscles pass through sleeve-like pulleys that lie within peripheral Tenon's capsule.142'506

These pulleys lie several millimeters posterior to the equator of the globe (Fig. 9-1), approximately 10 mm posterior to the insertion sites of the muscles. The pulleys contain not just fibrous tissue but also smooth muscle, which is innervated by several neurotransmitters—catecholamines, acetylcholine, and nitric oxide.143 The func-

tional importance of the fibromuscular pulleys is that they limit side-slip movement of the rectus muscles during eye rotations, a factor that had confounded prior attempts to mathematically model the properties of the orbit. Furthermore, the pulleys effectively change the point of origin of the rectus muscles, just as the trochlea changes the functional point of origin of the superior oblique muscle. Confirmation of the function of the pulleys comes from magnetic resonance imaging (MRI), which shows that the paths of rectus muscles remain fixed even during large eye rotations.105'141

The Pulling Directions of the

Extraocular Muscles and the

Planes of Rotation of the Eye

The eyes rotate about three axes (Fig. 9-3); one current convention refers to these axes as X (parasagittal), Y (transverse), and Z (vertical). All axes pass through the center of rotation of the globe. Translations (linear movements) of the globe are small, owing to the properties of Tenon's capsule, which suspends the eyeball. The pulling actions of the extraocular muscles are summarized in Table 9-2. The primary action of the muscle refers to the axis about which the eye

Figure 9-3. Axes of rotation of the eye (X, Y, Z) and

Listing's plane.

326 The Diagnosis of Disorders of Eye Movements

principally rotates when that muscle contracts; the secondary and tertiary actions refer to the axes about which there are lesser rotations. The horizontal recti rotate the eye horizontally about the Z axis, more or less irrespective of the vertical position of the globe. The superior recti are the main elevators of the eyes, and the inferior recti are the main depressors; these muscles also have smaller torsional and horizontal actions. The pulling actions of the oblique muscles are mainly torsional, but because they approach the eye from its medial aspect, their direction of pull is substantially affected by the horizontal position of gaze. For example, the superior oblique acts mainly as a depressor when the eye is adducted and mainly as an intorter when the eye is abducted (Fig. 9-4). The tertiary action of the oblique muscles is to abduct the eye.

Although in theory the eye could rotate about axes lying in any plane, in fact, the axes of rotation are confined to the equatorial or Listing's plane, which is perpendicular to the fixation line in primary position (Fig. 9-3). Thus, Listing's law states that any eye position can be reached from the primary position by rotation of the eye about a single axis lying in the equatorial

plane. One consequence of this scheme is that the vertical meridian of the eye,

which is earth-vertical and parasagittal with the eye in the primary position, re-

mains vertical when the eye rotates to a secondary position but systematically tilts with respect to gravity in any tertiary position. Danders' law states that the angle of tilt in any tertiary position of gaze depends upon the horizontal and vertical gaze angles, irrespective of how the eye reached that position of gaze. Both Bonders' and Listing's laws have been shown to apply approximately to saccadic and smooth-pursuit eye movements.176'177'616 Because the globe is suspended in the "drumhead" of fascia provided by Tenon's capsule, and the fibromuscular pulleys ensure relatively fixed pulling directions of the extraocular muscles, it has been suggested that Listing's and Bonders' laws are partially effected by these mechanical properties of the orbital tissues.415 Beviations from Listing's law do, however, occur for vestibular eye movements induced by head rotations in roll,421 for the eye movements occurring during sleep, and after ingesting alcohol.179'415 In one patient with alternating strabismus, the orientation of Listing's plane depended on which eye the subject chose to view with.411 Thus, it appears that orbital mechanics cannot be the sole factor that ensures that saccadic and pursuit eye movements obey Listing's law, but changes in smooth muscle pulley tone could mediate these central effects. Furthermore, electrophysiological evidence supports the view that the brain takes into

account deviations from Listing's law and corrects them.650 However, mathematical models suggest that orbital factors are more important than neural programing in constraining axes of eye rotations to Listing's plane.475 The functional significance of Listing's law or its changes with vergence are not clear. Various suggestions have been made though none is totally satisfactory. They include a relative simplicity of neural computation since patterns of innervation for a given position of gaze are reduced from three degrees of freedom to two (torsion is automatically specified—Donders' law); economy of work since the eyes take the straightest path to a new orbital position; and sensory considerations, to keep torsional disparity constant no matter what the viewing distance.641a

STRUCTURE AND FUNCTION OF EXTRAOCULARMUSCLE

Unique Characteristics of

Extraocular Muscle

Extraocular muscles differ anatomically, physiologically, and immunologically from limb muscle.499'501 Eye muscle fibers are smaller, more variable in size, and more richly innervated than limb muscle fibers. Some extraocular muscle fibers are amongst the fastest contracting and yet remain fatigue resistant.189 Motor unit size is the lowest known, being about 10 muscle fibers per motoneuron. Like limb muscles, the extraocular muscles contain twitch fibers that have a single endplate per fiber and can generate an all-or-none propagating response (action potential). In addition, there are nontwitch fibers that cannot generate action potentials and show graded contractions to trains of electrical pulse stimuli; these are similar to the tonic fibers found in amphibians.430'563 Fibers with intermediate properties also exist; they have multiple nerve terminals on individual

fibers but still generate slow action potentials.430

Another difference from limb musclesis that extraocular muscles preserve their

embryonic myosin in the proximal and distal portions of muscle fibers in the orbital layers (see following section).502 This preservation of embryonic myosin may partly account for the remarkable capacity of extraocular muscles to adapt to changes in innervation and disease states. Fibers with single and multiple nerve endplates have different antigens.461 One factor in this antigenic difference may lie in the structure of the acetylcholine receptor. Both the embryonic c^P^S type and adult a2pe5 isoforms of the acetylcholine receptor are present on multiply innervated, and some singly innervated, adult extraocular muscle fibers. Adult skeletal muscle and the levator of the eyelid possess only the adult isoform.257'286'287

Extraocular muscle is more susceptible to some disease processes (e.g., myasthenia gravis)289'499 and more resistant to others (e.g., Duchenne's dystrophy)285-316 than skeletal muscles. Furthermore, when disease does involve extraocular muscle, the histopathologic changes may be quite unlike those observed in skeletal muscle affected by a similar condition. For example, experimental denervation of the extraocular muscles causes little muscle atrophy but with a mononuclear infiltrate.499'503 Some of these findings would suggest a myopathic process if encountered in limb muscle.

Structure and Functionof

Extraocular Muscle Fiber Types

Each extraocular muscle has two distinct layers. Near the origin of each muscle, these lie in two concentric zones, but as the muscle is traced anteriorly, two parallel zones or layers are formed: a central global layer and a peripheral orbital layer. Each layer contains fibers more suited for either sustained contraction or brief rapid contraction. However, the orbital zone contains many fatigue-resistant twitch fibers. Using modern methods, six types

of fibers have been defined in the extraocular muscles (Fig. 9_5).502.596-598

In the orbital layer, about 80% are singly innervated fibers, which have fast-type my-

ofibrillar ATPase and high oxidative activity (with numerous mitochondria in dense clusters); these very fatigue-resistant fibers are not found in skeletal muscle or the eyelid. They alone show long-term effects after injection of botulinum toxin.595 The remaining 20% of orbital fibers are multiply innervated. They have twitch capacity near the center of the fiber and nontwitch

activity proximal and distal to the endplate band.

In the global layer, about 33% of fibers are singly innervated, fast twitch, and fatigue resistant. About 33% are pale, singly innervated fibers with fast-twitch properties but low fatigue resistance. About 25% are singly innervated fibers with fasttwitch properties, numerous mitochondria, and an intermediate level of fatigue resistance. The remaining 10% are multiply innervated fibers, with synaptic endplate along their entire length, as well as at the myotendinous junction, where there are

palisade organ proprioceptors. Like amphibian muscle, these fibers show tonic

properties, with slow, graded, nonpropagated responses to neural or pharmaco-

logical activation. Recent evidence sug gests that these muscle fibers receive

innervation from a separate group of motoneurons, which lie just outside the confines of the abducens and trochlear nuclei

and include the C subgroup of the oculomotor nucleus.85a

The levator palpebrae superioris contains the three singly innervated muscle types encountered in the global layer of the extraocular muscles, plus a true slow-twitch fiber type. The multiply innervated fiber types and the fatigue-resistant singly innervated type seen in the orbital layer are absent.

Although direct electrophysiological

confirmation of the contribution of each fiber type to different types of eye movement is lacking, electromyographic studies

by Scott and Collins, using miniature electrode needles with multiple recording sites, established a division of labor between global and orbital layers of extraocular muscle (Fig. 9-6).551 They found that orbital fibers are active throughout nearly the entire range of movement, but during fixation, global fibers are recruited only as the eye is called into the field of action of that muscle. It seems likely, therefore, that the singly innervated, fatigue-resistant orbital fibers play a key role in sustaining eye position and maintaining extraocular muscle "tone" in any eye position. During saccades, both global and orbital fibers are activated, but the activity of global fibers subsequently may fall, whereas that of orbital fibers is sustained. These findings are consistent with the presence of more fa- tigue-resistant fibers in the orbital layers. Further, it has been shown experimentally that "fast-fatigable" muscle fibers are the strongest,563 so such global fibers may be best able to generate rapid eye movements. Thus, the order of recruitment of fibers appears to reflect mainly their fatigability; the less fatigue-resistant fibers of the global layers may only be activated during saccades.

These findings might suggest that the properties of muscle fiber types differ from those of the ocular motoneurons, which appear to discharge for all types of eye movements, version or vergence.523 However, an alternative interpretation is that although each fiber can potentially contribute to all classes of eye movement, orbital, fatigue-resistant twitch fibers are most important for holding the eye in steady fixation, whereas global, pale, twitch fibers only become active when the eye is moved rapidly to a new orbital position. One special exception might be the multiply innervated tonic fibers, which do not generate action potentials and thus cannot be monitored by electromyographic activity. They appear to have motoneurons lying outside the oculomotor, trochlear and abducens nuclei,85a and may contribute to proprioception.

Extraocular Proprioception

Although human extraocular muscles contain muscle spindles,384'535 the palisade tendon organs seem most important for ocular proprioception.518'610 Afferents from these proprioceptors project via the ophthalmic branch of the trigeminal nerve and the Gasserian ganglion to the spinal trigeminal nucleus (pars interpolaris and pars caudalis).498 Proprioceptive inputs may also project centrally via the ocular motor nerves.204 From the trigeminal nucleus, proprioceptive information is distributed widely to structures involved in ocular motor control—the superior colliculus, vestibular nuclei, nucleus prepositus hypoglossi, cerebellum, and frontal eye fields—as well as to structures involved in visual processing—the lateral geniculate body, pulvinar, and visual cortex. The palisade endings are mainly associated with distal myotendinous junctions of the global, multiply innervated fiber type. This fiber type, which only accounts for about 10% of global fibers and is absent from the eyelid, might function similarly to the intrafusal fibers of skeletalmuscle.

What purpose could proprioception play in the normal control of eye movements? After all, vision provides continuous sensory feedback by which the brain can monitor the precision of gaze. Furthermore, no external loads are applied to the extraocular muscles (as they may be to skeletal muscles), and the extraocular muscles appear to lack a stretch reflex.312 After the trigeminal proprioceptors are severed, monkeys can still aim their eyes accurately after they are perturbed by electrical stimulation while in darkness.226 This evidence suggests that the brain monitors an efference copy or corollary discharge of ocular motor commands rather than relying on proprioception.

However, other evidence suggests that extraocular proprioception may play a role

in programing eye movements when visual cues are impoverished.12'654'655 If one eye is

artificially displaced with a suction contact lens and the subject views with the other eye, spatial localization is perturbed in the direction of forced eye rotation.199 Spatial localization is also impaired in patients who