13 Acquired Ocular Motility Disorders and Nystagmus JANET C. RUCKER Introduction Supranuclear Ocular Motility Control Clinical Approach and Diagnostic Tools Abnormal Spontaneous Eye Movements Ophthalmoparesis Nystagmus Extraocular Muscles Saccadic Intrusions The Neuromuscular Junction Cranial Nerve Palsies References Brainstem Disorders Key Points Eye movement disorders may be considered in two categories: those that cause incomplete eye movements (ophthalmoparesis) and those that cause excessive eye movements (saccadic intrusions and nystagmus). Central to an understanding and correct diagnosis of abnormal eye movements is the evaluation of ocular alignment, ocular motility, and each functional class of eye movements: optokinetic, vestibular, vergence, smooth pursuit, and saccades. Ophthalmoparesis is caused by dysfunction of extraocular muscles, the neuromuscular junction, cranial nerves, cranial nerve nuclei, and internuclear and supranuclear connections. The initial pathologic eye movement in nystagmus is a slow drift of the eye away from the desired position, whereas the initial pathologic eye movement in saccadic intrusions is an inappropriate saccade that intrudes on fixation. Identification of the characteristics of nystagmus (physiologic versus pathologic, jerk versus pendular) is necessary for diagnostic evaluation and treatment. Introduction The goal of all normal eye movements is to place and maintain an object of visual interest on each fovea simultaneously to allow visualization of a stable, single object. Any deviation from normal eye movements may degrade vision. The spectrum of ocular motility disorders ranges from absent or inadequate 312 13 Acquired Ocular Motility Disorders and Nystagmus 313 ocular motor function (ophthalmoplegia or ophthalmoparesis) to excessive ocu- lar motor function (spontaneous eye movements). This chapter is divided into three sections; the first details those aspects of the history and examination required for an accurate diagnosis of abnormal ocular motility, the second con- cerns acquired disorders of ophthalmoparesis, and the third concerns acquired abnormal spontaneous eye movements. Clinical Approach and Diagnostic Tools Ophthalmoparesis results in ocular misalignment; hence an object of visual interest falls on the fovea in one eye and on an extrafoveal location in the other eye, leading to the subjective appreciation of binocular diplopia (Fig. 13–1). When there are abnormal spontaneous eye movements, illusory motion of the visual world (oscillopsia) occurs if the subjective experience of retinal motion is in excess of that normally tolerated by the visual system (up to about 5 degrees per second for Snellen optotypes).1 An understanding of the nature and pathophysiology of these symptoms allows the correct identification and localization of an ocular motility disorder. Binocular diplopia may result from dysfunction of extraocular muscles, the neuromuscular junction, cranial nerves, cranial nerve nuclei, and internuclear and supranuclear connections. Oscillopsia may result from nystagmus and saccadic intrusions. When diplopia is present, it is essential to determine if the diplopia resolves with covering each eye in turn (binocular diplopia). If it persists with monocular covering (monocular diplopia), it is not attributable to ocular misalignment but rather to refractive error or other ocular causes.2–4 It should be determined if binocular diplopia is horizontal, vertical, or oblique; worse in a particular direc- tion of gaze; and worse at distance or near. Horizontal diplopia is caused by impaired abduction or adduction and vertical diplopia by impaired elevation Figure 13–1 Fixation with normal ocular alignment is represented by solid black lines. An image of the feather falls on each fovea simulta- neously and a single object is seen. Binocular diplopia, which develops with an ocular mis- alignment (lateral deviation of the right eye as depicted by the dashed arrow), occurs because the image of the feather falls on an extrafoveal location in the deviated right eye (dashed lines). (Adapted from Leigh RJ, Zee DS: The Neurology of Eye Movements, 3rd ed. Oxford, Oxford University Press, 1999, p 337.) 314 Neuro-Ophthalmology: Blue Books of Neurology or depression. Worsening diplopia in a particular gaze direction suggests that motility in that direction is impaired. The temporal course of the diplopia and any associated neurologic symptoms should be assessed; proximal muscle weak- ness, difficulty swallowing, and shortness of breath, for example, suggest neuro- muscular dysfunction, and a deterioration of monocular vision and proptosis suggest an orbital process. These historical features are also important in the evaluation of patients with oscillopsia and spontaneous eye movements. The neurologic and visual systems should be carefully examined in all patients with diplopia, ophthalmoparesis, oscillopsia, or abnormal spontaneous eye movements.5 The eye movement examination should include an assessment of ocular alignment and motility, as described in Chapter 1 (Fig. 13–2). In addition, stability of gaze fixation should be assessed with the eyes close to central position, viewing near and far targets, and at eccentric gaze angles. Prolonged observation for up to 2 minutes is necessary, as some types of nystagmus periodically change direction. Observation of the effect of removal of fixation on eye stability is also important, as nystagmus caused by peripheral vestibular dysfunction may only be visible under this circumstance. This can be achieved by transient coverage of the fixating eye during ophthalmoscopy in a dark room. Each functional class of eye movements should be examined in both horizon- tal and vertical directions. Optokinetic nystagmus occurs reflexively during self- rotation and can be elicited at the bedside with visual tracking of an optokinetic drum or tape with alternating black-and-white vertical stripes. It consists of slow tracking, smooth pursuit movements alternating with quick resetting saccadic movements.6 Vestibular eye movements hold an image steady on the fovea by means of compensatory eye movements during brief, nonsustained head move- ments, such as during walking. These eye movements may be evaluated clini- cally with passive head thrusts during which the examiner applies a low- amplitude, high-acceleration head rotation while the patient fixates a target.7,8 If vestibular function is normal, the patient will maintain fixation of the target during and after the head movement. If vestibular function is impaired, the patient will not be able to maintain fixation and a corrective saccade back to the target is seen following the head rotation. Examiner-applied passive head thrusts are more sensitive than patient-initiated active head thrusts for identify- ing vestibular dysfunction.9 Vergence eye movements consist of disconjugate convergent and divergent eye movements that maintain stability of a visual image during near and far gaze shifts. Smooth pursuit is a slow eye movement A Figure 13–2 Corneal light reflection test. A, Normal ocular alignment—a light shined in the center of one pupil B falls in the center of the other pupil. B, Exotropia—a light shined in the center of one pupil falls medial to the pupil C, center in the other eye. Esotropia—a light shined in C the center of one pupil falls lateral to the pupil center in the other eye. D, Right hypertropia—a light shined in the center of the pupil in the left eye falls below the pupil center in the right eye. D 13 Acquired Ocular Motility Disorders and Nystagmus 315 (velocity 20 to 50 degrees/second), which functions to hold the image of a moving target steady on the fovea and which can be assessed by having the patient follow a slowly moving target. Saccades are fast eye movements (velocity 300 to 500 degrees/second) that rapidly shift gaze to place an object of visual interest on the fovea.10 Saccades present a challenging task to the brain, as their execution requires a sudden, intense neural discharge to effect a high-velocity eye movement and to overcome the elastic, damping orbital pull of extraocular muscles and suspensory ligaments.10 This intense neural discharge is provided by brainstem neurons called burst neurons. Ophthalmoparesis EXTRAOCULAR MUSCLES Thyroid ophthalmopathy is typically painless and bilateral, although it may be asymmetric. It tends to affect the inferior and medial rectus muscles first, leading to restrictions of elevation and abduction. Although it is useful to obtain thyroid function studies (thyroid-stimulating hormone, triiodothyronine, and thyroxine), it may be associated with hyperthyroid, hypothyroid, or euthyroid states. Thyroid-stimulating antibodies correlate with the presence of thyroid eye disease and can be an important disease marker in the setting of a serologic euthyroid state.11–13 Orbital computed tomography (CT) or magnetic resonance imaging (MRI) scans demonstrate enlargement of involved extraocular muscle bodies with relative sparing of muscle tendon insertions at the globe (Fig. 13–3A). Coronal images are best, because muscle enlargement may be underestimated if only axial images are acquired. Treatment options include corticosteroids, radiation, and orbital decompression surgery, as discussed in Chapter 3. Discontinuation of smoking should be strongly advised, as smoking may worsen thyroid ophthal- mopathy and lessen treatment effect.14,15 Orbital pseudotumor is typically painful and unilateral. Any extraocular muscle may be involved;