When ocular electromyography became available, it became possible to study the cofiring and reciprocal innervation of the extraocular muscles. Normal muscle firing patterns could be compared with those of paralytic muscles, and recovery could be documented. However, ocular electromyography was available at only a few centers, required sophisticated equipment, and was not applicable to pediatric patients because of their discomfort and inability to cooperate sufficiently for the study. An objective test that could provide information about the strength of an extraocular muscle yet be relatively simple, inexpensive, safe, and able to be performed on patients of all ages would be a useful addition to the evaluation of patients with strabismus, providing information to assist in diagnosis and to aid in management decisions.

Direct measurements of muscle force are difficult to perform quantitatively and usually are not possible in the pediatric age group. Eye movements can be measured relatively easily and accurately with equipment available in many hospitals and medical centers, however.

The term saccadic movement applies to the rapid changes in eye position typically found between fixational pauses during reading.¹ Movements constituting the fast phase of nystagmus were noted to have similar characteristics. Saccades have a latency of 150 to 200 msec and, once started, cannot be stopped.² Electromyographic recordings during a saccade show a large motor unit input.³

The velocity of a saccadic eye movement is related directly to the force produced by an extraocular muscle and thus is an indicator of the strength of a rectus muscle. A saccade also acts as a stress test because the muscle must function fully to produce a saccadic movement with a normal, rapid velocity.

Although eye movements can be measured by a number of techniques and devices,⁴ electro-oculography has proven to be a readily available, relatively simple technique that provides sufficient accuracy for clinical purposes. It has been known since the early 1920s that certain electrical changes are associated with eye movement. The eye has a standing electrical potential or charge across it, like a weak battery, with the front of the globe positive and the back negative. The resting or “standing potential” is generated largely by the transepithelial potential across the retinal pigment epithelium. It varies from one to several millivolts.⁵ With electrodes placed on both sides and above and below the eye, potentials indicating both horizontal and vertical eye movements may be recorded without interference to normal eye movements. The method is useful and convenient for recording rotations in the range of 0.5 to 40 degrees. The method is linear over a segment of the range, and careful calibration can be used to determine the extent of large movements.

The technique of electro-oculography for saccadic velocity determinations is useful in infants and young children because head fixation is not required. Both average and peak velocities can be measured because inspection of the eye position tracing itself provides information about the amplitude of the saccade and the shape of the tracing for comparison with normal recordings.

Saccades usually are generated by voluntary eye movements of 20 to 40 degrees across the primary position, either horizontally or vertically. In patients in whom paralysis or restriction prevent rotations of this size, the largest eye movements possible are recorded.

Calibration is performed by having the subject make a 20-degree saccade using the eye being studied for fixation. A bowl perimeter can be useful in quantifying the size of the saccade for calibration.

With infants and young children, saccades can be generated involuntarily by the use of optokinetic or vestibular nystagmus. The rapid recovery phase of nystagmus is a saccadic eye movement. A small, rotating drum or optokinetic nystagmus tape can be used to elicit optokinetic nystagmus, whereas spinning an infant in his mother's arms can induce vestibular nystagmus. Normally rapid, recovery saccades of optokinetic nystagmus are shown in Figure 3, whereas the slow recovery saccades produced by the lateral rectus muscle in a patient with sixth nerve palsy are shown in Figure 4.

To provide reliable calibration in very young patients, the child's fixation with one eye can be obtained by showing a colorful, moving, noisy toy at a distance of one third of a meter. A 10-Δ prism is introduced before the fixing eye, and the resulting horizontal eye movement is recorded by electro-oculography. The recorded eye movement can be used for calibration as the distance the eye moved is known.⁶

During the studies, it seems to make little difference whether the paretic or nonparetic eye is used for fixation, as long as equal amplitude saccades are used for comparison.⁷ For calibration purposes, however, the eye in which saccades are to be measured must be used for fixation .

Raab⁸ found peak saccadic velocity determinations for 20-degree saccades to be distributed normally and range from 281 to 541 degrees per second. He concluded that peak horizontal saccadic velocities of less than 300 degrees per second are likely to be abnormally slow using his Tracoustics equipment.

Direct observation of the speed of saccadic movements is easy to do but is less accurate. When saccades are very slow, as in the case of a complete paralysis of a rectus muscle, direct observation is both simple and accurate. Rosenberg⁹ commented that slight differences in saccadic velocities may be difficult for an untrained observer to identify. By using a + 14- or + 20-diopter lens over one or both eyes, velocity differences became more readily apparent because of the magnification of the high plus lens.

SIXTH NERVE PALSY

The typical clinical picture of sixth nerve palsy is that of abduction deficiency with significant esotropia in primary gaze. Saccadic velocity, produced by the palsied lateral rectus muscle (toward abduction), can be compared with the speed of the movement toward adduction in the same eye (medial rectus function) and with abduction in the opposite eye (contralateral lateral rectus function) when the palsy is unilateral. Average normal saccadic velocity for a movement of 20 degrees or larger usually is between 200 and 320 degrees per second. Saccades produced by the palsied lateral rectus muscle vary from 40 degrees per second (Fig. 5) with complete paralysis to 160 degrees per second (Fig. 6) when only mild paresis is present.¹⁰ Recovery of the lateral rectus palsy can be documented by increased saccadic velocity with time.

In patients with marked or complete lateral rectus paralysis, visual observation of lateral saccades can reveal slowing. This slow movement is caused by relaxation of the antagonist medial rectus without active contraction of the lateral rectus muscle. When only mild to moderate lateral rectus palsy is present, eye movement recordings are needed to document the reduction in velocity.

Rosenbaum and associates¹¹ used horizontal saccadic velocity measurements to determine whether transposition surgery with botulinum injection to the medial rectus was indicated in patients with sixth nerve paresis or paralysis. Only those patients with marked slowing of abduction saccadic velocity underwent this procedure.

Subjects are unable to alter saccadic velocity for a fixed amplitude horizontal movement. Thus, slow saccades cannot be made voluntarily. A decrease in saccadic velocity is caused by an abnormality in the oculomotor apparatus.

Similar slowing of a saccade is noted following injection of Clostridium botulinum toxin into a rectus muscle. Velocity returns to normal in 4 to 6 weeks, when the effect of the toxin has worn off.

THIRD NERVE PALSY

Exotropia in primary gaze associated with limited adduction, elevation, and depression is the major clinical finding in third-nerve palsy. Ptosis and a nonreactive pupil also are noted frequently. Adduction saccades in the affected eye vary from an average velocity of 30 to 175 degrees per second. Vertical saccades vary from 10 to 150 degrees per second, depending on the extent of the palsy. These slower velocities are probably due to the fact that some of the vertical saccades may be smaller than 20 degrees in amplitude because of significant weakness of both the superior and inferior rectus muscles.

After complete third-nerve paralysis, the eye typically assumes a slightly hypotropic and markedly exotropic position. If this deviation persists, the lateral rectus and adjacent tissues usually become shortened and contractured and nasal rotation of the globe also becomes mechanically limited. If medial rectus function recovers, nasal rotation will remain deficient because of lateral restrictions. Saccadic velocity studies can reveal the extent of recovery of the medial, superior, and inferior rectus muscles, even if rotations remain limited.

SUPERIOR OBLIQUE PALSY

Although Rosenbaum and coworkers¹² reported slowing of peak velocity of downward saccades in superior oblique palsy, this finding has not been confirmed.¹³ Even when measured with the involved eye in the adducted position, upward and downward saccades appear normally and equally rapid (Fig. 7). It would seem as if the diagnosis of fourth-nerve palsy should be made on clinical grounds (e.g., small hypertropia, V pattern, antagonist inferior oblique overaction, positive Bielschowsky head tilt test, excyclotorsion) rather than on saccadic velocity measurements. Calculations of the superior oblique muscle's contribution to downward gaze in adduction (only 18%) support the concept that saccadic velocity will be affected minimally by paresis of this muscle.¹⁴

DUANE SYNDROME

In type I Duane syndrome (Huber's classification), there usually is a small-angle esotropia or no deviation in primary gaze. Abduction shows marked limitation, whereas adduction is only mildly limited and is associated with retraction of the globe and oblique overaction. The average abduction saccadic velocity usually is quite slow, whereas the average adduction velocity is only moderately reduced¹⁵ (Fig. 8). This is due to the lack of lateral rectus firing on attempted abduction along with paradoxical innervation of the lateral rectus on attempted adduction. These findings clearly differentiate type I Duane syndrome from lateral rectus palsy. Because the approach to therapy differs significantly in these two conditions, these diagnoses must not be confused.

In type II Duane syndrome, average abduction saccades generally are normal in speed, but adduction saccadic velocity is markedly subnormal. The typical type III Duane syndrome has slowed saccades both medially and laterally, presenting a distinctive picture.

THYROID OPHTHALMOPATHY

Limited elevation of one or both eyes, often accompanied by exophthalmos and eyelid retraction, is a common motility defect seen in patients with thyroid eye disease. Limitation of abduction, adduction, and depression also may be seen, in decreasing order of frequency. The forced traction test is invariably positive, most notably to upward gaze.

Upward and downward saccades essentially are equal in speed and are rapid (Fig. 9). This indicates that limitation of upward gaze is restrictive and not paretic and also applies to abnormalities of horizontal rotation.

A report by Hermann¹⁶ has shown evidence of inferior rectus weakness (with a slowing of the downward saccade) in two patients with relatively acute dysthyroid eye disease. This appears to be an unusual finding and is not typical of the findings in endocrine ophthalmopathy of prolonged duration.

Feldon and colleagues¹⁷ found decreased peak saccadic velocities in patients with Graves' disease and optic neuropathy. This finding seemed to be related to an increase in extraocular muscle volume and further limitation of ocular motility, both consistent with increased pressure on the optic nerve. As optic nerve compression improved during treatment, saccadic velocities improved, so that the eye movement recordings were a useful adjunct in evaluation of the course of Graves' ophthalmopathy.

ORBITAL FLOOR FRACTURE

In patients with orbital floor fracture, it may be difficult to assess the functional status of the inferior rectus muscle solely on the clinical findings. Orbital tissue incarceration often causes restriction of ocular elevation and depression, discomfort with attempted vertical rotations, and a vertical deviation in the primary position. Paresis of the inferior rectus muscle and orbital hemorrhage and edema may produce similar findings. Diplopia, in association with orbital floor fracture, usually is caused by incarceration of orbital tissues into the fracture site rather than by prolapse of orbital contents into the maxillary antrum alone. These tissues include orbital fat, inferior rectus and inferior oblique muscles, and their connective tissue sheaths. The inferior rectus muscle may be paretic or normal in its action, depending on the degree of injury caused by restriction at the fracture site.

In patients with normal inferior rectus function, downward saccades usually are rapid (Fig. 10).¹¹ Once the traumatic edema has subsided, there often is little or no vertical deviation in primary gaze. When the inferior rectus is paretic, downward saccades are slowed (Fig. 11) and a residual vertical deviation frequently is noted in the primary position.¹⁸ Upward saccades invariably are normal in velocity, even with limitation of full upward gaze. Preoperative slowing of downward saccades suggests that a hyperdeviation is likely to persist after orbital floor fracture repair.

BROWN SYNDROME

Brown syndrome has the characteristics of diminished elevation in adduction, improved elevation in the primary position, and normal or almost normal elevation in abduction. Results of the forced duction test, upward and inward, are positive.

Upward and downward saccades are equal and normally rapid. This is true for vertical movements in the primary position, adduction, and abduction and is similar to measurements in the opposite, uninvolved eye. This is consistent with the restrictive nature of this condition.

POSTOPERATIVE RESTRICTIONS

After orbital surgery, retinal detachment surgery, and strabismus surgery (especially multiple reoperations), there may be some limitation to full ocular rotation. Is this limitation due to mechanical restriction or weakness (or disinsertion) of an extraocular muscle? Restrictions may be the most frequent cause of limited motility.

Saccades, both horizontally and vertically, have normal velocity, indicating no evidence of rectus muscle weakness.

The forced duction test is a useful diagnostic step in patients with limitation of ocular movement. However, this test may be uncomfortable and, if the restriction is mild, may be difficult to interpret. Although modifications have been developed, the unwieldiness and imprecision of present techniques have not been overcome.

Saccadic velocity studies easily and reliably identify restriction in some patients with limited motility after orbital, retinal detachment, or repeated strabismus operations. In addition, the test can be performed on patients of all ages and is a noninvasive technique.

“DOUBLE ELEVATOR” PALSY

Double elevator palsy is a term frequently used to describe unilateral diminished ocular elevation present in all fields of gaze. Limited elevation may be due to innervational causes (supranuclear, nuclear, or infranuclear), restrictive mechanisms in the orbit, or a combination of both. The correct treatment of these problems depends on the proper identification of restriction or muscle weakness.

In patients with no vertical deviation in primary gaze, upward gaze limitation usually is mild to moderate and upward saccades generally are rapid and sharp¹⁹ (Fig. 12). This indicates a restriction to upward gaze without evidence of superior rectus paresis.

In a group of patients with a primary position hypotropia, some demonstrate normal upward saccades, whereas others show slowing of upward saccadic movements consistent with superior rectus paresis¹⁹ (Fig. 13).

Scott²⁰ found that the effect on peak velocity and isometric force from oblique paralysis was minimal, but quite a marked reduction resulted from vertical rectus paralysis.

When treating double elevator palsy, Dunlap²¹ suggested that medial rectus-lateral rectus transposition superiorly should be reserved only for dysfunction of neurogenic origin; dysfunction on a mechanical basis is not corrected by this technique. Therefore, forced duction testing must be performed to identify restrictions and saccadic velocity measurements must be performed to assess superior rectus muscle function before surgery.

LIMITED DOWNWARD GAZE

Although monocular downward gaze limitations are infrequent, they can be caused by innervational or restrictive factors, just as in patients with deficits of elevation. Appropriate management strategy requires knowledge of the forces available to move the globe downward and the presence of mechanical restrictions that limit downward gaze. Although the forced duction test provides information about restrictions, vertical saccadic velocity determinations can assess the active force available to move the eye inferiorly in patients with monocular limitation of downward gaze.

Most patients have a hypertropia in primary gaze. Most patients show slowing of downward saccades (Fig. 14), which is indicative of inferior rectus weakness.²²

Monocular limitation of elevation was not found commonly to be caused by superior rectus palsy.¹⁹ Although monocular limitation of depression may be seen less often, a larger percentage of patients had evidence of rectus muscle paresis. This suggests that restrictions in the superior portion of the orbit probably are less common than those in the inferior orbit.

MYASTHENIA GRAVIS

Approximately half of all patients with myasthenia gravis present with symptoms related to eye movements and lids. Response to intravenously administered edrophonium chloride (Tensilon) by improved oculomotor function is considered diagnostic. Such improvement may be uncertain or elusive. Tests to demonstrate equivocal degrees of improvement include red-green glass diplopia, tonography, ocular electromyography, and optokinetic nystagmus. Because saccadic velocities are affected by mild to moderate degrees of paresis, analysis of these movements can be a consistent, reliable, objective indicator of the effect of edrophonium on the oculomotor function of patients with myasthenia gravis.

Saccades, reduced in velocity due to myasthenia gravis, become rapid after edrophonium administration. This is demonstrated nicely using recordings of optokinetic nystagmus. A fatigue effect is noted with continued stimulation, followed by rapid recovery of good nystagmic eye movements and an increase in the velocity of the saccadic portion of the nystagmus²³ (Fig. 15). After the edrophonium has worn off, the pattern of eye movements returns to the preinjection level.

Several investigators have reported increased amplitude of optokinetic nystagmus after edrophonium administration to myasthenic patients.^24–26 Yee and coworkers²⁷ found that during large saccades, a high velocity cannot be sustained. After a rapid, initial movement of the saccade, velocity decreases rapidly and the eyes slowly drift toward the target. Intrasaccadic fatigue of extraocular muscle fibers, which normally generates the rapid eye movement in response to pulse innervation from the oculomotor neurons, appears to produce the sudden decrease in saccadic velocity.

CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA

In its early stages and milder forms, chronic progressive external ophthalmoplegia often is misdiagnosed. Patients frequently present with ptosis and ophthalmoplegia. The ophthalmoplegia tends to be symmetric comparing the two eyes, and both the lid and ocular motility deficits are unresponsive to administration of edrophonium, which is helpful in differentiating this entity from myasthenia gravis. In addition, no worsening is observed with fatigue.

Saccadic speed, both horizontally and vertically, is reduced in this group of patients. The degree of slowing varies among patients (a range of 20 to 150 degrees per second).²⁸ The slow velocity is symmetric between the two eyes of the same patient, however, which helps distinguish this condition from other ophthalmoplegias. This has diagnostic value because it may obviate the need for an unwarranted neurologic workup and point out the possibility of heart block in some of these patients.

INTERNUCLEAR OPHTHALMOPLEGIA

Lesions of the medial longitudinal fasciculus demonstrate deficient adduction and jerk nystagmus of the abducting eye. Patients often are orthotropic in the primary position, and adduction with convergence may be preserved. In some cases of internuclear ophthalmoplegia, the clinical signs are not obvious. The bilateral form almost always is indicative of multiple sclerosis; thus, a simple test that could establish the diagnosis would be valuable in patients who otherwise might require more formidable and prolonged studies.

Abduction saccades are normal in velocity, whereas adduction saccades in the uninvolved eye of patients with monocular internuclear ophthalmoplegia also are normal. Adduction saccades in the involved eye are reduced in speed, and the eye movement tracing demonstrates the abduction nystagmus well²⁹ (Fig. 16). In the early stage of internuclear ophthalmoplegia, when adduction appears full, saccades may be slow, a fact that is of use in the diagnosis.

Dell'Osso and associates³⁰ also found that recovery saccades of optokinetic nystagmus, produced by the involved medial rectus, are slow. Siroky and coworkers³¹ demonstrated slow recovery saccades produced by the medial rectus in postrotary nystagmus in patients with internuclear ophthalmoplegia. They showed that it was possible to discover the latent form of internuclear ophthalmoplegia in the early disease state by using eye movement recordings.

MÖBIUS SYNDROME

Möbius syndrome is characterized by congenital facial diplegia associated with limitations of horizontal eye movements. Vertical rotations are intact. Other anomalies sometimes seen include lagophthalmos, partial atrophy of the distal tongue, congenital heart defects, and extremity abnormalities.

Most patients are esotropic and have a range of horizontal eye movement as small as 10 degrees. Saccadic velocities are very slow, both toward abduction and adduction,³² indicating more than sixth-nerve involvement. Electromyographic evidence suggests the existence of a supranuclear lesion affecting the horizontal rectus muscles.³³

The rationale for the effectiveness of muscle transposition surgery has not always been clear. There has been some suggestion that central nervous system readjustment of ocular motor control can occur.³⁵ With the use of both ocular electromyography and central sixth-nerve stimulation, it has been shown that no change in the firing pattern of transposed lateral and superior rectus muscles occurred.³⁶ The eye movements observed after recovery from the transposition procedure could be explained entirely by the new position of the lateral rectus muscle insertion, with the lateral rectus acting in an unchanged manner.

Saccadic velocities before transposition surgery were found to be slow in patients with rectus muscle paralysis. After surgery, there was an immediate noticeable increase in saccadic speed (Fig. 17), although not to normal levels.³⁷ Recession-resection surgery in this group of patients resulted in no increase in velocity of the slow saccade measured preoperatively.

These studies suggest that the improved rotation and saccadic speed result from the mechanical effects of transposition surgery, not a central, relearning process.

The diagnosis may be confusing shortly after surgery because of pain, edema, and photophobia. A test that could be performed in the immediate postoperative period could be used with children and would give relevant, accurate information concerning the diagnosis of a disinserted or slipped muscle and would be a valuable adjunct in strabismus evaluation.

Surgery using a topical anesthetic has indicated that saccades are slowed moderately but not eliminated after horizontal rectus muscle disinsertion.³⁸ This probably is due to the persistence of posterior intermuscular and Tenon's fascial attachments of the disinserted muscle.

There is no change in saccadic speed after a rectus muscle recession of a usual amount. In patients with a surgically documented lost or disinserted muscle, there is a moderate reduction of saccadic velocity into the field of action of the disinserted muscle³⁹ (Fig. 18). The difference between agonist and antagonist velocities is around 50%. When the muscle can be located and resutured to the globe, the saccade returns to normal (Fig. 19).

Saccades produced by a paralytic rectus muscle are very slow and usually can be observed to “float.” Saccades caused by a disinserted muscle are somewhat more rapid, and eye movement recordings are helpful in documenting the reduced velocity. Early diagnosis is helpful because a slipped muscle is easier to locate within several days after surgery. Often, a suture remnant helps identify the muscle and the muscle may not have retracted very far posteriorly. In addition, scarring usually is mild and tissue dissection and exploration are less difficult. Good alignment with full rotations can be restored if the disinserted muscle can be found.

Aging of the neurologic system may produce similar changes. Elderly subjects commonly showed an increase in reaction time and a decrease in saccadic velocity.⁴² Multistep saccades, typically seen in patients with degenerative neurologic disease, often were noted in this older group of healthy patients.

Evidence has been found that during saccades, the central fibers (fibers closest to the globe) of an extraocular muscle are responsible primarily for overcoming the viscous forces of the globe and orbit and for achieving high velocities in response to the pulse change in innervation.⁴⁵ The orbital fibers are more important in maintaining the final position of the eye at the end of a saccade in response to the step change in innervation.

Mims and Treff⁴⁶ measured horizontal saccades in healthy subjects. They reported that percent differences between saccades produced by agonist-antagonist muscles averaged about 5% whereas differences between symmetric muscles averaged around 9%. They believed that this type of analysis of the data allows more accurate detection of pathology than comparison of a single saccadic velocity with an average of controls because of intersubject variability.

Scott²⁰ reported that full paralysis of a horizontal rectus muscle gives a saccadic velocity of 15% to 20% of normal values. This is consistent with average saccadic velocities of 30 to 50 degrees per second for movements of 20 degrees or more with complete paralysis, with a range of 200 to 320 degrees per second in healthy subjects.

Huber⁴⁷ concluded that “oculography represents an ideal method for the analysis of pathologic eye motility and furnishes some important measurable parameters for the prognostic and therapeutic evaluation of oculomotor disorders of different types.”

It does not yet seem possible to render high-quality diagnostic and therapeutic care to patients with some forms of strabismus without the availability of saccadic velocity recordings. The technique is noninvasive, relatively short, simple, and inexpensive, and can be used in patients of any age.⁴⁸ In cases of paresis, restriction, neuro-ophthalmic eye movement disorders, and possible slipped muscle, saccadic velocity measurements are a great assistance in proper diagnosis, and thus in determining appropriate management strategy. Saccadic velocity studies do not appear of value in some other forms of strabismus, including infantile esotropia, accommodative esotropia, and intermittent or constant exotropia.

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