usually pathologic.
Pursuit System
The pursuit system permits clear vision by maintaining foveation on a moving target and similarly provides foveal alignment when a person is moving through the environment. The neural substrate that controls pursuit movements at the cerebral level includes, among other areas, the FEF and the middle temporal (MT) area (where neurons preferentially respond to the speed and direction of moving stimuli), the medial superior temporal (MST) area, and the posterior parietal cortex. (Visual areas MT and MST are part of the dorsal visual processing stream, which plays an important role in detecting moving visual stimuli; see Chapter 1, Fig 1-23.) The descending pathways to the pons arise from an area at the confluence of the parietal, temporal, and occipital lobes and then pass through the posterior limb of the internal capsule. At the level of the brainstem, the pursuit system uses some of the same architecture described for saccades (the medial longitudinal fasciculus [MLF] and cranial nerve nuclei, in particular), with the addition of several other pontine nuclei. These nuclei project to the cerebellum, where the paraflocculus plays a role in sustaining pursuit movements.
Pursuit eye movements are tested by having the patient follow a predictably moving target horizontally and then vertically while the head and body are held in position. It is important that the target move relatively slowly—no faster than 30° per second (ie, one-third the distance from primary position to the far extent of the temporal visual field). It is virtually impossible to exceed this desired speed if the clinician’s whole body rocks side to side while holding up the fixation target rather than moving only the target. The latency to initiate the eye movements and the accuracy of following the moving target can be assessed. The gain of the eye movements should be 1—that is, the eyes should accurately follow the slowly moving stimulus. A low gain causes the eyes to lag behind the stimulus, which typically generates a saccade that allows the eyes to catch up to the stimulus.
Vergence
Vergence eye movements drive the eyes in opposite directions to maintain the image of an object on the fovea of both eyes as the object moves toward or away from the observer. Such movements are driven primarily by a disparity in the relative location of images on the retinas. The cerebral structures controlling vergence movements in primates are not well understood but involve binocularly driven cortical cells as well as brainstem neurons located in the mesencephalic reticular formation, just dorsal to the third nerve nuclei. Convergence is tested with an accommodative target that has enough visual detail to require an effort to see it clearly (a penlight or finger is not adequate). Apparent convergence deficiencies may result from poor patient effort, which may limit the clinical usefulness of such testing.
Clinical Disorders of the Ocular Motor Systems
Ocular Stability Dysfunction
The stability of ocular fixation may be disrupted by several types of abnormal eye movements known
collectively as saccadic intrusions (see Chapter 9), which are of brief duration, quite rapid, and in most cases small amplitude. The most common intrusions are square-wave jerks (SWJs), which lead the eyes off and then back onto the target with symmetric movements. Infrequent SWJs may be observed in patients with normal vision, especially during smooth pursuit movements, and often occur quite frequently or near continuously in patients with progressive supranuclear palsy (PSP) or certain cerebellar diseases. They may also be seen with cigarette smoking.
Square-wave jerks can be distinguished from other eye movement abnormalities such as nystagmus by clinical observation. They consist only of fast phases and lack periodicity. Further, SWJs, which can range in amplitude from 0.5° to >5° (macrosquare-wave jerks), are of much smaller amplitude than the eye movements that typify pendular nystagmus. The movements in pendular nystagmus are more sustained and oscillate across a fixation point, whereas those in SWJs cause the eye to move off to one side and then back onto fixation after a brief intersaccadic interval. Symptoms of higher-order cognitive disorders such as dementing illnesses or attention deficit disorder can confound the determination of whether a true ocular motor instability exists. See Chapter 9 for further discussion of saccadic intrusions.
Vestibular Ocular Dysfunction
Eye movement abnormalities can develop from either peripheral or central disruptions of vestibular activity, although peripheral end-organ disease of the semicircular canals is by far the most common cause of such abnormalities. (See the earlier section, Vestibular Ocular Reflex, for clinical assessment of VOR gain.) Patients with vestibular disease often have nystagmus (see Chapter 9). Peripheral disease can also impair the otolithic organs, which, when disrupted unilaterally, may produce skew deviation or an ocular tilt reaction (ie, a combined head tilt, skew deviation, and cyclotorsional rotation of the eyes; Fig 7-2). With an ocular tilt reaction, the head tilt and cyclotorsion (upper poles of both eyes) rotate away from the hypertropic eye, which is opposite to the normal compensatory rotation mediated by the VOR. The subjective visual vertical may be tilted in the direction of the ocular rotation, although the patient may not recognize that such a shift has occurred.
Figure 7-2 Ocular tilt reaction. The apparent tilt of the environment (1) is compensated for by an ocular tilt reaction (2) to achieve the illusion of normal upright orientation (3). With the ocular tilt reaction, the upper poles of each eye rotate toward
the lower ear. (Modified with permission from Kline LB, Bajandas FJ. Neuro-Ophthalmology Review Manual. 6th ed. Thorofare, NJ: Slack; 2008:71. Modified from Brandt T, Dieterich M. Pathological eye-hand coordination in roll: tonic ocular tilt reaction in mesencephalic and medullary lesions. Brain. 1987;110(Pt 3):649–666.)
Vestibular imbalance is common with lesions of the caudal brainstem (lower pons and medulla) because of disruption to the vestibular nuclei or their interconnections. One of the better known stroke syndromes involving this area is the lateral medullary syndrome (or Wallenberg syndrome). In general, damage to a lateral region of the brainstem disrupts the sensory pathways, and therefore Wallenberg syndrome is one type of “stroke without paralysis” (see Chapter 2, Fig 2-6). Patients may present with
ipsilateral loss of facial pain and temperature sensation (involvement of the descending tract of
CN V)
contralateral loss of hemibody pain and temperature sensation (involvement of the lateral spinothalamic tract)
ipsilateral cerebellar ataxia (damage to spinocerebellar tracts) ipsilateral first-order Horner syndrome
the ocular tilt reaction (sometimes)
In addition, patients may have dysarthria, dysphagia, vertigo, or persistent hiccups; there is no extremity weakness.
Although the lateral medulla is in the distribution of the posterior inferior cerebellar artery, Wallenberg syndrome usually results from occlusion of the more proximal vertebral artery. Consequently, patients may experience lateropulsion, the sensation of being pulled to one side, which results from damage to the vestibular nuclei. Patients may also manifest ocular lateropulsion; this effect can be tested by examination of horizontal pursuit and saccadic movements, which will reveal a bias that produces hypermetric movements toward the side of the lesion and hypometric movements away from the side of the lesion. Vertical saccades may follow an elliptical path as the eyes deviate toward the side of the lesion during the vertical movement. Finally, this directional bias also can be observed by noting that the eyes turn toward the side of the lesion after visual fixation is removed for a few seconds (by, for instance, having a patient close his or her eyes).
Although an intact VOR is essential for clear viewing of a stationary object during head motion, there are situations when stable foveation depends on the ability to cancel or suppress the VOR, such as when viewing an object that moves with the head. VOR suppression can be assessed by having the patient hold a near card in an outstretched hand and fixate on it while being rotated from side to side in the examination chair (Fig 7-3). Normal VOR suppression allows the eyes to maintain fixation on the card during rotation without requiring catch-up saccades; impaired VOR suppression is evidenced by the eyes moving off the target during rotation. As directed by the VOR, rotation to the patient’s right is met with conjugate eye movement to the patient’s left, followed by a corrective saccade rightward, back to the target. Impaired VOR suppression implies cerebellar disease and is particularly common in multiple sclerosis. It is normal in such assessments for the patient to exhibit catch-up saccades during the first 4 or 5 rotations but not thereafter.
Figure 7-3 Clinical assessment of vestibular ocular reflex suppression. A, The patient is seated in a swivel chair, fixating on the letters of a near card held at arm’s length. B, If VOR suppression is normal (intact), the eyes maintain fixation on the target as the chair, the patient’s head and arms, and the card rotate together as a unit. C, Conversely, if VOR suppression is impaired, the eyes are dragged off the target during rotation owing to an inability to cancel the VOR. In this