example, the chair is rotated to the patient’s right, and the VOR moves the eyes to the patient’s left, prompting a rightward saccade to regain the target; this result likely indicates right cerebellar system pathology. (Illustration b y Christine Gralapp.)

Optokinetic Nystagmus Dysfunction

Optokinetic nystagmus represents the combined response of the optokinetic and smooth pursuit systems. Separation of the optokinetic contribution from the smooth pursuit component of the response generally requires specialized experience or testing equipment. Abnormalities of the smooth pursuit or saccadic components, however, can be recognized by using an OKN drum. Asymmetry of the drum-induced responses can be caused by a unilateral lesion of the cerebral pathways that descend from the ipsilateral parietal, middle temporal, or medial superior temporal areas to the brainstem ocular motor centers. An asymmetry of OKN responses produced by rotating the drum’s stripes toward the patient’s right suggests a lesion in the right cerebrum. Typically, relatively large lesions of the parietal or parietal-occipital cortex are required to produce drum-induced asymmetries; these lesions are usually accompanied by a homonymous hemianopia. A lesion confined to the occipital lobe (eg, as usually occurs secondary to stroke within the distribution of the posterior cerebral artery) also produces a homonymous hemianopia but not OKN asymmetry. Hence, OKN testing can provide clinical insight into the location and extent of a cerebral lesion that produces a homonymous hemianopia.

Saccadic Dysfunction

Saccadic disorders may produce delayed latency to initiate eye movements, reduced speed of eye movements, or poor accuracy of eye movements (eg, hypometria or hypermetria). The specific saccadic disorder relates to the pattern of neural activity delivered to the ocular motoneurons. Slow saccades result from a neural pulse with reduced peak activity. An inappropriate pulse amplitude will produce an inaccurate saccade, and drifting off the target will occur when the step is insufficient for the given pulse amplitude (see the earlier section, Saccadic System, and Chapter 9, Gaze-Evoked Nystagmus). Saccadic dysfunction may also produce unwanted saccadic intrusions because of faulty suppression mechanisms, which may disrupt ocular fixation (see the earlier section, Ocular Stability Dysfunction, and Chapter 9, Saccadic Intrusions).

When a patient appears unable to initiate saccades, the doll’s head maneuver can demonstrate if this inability is the result of a supranuclear or infranuclear lesion. In the presence of a supranuclear lesion, the doll’s head maneuver can excite the vestibular pathways to drive the eyes in a manner that could not be initiated volitionally via descending pathways from the FEFs to the ocular motor nuclei. In other cases, saccades are initiated only after prolonged latency. Assessment of saccadic latency must take into account the patient’s age; a gradual increase in latency may occur with advancing age. Patients with PSP have slow volitional saccades, especially in the vertical plane, but their reflexive saccades (those directed to an unanticipated target, like a ball thrown toward a patient or the fast phases of OKN) often are initially normal. Other central nervous system disorders that cause slow saccades include cerebellar degeneration, Huntington disease, Wilson disease, Whipple disease, and pontine disease.

Central lesions that alter saccadic speed usually produce slower-than-normal saccades, which are also associated with a variety of peripheral lesions (including nuclear, infranuclear, neuromuscular, or restrictive abnormalities). Peripheral lesions almost always produce slowed saccadic movements

that are hypometric. In contrast, slow saccades with normal amplitude are typical of central lesions, especially of the cerebral hemispheres or basal ganglia. Irrespective of the location of a central lesion, slowed saccades ultimately result from lack of activation of the burst neurons or lack of inhibition from the omnipause neurons, both of which are in the paramedian pontine reticular formation. Saccadic slowness confined to the horizontal plane suggests pontine disease, whereas saccadic slowness confined to the vertical plane suggests dysfunction of the midbrain. All these cases typically include a prolonged latency to initiate eye movements.

Hypometric saccades can be observed with peripheral or central lesions, whereas hypermetric saccades are usually the result of disease of the cerebellum or its interconnections. Myasthenia gravis may produce faster-than-normal (“lightning-like”) saccades, although these occur only over a reduced range of amplitudes.

The accuracy of saccadic eye movements can be difficult to assess in patients with significant bilateral loss of vision, especially those with large visual field defects (eg, homonymous hemianopia and bitemporal hemianopia). Thus, describing the presence of hypometric saccades in this group of patients requires caution.

The most common saccadic dysfunction is part of normal aging; that is, the conjugate limitation of upgaze characterized by eye movements that have reduced range but normal velocity. Abnormalities of saccadic function are relatively nonspecific with regard to etiology and site of the lesion, but notable exceptions occur in which saccadic abnormalities provide important clues to the diagnosis. These exceptions include

obviously slowed saccades in a patient with extrapyramidal (ie, Parkinson-like) syndrome with imbalance and impaired cognition, which suggest a diagnosis of PSP

hypermetric saccades, which usually indicate disease of the cerebellum or its outflow pathways unidirectional hypermetric saccades, ocular lateropulsion, and hypermetric pursuit movements, which are generally present as part of the lateral medullary syndrome (Wallenberg syndrome)

Ocular motor apraxia

An extreme instance of saccadic dysfunction is ocular motor apraxia. (An apraxia is an inability to voluntarily initiate a movement that can be initiated by another means, usually via a reflex, which reveals that a paralysis is not present.) Patients with congenital ocular motor apraxia characteristically use horizontal head thrusts past the point of interest, employing the VOR to move the eyes into extreme contraversion until foveation on the target is possible; this maneuver is followed by slower head rotation in the opposite direction to primary position while the eyes maintain target fixation. Vertical eye movements occur normally, as do nonvolitional saccades that occur as a reflex to a moving object or sound. The location of the lesion that causes congenital ocular motor apraxia is not known but probably is above the brainstem centers that drive volitional saccades. Patients with this condition may have other neurologic abnormalities, including delayed development. Ocular motor apraxia is associated with several diseases, including ataxia telangiectasia, Pelizaeus-Merzbacher disease, Niemann-Pick disease type C, Gaucher disease, TaySachs disease, Joubert syndrome, abetalipoproteinemia (causing vitamin E deficiency), and Wilson disease.

Acquired ocular motor apraxia results from bilateral lesions of the supranuclear gaze pathways of the frontal and parietal lobes, usually from bilateral strokes, often as part of an anoxic encephalopathy following either cardiac arrest or coronary artery bypass grafting. This condition has

also been observed after thoracic aortic aneurysm repair. Patients often blink to break the fixation and then turn their head toward a new point of interest. Bilateral lesions at the parieto-occipital junction may impair the guidance of volitional saccades. Such inaccurate saccades, together with optic ataxia (inaccurate arm pointing; as when a patient misdirects his or her hand when attempting to shake yours, despite being able to see your hand) and simultanagnosia (disordered visual attention that makes it difficult for a patient to perceive all the major features of a scene at once) are known as the Balint syndrome; this syndrome is often associated with cognitive dysfunction (see Chapter 6).

Cogan DG. Congenital ocular motor apraxia. Can J Ophthalmol. 1966;1(4):253–260.

Gaze palsy, gaze preference, and tonic deviations

Gaze palsy is a symmetric limitation of the movements of both eyes in the same direction (ie, a conjugate ophthalmoplegia). Gaze preference is an acute inability to produce gaze contralateral to the side of a cerebral (supranuclear) lesion; it is accompanied by a tendency for tonic deviation of the eyes toward the side of the lesion. In such cases, the doll’s head maneuver generates a full range of horizontal eye movements because the infranuclear pathways are intact. Stroke is the most common etiology for this type of cerebral injury. The eye movement dysfunction is generally temporary, lasting only days or weeks. Presumably, alternative cerebral–bulbar pathways (perhaps from the parietal lobe) become increasingly capable of generating the saccades.

In contrast, brainstem lesions that produce a horizontal gaze palsy disrupt eye movements toward the side of the lesion (opposite to the pattern observed with lesions of the FEF) (Fig 7-4). With pontine lesions (nuclear and infranuclear), the final common site for supranuclear inputs (from volitional, reflex, and vestibular centers) is damaged, and thus the doll’s head maneuver is ineffective in driving the paretic eyes. Bilateral pontine injury can abolish all horizontal eye movements. This devastating injury still allows vertical eye movements, which often occur spontaneously (ie, ocular bobbing; see Chapter 9).

Figure 7-4 Axial MRI scan of a brain. T1-weighted image without contrast shows signal hyperintensity (arrows) in the bilateral pons. This 67-year-old patient presented with “trouble moving my eyes” and was found to have a virtually complete horizontal gaze palsy, consistent with ischemia involving the paramedian pontine reticular formation on both

sides. She had no other focal neurologic deficits. (Courtesy of Prem S. Sub ramanian, MD, PhD.)

Congenital horizontal gaze palsy can occur as part of Möbius syndrome, in which aplasia of the sixth nerve nuclei is accompanied by bilateral facial paresis. A gaze palsy occurs, rather than an ipsilateral limitation, because the sixth nerve nucleus also contains internuclear neurons destined for the contralateral oculomotor nucleus (CN III) via the MLF.

Vertical gaze palsies can manifest as selective limitation of upgaze or downgaze. In either case, the lesion is usually in the midbrain. Limitation of conjugate upgaze occurs with damage to the pretectum, an isthmus between the superior colliculi and the thalamus. Supranuclear fibers decussate through the pretectum as they pass to the riMLF, the midbrain structure that functions as the saccadic generator for vertical eye movements (and thus is the homologue for the paramedian pontine reticular formation for horizontal saccades). The dorsal midbrain syndrome (also known as the pretectal or

Parinaud syndrome; Fig 7-5) includes

conjugate limitation of vertical gaze (usually upgaze)

co-contraction of extraocular muscles with attempted upgaze (convergence-retraction nystagmus)

mid-dilated pupils with light–near dissociation retraction of the lids in primary position (Collier sign) skew deviation

disruption of convergence (convergence spasm or convergence palsy) increased square-wave jerks

Figure 7-5 A, A patient with a germinoma pressing on the pretectum shows a poor pupillary light reaction. B, The near reaction of the pupils is good. C, Attempted upgaze is poorly done. D, Magnetic resonance imaging (T1 with contrast) showing pineal (white arrow) and chiasmal (yellow arrow) germinoma with involvement of the dorsal midbrain, located

beneath the pineal lesion. (Parts A–C used with permission from Alb ert DM, Jakob iec FA, eds. Principles and Practice of Ophthalmology. Vol 2. Philadelphia: Saunders; 1994:2476. Part D courtesy of Prem S. Sub ramanian, MD, PhD.)

Dorsal midbrain syndrome often includes only a subset of these signs, although the limitation of conjugate upgaze is the most common feature. Common etiologies of this syndrome include mass lesions (especially pineal-based tumors), hydrocephalus, multiple sclerosis, and stroke.

The pretectum is the terminal structure supplied by the arteries of Percheron (small penetrating arteries that arise from the area around the top of the basilar artery; see Chapter 1). Stenosis at the origin of these vessels, disease of the more proximal basilar artery, and entrapment of emboli can each compromise flow through these vessels. Emboli that lodge at the top of the basilar artery can produce efferent and afferent neuro-ophthalmic problems.

Deviation of the eyes may occur with seizures involving any cerebral lobe. Most notably, a lesion of the FEF that causes excess neural activity, like a focal seizure, will drive the eyes contralaterally during the period of the seizure. The head also may turn contralateral to the seizure focus during the ictus. In the post-ictal state, when there may be lingering hypoactivity of the FEF neurons, the eyes