Horizontal-gaze abnormalities are more common than vertical ones. Because the horizontal-gaze system depends on unilateral gaze centers and pathways, it is more vulnerable than the vertical-gaze system, which has bilateral input. Horizontal-gaze paresis can vary from (a) gaze-evoked nystagmus to (b) slowing or dysmetria of the movement to (c) a total inability to move the eyes in the involved direction of gaze. Severe gaze paralysis results in conjugate deviation of the eyes in the opposite direction at rest.
The most common abnormalities in this group are gaze palsies resulting from a cerebrovascular accident (CVA). Localization of the lesion depends on concurrent neurologic findings such as hemiparesis, visual field loss, and cranial nerve palsies. The following discussion covers saccade abnormalities first and then pursuit abnormalities.
An isolated horizontal-gaze paresis is rare. The lesion can be located anywhere in the horizontal-gaze pathways and cannot be localized more specifically without other neurologic signs and symptoms.
Horizontal-Gaze Paresis with Hemiparesis
The FEF lies immediately anterior to the motor strip in each hemisphere, both areas receiving branches of the middle cerebral artery. These regions initiate commands for movement contralaterally: horizontal saccades in the FEF and voluntary movement of the face, body, and limbs in the motor strip. When a CVA involving the middle cerebral artery occurs, the patient can present with a contralateral hemiparesis and gaze palsy. In extensive strokes, the patient has conjugate deviation of the eyes "toward the lesion." Theoretically, the combination of hemiparesis and gaze palsy toward the same side as the hemiparesis can occur in a lesion of the corticobulbar and corticospinal tracts down to the level of the trochlear nucleus. In clinical settings, however, the lesion is almost always in the cortical distribution of the middle cerebral artery.
As the patient recovers, the eyes come back to the, midline, and the speed and accuracy of the horizontal saccades gradually improve. Improvement may not occur if a previous stroke has affected the opposite FEF, which assumes the function of the damaged gaze center through the ipsilateral system.
If the patient presents with a saccadic horizontal-gaze palsy to one side and a hemiparesis on the opposite side, then the lesion must be in the pons. The PPRF or the abducens nucleus could be the site of the lesion, since all fibers from the PPRF go to the abducens nucleus, as discussed above. Oculocephalic maneuvers or calories, which bypasses the PPRF, can differentiate between the two sites. If the abducens nucleus is af-fected, the infranuclear input will not generate a response. Dysfunction of the pontine gaze system does not recover well, often leaving the patient with a persistent deficit.
INO occurs when a lesion is present in the medial longitudinal fasciculus, which connects the abducens nucleus with the medial rectus subnucleus of the oculomotor complex. Therefore, when the PPRF burst cells fire, the lateral rectus responds, but the opposite medial rectus responds poorly. The lesion is ipsilateral to the eye with the adduction weakness. The patient exhibits decreased adduction and abduction nystagmus. The affected eye can be either orthotropic in primary position or abducted. The severity of the adduction abnormality varies from total inability to adduct the eye during a saccade to a mild abnormality consisting of an adduction lag. In the latter case, the clinician will see the abducting eye arrive at the final gaze position earlier than the adducting eye. Characteristically, the abducting eye displays jerk nystagmus in the direction of gaze with an INO. The cause of the nystagmus is debated. The well-known maxim is that a young patient with INO has multiple sclerosis and an elderly patient has a CVA. For the most part, this generalization is useful. However, other causes such as tumor, infection, trauma, and drug intoxications have to be considered. INO is specific for the anatomic site of the lesion but not for the cause. A young patient with bilateral INO most often does have demyelinating disease (Fig. 15.7).
Figure 15.7 Postmortem section from a patient with multiple sclerosis and diplopia. The arrows point to a demyelinated plaque in the pontine tegmentum involving the medial longitudinal fasciculus bilaterally. The patient most likely had bilateral internuclear ophthalmoplegia. (From Schochet SS Jr, Nelson J. Atlas of Clinical Neuropathology. Norwalk, CT: Appleton & Lange 1989. Used with permission of the publisher.)
Cogan separated INO into two separate groups on the basis of involvement or sparing of adduction with the near reflex. The near-reflex pathways do not go below the oculomotor complex; therefore, if convergence is normal, then the lesion is below the oculomotor nuclei, and if not, the lesion is in the medial longitudinal fasciculus at the level of the nuclei. Cogan named these posterior INO and anterior INO, respectively.
Lutz also proposed a posterior INO and anterior INO, but his criteria differ from those of Cogan. The anterior INO of Lutz has the same criteria as the posterior INO of Cogan. The posterior INO of Lutz is a disconnection of the fibers from the PPRF to the abducens nucleus that causes an abduction abnormality and spares adduction. The posterior INO of Lutz is extremely rare and depends on proof of preserved function of the sixth nerve during pursuit or vestibular eye movements.
A lesion involving the PPRF, the abducenti nucleus, or both and the ipsilateral medial longitudinal fasciculus causes the one-and-one-half syndrome (Fig. 15.8). The patient has a horizontal-gaze palsy ipsilateral to the lesion and an INO in the ipsilateral eye. Motility testing shows paralysis of all horizontal eye movements except abduction or the contralateral eye. The lesion is on the side of the immobile eye. The genu of the facial nerve may be affected as it arches over the abducens nucleus, causing a peripheral seventh-nerve palsy. This syndrome is specific for a midline pontine lesion. The causes are similar to those in INO.
Figure 15.8. Location within the pons of the lesions responsible for the one-and-one-half syndrome (dotted area) and internuclear ophthalmoplegia (diagonal lines). VI, abducem nucleus; MLF, medial longitudinal fasciculus; PPRF parapontine reticular formation.
Conjugate Horizontal Gazes and Seizures
During a seizure, the eyes may deviate to one side. In contrast to a destructive lesion, stimulation, or "irritation," of the FEF in seizure patients causes contralateral deviation of the eyes. Therefore, a patient with an irritative focus in the left frontal region may have deviation of the eyes to the right as part of the seizure. This generalization usually is true, but studies of seizure patients have revealed that in some cases, the deviation is ipsilateral to the focus.
Congenital Ocular Motor Apraxia
Cogan initially described a unique gaze disturbance in infants and children that he named ocular motor apraxia (OMA). An affected child has difficulty performing horizontal saccades to commands. To move the eyes, the child uses a head thrust in the direction of desired gaze, resulting in passive movement of the eyes in the opposite direction. Once the eyes reach the desired position or target, they maintain fixation. The head, which overshoots the target position, is then slowly brought back so the eyes are in primary gaze position. Spontaneous and reflex saccades are more easily performed than command saccades. With maturation, the patient's eye movements usually improve with less need for head thrusts to generate saccades. Eye-movement recordings have shown abnormalities in saccadic latency and amplitude but not velocity, suggesting that the PPRF burst neurons are intact. Pursuit eye-movement recordings may show hypometric abnormalities.
The exact anatomic site of abnormality in congenital OMA is unknown. Recent reports of patients with OMA, however, document diffuse neurologic involvement resulting in slow motor and speech development. In addition, agenesis of the corpus callosum and hypoplasia of the cerebellum have been seen on scans. A brainstem tumor has been reported in one patient with the clinical findings of OMA. Patients with OMA should be followed and scanned if the condition worsens. The clinical findings of OMA also have been seen in Pelizaeus-Merzbacher disease and spinocerebellar degeneration.
Unilateral Pursuit Paresis
A patient with a lesion of the parieto-occipital junction may have decreased ability to pursue a target in the ipsilateral direction and, instead of normal pursuit movements, will use small saccades to follow a target (saccadic pursuit or cogwheel pursuit). A contralateral homonymous field loss is often present in these patients because of the proximity of the optic radiations to the pursuit gaze center. Optokinetic nystagmus (OKN) is absent or decreased ipsilateral to the lesion. Before the development of scanners, patients with homonymous field loss underwent OKN testing to differentiate tumors from posterior cerebral artery infarcts. The pursuit gaze area receives blood from the middle cerebral artery, whereas the occipital cortex is supplied by the posterior cerebral artery. Therefore, normal pursuit function on OKN testing favors a posterior cerebral infarct, and dysfunction favors a tumor that extends beyond arterial supply zones.
Unilateral pursuit paresis also can be seen in patients with unilateral cerebellar lesions. These patients will usually have other signs and symptoms of ataxia.
Bilateral Pursuit Paresis
A patient with bilateral pursuit paresis is unable to pursue a target smoothly. Saccadic pursuit, also called cogwheel pursuit, is the clinical finding. This abnormality is not anatomically specific and can be seen with diffuse disease of the hemispheres, cerebellum, or stem. Impaired attention or sedative chugs also can cause bilateral pursuit paresis.