Horizontal Nystagmus

As discussed in Chap. 9, children with infantile esotropia, in rare cases, have horizontal nystagmus associated with head shaking, or head nodding that resolves following surgical realignment.86 Because many patients with spasmus nutans manifest esotropia, dissociated vertical deviation, and latent nystagmus,230 it is not known whether this condition represents a variant of spasmus nutans.

Latent Nystagmus

Latent nystagmus refers to a bilateral conjugate horizontal jerk nystagmus that occurs when either eye is occluded.85 It accompanies infantile strabismus and is most commonly seen in children with a history of infantile esotropia. In most conditions in which the ocular oscillation of latent nystagmus occurs under binocular viewing conditions, complete absence of nystagmus occurs only when patients bifixate. In most patients with this condition, the intensity of the nystagmus increases as monocular occlusion increases. The oscillation can appear clinically “silent” under binocular viewing conditions, but is always present when measured with eye movement recordings.145 In latent nystagmus, the nasally directed slow phase in the fixating eye is followed by a temporally directed corrective ­saccade.85 The amplitude of latent nystagmus increases when the fixating eye is moved into abduction and decreases in adduction. Latent nystagmus obeys Alexander’s law (which states that, in patients with peripheral vestibular nystagmus, the amplitude of the jerk nystagmus increases in the direction of the fast phase and decreases but never reverses in the direction of the slow phase), whereas infantile nystagmus may appear to obey this law if the patient has a “latent” component and is examined under monocular conditions. The fact that manifest latent nystagmus obeys Alexander’s law reflects the fact that it is tied into the same circuitry as peripheral vestibular nystagmus.

The finding of latent nystagmus correlates with the finding of nasotemporal asymmetry when either eye follows horizontal optokinetic targets.85 Nasotemporal asymmetry refers to the clinical finding of normal nasally directed optokinetic responses and impaired temporally directed optokinetic responses under conditions of monocular viewing. Monocular nasotemporal optokinetic asymmetry is normal in infants until approximately 22 weeks of age.413 Absence of cortical binocularity leads to the retention of this primitive optokinetic bias.85 Although nasotemporal asymmetry is usually observed in the setting of infantile esotropia, it may occur with other forms of early infantile strabismus as well. In patients with a history of

­strabismus, the finding of nasotemporal asymmetry confirms that the eyes were misaligned within the first year of life.85

Tychsen and colleagues540,541 proposed that latent nystagmus and its underlying nasotemporal asymmetry reflect the effect of the immature visual motion processing system on the smooth pursuit movements. The extrastriate motion processing system is localized to the dorsal parieto-occipital pathways, which extend from the primary visual area to the extrastriate middle temporal (MT) visual area. It receives its major inputs from the magnocellular neurons in the geniculate body. This mechanism has not received experimental support.340,493 Single unit recordings from middle temporal neurons of monkeys with early-onset artificial strabismus have suggested that the pursuit defect is not due to altered cortical vision motion processing, but that the asymmetry in pursuit may be a consequence of an imbalance in binocular visual input to downstream areas responsible for horizontal optokinetic nystagmus.335

Brodsky and Tusa85 have proposed that latent nystagmus is a unique form of vestibular nystagmus that is evoked by unbalanced visual input from the two eyes rather than unequal rotational input from the two labyrinths. According to their hypothesis, the two eyes function as accessory vestibules, allowing unbalanced visual input to modulate optokinetic responses in the horizontal plane. As discussed in Chap. 7, latent nystagmus and dissociated vertical divergence are primitive visuo-vestibular eye movements that are expressed in the setting of infantile strabismus. The neurophysiologic substrate for latent nystagmus is operative in lateral-eyed, afoveate animals, which have a monocular nasotemporal asymmetry to horizontal optic flow. The same subcortical optokinetic bias is present in early human infancy and persists when strabismus precludes maturation of normal binocular cortico-pretectal pathways from MT/MST. Because this optokinetic bias influences horizontal pursuit velocity, latent nystagmus is easily misinterpreted as a cortical pursuit imbalance.

When this primitive monocular nasal optokinetic bias is operative, visual input from the fixating eye to the contralateral nucleus of the optic tract evokes a visuo-vestibular counterrotation of the eyes that corresponds to a turning or twisting movement of the body toward the object of regard (Fig. 8.13). In this setting, unbalanced binocular visual input can induce a motion bias in the vestibular nucleus to generate the visual counterpart of horizontal labyrinthine nystagmus, namely latent nystagmus. As the eyes rotate frontally during evolution, this visuo-vestibular function is sacrificed, but the CNS retains these latent subcortical visual pathways. Thus, strabismus disrupts binocular cortical connections to provide the permissive cause while primitive subcortical visuovestibular reflexes that are operative in lateral-eyed animals provide the proximate cause of latent nystagmus.

Fig. 8.13  Neuroanatomical pathways modulating latent nystagmus. Cortical input to temporally directed movement, which is present only in frontal-eyed animals, requires the establishment of normal binocular cortical connections. This input is absent in humans with infantile strabismus. Direct crossed pathways from the eye to the nucleus of the optic tract provide nasalward subcortical optokinetic responses even when binocular cortical connections are absent (R and L represent monocular cortical cells corresponding to the right and left eyes, respectively). Note that the nucleus of the optic tract (NOT) relays horizontal visuo-vestibular information to the vestibular nucleus (VN), where it is integrated with horizontal vestibular input from the labyrinths to establish horizontal extraocular muscle tonus. LGN indicates lateral geniculate nucleus; CC, corpous callosum; V1, abducens nucleus; III, oculomotor nucleus; LR, lateral rectus muscle; MR, medial rectus muscle; AC, anterior canal; PC, posterior canal; and HC, horizontal canal).

Used, with permission, from Brodsky MC, et al85

Vestibular eye movements (which involve gaze holding) and pursuit eye movements (which involve gaze shifting) are normally thought of as diametrical functions that require different control centers. However, visuo-vestibular eye movements provide the afoveate pursuit system. While pursuit is conducted by moving the eyes with the target, “pursuit” in afoveate animals is accomplished by holding the eyes still in space during head or body movements. The phylogenetic continuum between “pursuit” eye movements and “visuovestibular” eye movements may explain why higher cortical centers such as MS/MST connect to lower centers such as NOT to orchestrate latent nystagmus.

Eye movement recordings show that most patients who appear to have latent nystagmus have subclinical nystagmus under binocular conditions.4 Manifest latent nystagmus can be viewed as a latent nystagmus that is made manifest by amblyopia or strabismus. In manifest latent nystagmus, the brain suppresses one eye, which causes it to be physiologically “occluded.” Under such circumstances, both eyes develop a small-amplitude conjugate horizontal jerk nystagmus that

Table 8.7  Manifest latent nystagmus

Small-amplitude, horizontal jerk nystagmus

Fast phase to the right when left eye occluded; fast phase to the left when right eye occluded

Increases in abduction, dampens in adduction of the fixating eye Head turn to fixate in adduction with the preferred eye

May improve or resolve with treatment of amblyopia or strabismus

increases when the fixating eye moves toward abduction and decreases when the fixating eye is in adduction. From a neurological perspective, the association between manifest latent nystagmus and congenital esotropia and a head turn has also been given the eponym of Ciancia syndrome.

Hertle has pointed out that a nystagmus that reverses direction with alternate occlusion must be either latent nystagmus or infantile nystagmus with a latent component. This finding therefore signifies benignity.278 Affected children assume a head turn to place the fixating eye in adduction and thereby damp the nystagmus (Table 8.7). A child with conjugate horizontal nystagmus who fixates monocularly in abduction cannot have latent nystagmus and must therefore have infantile nystagmus.

Latent nystagmus offers parents a unique opportunity to self-monitor their child for the development of amblyopia. Several clinical features of latent nystagmus predict the progression of amblyopia. First, a new-onset manifest latent nystagmus indicates the development of amblyopia, and parents can be trained to occlude or penalize the appropriate eye (right eye for a right-beating nystagmus and left eye for leftbeating nystagmus) when it occurs. Second, the appearance of an increasing head turn indicates amblyopia of the eye that is not fixating in adduction. Third, the intensity of latent nystagmus is greater during fixation with the poorer-seeing eye, so parents can cover each eye and institute therapy when increasing asymmetry in the intensity is observed.

In contradistinction to infantile nystagmus, eye-movement recordings in manifest latent nystagmus show a rapid slip off the fovea following refixation saccades (referred to as a decreasing-velocity or decreasing-exponential waveform) (Fig. 8.14). The primary defect in latent nystagmus is a linear slow-phase drift that displaces the image of regard from the fovea to the nasal retina, followed by a refoveating fast phase.166 However, Dell’Osso161,166 has demonstrated that some patients with manifest latent nystagmus develop a strategy of making a saccade beyond the target, thereby allowing the decreasingvelocity tail of the waveform to provide foveation. Patients who have latent nystagmus with slow-phase velocities greater than 4 degrees/s develop a secondary adaptation that permits foveation at the end of the slow-phase deceleration. This saccadic overshoot is not part of the primary defect but an adaptation to improve vision in the setting of manifest latent nystagmus. This adaptive strategy serves to transfer the slow component of the drift onto the fovea, which probably accounts for the good visual acuity in these children.

Fig. 8.14  Comparison of eye movement recordings (position tracings) in manifest latent nystagmus and infantile nystagmus. Upward deflection corresponds to rightward eye movement. In manifest latent nystagmus (top) each leftward fast phase is followed by decreasing-velocity drift off target with no intervening foveation period. In infantile nystagmus (bottom), each rightward fast phase is followed by foveation period before eyes drift off target in increasing-velocity slow phase. Adapted, with permission, from von Noorden et al556

Manifest latent nystagmus may be mistaken for acquired nystagmus because it may not become clinically apparent for several years. Affected children may be subjected to an extensive neurological workup if the associated ocular findings are not recognized. The characteristic clinical finding is that manifest latent nystagmus changes direction when the eyes are alternately occluded (i.e., it is right-beating when the left eye is occluded and left-beating when the right eye is occluded). Although this clinical finding is highly suggestive of manifest latent nystagmus, it can also reflect infantile nystagmus with a latent component.

In the child with congenital esotropia, latent nystagmus, and alternating fixation, the manifest latent nystagmus may superficially resemble periodic alternating nystagmus.257 Some patients with latent nystagmus can induce a manifest latent nystagmus by simply imagining that one eye is occluded. Bright illumination in one eye often has a similar effect to occlusion and causes a latent nystagmus to manifest.504 Patients, in rare cases, have been reported to release and suppress latent nystagmus at will.343

In addition to occurring in patients with congenital esotropia and amblyopia, manifest latent nystagmus is a common manifestation in infants with congenital unilateral visual loss resulting from microphthalmos, congenital cataract, or optic disc anomalies.104,370 These infants develop a face turn toward the good eye (i.e., an infant with left microphthalmos takes a right face turn to damp the nystagmus in the right eye by keeping it positioned in adduction). Parents may misinterpret this phenomenon and believe that the child is turning his face to view objects with his bad eye. Infants with congenital unilateral visual loss also tend to develop a sensory esotropia. Latent nystagmus is common in patients with periventricular leukomalacia, so a history of

prematurity­ and walking difficulty should be sought. It is unclear whether the latent nystagmus in periventricular­ leukomalacia results from horizontal strabismus, from an afferent disturbance at the level of the optic radiations, or from selective involvement of efferent corticotectal pathways that subserve monocular temporal optokinetic responses by the bilateral subcortical periventricular white matter lesions. Older patients who develop manifest latent nystagmus occasionally note oscillopsia.370

Treatment of Manifest Latent Nystagmus

Manifest latent nystagmus should be viewed as a treatable form of nystagmus. Zubcov et al606 have shown that successful occlusion therapy or surgical realignment of the eyes diminishes the intensity of manifest latent nystagmus. It is a common misconception that occlusion therapy is futile or even contraindicated in patients with amblyopia and latent nystagmus.556 Some authors have advocated optical or atropine penalization for amblyopia treatment in patients with latent nystagmus. It is now well established, however, that occlusion therapy is effective in patients with latent nystagmus.556 Simonsz and Kommerell504 have demonstrated that the slow-phase speed of latent nystagmus in the amblyopic eye diminishes over 2 or 3 days during prolonged occlusion of the better eye and that the slow-phase speed in the better eye increases by a commensurate amount. They caution that early visual improvement during occlusion therapy probably reflects an occlusion-induced short-term change in the nystagmus waveform rather than true sensory visual improvement. Because manifest latent nystagmus often occurs in the setting of congenital esotropia with superimposed amblyopia, it is not surprising that treatment of the underlying conditions can convert a manifest-latent nystagmus to a latent nystagmus (i.e., eliminate the manifest component).606

Children who have manifest-latent nystagmus associated with unilateral congenital visual loss (unilateral microphthalmos, congenital cataract, or optic disc anomalies) may require a large recession of the medial rectus muscle of the adducted eye to transfer the null zone into primary position and eliminate the sensory esotropia.

Parents are understandably reluctant to permit surgery on the seeing eye, despite the fact that the torticollis may be more cosmetically and functionally disabling than the strabismus. In this particular situation, Jampolsky306 has cautioned that it is often necessary to perform additional recessions of the medial and lateral rectus muscles of the normal contralateral eye to eliminate horizontal incomitance. Adults with congenital blindness in one eye and large