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Clinical Sciences |

Primary Oblique Muscle Overaction:  The Brain Throws a Wild Pitch FREE

Michael C. Brodsky, MD; Sean P. Donahue, MD, PhD
[+] Author Affiliations

From the Departments of Ophthalmology and Pediatrics, University of Arkansas for Medical Sciences, Little Rock (Dr Brodsky); and the Departments of Ophthalmology and Visual Sciences, Pediatrics, and Neurology, Vanderbilt University School of Medicine, Nashville, Tenn (Dr Donahue).


Arch Ophthalmol. 2001;119(9):1307-1314. doi:10.1001/archopht.119.9.1307.
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Published online

Background  Sensorimotor and orbital anatomical mechanisms have been invoked to explain primary oblique muscle overaction.

Methods  Review of primitive visuo-vestibular reflexes and neuroanatomical pathways corresponding to vestibulo-ocular reflexes, and correlation with known clinical abnormalities in patients with primary oblique muscle overaction.

Results  Bilateral superior oblique muscle overaction, which corresponds to a backward pitch in lateral-eyed animals, can occur when structural lesions involving the brainstem or cerebellum increase central otolithic input to the extraocular muscle subnuclei that modulate downward extraocular muscle tonus. Bilateral inferior oblique overaction, which corresponds to a forward pitch in lateral-eyed animals, may result from visual disinhibition of central vestibular pathways to the extraocular muscle subnuclei that modulate upward extraocular muscle tonus.

Conclusions  Primary oblique muscle overaction recapitulates the torsional eye movements that occur in lateral-eyed animals during body movements or directional luminance shifts in the pitch plane. These primitive ocular motor reflexes become manifest in humans when early-onset strabismus or structural lesions within the posterior fossa alter central vestibular tone in the pitch plane.

Figures in this Article

PRIMARY oblique muscle overaction is a common ocular motility disorder characterized by vertical incomitance of the eyes in lateral gaze.1 In primary inferior oblique muscle overaction, an upshoot of the adducting eye occurs when gaze is directed into the field of action of the inferior oblique muscle, producing a greater upward excursion of the adducted eye than of the abducted eye.1 The opposite occurs in primary superior oblique muscle overaction. Although ductions appear to be normal and there is no evidence of yoke muscle paresis, alternate cover testing discloses a vertical tropia of similar magnitude in the abducting eye. Primary inferior oblique muscle overaction is usually associated with ocular extorsion and V-pattern strabismus, whereas primary superior oblique muscle overaction is usually associated with ocular intorsion and A-pattern strabismus.25 Superior oblique muscle overaction is often accompanied by other neurologic disease, whereas inferior oblique muscle overaction generally occurs in children who have congenital esotropia but no other overt neurologic abnormalities. Surgical weakening of the overacting oblique muscles improves versions, eliminates the associated A or V pattern, and reduces torsion.

In 1916, Ohm68 postulated that pattern strabismus and oblique muscle overaction may be due to abnormal vestibular innervation. Almost a century later, a unifying neurologic mechanism to explain primary oblique muscle overaction remains elusive. This ocular motor phenomenon seems to defy fundamental principles of physiology since nowhere else in the body do individual muscles bilaterally overact.

The primary function of the oblique muscles in lower vertebrates such as fish is to counterrotate the eyes torsionally in response to pitch (fore-and-aft) movements of the body.9,10 As a fish pitches its body to swim upward or downward, a compensatory "wheel" rotation of the eyes is produced by the oblique muscles in response to vestibular stimulation.9 The existence of this physiologic oblique muscle overaction in lower animals led us to question whether a central vestibular imbalance in the pitch plane might offer an explanation for the occurrence of primary oblique muscle overaction in humans. Clinical observations suggest that an imbalance in central vestibular premotor output to the extraocular muscle subnuclei can produce the primary oblique muscle overaction that accompanies congenital strabismus. This central vestibular imbalance develops when early loss of binocular vision or neurologic disease alters central vestibular output in the pitch plane to produce excessive tonus of the extraocular muscles that elevate the eyes (in the case of congenital esotropia and inferior oblique muscle overaction) or depress the eyes (in the case of neurologic disease and superior oblique muscle overaction).

The term tonus was originally coined by Ewald11 to describe the state of excitation of a living muscle during rest. In 1977, Meyer and Bullock12 advanced their tonus hypothesis, which states that neuronal tonus pools within the central nervous system receive multisensory input and that tonus asymmetries between antagonistic pools can produce tonic motor responses. According to this hypothesis, the eyes are not merely sensory organs but components of a multimodally driven tonus pool that calibrates baseline muscle tone (ie, tonus-inducing organs).12,13 This hypothesis explains how sensory information collected by the eyes can help to govern extraocular muscle tonus. The bilateral positioning of the eyes and ears permits them to function as balance organs. Visual and graviceptive input are yoked together within the central vestibular system to determine optimal postural orientation.

In his early pioneering studies of vision-dependent tonus responses in fish, von Holst14 found that a posterior shift of a dorsal light source induces a pitch-up movement of the body, whereas an anterior shift induces a pitch-down movement, as if the animal is programmed to position the body so that the light source retains a dorsal orientation(Figure 1). With the body stabilized in the upright position, an overhead light moving fore-and-aft evokes a wheel-turning movement of both eyes, which rotate to maintain torsional alignment with the light source (Figure 1).1416 Since light normally comes from overhead when a fish is upright, a posterior movement of the light is registered as a pitch forward movement of the body (ie, a movement of the body away from the light). This change in visual input evokes increased tonus to the inferior oblique muscles, which extort the eyes (Figure 1). The observation that visual and vestibular input can alter postural and extraocular muscle tonus to produce a physiologic bilateral oblique muscle overaction in lower animals suggests that similar excitatory stimuli may be operative in strabismic humans with primary oblique muscle overaction.

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Figure 1.

Physiologic effects of gravistatic(postural) and visual input to the oblique muscle tonus in fish. These bilateral torsional eye movements function to align the eyes with the perceived visual vertical by modulating oblique muscle tonus. A, A pitch-down body movement evokes increased inferior oblique muscle tonus and extorsion of the eyes. B, A pitch-up movement evokes increased superior oblique muscle tonus and intorsion of the eyes. C, In the unrestrained fish, an anterior light source evokes a pitch-down body movement. D, In the unrestrained fish, a posterior light source evokes a pitch-up body movement. E, In the restrained fish, anterior movement of overhead light evokes increased superior oblique muscle tonus and intorsion of both eyes. F, In the restrained fish, posterior movement of overhead light evokes increased inferior oblique muscle tonus and extorsion of both eyes.

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To understand why primary oblique muscle overaction so often accompanies early-onset strabismus, it is instructive to examine the components of central vestibular tone that influence eye position. The primary function of the vestibuloocular system is to maintain eye position and stabilize fixation during head movements.16 Vestibulo-ocular movements are the most primitive of all extraocular movements. As expounded by Walls,

. . . the primitive function of the eye muscles was not to aim the eyes at all. Their original actions were all reflex and involuntary, and were designed to give the eyeball the attributes of a gyroscopically-stabilized ship, for the purpose of maintaining a constancy of the visual field despite chance buffetings and twistings of the animals body by water currents.9(p303)

In the rabbit, for example, a rightward body tilt along its long axis causes the right eye to be lower in space than the left eye. This tilt elicits a compensatory vertical divergence of the eyes to elevate the right eye and depress the left eye, thereby stabilizing the eyes in space.1719 A pitch forward of the body would produce a compensatory extorsional movement of both eyes.14,15,20

Now consider the same pitch-down body movement in a rabbit that is fixating with the right eye maximally abducted and the left eye maximally adducted(Figure 2). Since the eyes are laterally placed in the rabbit, this position of gaze would direct the left visual axis anterior to its neutral position and the right visual axis posterior to its neutral position. A forward pitch in the body plane with the eyes in this position would tilt the left visual axis to a lower position in space than the right visual axis (Figure 2). This tilt would necessitate compensatory vestibulo-ocular innervation to increase upward tonus in the left eye and increase downward tonus in the right eye, while extorting both eyes in response to the body pitch. Conversely, if the body were pitched back during dextroversion, the higher visual axis of the adducted left eye would necessitate increased downward tonus in the left eye and increased upward tonus in the right eye to stabilize the position of the eyes in space. The necessary vestibulo-ocular movements, which correspond to the vertical divergence in lateral gaze seen in humans with primary oblique muscle overaction, are programmed at an early evolutionary stage to assure stability of the visual field in all fields of gaze. In 1996, Zee18 formulated this hypothesis to explain how the alternating skew deviation in lateral gaze that occurs in humans could be a reversion to a phylogenically old otolith-mediated righting reflex in lateral-eyed animals. Zee's hypothesis also explains how superior oblique muscle overaction with alternating hypotropia of the adducting eye reflects a pitch-up otolithic bias and a downward tonus bias to the extraocular muscle plant, whereas inferior oblique muscle overaction with alternating hypertropia of the adducting eye would result from a pitch-down otolithic bias and an upward tonus bias to the extraocular muscle plant.

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Figure 2.

Overhead view of a rabbit fixating an object in the right posterior visual field. Solid lines correspond to the visual axis of the abducted right eye and the adducted left eye. When the rabbit pitches forward (as when starting to run down a hill), the head rotates downward and the tail rotates upward. Although both eyes move downward in space, the left visual axis (which is directed toward the nose) rotates downward, while the right visual axis (which is directed toward the tail) rotates upward(curved arrows). This divergence of the visual axes corresponds to a right hypertropia that must be neutralized by vestibular innervation to elevate the lower left eye and depress the higher right eye. The compensatory vertical divergence for a pitch-forward position corresponds to primary inferior oblique muscle overaction.

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In lateral-eyed animals and in humans, the semicircular canals are roughly aligned with the extraocular muscles (Figure 3).17 When the head is rotated in a particular plane, a semicircular canal within the labyrinth detects acceleration and sends excitatory innervation to the extraocular muscle(s). Within the brainstem and cerebellum, peripheral vestibular input is summated to produce appropriate innervation to the extraocular muscle subnuclei and maintain the position of the eyes in space (Figure 4).1822 Each anterior semicircular canal provides excitatory innervation to the ipsilateral superior rectus and the contralateral inferior oblique muscles while inhibiting the yoked ipsilateral inferior rectus and contralateral superior oblique muscles(Figure 4). Likewise, each posterior semicircular canal system provides excitatory innervation to the ipsilateral superior oblique and the contralateral inferior rectus muscles while inhibiting the ipsilateral inferior oblique and the contralateral superior rectus muscles. In humans, a pitch-up movement of the head (as occurs when raising the chin) activates both posterior semicircular canals, which send excitatory innervation to both depressors in both eyes. Like their target extraocular muscles, the semicircular canal pathways have a push-pull (yoke) relationship, so that activation of one canal inhibits the antagonist canal.19 Thus, the pitch-up movement that excites both posterior canals also inhibits both anterior semicircular canals, which send inhibitory innervation to the ocular elevators. The result is an equal contraversive movement of both eyes to adjust for the pitch-up head movement. Injury to or inhibition of anterior canal pathways subserving upward eye movements causes a functional activation of the posterior canal downgaze pathways and produces downward eye movements.22

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Figure 3.

The close anatomical relationship of the semicircular canals and the extraocular muscles in humans is shown. Figure modified with permission from Simpson and Graf.17

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Figure 4.

Neuroanatomical projections from the labyrinths to the extraocular muscles. The orientation of the anterior semicircular canal corresponds to that of the ipsilateral superior rectus and contralateral inferior oblique muscles. The orientation of the posterior semicircular canals corresponds to that of the ipsilateral superior oblique and contralateral inferior rectus muscles. The orientation of each horizontal canal corresponds to that of the horizontal rectus muscles. Turning the head to the right stimulates the right horizontal canal to increase excitatory innervation to the right medial rectus muscle and left lateral rectus muscle so that the eyes rotate equally and opposite to the direction of head rotation. HC indicates horizontal canal; AC, anterior canal; PC, posterior canal; LVN, lateral vestibular nucleus; MVN, medial vestibular nucleus; VI, abducens nucleus; MLF, medial longitudinal fasciculus; IV, trochlear nucleus; III, oculomotor nucleus; SR, superior rectus muscle; MR, medial rectus muscle; LR, lateral rectus muscle; and IO, inferior oblique muscle. Data modified with permission from Tusa.21

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In addition to the semicircular canals, each labyrinth contains otolithic sensors consisting of the utricle and the saccule.19 While the semicircular canals respond to angular acceleration and produce dynamic vestibuloocular movements, the parallel otolithic system responds to linear acceleration and is sensitive to changes in static head position.19 Damage to the semicircular canal pathways produces phasic ocular deviations and nystagmus, while damage to the otolithic projections corresponding to the semicircular canal pathways causes tonic ocular deviations(strabismus).19,2325 The otolithic pathways are not as well studied, but are believed to have similar projections to the corresponding canal pathways.19 For the sake of simplicity, we refer to the otolithic pathways corresponding to a particular canal pathway simply as the anterior canal or posterior canal system, recognizing the similarity in projections between the otoliths and semicircular canals. Likewise, we also use the term anterior (or posterior) canal predominance to mean "predominance of the otolithic pathways corresponding to those of the anterior (or posterior) semicircular canals."

The otolithic pathways corresponding to the anterior and posterior semicircular canals are under different inhibitory control (Figure 5).19,21,22,26,27 The anterior canals receive inhibitory connections from the cerebellar flocculi, while the posterior canals do not. Thus, a structural lesion or metabolic abnormality that inhibits output from the cerebellar flocculi can also disinhibit the anterior canals, resulting in an upward deviation of the eyes.21 Conversely, bilateral lesions of the ventral tegmental tract or brachium conjunctivum can injure central pathways from the anterior semicircular canals and produce a posterior canal predominance, resulting in tonic downgaze. Maturation of cerebellar floccular inhibition to anterior canal pathways may be dependent on normal visual experience early in life. Ocular stabilization is normally modulated by visual and vestibular input. When binocular visual input is preempted, this multisensory mechanism may fall under greater weight of labyrinthine control, allowing excitatory anterior canal output to predominate.28

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Figure 5.

Segregation of pathways controlling anterior and posterior canal tone. Only the anterior canal pathways receive inhibitory innervation by the cerebellar flocculus. A loss of modulation from the cerebellar flocculi could disinhibit the anterior canals and produce an upward tonus imbalance, leading to bilateral inferior oblique muscle overaction, bilateral extorsion, and V-pattern strabismus. FLO indicates flocculus; NOD, nodulus; AC, anterior canal; PC, posterior canal; HC, horizontal canal; SVN, superior vestibular nucleus; VTT, ventral tegmental tract; MVN, medial vestibular nucleus; MLF, medial longitudinal fasciculus; BC, brachium conjunctivum; III N, oculomotor nucleus (S, I, O, and M represent the oculomotor subnuclei); SR, superior rectus muscle; and IR, inferior rectus muscle. Data modified with permission from Tusa.21

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A bilateral lesion that injures both anterior canal pathways or disinhibits both posterior canal pathways will increase prenuclear innervation to the superior oblique and inferior rectus subnuclei, resulting in a posterior canal predominance and increased downward tonus to both eyes. This downward tonus must be overcome by fixational innervation (Figure 6). Since the inferior rectus muscles retain their vertical field of action in adduction while the superior oblique muscles have minimal vertical action in abduction, this downgaze predominance would produce a relative overdepression of the adducting eye in lateral gaze (Figure 7). Activation of both superior oblique muscles produces bilateral intorsion in the primary position and an A pattern due to the tertiary abducting action of the superior oblique muscles in downgaze. In addition, binocular intorsion rotates the inferior rectus insertions laterally and reduces the adducting action of the inferior rectus muscles in downgaze.

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Figure 6.

Superior oblique muscle overaction. A, Vestibular innervation. A central vestibular tonus imbalance corresponding to bilateral posterior canal predominance would produce tonic downgaze, divergence, and intorsion of the eyes if unopposed by fixational innervation. B, Vestibular plus fixational innervation. Fixational innervation, which conforms to the Hering law, recruits bilateral innervation to the superior rectus and inferior oblique muscles to negate the vertical component of the downward tonus bias. Fixational innervation allows a disconjugate intorsional bias to persist. PC indicates posterior canal; HC, horizontal canal; and AC, anterior canal.

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Figure 7.

Superior oblique muscle overaction. The observed eye movements in different fields of gaze are a summation of fixational innervation that conforms to Hering's law, and an underlying central vestibular imbalance that does not. All 4 depressors are receiving excessive vestibular innervation. Since the vertical action of the superior oblique muscles is maximal in adduction, the adducting eye exhibits a downshoot in adduction relative to the abducting eye. The tertiary abducting effects of the overacting superior oblique muscles are maximized by vestibular innervation in downgaze and minimized by fixational intervation in upgaze, producing an A pattern.

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The vestibuloocular pathways pass through the posterior fossa and are susceptible to injury when structural abnormalities involve the brainstem or the cerebellum. In children with hydrocephalus and myelomeningocele, the constellation of A-pattern strabismus, bilateral superior oblique muscle overaction, and bilateral intorsion is often associated with tonic downgaze early in life.2938 Children with myelomeningocele not only have hydrocephalus but also frequently have an associated Chiari II malformation.35,36 Since prenuclear input to the vestibular system from the vestibulocerebellum is primarily inhibitory, bilateral compression of or injury to those vestibulocerebellar pathways activating the anterior canals would disinhibit the posterior canals and increase extraocular muscle tonus in their target muscles.

Previous investigators3540 have speculated that bilateral superior oblique muscle overaction may be supranuclear or prenuclear in nature, citing the frequency with which it accompanies defective upgaze. Biglan37,38 attributed the overacting superior oblique muscles, A pattern, and chronic downward deviations of the eyes in children with myelomeningocele to defects in the vertical gaze pathways producing either a failure to inhibit the downgaze pathways or excessive stimulation of downward gaze. Acute comitant esotropia caused by neurologic disease such as hydrocephalus or Chiari malformation is often associated with bilateral superior oblique muscle overaction.39 Although orbital anatomical factors have also been implicated as a cause of superior oblique muscle overaction in hydrocephalus,1,29 the high frequency of structural abnormalities within the posterior fossa led Hamed35,36 and colleagues to propose that superior oblique muscle overaction and alternating skew deviation in lateral gaze may share a common neuroanatomical substrate. Recently, Hoyt41 has observed that premature infants with periventricular leukomalacia or intraventricular hemorrhage may initially manifest a tonic downgaze that evolves into an A-pattern esotropia and bilateral superior oblique muscle overaction.

Clinical observations and eye movement recordings have documented abnormal ocular responses to vestibular stimulation in children with strabismus.4245 Gait and postural control have also been studied in children with different kinds of strabismus, and a defect of postural stability has been demonstrated in esotropic but not exotropic children.46,47 The high prevalence of incoordination and balance disorders in children with"isolated" congenital esotropia also supports the notion that early loss of single binocular vision associated with congenital esotropia may affect central vestibular tone.47

Humans display an inherent upward tonus predominance of the eyes, which correlates with anatomical differences in the orientation of the anterior and posterior canals.28 This inherent up-down asymmetry in central pathways may explain why vertical vestibular optokinetic responses normally favor upward rather than downward slow phases.4851 It may also explain why a slight downbeat nystagmus may be seen in individuals attempting to fixate an imaginary target in darkness28,52 and why a hyperphoria of the adducting eye can often be elicited in individuals fixating in lateral upgaze with a Maddox rod covering one eye.53 The development of single binocular vision serves to increase downward tonus to the extraocular muscles and hold this inherent upward bias in check. Conversely, the disruption of single binocular vision associated with congenital esotropia reduces downward tonus to the extraocular muscles, perhaps by disrupting maturation of inhibitory pathways from the cerebellar flocculi to the anterior canals. The resulting anterior canal predominance would increase upward tonus in the extraocular muscles and predispose to bilateral inferior oblique muscle overaction(Figure 8).

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Figure 8.

Primary inferior oblique muscle overaction. A, Visuovestibular innervation. Failure to develop normal binocular vision is associated with increased upward tonus to the eyes, perhaps through reduced anterior canal inhibition from the cerebellar flocculi. A central vestibular tonus imbalance corresponding to bilateral anterior canal predominance would produce tonic upgaze, horizontal divergence, and extorsion of the eyes if unopposed by fixational innervation. B, Visuovestibular plus fixational innervation. Fixational innervation recruits equal innervation from the inferior rectus and superior oblique muscles to negate the vertical component of the upgaze bias, and allows the disconjugate extorsional bias to persist. PC indicates posterior canal; HC, horizontal canal; and AC, anterior canal.

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Prolonged occlusion of one eye can also induce inferior oblique muscle overaction in nonstrabismic humans with normal stereopsis,54,55 suggesting that either prolonged interruption or early loss of single binocular vision may also be registered as forward pitch (ie, away from the light). The retention of this primitive vision-dependent tonus mechanism in humans would explain why poor sensory fusion leads to inferior oblique muscle overaction rather than superior oblique muscle overaction. The "neurologic lesion" that induces this central vestibular imbalance is loss of binocular visual input.

Primary oblique muscle overaction appears to defy Hering's law,56 which dictates that, in any volitional conjugate movement, both eyes receive equal innervation. As summarized by Bielschowsky,"all of the muscles of both eyes always participate in each movement; one half experiences an increase in tonus and the other half a decrease."57(p178) This control system optimizes binocular vision in all positions of gaze.5658 Although Hering's law requires that the ocular motor system synthesize a conjugate signal to the motor neurons involved in the execution of any ocular movement, it should be evident from the previous discussion that equal innervation to any set of vertical yoke muscles would produce dissociated movements of the 2 eyes. To execute conjugate vertical eye movements, the extraocular muscles of both eyes must receive appropriate innervation to move the eyes equally rather than receiving equal innervation.

Hering56 made reference only to voluntary eye movements as conforming to his law of equal innervation. Since the semicircular canals and their corresponding otolithic pathways segregate innervation to each set of yoke muscles, it is not surprising that dissociated eye movements of central origin are generally associated with vestibular disease. Paradoxically, these dissociated movements may reflect the fact that the vertical yoked muscles receive roughly equal innervation rather than the necessary innervation to rotate the eyes equally in one plane.

Our model of primary oblique muscle overaction as a pitch plane imbalance predicts that oblique muscles overact bilaterally in conjunction with rather than relative to their yoke vertical rectus muscles. In primary gaze, the torsional action of the overacting oblique muscles predominates in both eyes, producing the bilateral extorsion observed in primary inferior oblique muscle overaction and the bilateral intorsion observed in primary superior oblique muscle overaction. When both sets of elevators or depressors receive excessive central vestibular innervation, adduction of either eye produces excessive vertical excursion of the adducting eye as it moves into the vertical field of action of the overacting oblique muscle (Figure 7). In this context, an upward tonus imbalance to both eyes manifests as bilateral overelevation of the adducting eye, and a downward tonus imbalance manifests as bilateral overdepression of the adducting eye. Volitional gaze out of the vertical field of action of the overacting yoke muscles recruits physiologic innervation to counterbalance the vertical tonus imbalance, while gaze into the vertical field of action of the overacting yoke muscles allows this underlying tonus imbalance to predominate, producing the A and V patterns observed clinically (Figure 7). The ocular torsion produced by primary oblique muscle overaction also initiates a cascade of secondary mechanical events, including rotational displacement of the rectus muscle insertions, oblique muscle length adaptation, and mechanical tightening of the oblique muscles, as detailed elegantly by Guyton and Weingarten.5 These peripheral responses augment the overelevation or overdepression of the adducting eye and the corresponding A and V pattern observed clinically.

This neurologic model would also explain why primary oblique muscle overaction is usually associated with a negative Bielschowsky head-tilt test.1,59 A head tilt to either side recruits ipsilateral otolithic innervation to stimulate 1 of the 2 overacting vertical muscles in each eye while inhibiting the other. The net result for each eye is a minimal change in vertical tonus in the primary position. However, this model would predict that pitching the head forward and backward (ie, a vertical head-tilt test) would superimpose a physiologic tonus imbalance on the underlying central vestibular tonus imbalance in the pitch plane and thereby alter the amplitudes of an existing A or V pattern and the amplitudes of the associated hyperdeviations in lateral gaze. Accordingly, the clinical practice of pitching the patient's head forward and backward to obtain strabismus field measurements in upgaze and downgaze would augment an existing A or V pattern.

Dissociated vertical divergence may coexist with primary oblique muscle overaction.60 Dissociated vertical divergence has been attributed to a central vestibular tonus imbalance in the roll plane induced by fluctuations of binocular visual input.60,61 This hypothesis is based on physiologic studies60,61 in fish that show that unequal visual input to the 2 eyes induces a reflex body tilt in the roll (frontal) plane toward the side with greater visual input. This dorsal light reflex is a balancing movement that uses light from the sky as a visual reference to maintain vertical orientation by equalizing luminance input to the 2 laterally placed eyes. In a vertically restrained fish, unequal visual input induces a vertical divergence of the eyes, with depression of the eye that has greater visual input and elevation of the eye that has lesser visual input. This vertical divergence of the eyes corresponds to the dissociated vertical divergence seen in humans who fail to develop single binocular vision secondary to early-onset strabismus.

In humans with dissociated vertical divergence, suppression or mechanical occlusion of one eye increases upward tonus to the extraocular muscles of that eye and downward tonus to the extraocular muscles of the opposite eye.60,61 Simultaneous recruitment of central vestibular innervation to both elevators in the visually deprived eye has been invoked to explain the spontaneous overelevation in adduction that can be observed with dissociated vertical divergence, when no V pattern or baseline extorsion is present.60 The observation that decreased visual input increases upward tonus to one eye (in the case of dissociated vertical divergence) and to both eyes (in the case of inferior oblique muscle overaction) attests to the retention of primitive vision-induced tonus mechanisms62,63 in humans, and to the atavistic resurgence of these primitive subcortical reflexes when strabismus precludes the development of binocular vision. Our neurologic model of primary oblique muscle overaction as a central vestibular tonus imbalance in the pitch plane complements the recently proposed theory of dissociated vertical divergence as a central vestibular tonus imbalance in the roll (frontal) plane, and begs the question of whether latent nystagmus might be similarly driven by a central vestibular tonus imbalance in the yaw (axial) plane.

Most of the mechanisms invoked to explain the existence of A and V patterns with oblique muscle overaction have described orbital anatomical abnormalities that could account for the abnormal movements on a biomechanical basis.6475 It is beyond the scope of this article to review and critique all of them. In some patients, neurologic and anatomical causes of oblique muscle overaction may coexist. Children with hydrocephalus and tonic downgaze, for example, may also have frontal bossing with anterior displacement of the trochlea, which can increase tension on the superior oblique muscles and produce a mechanical superior oblique muscle overaction.1,29 Recently, Clark76 and Demer77 and their colleagues have used magnetic resonance imaging to demonstrate that heterotopia of extraocular muscle pulleys within the orbits can also produce overelevation or overdepression of the adducting eye and simulate oblique muscle overaction. Orbital pulley malposition may account for some children who have superior oblique muscle overaction and A-pattern strabismus in the absence of neurologic disease. Since orbital anatomical abnormalities can produce excessive vertical excursion of one or both eyes in the field of action of the oblique muscles, many authorities advocate use of the descriptive terms overelevation and overdepression of the adducting eye rather than the diagnostic term overaction of the oblique muscles to characterize these movements.1,76

Lower lateral-eyed animals use light from the sky above and gravity from the earth below as major sources of sensory input to neuronal tonus pools within the central vestibular system. These neuronal tonus pools calibrate extraocular muscle and postural tonus to maintain vertical orientation. In lower animals, oblique muscle tonus is determined by luminance and gravitational input in the pitch plane. In humans, the brain leverages visual and gravistatic sensory input to calibrate extraocular muscle tonus in the pitch plane. Early loss of single binocular vision is treated by the central vestibular system as forward pitch, necessitating increased upward tonus to the extraocular muscles and manifesting as primary oblique muscle overaction. Neurologic lesions within the posterior fossa can produce the opposite central vestibular imbalance, in which a backward pitch evokes increased downward tonus to the extraocular muscles and produces primary superior oblique muscle overaction. This duality reflects an ancestral bimodal tuning of central vestibular output to the extraocular muscles that is subordinate to binocular vision in humans.

Accepted for publication January 12, 2001.

This study was supported in part by a grant from Research to Prevent Blindness Inc, New York, NY. Dr Donahue is a recipient of a career development award from Research to Prevent Blindness Inc.

Corresponding author and reprints: Michael C. Brodsky, MD, Department of Ophthalmology, Arkansas Children's Hospital, 800 Marshall, Little Rock, AR 72202.

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Graf  WMeyer  DL Eye position in fishes suggest different modes of interaction between commands and reflexes. J Comp Physiol. 1978;128241- 250
Link to Article
Tusa  RJ Nystagmus: diagnostic and therapeutic strategies. Semin Ophthalmol. 1999;1465- 73
Link to Article
Brandt  TDieterich  M Central vestibular syndromes in roll, pitch, and yaw planes. Neuro-ophthalmology. 1995;15291- 303
Link to Article
Brandt  TDieterich  M Vestibular syndromes in the roll plane: topographic diagnosis from brainstem to cortex. Ann Neurol. 1994;36337- 347
Link to Article
Dieterich  MBrandt  T Wallenberg's syndrome: lateropulsion, cyclorotation, and subjective visual vertical in thirty-six patients. Ann Neurol. 1992;31399- 408
Link to Article
Glasauer  SDieterich  MBrandt  T Simulation of pathological ocular counter-roll and skew torsion by a 3-D mathematical model. Neuroreport. 1999;101843- 1848
Link to Article
Baloh  RWSpooner  JW Downbeat nystagmus: a type of central cerebellar nystagmus. Neurology. 1981;31304- 310
Link to Article
Straumann  DZee  DSSolomon  D Three-dimensional kinematics of ocular drift in humans with cerebellar atrophy. J Neurophysiol. 2000;831125- 1140
Böhmer  AStraumann  D Pathomechanism of mammalian downbeat nystagmus due to cerebellar lesion: a simple hypothesis. Neurosci Lett. 1998;250127- 130
Link to Article
France  TD Strabismus in hydrocephalus. Am Orthopt J. 1975;25101- 105
France  TD The association of "A" pattern strabismus with hydrocephalus. Moore  SMein  JStockbridge  LedsOrthoptics: Past, Present, Future: Transactions of the Third International Orthoptic Congress, Boston, July 1-3, 1975. New York, NY Stratton1976;287- 292
Rabinowicz  IMWalker  JW Disorders of ocular motility in children with hydrocephalus. Moore  SMein  JStockbridge  LedsOrthoptics: Past, Present, Future: Transactions of the Third International Orthoptic Congress, Boston, July 1-3, 1975. New York, NY Stratton1976;279- 286
Maloley  AWeber  SSmith  DR A and V patterns of strabismus in meningomyelocele. Am Orthopt J. 1977;27115- 118
Gaston  H Does the spina bifida clinic need an ophthalmologist? Z Kinderchir. 1985;40suppl 146- 50
Lennerstrand  GGallo  JE Neuro-ophthalmological evaluation of patients with myelomeninocele and Chiari malformations. Dev Med Child Neurol. 1990;32415- 422
Link to Article
Hamed  LM Overaction of the superior oblique muscle: some nosologic considerations. Am Orthopt J. 1993;4382- 86
Hamed  LMMaria  BLQuisling  RGMickle  JP Alternating skew on lateral gaze: neuroanatomic pathway and relationship to superior oblique overaction. Ophthalmology. 1993;100281- 286
Link to Article
Biglan  AW Ophthalmological complications of meningomyelocoele: a longitudinal study. Trans Am Ophthalmol Soc. 1990;88389- 462
Biglan  AW Strabismus associated with meningomyelocele. J Pediatr Ophthalmol Strabismus. 1995;32309- 314
Hoyt  CSFredrick  DR Serious neurologic disease presenting as comitant esotropia. Rosenbaum  ALSantiago  APedsClinical Strabismus Management: Principles and Surgical Techniques. Philadelphia, Pa WBSaunders Co1999;152- 162
Keane  JR Alternating skew deviation: 47 patients. Neurology. 1985;35725- 728
Link to Article
Hoyt  CS Ocular motor consequences of cortical visual impairment.  Paper presented at: Jampolsky Festschrift April 10, 2000 San Francisco, Calif
Hoyt  CS Abnormalities of the vestibular response in congenital esotropia. Am J Ophthalmol. 1982;93704- 708
Hoyt  CSMousel  DKWeber  AA Transient supranuclear disturbances of gaze in healthy neonates. Am J Ophthalmol. 1980;89708- 713
Doden  WAdams  A Elektronystagmographische Ergebnisse der Prüfung des optischvestibulären Systems bei Schielenden. Ber Dtsch Ophthalmol Ges. 1957;60316- 317
Salman  SDvon Noorden  GK Induced vestibular nystagmus in strabismic patients. Ann Otol Rhinol Laryngol. 1970;79352- 357
Sandstedt  POdenrick  PLennerstrand  G Gait and postural control in children with divergent strabismus. Binocul Vis Eye Muscle Surg Q. 1986;1141- 146
Lennerstrand  G Central motor control in concomitant strabismus. Graefes Arch Clin Exp Ophthalmol. 1988;226172- 174
Link to Article
Baloh  RWDemer  JL Optokinetic-vestibular interaction in patients with increased gain in the vestibulo-ocular reflex. Exp Brain Res. 1991;83427- 433
Link to Article
Baloh  RWRichman  LYee  RDHonrubia  V The dynamics of vertical eye movements in normal human subjects. Aviat Space Environ Med. 1983;5432- 38
Böhmer  ABaloh  RWL Vertical optokinetic nystagmus and optokinetic after nnystagmus in humans. J Vestib Res. 1990;1309- 315
Matsuo  VCohen  B Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: up-down asymmetry and effects of gravity. Exp Brain Res. 1984;53197- 216
Link to Article
Goltz  JCIrving  ELSteinbach  MJEizenman  M Vertical eye position control in darkness: orbital position and body orientation interact to modulate drift velocity. Vision Res. 1997;37789- 798
Link to Article
Slavin  MLPotash  SDRubin  SE Asymptomatic physiologic hyperdeviation in peripheral gaze. Ophthalmology. 1988;95778- 781
Link to Article
Liesch  ASimonsz  HJ Up- and downshoot in adduction after monocular patching in normal volunteers. Strabismus. 1993;125- 36
Link to Article
Neikter  B Effects of diagnostic occlusion on ocular alignment in normal subjects. Strabismus. 1994;267- 77
Link to Article
Hering  E In: The Theory of Binocular Vision. Bridgeman  BStark  Ltrans New York, NY Plenum Press1868;
Bielschowsky  A Disturbances of the vertical motor muscles of the eyes. Arch Ophthalmol. 1938;20175- 200
Link to Article
Mays  L Has Hering been hooked? Nat Med. 1998;4889- 890
Link to Article
Parks  MMMitchell  PR Oblique muscle dysfunction. Tasman  WJaeger  EAedsDuane's Clinical Ophthalmology. Philadelphia, Pa JB Lippincott1991;1- 9
Brodsky  MC DVD remains a moving target! J AAPOS. 1999;3325- 327
Link to Article
Brodsky  MC Dissociated vertical divergence: a righting reflex gone wrong. Arch Ophthalmol. 1999;1171216- 1222
Link to Article
Graf  WMeyer  DL Central mechanisms counteract visually induced tonus asymmetries: a study of ocular responses to unilateral illumination in goldfish. J Comp Physiol. 1983;150473- 481
Link to Article
Pfeiffer  W Equilibrium orientation in goldfish. Int Rev Gen Exp Zool. 1964;177- 111
Urist  MJ The etiology of so-called A and V syndromes. Am J Ophthalmol. 1958;46835- 844
Vallesca  A The A and V syndromes. Am J Ophthalmol. 1961;52172- 195
Breinen  GM Vertically incomitant horizontal strabismus: the A-V syndromes. N Y State J Med. 1961;612243- 2249
Brown  HW Vertical deviations [In Symposium, Strabismus]. Trans Am Acad Ophthalmol Otolaryngol. 1953;57157- 162
Urrets-Zavalia  ASolares-Zamora  JOlmos  HR Anthropological studies on the nature of cyclovertical squint. Br J Ophthalmol. 1961;45578- 596
Link to Article
Fink  W The role of developmental anomalies in vertical muscle deficits. Am J Ophthalmol. 1955;40529- 553
Gobin  MH Sagittalization of the oblique muscles as possible cause for the "A,""V," and "X" phenomena. Br J Ophthalmol. 1968;5213- 18
Link to Article
Nakamura  TAwaya  SMiyake  SL Insertion anomalies of the horizontal muscles and dysfunctions of the oblique muscles in the A-V patterns [in Japanese]. Nippon Ganka Gakkai Zasshi. 1991;95698- 703
Postic  G Etiopathogénie des syndromes A et V. Bull Mem Soc Fr Ophtalmol. 1965;78240- 252
Limón de Brown  EMonasterio  FOde Saint Martine  RFeldman  MS Estrabismo en el sindrome de Treacher-Collins-Franceschetti. Cir Cir. 1993;60210
Locke  JC Heterotopia of the blind spot in ocular vertical muscle imbalance. Am J Ophthalmol. 1968;65362- 374
Saunders  RAHolgate  RC Rectus muscle position in V-pattern strabismus: a study with coronal computed tomography scanning. Graefes Arch Clin Exp Ophthalmol. 1988;226183- 186
Link to Article
Clark  RAMiller  JMRosenbaum  ALDemer  JL Heterotopic muscle pulleys or oblique muscle dysfunction? J AAPOS. 1998;217- 25
Link to Article
Demer  JLOh  SYPoukens  V Evidence for active control of rectus extraocular muscle pulleys. Invest Ophthalmol Vis Sci. 2000;411280- 1290

Figures

Place holder to copy figure label and caption
Figure 1.

Physiologic effects of gravistatic(postural) and visual input to the oblique muscle tonus in fish. These bilateral torsional eye movements function to align the eyes with the perceived visual vertical by modulating oblique muscle tonus. A, A pitch-down body movement evokes increased inferior oblique muscle tonus and extorsion of the eyes. B, A pitch-up movement evokes increased superior oblique muscle tonus and intorsion of the eyes. C, In the unrestrained fish, an anterior light source evokes a pitch-down body movement. D, In the unrestrained fish, a posterior light source evokes a pitch-up body movement. E, In the restrained fish, anterior movement of overhead light evokes increased superior oblique muscle tonus and intorsion of both eyes. F, In the restrained fish, posterior movement of overhead light evokes increased inferior oblique muscle tonus and extorsion of both eyes.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Overhead view of a rabbit fixating an object in the right posterior visual field. Solid lines correspond to the visual axis of the abducted right eye and the adducted left eye. When the rabbit pitches forward (as when starting to run down a hill), the head rotates downward and the tail rotates upward. Although both eyes move downward in space, the left visual axis (which is directed toward the nose) rotates downward, while the right visual axis (which is directed toward the tail) rotates upward(curved arrows). This divergence of the visual axes corresponds to a right hypertropia that must be neutralized by vestibular innervation to elevate the lower left eye and depress the higher right eye. The compensatory vertical divergence for a pitch-forward position corresponds to primary inferior oblique muscle overaction.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

The close anatomical relationship of the semicircular canals and the extraocular muscles in humans is shown. Figure modified with permission from Simpson and Graf.17

Graphic Jump Location
Place holder to copy figure label and caption
Figure 4.

Neuroanatomical projections from the labyrinths to the extraocular muscles. The orientation of the anterior semicircular canal corresponds to that of the ipsilateral superior rectus and contralateral inferior oblique muscles. The orientation of the posterior semicircular canals corresponds to that of the ipsilateral superior oblique and contralateral inferior rectus muscles. The orientation of each horizontal canal corresponds to that of the horizontal rectus muscles. Turning the head to the right stimulates the right horizontal canal to increase excitatory innervation to the right medial rectus muscle and left lateral rectus muscle so that the eyes rotate equally and opposite to the direction of head rotation. HC indicates horizontal canal; AC, anterior canal; PC, posterior canal; LVN, lateral vestibular nucleus; MVN, medial vestibular nucleus; VI, abducens nucleus; MLF, medial longitudinal fasciculus; IV, trochlear nucleus; III, oculomotor nucleus; SR, superior rectus muscle; MR, medial rectus muscle; LR, lateral rectus muscle; and IO, inferior oblique muscle. Data modified with permission from Tusa.21

Graphic Jump Location
Place holder to copy figure label and caption
Figure 5.

Segregation of pathways controlling anterior and posterior canal tone. Only the anterior canal pathways receive inhibitory innervation by the cerebellar flocculus. A loss of modulation from the cerebellar flocculi could disinhibit the anterior canals and produce an upward tonus imbalance, leading to bilateral inferior oblique muscle overaction, bilateral extorsion, and V-pattern strabismus. FLO indicates flocculus; NOD, nodulus; AC, anterior canal; PC, posterior canal; HC, horizontal canal; SVN, superior vestibular nucleus; VTT, ventral tegmental tract; MVN, medial vestibular nucleus; MLF, medial longitudinal fasciculus; BC, brachium conjunctivum; III N, oculomotor nucleus (S, I, O, and M represent the oculomotor subnuclei); SR, superior rectus muscle; and IR, inferior rectus muscle. Data modified with permission from Tusa.21

Graphic Jump Location
Place holder to copy figure label and caption
Figure 6.

Superior oblique muscle overaction. A, Vestibular innervation. A central vestibular tonus imbalance corresponding to bilateral posterior canal predominance would produce tonic downgaze, divergence, and intorsion of the eyes if unopposed by fixational innervation. B, Vestibular plus fixational innervation. Fixational innervation, which conforms to the Hering law, recruits bilateral innervation to the superior rectus and inferior oblique muscles to negate the vertical component of the downward tonus bias. Fixational innervation allows a disconjugate intorsional bias to persist. PC indicates posterior canal; HC, horizontal canal; and AC, anterior canal.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 7.

Superior oblique muscle overaction. The observed eye movements in different fields of gaze are a summation of fixational innervation that conforms to Hering's law, and an underlying central vestibular imbalance that does not. All 4 depressors are receiving excessive vestibular innervation. Since the vertical action of the superior oblique muscles is maximal in adduction, the adducting eye exhibits a downshoot in adduction relative to the abducting eye. The tertiary abducting effects of the overacting superior oblique muscles are maximized by vestibular innervation in downgaze and minimized by fixational intervation in upgaze, producing an A pattern.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 8.

Primary inferior oblique muscle overaction. A, Visuovestibular innervation. Failure to develop normal binocular vision is associated with increased upward tonus to the eyes, perhaps through reduced anterior canal inhibition from the cerebellar flocculi. A central vestibular tonus imbalance corresponding to bilateral anterior canal predominance would produce tonic upgaze, horizontal divergence, and extorsion of the eyes if unopposed by fixational innervation. B, Visuovestibular plus fixational innervation. Fixational innervation recruits equal innervation from the inferior rectus and superior oblique muscles to negate the vertical component of the upgaze bias, and allows the disconjugate extorsional bias to persist. PC indicates posterior canal; HC, horizontal canal; and AC, anterior canal.

Graphic Jump Location

Tables

References

von Noorden  GK Binocular Vision and Ocular Motility: Theory and Management of Strabismus. 5th St Louis, Mo Mosby–Year Book Inc1996;367- 391
Piper  HF Über die Bedeutung des V- and A-Phänomens beim Schielen. Sitzungsbericht 107 Versammlung Rheinland Westfalen Augenärzte. 1963;63
Piper  HF Verlagerte Muskelansätze als eine Urwsache des Schrägschielens(und ihre operative Korrektur). Sitzungsbericht 109 Versammlung Rheinland Westfalen Augenärzte 1964;86
Weiss  JB Ectopies et pseudoectopies maculaires par rotation. Bull Mem Soc Fr Ophtalmol. 1966;79329- 349
Guyton  DLWeingarten  PE Sensory torsion as the cause of primary oblique muscle overaction/underaction and A- and V-pattern strabismus. Binocul Vis Eye Muscle Surg Q. 1994;9suppl209- 235
Ohm  J Das Ohrlabyrinth als Erzeuger des Schielens. Z Augenheilk. 1917;36253- 273
Ohm  J Einige Abildungen von vestibulärem Schielen. Z Augenheilk. 1918;39204- 207
Ohm  J Schrägschielen. Arch Augenheilk. 1928;39619- 643
Walls  GL The Vertebrate Eye and Its Adaptive Radiation.  Bloomfield Hills, Mich Cranbrook Institute of Science1942;303
Traill  ABMark  RF Optic and static contributions to ocular counter-rotation in carp. Exp Biol. 1970;52109- 124
Ewald  JR Physiologische Untersuchungen über das Endorgan des Nervus Oktavus.  Wiesbaden, Germany Bergmann1892;
Meyer  DLBullock  TH The hypothesis of sense-organ-dependent tonus mechanisms: history of a concept. Ann N Y Acad Sci. 1977;2903- 17
Link to Article
Brodsky  MC Vision-dependent tonus mechanisms of torticollis: an evolutionary perspective. Am Orthopt J. 1999;49158- 162
von Holst  E Über den Lichtrückenreflex bei der Fische. Pubbl Stn Zool Napoli II. 1935;15143- 158
von Holst  E Die Gleichgewichtssine der Fische. Verh Dtsch Ges Zool. 1935;37109- 114
Walls  GL The evolutionary history of eye movements. Vision Res. 1962;269- 80
Link to Article
Simpson  JIGraf  WG Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Ann N Y Acad Sci. 1981;37420- 30
Link to Article
Zee  DS Considerations on the mechanisms of alternating skew deviation in patients with cerebellar lesions. J Vestib Res. 1996;6395- 401
Link to Article
Leigh  RJZee  DS The Neurology of Eye Movements. 3rd New York, NY Oxford University Press Inc1999;19- 89
Graf  WMeyer  DL Eye position in fishes suggest different modes of interaction between commands and reflexes. J Comp Physiol. 1978;128241- 250
Link to Article
Tusa  RJ Nystagmus: diagnostic and therapeutic strategies. Semin Ophthalmol. 1999;1465- 73
Link to Article
Brandt  TDieterich  M Central vestibular syndromes in roll, pitch, and yaw planes. Neuro-ophthalmology. 1995;15291- 303
Link to Article
Brandt  TDieterich  M Vestibular syndromes in the roll plane: topographic diagnosis from brainstem to cortex. Ann Neurol. 1994;36337- 347
Link to Article
Dieterich  MBrandt  T Wallenberg's syndrome: lateropulsion, cyclorotation, and subjective visual vertical in thirty-six patients. Ann Neurol. 1992;31399- 408
Link to Article
Glasauer  SDieterich  MBrandt  T Simulation of pathological ocular counter-roll and skew torsion by a 3-D mathematical model. Neuroreport. 1999;101843- 1848
Link to Article
Baloh  RWSpooner  JW Downbeat nystagmus: a type of central cerebellar nystagmus. Neurology. 1981;31304- 310
Link to Article
Straumann  DZee  DSSolomon  D Three-dimensional kinematics of ocular drift in humans with cerebellar atrophy. J Neurophysiol. 2000;831125- 1140
Böhmer  AStraumann  D Pathomechanism of mammalian downbeat nystagmus due to cerebellar lesion: a simple hypothesis. Neurosci Lett. 1998;250127- 130
Link to Article
France  TD Strabismus in hydrocephalus. Am Orthopt J. 1975;25101- 105
France  TD The association of "A" pattern strabismus with hydrocephalus. Moore  SMein  JStockbridge  LedsOrthoptics: Past, Present, Future: Transactions of the Third International Orthoptic Congress, Boston, July 1-3, 1975. New York, NY Stratton1976;287- 292
Rabinowicz  IMWalker  JW Disorders of ocular motility in children with hydrocephalus. Moore  SMein  JStockbridge  LedsOrthoptics: Past, Present, Future: Transactions of the Third International Orthoptic Congress, Boston, July 1-3, 1975. New York, NY Stratton1976;279- 286
Maloley  AWeber  SSmith  DR A and V patterns of strabismus in meningomyelocele. Am Orthopt J. 1977;27115- 118
Gaston  H Does the spina bifida clinic need an ophthalmologist? Z Kinderchir. 1985;40suppl 146- 50
Lennerstrand  GGallo  JE Neuro-ophthalmological evaluation of patients with myelomeninocele and Chiari malformations. Dev Med Child Neurol. 1990;32415- 422
Link to Article
Hamed  LM Overaction of the superior oblique muscle: some nosologic considerations. Am Orthopt J. 1993;4382- 86
Hamed  LMMaria  BLQuisling  RGMickle  JP Alternating skew on lateral gaze: neuroanatomic pathway and relationship to superior oblique overaction. Ophthalmology. 1993;100281- 286
Link to Article
Biglan  AW Ophthalmological complications of meningomyelocoele: a longitudinal study. Trans Am Ophthalmol Soc. 1990;88389- 462
Biglan  AW Strabismus associated with meningomyelocele. J Pediatr Ophthalmol Strabismus. 1995;32309- 314
Hoyt  CSFredrick  DR Serious neurologic disease presenting as comitant esotropia. Rosenbaum  ALSantiago  APedsClinical Strabismus Management: Principles and Surgical Techniques. Philadelphia, Pa WBSaunders Co1999;152- 162
Keane  JR Alternating skew deviation: 47 patients. Neurology. 1985;35725- 728
Link to Article
Hoyt  CS Ocular motor consequences of cortical visual impairment.  Paper presented at: Jampolsky Festschrift April 10, 2000 San Francisco, Calif
Hoyt  CS Abnormalities of the vestibular response in congenital esotropia. Am J Ophthalmol. 1982;93704- 708
Hoyt  CSMousel  DKWeber  AA Transient supranuclear disturbances of gaze in healthy neonates. Am J Ophthalmol. 1980;89708- 713
Doden  WAdams  A Elektronystagmographische Ergebnisse der Prüfung des optischvestibulären Systems bei Schielenden. Ber Dtsch Ophthalmol Ges. 1957;60316- 317
Salman  SDvon Noorden  GK Induced vestibular nystagmus in strabismic patients. Ann Otol Rhinol Laryngol. 1970;79352- 357
Sandstedt  POdenrick  PLennerstrand  G Gait and postural control in children with divergent strabismus. Binocul Vis Eye Muscle Surg Q. 1986;1141- 146
Lennerstrand  G Central motor control in concomitant strabismus. Graefes Arch Clin Exp Ophthalmol. 1988;226172- 174
Link to Article
Baloh  RWDemer  JL Optokinetic-vestibular interaction in patients with increased gain in the vestibulo-ocular reflex. Exp Brain Res. 1991;83427- 433
Link to Article
Baloh  RWRichman  LYee  RDHonrubia  V The dynamics of vertical eye movements in normal human subjects. Aviat Space Environ Med. 1983;5432- 38
Böhmer  ABaloh  RWL Vertical optokinetic nystagmus and optokinetic after nnystagmus in humans. J Vestib Res. 1990;1309- 315
Matsuo  VCohen  B Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: up-down asymmetry and effects of gravity. Exp Brain Res. 1984;53197- 216
Link to Article
Goltz  JCIrving  ELSteinbach  MJEizenman  M Vertical eye position control in darkness: orbital position and body orientation interact to modulate drift velocity. Vision Res. 1997;37789- 798
Link to Article
Slavin  MLPotash  SDRubin  SE Asymptomatic physiologic hyperdeviation in peripheral gaze. Ophthalmology. 1988;95778- 781
Link to Article
Liesch  ASimonsz  HJ Up- and downshoot in adduction after monocular patching in normal volunteers. Strabismus. 1993;125- 36
Link to Article
Neikter  B Effects of diagnostic occlusion on ocular alignment in normal subjects. Strabismus. 1994;267- 77
Link to Article
Hering  E In: The Theory of Binocular Vision. Bridgeman  BStark  Ltrans New York, NY Plenum Press1868;
Bielschowsky  A Disturbances of the vertical motor muscles of the eyes. Arch Ophthalmol. 1938;20175- 200
Link to Article
Mays  L Has Hering been hooked? Nat Med. 1998;4889- 890
Link to Article
Parks  MMMitchell  PR Oblique muscle dysfunction. Tasman  WJaeger  EAedsDuane's Clinical Ophthalmology. Philadelphia, Pa JB Lippincott1991;1- 9
Brodsky  MC DVD remains a moving target! J AAPOS. 1999;3325- 327
Link to Article
Brodsky  MC Dissociated vertical divergence: a righting reflex gone wrong. Arch Ophthalmol. 1999;1171216- 1222
Link to Article
Graf  WMeyer  DL Central mechanisms counteract visually induced tonus asymmetries: a study of ocular responses to unilateral illumination in goldfish. J Comp Physiol. 1983;150473- 481
Link to Article
Pfeiffer  W Equilibrium orientation in goldfish. Int Rev Gen Exp Zool. 1964;177- 111
Urist  MJ The etiology of so-called A and V syndromes. Am J Ophthalmol. 1958;46835- 844
Vallesca  A The A and V syndromes. Am J Ophthalmol. 1961;52172- 195
Breinen  GM Vertically incomitant horizontal strabismus: the A-V syndromes. N Y State J Med. 1961;612243- 2249
Brown  HW Vertical deviations [In Symposium, Strabismus]. Trans Am Acad Ophthalmol Otolaryngol. 1953;57157- 162
Urrets-Zavalia  ASolares-Zamora  JOlmos  HR Anthropological studies on the nature of cyclovertical squint. Br J Ophthalmol. 1961;45578- 596
Link to Article
Fink  W The role of developmental anomalies in vertical muscle deficits. Am J Ophthalmol. 1955;40529- 553
Gobin  MH Sagittalization of the oblique muscles as possible cause for the "A,""V," and "X" phenomena. Br J Ophthalmol. 1968;5213- 18
Link to Article
Nakamura  TAwaya  SMiyake  SL Insertion anomalies of the horizontal muscles and dysfunctions of the oblique muscles in the A-V patterns [in Japanese]. Nippon Ganka Gakkai Zasshi. 1991;95698- 703
Postic  G Etiopathogénie des syndromes A et V. Bull Mem Soc Fr Ophtalmol. 1965;78240- 252
Limón de Brown  EMonasterio  FOde Saint Martine  RFeldman  MS Estrabismo en el sindrome de Treacher-Collins-Franceschetti. Cir Cir. 1993;60210
Locke  JC Heterotopia of the blind spot in ocular vertical muscle imbalance. Am J Ophthalmol. 1968;65362- 374
Saunders  RAHolgate  RC Rectus muscle position in V-pattern strabismus: a study with coronal computed tomography scanning. Graefes Arch Clin Exp Ophthalmol. 1988;226183- 186
Link to Article
Clark  RAMiller  JMRosenbaum  ALDemer  JL Heterotopic muscle pulleys or oblique muscle dysfunction? J AAPOS. 1998;217- 25
Link to Article
Demer  JLOh  SYPoukens  V Evidence for active control of rectus extraocular muscle pulleys. Invest Ophthalmol Vis Sci. 2000;411280- 1290

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